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Bulletin of Insectology 58 (2): 141-152, 2005
ISSN 1721-8861
The accompanying fauna of Osmia cornuta and Osmia rufa
and effective measures of protection
Miloje KRUNIĆ1, Ljubiša STANISAVLJEVIĆ1, Mauro PINZAUTI2, Antonio FELICIOLI3
1Institute of Zoology, Faculty of Biology, University of Belgrade, Serbia and Montenegro
2Dipartimento di Coltivazione e Difesa delle Specie Legnose, Sez. Entomologia Agraria, Università di Pisa, Italy
3Dipartimento di Anatomia, Biochimica e Fisiologia veterinaria, Università di Pisa, Italy
Abstract
The present paper treats species of the fauna accompanying Osmia cornuta (Latreille) and O. rufa (L.), with special attention to
measures of protection against the most significant organisms that restrict their populations. The most significant organisms that
restrict Osmia populations are the fly Cacoxenus indagator Loew and the mite Chaetodactylus osmiae Dufour. The wasp Mono-
dontomerus obscurus Westwood is a significant organism that restricts Osmia populations in paper tubes used as nesting material,
and is found sporadically in marsh reeds used for this purpose in the vicinity of Belgrade. However, it was not present in lamellar
boxes. Anthrax anthrax Schrank is an important organism restricting populations of O. cornuta and O. rufa in several localities in
the vicinity of Pisa (Italy). The other species of the accompanying fauna exerted no significant influence on the abundance of
populations of these bees in the vicinity of Belgrade. Species of the accompanying fauna are grouped in the following categories:
cleptoparasites, parasitoids, nest destroyers, predators, cleptobionts, and accidental nest residents.
Key words: orchard bees, Osmia cornuta, Osmia rufa, accompanying fauna, parasites, parasitoids.
Introduction
The use of Osmia for pollination of orchards was first
attempted during the second half of the last century in
Japan with the species Osmia cornifrons (Radoszkow-
ski) (Maeta and Kitamura, 1964, 1965). From the very
beginning, satisfactory results were obtained in using
these species as orchard pollinators, and the practice has
been continued and advanced down to the present day.
Today the majority of apple orchards in Japan are polli-
nated with the aid of Osmia (Maeta, 1978; Sekita,
2001). Encouraged by the successful commercialisation
of Megachile rotundata (F.), and by the results achieved
by Japanese authors with their species of Osmia, inves-
tigators in the United States during the 1970's and
1980's started to investigate the American native species
Osmia lignaria Say as a pollinator of orchards (Torchio,
1976; Bosch and Kemp, 2001), somewhat later exam-
ining the possibility of using a species introduced from
Japan (O. cornifrons) for this purpose (Batra, 1998). At
the same time, investigations were initiated on the pos-
sibility of using as pollinators Osmia rufa (L.) in Den-
mark (Holm, 1973; Kristjansson, 1989), England (Raw,
1972), and Osmia cornuta (Latreille) in Spain (Bosch,
1994), Serbia (Krunić et al., 1995, 2001), and Italy
(Pinzauti, 1992; Felicioli, 1995; Ladurner et al., 2002;
Maccagnani et al., 2003). The technology of raising O.
cornuta is known today, and this bee can be reared in
the desired numbers (Stanisavljević, 2000).
Many parasitoids, predators, nest destroyers, and acci-
dental nest residents can be found in the nests of O. cor-
nuta and O. rufa in Southeastern Europe. With the in-
crease in bee populations, the accompanying fauna also
increases in both diversity and abundance. For man-
agement and multiplication of populations of O. cornuta
and O. rufa, control of certain species of the accompa-
nying fauna is essential, both during the period of activ-
ity of the bees and during the periods of their develop-
ment and overwintering. There are various measures of
protection against the accompanying fauna, some of
which depend upon the type of nesting material used.
For example, cocoons of O. cornuta and O. rufa in pa-
per tubes are often parasitized by the wasp Monodon-
tomerus obscurus Westwood. Insectivorous birds find it
easy to extract paper tubes with cocoons from wooden
blocks. Birds and mice destroy tubes on the ground and
eat the cocoons inside. In this way, in a short time birds
can destroy a large part not only of bee populations in
paper tubes, but also of populations in reeds (figure 1).
They can destroy easily bee populations before and
during overwintering if the reeds are not adequately
protected. Nests of O. cornuta and O. rufa in lamellar
boxes are better protected against some parasitoids and
birds, but they often house the coleopteran Trichodes
apiarius L., the mite Chaetodactylus osmiae Dufour, the
fly Anthrax anthrax Schrank, certain Dermestidae, and
other species of the accompanying fauna.
Figure 1. Reed nest destroyed by birds.
(In colour at www.bulletinofinsectology.org)
142
Of all species of the accompanying fauna, the most
significant organisms that restrict populations of O. cor-
nuta and O. rufa in Southeast Europe are the dipteran
Cacoxenus indagator Loew and the mite Ch. osmiae
(Krunić et al., 1995; Stanisavljević, 1996; Krunić et al.,
1999). In several localities around Pisa (Italy) a signifi-
cant organism that restricts Osmia populations is the
dipteran A. anthrax (Felicioli, 2000), which is very rare
in populations in the vicinity of Belgrade. The abun-
dance and diversity of individual members of the ac-
companying fauna vary from one locality to the next, as
well as from season to season. Apart from fungal dis-
eases caused by spores of Ascosphaera spp. (so-called
chalkbrood), other diseases of O. cornuta and O. rufa
are unknown to date. In populations in the vicinity of
Belgrade, we had no significant presence of fungal dis-
eases caused by Ascosphaera spp., probably because
80% of the nesting material used in every season con-
sisted of previously unused reeds, while reeds that had
been used during the previous season represented only
20%. Spores of fungal diseases are resistant and persist
for years in used nesting material. Because of the danger
of fungal diseases and Ch. osmiae, lamellar boxes that
are used every year should be subjected to high tem-
perature or treatment with a 0.07% solution of endosul-
fan before use (Krunić et al., 2001). It is recommend-
able to burn reeds used for several seasons after emer-
gence of the bees.
The following species of the accompanying fauna
were registered in populations of O. cornuta and O. rufa
in Southeastern Europe, they are grouped in the fol-
lowing categories: cleptoparasites, parasitoids, nest de-
stroyers, predators, cleptobionts, and accidental nest
residents as reported in a previously published paper
(Krunić et al., 1995).
Cleptoparasites
Cacoxenus indagator Loew (Diptera Drosophilidae).
This species is distributed on the continent of Europe
(Julliard, 1947; Kekić, 2002).
Adults of C. indagator are 3 to 3.5 mm long. The tho-
rax is light-grey, the abdomen black with light trans-
verse bands. The large eyes are brown to dirty-red in col-
our (figure 2). Females of C. indagator lay their eggs on
the pollen provisions in nests of O. cornuta and O. rufa.
Larvae develop from the eggs and feed actively until
they reach the overwintering prepupal stage (figure 3).
With the increase of daily temperatures in spring, bar-
rel-shaped pupae develop from the prepupae over a pe-
riod of several days. Adults appear after a relatively
short duration of the pupal stage (about 22 days at 20 -
25 °C) (Stanisavljević, 1996). The last instar larvae of
this fly are able to migrate from the internal cells to the
vestibule of the tunnel by perforating the mud partitions
with their mouth parts. Due to this larval behaviour it is
often possible to observe large amounts of larvae or pu-
pae (20 to 40) in the vestibule of the nest (Julliard,
1948) (figure 4). Earlier emergence of bees from the
nest, which is accompanied by perforation of its parti-
tions, facilitates the subsequent unhindered departure of
C. indagator adults. The length of the active period of
adults of C. indagator is synchronized with the comple-
tion of the active period of O. cornuta (Stanisavljević,
1996).
C. indagator is very frequent in populations of O.
cornuta and O. rufa in the wider area of Belgrade. In
nature it usually appears 2-3 weeks after the appearance of
the first individual orchard bees, i.e., at the end of March
Figure 2. C. indagator, female.
(In colour at www.bulletinofinsectology.org)
Figure 3. C. indagator, overwintering prepupal stage.
(In colour at www.bulletinofinsectology.org)
Figure 4. C. indagator, large amount of larvae or pupae
in the vestibule of the O. rufa nest.
(In colour at www.bulletinofinsectology.org)
143
or in April. At the beginning, males and females of C.
indagator can be seen in the shelter, but only females
remain after mating, which lasts up to 10 days
(Stanisavljević, 1996). The females appear to be con-
tinuously on “guard duty” at the side of a reed near the
opening of a bee nest (figure 5). When a female bee
leaves the nest, the fly hurriedly enters it, lays an egg on
the pollen provision, rapidly departs, and awaits the next
opportunity (Julliard, 1947, 1948; Coutin and Desmier
de Chenon, 1983; Stanisavljević, 1996). Sometimes a
female bee surprises a C. indagator female in its nest.
Being considerably smaller than the bee, the female fly
readily abandons the nest in this case. Females of O.
cornuta dive frequently on females of C. indagator, but
this has no effect on the protection of their nests. The
placing of strips of sticky paper on bundles at a certain
distance from the reed openings, where C. indagator
females usually wait for bees to leave their nests, did
not yield significant results in controlling this clepto-
parasite. Only limited numbers of C. indagator indi-
viduals got stuck on the paper (Stanisavljević, 1996).
Individuals of C. indagator are accustomed to mass
flight of orchard bees, and in most cases they do not re-
act to their movement. Such behavior allows them to be
collected with an aspirator, during which they make no
sudden attempt to escape. This method yielded satis-
factory results for the control of this cleptoparasite in
multiplication shelters (Krunić et al., 2001). Such a
method of removal cannot be used in nests disposed in
orchards because it would entail a great loss of time
with a negligible result. However, when C. indagator
populations in multiplication shelters were removed
with an aspirator in successive years, then their abun-
dance in the whole managed bee population was consid-
erably reduced (Stanisavljević, 1996). The number of
larvae of C. indagator in nest cells varies. When only
two or three larvae of the cleptoparasite are present in
the nest, the bee larva will develop alongside them and
spin a cocoon, that is noticeably smaller than usual
(Juillard, 1948; Raw, 1972; Stanisavljević, 1996). At
some localities, we found 10-20 tiny larvae of C. inda-
gator in certain cells of O. cornuta. In such circum-
stances, the bee larva has no chance to develop. When
present in large numbers, C. indagator larvae can perfo-
rate the wall of the neighboring cell or of several cells in
a row and consume their contents, too. The number of
cells infested with C. indagator varied significantly
from one locality to the next and from year to year.
Without mechanical control, this cleptoparasite can be-
come very abundant in nests in the area of Belgrade and
significantly reduce multiplication of populations of O.
cornuta and O. rufa.
Populations of O. cornuta reared in almond orchards
in Spain were not infested or negligibly infested with C.
indagator, because bees in those orchards for the most
part complete their activity before the hatching of these
cleptoparasites (Bosch, 1992). In Italy, wild populations
of O. cornuta are infested at low levels, while O. rufa
populations can show high levels of C. indagator infes-
tation due to the differences in the flying season of the
two bee species. Both O. cornuta and O. rufa managed
populations, if released in April, showed high levels of
Figure 5. C. indagator, female at the side of a reed near
the openings of bee nests.
(In colour at www.bulletinofinsectology.org)
infestation if the nests of the orchard bees were not re-
newed every year or if the C. indagator adults weren’t
captured (Felicioli, 2000).
Chaetodactylus osmiae Dufour (Acarina Chaetodactyli-
dae). This mite is distributed in Europe as far north as
Denmark, as far as the Urals in the east, to the southern
limits of the Balkan Peninsula in the south, and as far as
the Atlantic Coast (including Great Britain) in the west.
It is found in the nests of many European species of
solitary bees (Černy and Samšiňák, 1971).
Mites of the genus Chaetodactylus have very similar
development, with two reproductive cycles that repeat
themselves periodically (Zachvatkin, 1941).
The direct cycle consists of the following stages: egg,
larva, protonymph, tritonymph, adult (male and female).
This cycle appears when the bee nest contains abun-
dance of food (pollen and nectar). The nest then most
often also contains enough moisture for the direct de-
velopment of the mites. In this case, the development
cycle is short and can repeat itself as many as ten times
in a single season. The number of cycles depends exclu-
sively on the amount of pollen and nectar, moisture
content of the surroundings and temperature
(Stanisavljević, 1996).
The indirect cycle differs from the direct cycle in the
appearance of a very resistant stage that enters dor-
mancy, the so-called hypopus (figure 6, a and b). The
hypopus that appears sporadically in the life cycle of
mites of the order Astigmata, is also called a heteromor-
phic deutonymph, while the tritonymph is called a ho-
meomorphic deutonymph. The hypopus occurs in two
basic forms, mobile and immobile (encysted) (Krom-
bein, 1962; Fain, 1966). The indirect cycle unfolds ac-
cording to the following scheme: egg, larva, pro-
tonymph, hypopus (mobile or immobile), tritonymph,
adult. This type of cycle (facultative hypopodia) sets in
when environmental conditions are unfavorable for de-
velopment of the direct cycle, i.e., when there is not
enough moisture and food in the cell. The hypopus is a
supplementary stage between the protonymph and tri-
tonymph stage and in fact represents the deutonymph
stage. A characteristic distinction of this facultative
stage in the development of all mites of the order
Astigmata (and of Ch. osmiae) in relation to the deu-
tonymphs of other mites is that it lacks a mouth and
mouth parts and does not feed, but rather exists at the
144
Figure 6a. Ch. osmiae, mobile hypopi.
(In colour at www.bulletinofinsectology.org)
Figure 6b. Ch. osmiae, immobile hypopi.
(In colour at www.bulletinofinsectology.org)
expense of reserves accumulated in the preceding stage.
The hypopus represents a resistant form which ensures
survival under the unfavorable environmental condi-
tions that occur in bee nests at the end of the summer
and throughout the winter. It also ensures dispersal of
the species.
The existence of two types of hypopus is an adapta-
tion linked to dispersal and preservation of the species.
To be specific, the mobile type of hypopus possesses
four pairs of well-developed legs with specialized hook-
like outgrowths that enable it to attach itself easily to
adult bees (figure 7). The immobile type of hypopus has
short legs, and its parts for attachment are very rudi-
mentary (figure 6b). They do not emerge from the skin
(exuviae) of the protonymph until the moment of their
activation, i.e., transformation into tritonymphs
(Stanisavljević, 1996).
Mobile and immobile hypopi are of virtually equal
significance for the survival of this species of mite. The
mobile type of hypopus is significant for dispersal and
transfer. Its development cycle is synchronized with the
development cycle of the bees. This is the form of the
mite that is transferred from the old to the new nest, i.e.,
from one generation of bees to their progeny by means
of the bee as a host, which carries them on its body at
the time of emergence. Encysted hypopi always remain
Figure 7. Ch. osmiae on O. cornuta female.
(In colour at www.bulletinofinsectology.org)
in the old nest of the host bee. This encysted form of
mite awaits the arrival of a bee of the same or some
other species that will take over the old abandoned nest.
The immobile type of hypopus has the primary role of
preservation of the species under unfavorable condi-
tions, since it is capable of remaining in the dormant
state for several years until conditions for its activation
are achieved (Seidelmann, 1990). Under favorable con-
ditions, it is activated and develops into a tritonymph,
which develops into an adult female.
When transported into a cell of the host, a mobile hy-
popus continues its development cycle. It is transformed
into a tritonymph, which is very active, feeds at an ac-
celerated rate, and rapidly develops into an adult female.
Females of Ch. osmiae lay eggs from which males de-
velop very rapidly. They mate with their mothers or
with other females found in the same cell. After mating,
the females lay eggs from which the complete (direct)
cycle proceeds and repeats itself, with the result that a
large colony of mites is soon formed.
Under the climatic conditions of the Southeastern
Europe, encysted hypopi appear from the middle of
August onward, while the first mobile hypopi appear at
the end of August (Stanisavljević, 1996).
According to some authors (Van Lith, 1957; Krom-
bein, 1962; Seidelmann, 1990), mites of the genus
Chaetodactylus sometimes consume the contents of bee
eggs and even certain later stages of development in ad-
dition to pollen and nectar. These mites are incapable of
perforating the wall of the bee's cocoon. In certain cells,
we found a tiny cocoon with a developed bee inside and
a multitude of mite hypopi around it. Under such condi-
tions, the bee's cocoon is considerably reduced in size
due to a shortage of food during larval development
(Stanisavljević, 1996).
Male and female bees during emergence from the nest
pass through cells with many mobile mite hypopi,
which they carry with them in sometimes great num-
bers. Certain females can be completely yellow from the
multitude of hypopi on their bodies (figure 7). The hy-
popi undergo mass multiplication if they come across
pollen in the nest cell. When the female bee closes a cell
infested with hypopi, they most often fill all of the space
in it. If reeds for bee nesting were used several years in
145
a row, then infestation with the mite Ch. osmiae in our
populations at certain localities attained more than 50%
of established cells (Krunić et al., 2001). If cocoons are
infested with these mites, it is useful to disinfect them
with endosulfan (a 0.007% aqueous solution) before
taking them into the field. Treating cocoons of O. cor-
nuta and O. rufa during the winter period with a 0.007%
solution of endosulfan for a period of 3 min is a very
effective method of controlling all stages in develop-
ment of the mite Ch. osmiae. It was found that such
treatment of cocoons had no negative effect on the bees
inside (Krunić et al., 2001). In Japan, endosulfan is di-
rectly sprayed on empty and already inhabited reeds to
control the mite Chaetodactylus nipponicus Kurosa,
which greatly reduces populations of the bee O. corni-
frons. If Osmia cocoons are not stripped from the reeds,
there will always remain a certain percentage of mites in
them that survive this treatment (Yamada, 1990; Sekita
and Yamada, 1993). For this reason, stripping of co-
coons from the nesting material and treating them with
endosulfan is a much more effective way of controlling
this cleptoparasite.
In some years with extremely high summer tempera-
tures (between 30 and 40 °C) and no precipitation for a
longer period of time, we observed mass mortality of
mites in bee nests in the vicinity of Belgrade. In Japan
heat treatment is a common practice to control Ch. nip-
ponicus (Sekita and Yamada, 1993). The presence of
mites in our populations in the following years was
negligible. A succession of rainy summers without dry
periods or extremely high temperatures favors mass de-
velopment of hypopi in cells, with the result that the in-
festation in bee populations then increases significantly.
Chrysis ignita L. (Hymenoptera Chrysididae). The
Chrysididae are distributed in the Palearctic and Nearc-
tic, and the species Ch. ignita is encountered virtually
all over Europe (Bouček, 1957). Adults have a metallic
luster and body length of 5-10 mm. The head and thorax
are coloured shiny blue-green, sometimes with a golden
reflection. The abdomen is dark ruby-red. The underside
of the abdomen is concave, which enables the insect to
roll itself up into a defensive ball when threatened
(Kimsey and Bohart, 1990).
These insects develop in the nests of bees and wasps.
Their larvae feed on reserves of food gathered earlier by
the host for its own progeny. They are often able to in-
fest several successive cells in the nest of solitary bees.
The prepupae of Ch. ignita spin an oval-shaped semi-
transparent cocoon, in which they overwinter. The spe-
cies Ch. ignita is sporadically registered in nests of O. cor-
nuta and O. rufa in the vicinity of both Belgrade and Pisa.
Parasitoids
Monodontomerus obscurus Westwood (Hymenoptera
Torymidae). This species is distributed in the north of
Europe from the Moscow Province in Russia through
Moldavia and the Caucasus to Central Asia (Nikol-
skaya, 1952; Bouček, 1977; Medvedev, 1978). It was
introduced to North America, where it parasitizes spe-
cies of the genera Megachile and Osmia (Hobbs and
Krunić, 1971; Eves, 1970; Eves et al., 1980).
The adults are metallic blue-green in colour, with red
eyes. The females have a thin and supple ovipositor.
They are 3.8-4.9 mm long, while males are somewhat
smaller and measure 2.4-3.0 mm in length
(Stanisavljević, 1996) (figure 8). Adults emerge through
the single uniform opening (the emergence opening,
about 1 mm in diameter) on the bee cocoon that is in
correspondence of a hole of the same diameter that
these little wasps make in the surface of the nest
(Arundo or Phragmites reed) (Felicioli, 2000) (figure
9a). The female perforates with its ovipositor the reed
nest, and the cocoon and integument of the host larvae,
Figure 8. M. obscurus, adults.
(In colour at www.bulletinofinsectology.org)
Figure 9a. M. obscurus, Phragmites cane with the
emergence openings.
(In colour at www.bulletinofinsectology.org)
Figure 9b. M. obscurus, overwintering prepupa in co-
coons.
(In colour at www.bulletinofinsectology.org)
146
injects a paralyzing fluid, and then lays several eggs on
or near the mature bee larva (Hobbs and Krunić, 1971;
Stanisavljević, 1996). Larvae of the ecto-parasitoid feed
on prepupae or white pupae of the bee. If an egg is laid
in a cocoon with a dark pupa or adult bee, both the host
and the parasitoid will die. Larvae of the parasitoid are
white in colour, equipped with many bristles, and about
2.5 mm long upon reaching maturity (figure 9b). M. ob-
scurus overwinters in the prepupal stage. Up to three
generations of M. obscurus annually are possible in the
vicinity of Belgrade (Krunić et al., 1999).
The parasitoid M. obscurus is frequently present in the
nests of solitary bees. From 3 to 27 of parasitoids (10 on
average) can develop in a single cell of O. cornuta
(Stanisavljević, 1996). It easily penetrates paper tubes
and massively parasitizes O. cornuta and O. rufa. We
found M. obscurus specimens sporadically in bee nests
in reeds, but did not find any in lamellar boxes in the
vicinity of Belgrade. However, M. obscurus is found in
significant numbers in both kinds of reeds (Phragmites
and Arundo), but in very low numbers in lamellar boxes
in the area of Pisa (Italy).
Melittobia acasta Walker (Hymenoptera Eulophidae).
The species M. acasta spread from Europe to many
other regions. It infests a large number of genera of
bees, wasps, and some flies from Europe to Japan,
North America, South America, and New Zealand
(Medvedev, 1978; Dahms, 1984).
This wasp is often found in managed populations of
solitary bees and bumblebees, to which it generally
causes great damage due to its high reproductive poten-
tial, short life cycle, and significantly greater number of
females (95%) than males (Dahms, 1984; Macfarlane and
Donovan, 1989). The sexes of M. acasta differ in size,
appearance of the head and wings, and colour. In addition
to being larger and darker, the females have shorter knee-
like antennae and larger functional wings. M. acasta
overwinters as a prepupa in a cell of the host. Mating
takes place inside the host cocoon, and only fertilized fe-
males emerge from the cocoon. There are several genera-
tions during the season, and the development cycle usu-
ally lasts about two weeks (Hobbs and Krunić, 1971).
In the case of O. cornuta, we found only a few co-
coons infested with M. acasta over the last 20 years.
Figure 10. L. dorsigera, adult.
(In colour at www.bulletinofinsectology.org)
Leucospis dorsigera F. (Hymenoptera Leucospididae).
This is a Palearctic species (Medvedev, 1978; Madl,
1989). Adult specimens are black with yellow markings
on the body and legs. They measure 6-9 mm in length
and are recognizable by their expanded and elongated
hind legs (figure 10). Females of L. dorsigera lay eggs
on a prepupa or pupa in the cocoon of the host. The lar-
vae of this wasp usually do not spin a cocoon, but rather
pupate in the cocoon of the host. Under European con-
ditions, the species L. dorsigera most often has two
generations a year. It was found sporadically in reeds
with nests of O. cornuta and O. rufa, but did not cause
any significant damage in populations of these bees.
Anthrax anthrax Schrank (Diptera Bombyliidae). This
species belongs to the fauna of Western Europe. Body
length is 10-13 mm. The body is black with an almost
round head, the wings darkly sooty (figure 11). Charac-
teristic tiny white husks are discernible on the abdomen.
The females of this fly are attracted by the colour con-
trast created by a black disc on a different coloured
background (Marston, 1964). When a female of A. an-
thrax hovers in front of the entrance of a solitary bee
nest, it almost unerringly pitches an egg right into the
nest with a flexure of the rear end of its body (Grandi,
1951). The first instar larva of this species is called
planidium and is characterised by a high mobility so
that it reaches the bee pollen provision before sealing
occurs. It is still not clear if the planidium could pass
through the mud partitions as described by Fabre (1937)
or not. The planidium will not feed himself for a long
time until the bee larva spins the cocoon. This is the
right moment for the planidium to parasite the bee lar-
vae. Once the bee has reached the pupal stage, the para-
sitization may occur. In this case it is possible to find
the fragmented parts of the adult bee and the living fly
larva together in the cocoon (figure 12).
This fly is present in almost all the Tuscany ecosystems
(Italy) showing a parsivoltine and/or bivoltine cycle
(Felicioli and Pinzauti, 1998), while it is univoltine in
Spain (Fabre, 1937) and bivoltine in France (Du Merle,
1972).
Within some of the managed populations of both O.
cornuta and O. rufa in Italy almost 50% of the sealed
tunnels resulted parasitized by A. anthrax. The pupa of
Figure 11. A. anthrax, adult.
(In colour at www.bulletinofinsectology.org)
147
Figure 12. A. anthrax, larva feeding on O. cornuta
pupa.
(In colour at www.bulletinofinsectology.org)
Figure 13. A. anthrax, “armed pupa” in O. cornuta co-
coon.
(In colour at www.bulletinofinsectology.org)
this fly is characterised by a crest on the head so that it
is defined as “armed pupa” (figure 13). The presence of
the crest allows the pupa to open the cocoon and de-
stroy the mud partitions of all the cells in order to reach
the outside of the nest. Once the armed pupa has
reached and perforated the last mud plug the fly will
emerge leaving the host remains in its place. It is often
possible to find hundreds of them already in the mud
plug or on the floor near the Osmia nests.
The damage that this fly may cause is direct and/or in-
direct: the direct one is that each fly planidium kills the
Osmia larva and it usually happens in the inner part of
the nest containing the future female bees; the indirect
damage is caused by armed pupae that start migration
towards the outside of the nest during August (50% of
the fly population). They crush all the cocoons contain-
ing bees still at the larval stage present in the nest, kill-
ing all of them and causing a very high mortality in the
Osmia populations. In this case A. anthrax could be
considered a nest destroyer (Felicioli, 2000).
In the area of Belgrade, the species A. anthrax is spo-
radically found in nests of O. cornuta and O. rufa. In
Italy, on the other hand, this parasitoid is common, and
in some localities it can parasitize up to 95% of the total
number of cocoons (Felicioli, 2000). Osmia cocoons in
lamellar boxes are much more frequently parasitized
than cocoons in reeds, 47% and 5% respectively
(Pratesi, 2004). A. anthrax is frequently present in
populations of O. rufa in Germany, where it attains a
degree of infestation of about 2% (Seidelmann, 1990).
The use of yellow painted lamellar boxes with only
0.5 cm deep black coloured holes induces Anthrax fe-
males to hover and spray their eggs in these “virtual”
bee tunnels so that the combined use of these “Anthrax
egg traps” and reed nests allows to highly reduce the
percent of parasitization. Moreover, the imago flies usu-
ally emerge one week to fifteen days after the Osmia
females, so that the practice of destroying the nests after
the emergence of female bees is a useful method to re-
duce the fly parasitization (Pratesi, 2004).
Predators
Trichodes apiarius L. (Coleoptera Cleridae). The spe-
cies T. apiarius is distributed all over Europe. Adults
are often present on flowers of Compositae, where they
feed on pollen and nectar. The body of adults is black-
coloured, with conspicuously dark-red forewings. Males
are 6.5-13 mm long, females up to 17 mm. Females lay
their eggs in plant flowers or in various cracks, for ex-
ample in cracks of lamellar boxes for solitary bees. The
eggs are orangish-red and have the form of an elongated
oval measuring on average about 2 mm in length. Lar-
vae hatched from the eggs enter the nests of solitary
bees and find eggs or larvae of the host, which they con-
sume. After eating the content of one cell, they go on to
the next cells, and consume their content as well. Larvae
of T. apiarius at the first stages of development can be
found in nests of Osmia at the end of June or beginning
of July (Stanisavljević, 1996). They remain there until
winter, when their development reaches the prepupal
stage. The pinkish-red mature larva is 16-20 mm long
and has a developed black head capsule (figure 14). The
last larval stage spins a cocoon in spring and metamor-
phoses into a pupa in the course of about two weeks.
Depending upon the external temperature conditions,
emergence of adults lasts up to one month. The devel-
opment cycle is completed in a year (Carré, 1980).
Figure 14. T. apiarius, larva.
(In colour at www.bulletinofinsectology.org)
148
We found T. apiarius in nests of O. cornuta and O.
rufa in lamellar boxes and sporadically in reeds. It is
most often the case that one larva destroys all the cells
in a nest.
Insectivorous birds (Parus major L.; Pica pica L.; Den-
drocopus spp; Motacilla alba L.) are frequent predators
of orchard bees. During the period of activity of the
bees, some birds feed on them, especially when there
are not enough other active insects due to low tempera-
tures. O. cornuta flies at relatively low temperatures,
when it is an easy prey for birds. However, insectivo-
rous birds can cause much greater damage to bee popu-
lations when they destroy their nests and extract co-
coons before and during the period of hibernation. For
this reason, nests must often be protected with chicken
wire when the foraging activity of the bees ceases. The
large concentration of bees at locations where they col-
lect damp soil for their nests can also attract certain in-
sectivorous birds, so that it is sometimes necessary to
protect those places, too, with chicken wire.
For protection against birds during the foraging activ-
ity of orchard bees, shiny plastic strips or mirrors that
move in the wind should be used to repel birds if it is
unfeasible to install chicken wire.
Nest destroyers
Ptinus fur L. (Coleoptera Ptinidae). This species is
widely distributed in the Holarctic (Bei-Bienko et al.,
1949).
Adults are reddish-brown to black in colour, with
yellow hairs. Each forewing has two white fields (figure
15a). The body of adults is 3-5 mm in length and about
3 mm wide. The antennae are long, often exceeding
body length (Stanisavljević, 1996). Although they pos-
sess wings, specimens of this species do not fly. They
are often present in the nests of many solitary bees. Fe-
males lay their eggs between the mass of pollen and the
walls of the cell. Larvae are white and bent. The pre-
pupa develops into pupa and later into overwintering
adult. Some pupation chambers of P. fur are inside mud
partitions (figure 15b), but several can be present to-
gether with the bee cocoon. Adults emerge from the co-
coons at the beginning of the next spring. They have
one generation a year. P. fur is often found in our bee
populations, especially in used nesting material, where
it feeds on waste of plant and animal origin. Under the
conditions of south-eastern Europe, it does not cause
significant damage to the bees.
Trogoderma glabrum Herbst (Coleoptera Dermestidae).
This native member of the European fauna was intro-
duced to North America and can therefore be found
throughout the entire Holarctic (Eves et al., 1980).
Adults are oval-shaped and dark-black in colour. Vir-
tually the entire surface of the forewings is overgrown
with tiny black hairs. Three transverse bands of white
hairs are especially conspicuous on the forewings. In
older adults, the hairs drop off due to constant move-
ment through the substrate, so that the surface of the
Figure 15a. P. fur, adult dorsal and ventral view.
(In colour at www.bulletinofinsectology.org)
Figure 15b. P. fur, cocoon in Osmia nest.
(In colour at www.bulletinofinsectology.org)
forewings acquires a metallic black luster. Females
measure 6-7 mm, while males are somewhat smaller.
The females lay their eggs in nests of solitary bees and
some other insects. The young larva is reddish-brown in
colour and covered with long hairs. The mature larva
attains a length of up to 6 mm. The life cycle of T. glab-
rum varies considerably as a function of temperature
and availability of food reserves. The larvae are most
often phytophagous, but it is not rare that this species
also feeds on various kind of animal food, mainly parts
of the bodies of dead insects. The species T. glabrum
overwinters in all larval stages.
The presence of a large number of larvae of this spe-
cies in different stages of development was observed in
old nests of O. cornuta and O. rufa bees (figure 16).
Under our conditions, it does not cause significant dam-
age to the bees.
Figure 16. T. glabrum larvae in Osmia nest.
(In colour at www.bulletinofinsectology.org)
149
Plodia interpunctella Hübner (Lepidoptera Pyralidae).
Larvae of P. interpunctella were registered in greater
numbers in nests of O. cornuta and O. rufa in lamellar
boxes than in reed bundles (Stanisavljević, 1996). They
exerted no significant harmful influence in our bee
populations.
Eumenid wasps: Ancistrocerus parietum L.; Ancistroce-
rus sp.; Symmorphus sp. (Hymenoptera Eumenidae).
During the summer, these wasps enter empty reed bun-
dles prepared for orchard bees and build cells in them in
series (which they partition with damp soil, as bees do).
They lay one single egg per cell and then provision it
with larvae of Lepidoptera (Geometridae and Tortrici-
dae) and Coleoptera (Curculionidae and Chrysomeli-
dae). When the larva reaches the maturity, it spins a
transparent cocoon. If the wasps overmultiply in the
summer or face a shortage of empty reeds, they are ca-
pable of digging out sealed nests of O. cornuta and O.
rufa. They withdraw the content of the bee nests and
then build their own. Adults are active during the sum-
mer months, too. Many species of eumenids have only
one generation throughout the year.
Cleptobionts
When females of O. cornuta and O. rufa bring the first
loads of pollen and nectar to nests in multiplication
shelters, they attract different cleptobionts, primarily
ants, immediately upon installation of the nesting mate-
rial. Attracted by the odour, they enter lamellar boxes
and inhabited reeds. Several days after the onset of bee
activity, a certain amount of pollen spilled by the bees
(and not rarely even whole loads) can be found under
the multiplication shelter and sometimes on reed bun-
dles and in the reeds next to the openings. The ants mas-
sively collect pollen from the piles under shelters and
from reeds, and carry it away to their own nests. Despite
the frequent presence of ants around reeds and lamellar
boxes during the period of bee activity, we did not ob-
serve them aggressively entering Osmia nests, and car-
rying away pollen and nectar. When the bees stop for-
aging, the abundance of ants in and around the shelter
also declines. Although ants were sporadically seen in
multiplication shelters all summer long, they were not
observed to harm closed nests. If the soil under the
shelter was sandy (which was the case at several of our
localities), craters very soon appeared containing larvae
of ant lions (Euroleon nostras Fourcroy), which hunted
ants for food. It was not observed that the ant lions also
hunted old female bees, which often crawled below the
shelter and across their craters. In addition to collecting
pollen, the ants also carried away dead male bees, which
are often found under the shelter. In certain seasons
when ants appeared in unusually great numbers, appro-
priate protective measures were taken (strips of sticky
paper were set out or an insecticide was sprinkled
around the supporting columns of the shelter). The
sticky strips protected the bee nests not only from ants,
but also from lizards (which are often seen among reeds
in shelters) and from possible nocturnal visits by mice.
The ants we observed (Formica cunicularia Latreille, F.
rufibarbis F., F. balcanina Petrov & Collingwood, Tet-
ramorium caespitum L., and Camponotus fallax Nylan-
der) are cleptobionts, and their harmful influence on
bees was negligible. Some species of ants in the vicinity
of Belgrade can attack weak honeybee societies in an
organized way, and "rob" and destroy them. For this
reason, we employed preventive protective measures
against ants on Osmia multiplication shelters.
Accidental nest residents
Osmia coerulescens L. This species is distributed in
Southeast Europe and is a significant pollinator of Le-
guminosae. In the area of Belgrade, it has two genera-
tions a year. In the Pannonian Depression, it often in-
habits lamellar boxes of M. rotundata in alfalfa fields.
We found it very sporadically in narrow reeds and
lamellar boxes set out for O. cornuta and O. rufa. It
overwinters as a diapausing adult in transparent co-
coons.
Liposcelis divinatorius Müller (Psocoptera Liposceli-
dae). Adults of the species L. divinatorius (the book
louse) were found for the most part in old reeds with a
lot of pulverized material in them. They did not cause
any significant damage to the bees.
Lepisma saccharina L. (Thysanura Lepismatidae). This
species was found sporadically in nests of O. cornuta
and O. rufa.
Forficula auricularia L. (Dermaptera Forficulidae).
Specimens of this species enter reeds and lamellar boxes
in order to feed on organic waste in bee nests. They are
often found in previously inhabited reeds, and fre-
quently take refuge in empty reeds for the purpose of
overwintering. They represent no significant threat in
nests of populations of O. cornuta and O. rufa.
Vespid wasps: Vespula germanica L., Polistes gallicus
L. and P. bischoffi Weyrauch (Hymenoptera Vespidae).
In the fall, queens of these wasp species often enter
empty reeds in bundles with orchard bee nests, where
they spend the winter. They were not observed to dig up
nests in order to overwinter in such places.
Xylocopa violacea L. (Hymenoptera Apidae). Speci-
mens of X. violacea were frequently registered in the
vicinity of multiplication shelters of O. cornuta and O.
rufa, especially at the beginning of spring. From time to
time, they entered large-diameter reeds, in which they
sporadically established nests. Overwintering adults
were sometimes found in large-diameter reeds in the
fall.
The genus Megachile: Megachile pilicrus Morawitz,
Megachile spp. (Hymenoptera Megachilidae). In Serbia
and in Italy the bees of this genus usually appear at the
end of spring, and are present all summer until the be-
ginning of fall. They build nests of leaves, deposit pol-
150
len in them, and then lay an egg on that mass. The lar-
vae spin a cocoon when they reach the prepupal stage
and overwinter at that stage. These bees sporadically
established their nests in our bundles for O. cornuta and
O. rufa (figure 17).
The genus Chalicodoma (Chalicodoma hungarica Moc-
sary, Chalicodoma sp.) (Hymenoptera Megachilidae).
Species of this genus build nests of fine sand or soil
mixed with salivary gland secretions. From 7 to 10 cells
in a row are found in one single nest. After drying, the
cells are very firm and hard. The females bring nectar and
pollen into the cell and lay an egg on this mass. Species
of the genus Chalicodoma overwinter as prepupae, and
adults appear at the beginning of the summer. They often
build nests in empty reeds in bee shelters (figure 18).
Figure 17. Nest of the genus Megachile in Phragmithes
cane.
(In colour at www.bulletinofinsectology.org)
Figure 18. Nest of the genus Chalicodoma in Phrag-
mithes cane.
(In colour at www.bulletinofinsectology.org)
Figure 19. Nest of the genus Anthidium in Phragmithes
cane.
(In colour at www.bulletinofinsectology.org)
The genus Anthidium: Anthidium florentinum F., A.
melanurum Klug (Hymenoptera Megachilidae). Species
of this genus build nests in empty reeds for O. cornuta
and O. rufa by first lining the cavity with moist wooly
material collected from surrounding plants. They usu-
ally overwinter as prepupae or diapausing adults. Their
nests were often found in reeds at all the localities
where O. cornuta and O. rufa were reared (figure 19).
Conclusion
O. cornuta and O. rufa have a characteristic accompa-
nying fauna in every region where they are reared for
the pollination of orchards. With increasing abundance
of the bees, the accompanying fauna increases in both
diversity and abundance. Effective measures of pro-
tecting populations from the most harmful species of the
accompanying fauna are being developed. If protective
measures are taken, the accompanying fauna will not
represent a limiting factor to the utilisation of these bees
for orchard pollination.
Acknowledgements
The research was partly supported by the Ministry of
Science and Environmental Protection of the Republic
of Serbia and Montenegro.
References
BATRA S. W. T., 1998.- Management of Hornfaced bees for
orchard pollination.- University of Idaho.
BEI-BIENKO G. I., BOGDANOV-KATJIKOV N. N., FALJIKENŠTEIN
B. YU., ČIGAREV A. G., ŠCEGOLEV V. N., 1949.- Agricul-
tural entomology: pest of agricultural crops and their pro-
tection measures II.- Nauka, Moscow - Leningrad. [in Rus-
sian].
BOSCH J., 1992.- Parasitism in wild and managed populations
of the almond pollinator Osmia cornuta (Latr.) (Hymenop-
tera, Megachilidae).- Journal of Apicultural Research, 31
(2): 77-82.
BOSCH J., 1994.- Improvement of field management of Osmia
cornuta (Latreille) (Hymenoptera, Megachilidae) to polli-
nate almond.- Apidologie, 25: 71-83.
BOSCH J., KEMP W., 2001.- How to manage the blue orchard
bee as orchard pollinator.- Sustainable Agriculture Network
National Agricultural Library, Beltsville, MD, USA.
BOUČEK Z., 1957.- Chrysididea: Chrysididae, pp. 319-326. In:
(KRATOCHVIL J. R., Ed.) Klič zvířeny ČSR II., Třásnokřídlí,
blanokřídlí, řasnokřídlí, brouci.- Československá akademie
věd, Praha.
BOUČEK Z., 1977.- A faunistic review of the Yugoslavian
Chalcidoidea (Parasitic Hymenoptera).- Acta entomolgica
Jugoslavica, 13 Suppl.: 3-145.
BROWNE F. B., 1959.- On the life history of Melittobia acasta,
Walker; a chalcid parasite of bees and wasps.- Parasitology,
14: 349-370.
CARRE S., 1980.- Biologie de deux prédateurs de l'abeille
solitaire Megachile rotundata F. (=pacifica Panz.)
(Hymenoptera, Megachilidae): Trichodes alvearius F. et
Trichodes apiarius L. (Coleoptera, Cleridae).- Apidologie,
11 (3): 255-295.
151
ČERNY V., SAMŠIŇÁK, K., 1971.- Acaridiae, pp. 495-509. In:
Klíč zvířeny ČSSR IV., želvušky, jazyčnatky, klepítkatci:
sekáči, pavouci, štíři, roztoči (DANIEL M., ČERNÝ V., Eds).-
Československá akademie věd, Praha.
COUTIN R., DESMIER DE CHENON R., 1983.- Biologie et
comportement de Cacoxenus indagator Loew. (Diptera,
Drosophilidae) cleptoparasite d’Osmia cornuta Latr.
(Hymenoptera, Megachilidae).- Apidologie, 14 (3): 233-240.
DAHMS E. C., 1984.- A review of the biology of species in the
genus Melittobia (Hymenoptera: Eulophidae) with interpre-
tations and additions using observations on Melittobia aus-
tralica.- Memoirs of the Queensland Museum, 21: 337-360.
DU MERLE M. P., 1972.- Quelques donnèes sur la biologie des
Dipteres Bombyliidae.- Bulletin de la Société entomologique
de France, 77: 190-201.
EVES J. D., 1970.- Biology of Monodontomerus obscurus West-
wood, a parasite of the Alfalfa Leafcutting bee Megachile ro-
tundata (Fabricius) (Hymenoptera: Torymidae; Megachili-
dae).- Melanderia, 4: 1-18.
EVES D. J., MAYER F. D., JOHANSEN A. C., 1980.- Parasites,
predators, and nest destroyers of the alfalfa leafcutting bee,
Megachile rotundata.- A Western Regional Extension Pub-
lication, Washington State.
FABRE J. H., 1937.- Ricordi entomologici. Studi sull’istinto e i
costumi degli insetti, Serie Terza. 3 (translated by C.
SINISCALCHI).- Sonzogno Editore, Milano.
FAIN A., 1966.- Notes sur la biologie des Acariens du genre
Chaetodactylus et en particulier de C. osmiae, parasite des
abeilles solitaires Osmia rufa et O. cornuta en Belgique
(Sarcoptiformes: Chaetodactylidae).- Bulletin et Annales de
la Société Royale d’Entomologique de Belgique, 102: 249-
261.
FELICIOLI A., 1995.- Studi bio-etologici e applicati su Osmia
cornuta Latreille (Hymenoptera: Megachilidae), potenziale
impollinatore di piante di interesse agrario. 73p., Doctoral The-
sis, University of Pisa, Faculty of Agriculture, Italy.
FELICIOLI A., 2000.- Le osmie, pp. 159-188. In: Api e impollina-
zione (PINZAUTI M., Ed.).- Giunta Regionale Toscana, Firenze.
FELICIOLI A., PINZAUTI M., 1998.- The impact of the solitary
bee parasite Anthrax anthrax Schrank (Diptera, Bombylii-
dae) on a wild population of the mason bee Osmia cornuta
Latr. (Hymenoptera, Megachilidae), p. 54. In: Fourth Inter-
national Congress of Dipterology, Abstracts Volume, Keble
College, Oxford, UK.
GRANDI G., 1951.- Introduzione allo studio dell’entomologia.-
Edizioni Agricole, Bologna, Italy.
HOBBS G. A., KRUNIC M. D., 1971.- Comparative behavior of
three chalcidoid (Hymenoptera) parasites of the alfalfa leaf-
cutter bee, Megachile rotundata, in the laboratory.- Cana-
dian Entomologist, 103 (5): 674-685.
HOLM S. N., 1973.- Osmia rufa L. (Hymenoptera) as a polli-
nator of plants in greenhouses.- Entomologica Scandinavica,
4 (3): 217-223.
JULLIARD C., 1947.- Contribution à l'etude d'un parasite
(Cacoxenus indigator Loew., Drosophilidae) d'Osmia rufa.-
Mitteilungen der Schweizrischen Entomologischen
Gesellschaft, 20: 587-594.
JULLIARD C., 1948.- Le comportement des larves de Cacoxe-
nus indagator Loew. Dans le nids d’Osmia rufa L.-
Mitteilungen der Schweizrischen Entomologischen Gesell-
schaft, 21: 547-554.
KEKIĆ V., 2002.- The Drosophilae (Drosophilidae, Diptera) of
Yugoslavia.- Monographs of the Institute of Zoology, Bel-
grade, 6: 109-120.
KIMSEY L. S., BOHART R., 1990.- The Chrysidid wasps of the
World.- Oxford University Press.
KRISTJÁNSSON K., 1989.-Investigations on the possibilities of
using the solitary bee Osmia rufa L. as a pollinator in Den-
mark. 146 p., Doctoral thesis, Department of Crop Science,
University Copenhagen, Denmark.
KROMBEIN K. V., 1962.- Natural history of Plumers Islands,
Maryland. XVI. Biological notes on Chaetodactylus krom-
beini Baker, a parasitic mite on the Megachilid bee, Osmia
(Osmia) lignaria Say (Acarina: Chaetodactylidae).- Pro-
ceedings of the Biological Society of Washington, 75: 237-
250.
KRUNIĆ M., PINZAUTI,A., FELICIOLI A., STANISAVLJEVIĆ Lj.,
1995.- Further observations on Osmia cornuta Latr. and O.
rufa L. as alternative fruit pollinators, domestication and
utilization.- Archives Biological Sciences Belgrade, 47 (1-
2): 59-66.
KRUNIĆ M., STANISAVLJEVIĆ LJ., BRAJKOVIĆ M., TOMANOVIĆ
Ž., 1999.- Further investigations on the accompanying fauna
of orchard bees Osmia cornuta Latr. and O. rufa (L.).- Con-
tributions to the Zoogeography and Ecology of the Eastern
Mediterranean Region, 1: 287-291.
KRUNIĆ M., STANISAVLJEVIĆ LJ., BRAJKOVIĆ M., TOMANOVIĆ
Ž., RADOVIĆ I., 2001.- Ecological studies of Osmia cornuta
(Latr.) (Hymenoptera, Megachilidae) populations in Yugo-
slavia with special attention to their diapause.- Acta Hor-
ticulturae, 561: 297-301.
LADURNER E., SANTI F., MACCAGNANI B., MAINI S., 2002.-
Pollination of caged hybrid seed red rape, Brassica oleracea
(Brassicaceae), with Osmia cornuta (Latreille) and Apis
mellifera L. (Hymenoptera Megachilidae and Apidae).-
Bulletin of Insectology, 55 (1-2): 9-11.
MACCAGNANI B., LADURNER E., SANTI F., BURGIO G., 2003.-
Osmia cornuta (Latreille) (Hymenoptera, Megachilidae) as a
pollinator of pear (Pyrus communis L.): fruit- and seed-set.-
Apidologie, 34: 207-216.
MACFARLANE R. P., DONOVAN B. J., 1989.- Melittobia spp. as
parasitoids of bumble and lucerne leafcutting bees and their
control in New Zealand, pp. 274-277. In: Proceedings of the
42nd weed and pest control conference, Taranaki Country
Lodge, New Plymouth 8-10 August 1989.
MADL M., 1989.- Zur Kenntnis der paläarktischen Leucospis-
Arten unter besonderer Berücksichtigung der Fauna
Österreichs.- Entomofauna, 10 (12): 197-201.
MAETA Y., 1978.- Comparative studies on the biology of bees
of the genus Osmia of Japan, with special reference to their
management for pollinations of crops (Hymenoptera: Mega-
chilidae).- Bulletin of Tohoku Nature Agricultural Experi-
mental Station, 57: 1-221.
MAETA Y., KITAMURA T., 1964.- Studies on the apple pollina-
tion of Osmia. I. Idea and present conditions in utilizing
Osmia as pollinators of apples in Japan.- Kontyû, 32: 45-52.
MAETA Y., KITAMURA T., 1965.- Studies on the apple pollina-
tion of Osmia. II. Characteristics and underlying problems in
utilizing Osmia.- Kontyû, 33: 17-34.
MARSTON N., 1964.- The biology of Anthrax limatulus Fur
(Osten Sacken), with a key to and descriptions of pupae of
some species in the Anthrax albofasciatus and trimaculatus
Groups (Diptera: Bombyliidae).- Journal of The Kansas
Entomological Society, 37 (2): 89-105.
MEDVEDEV G. S., 1978.- Keys to the insects of the European
part of the USSR. III. Hymenoptera (part 1 and 2).- A. N.
SSSR, Nauka, Leningrad.
NIKOLSKAJA M. N., 1952.- Chalcidy fauny SSSR.- Izdatelstvo
Akademii Nauk SSSR, Moscow-Leningrad.
PINZAUTI M., 1992.- Some observations the bio-ethology,
flight and foraging activity of Osmia cornuta Latr. (Hy-
menoptera, Megachilidae) during strawberry pollination.-
Apicoltura, 8: 7-15.
PRATESI D., 2004.- Relazione ospite parassita tra l’ape solita-
ria Osmia cornuta Latr. (Hymenoptera, Megachilidae) e il
dittero ecto-parassitoide Anthrax anthrax Schrank (Diptera,
Bombyliidae): note etologiche, ecologiche ed applicative. 76
p., Thesis, University of Pisa.
152
RAW A, 1972.- The biology of the solitary bee Osmia rufa (L.)
(Megachilidae).- Transactions of the Royal Entomological
Society of London, 124 (3): 213-229.
SEIDELMANN K., 1990.- Zur Parazitenkontrolle in
Stammzuchten der Roten Mauerbiene Osmia rufa L.-
Wissenschaftliche Zeitschrift der Martin Luther Universität,
Halle-Wittenberg, 39 (5): 25-34.
SEKITA N., 2001.- Managing Osmia cornifrons to pollinate
apples in Aomori Prefecture, Japan.- Acta Horticulturae,
561: 303-307.
SEKITA N., YAMADA M., 1993.- Use of Osmia cornifrons (Ra-
doszkowski) for pollination of apples in Aomori Prefecture,
Japan.- JARQ, Japan Agricultural Research Quarterly, 26
(4): 264-270.
STANISAVLJEVIĆ Lj., 1996.- The impact of accompanying
fauna on the populations of newly domesticated solitary
bees Osmia cornuta (Latr.) and O. rufa (L.) (Megachilidae,
Hymenoptera). 112 p., Master Thesis, Faculty of Biology,
University of Belgrade.
STANISAVLJEVIĆ Lj., 2000.- Ecological studies of Osmia cor-
nuta (Latr.) and O. rufa (L.) (Megachilidae, Hymenoptera)
with especial attention to their status and significance as
plant pollinators. 304 p., Doctoral Thesis, Faculty of Biol-
ogy, University of Belgrade.
TORCHIO P. F., 1976.- Use of Osmia lignaria Say (Hymenop-
tera: Apoidea, Megachilidae) as a pollinator in an apple and
prune orchard.- Journal of the Kansas Entomological Soci-
ety, 49 (4): 475-482.
VAN LITH J. P., 1957.- On the behavior of Cheatodactylus
mites (Acar., Tyr.) in the nests of Osmia rufa L. and Che-
lostoma florisomne (L.) (Apidae, Megachilidae).- Ento-
mologische Berichten, 17: 197-198.
YAMADA M., 1990.- Control of Chaetodactylus mite, Chaeto-
dactylus nipponicus Kurosa, an important mortality agent of
hornfaced bee, Osmia cornifrons Radoszkowski.- Bulletin of
the Aomori Apple Experiment Station, 26: 39-77.
ZACHVATKIN A. A., 1941.- Tyroglifoidiie kleshchi (Tyro-
glyphoidea).- Fauna SSSR, Paukoobraznue, Vol. 6 (1),
Izdatel’stvo Akademii Nauk Publ, Moscow-Leningrad.
Authors’ addresses: Miloje KRUNIĆ, Ljubiša
STANISAVLJEVIĆ, Institute of Zoology, Faculty of Biology,
University of Belgrade, Studentski trg 16, 11000 Belgrade, Ser-
bia and Montenegro; Mauro PINZAUTI, Dipartimento di Colti-
vazione e Difesa delle Specie Legnose, Sez. Entomologia
Agraria, Università di Pisa, via S. Michele degli Scalzi 2, 56100
Pisa, Italy; Antonio FELICIOLI (corresponding author, e-mail:
a.felicioli@vet.unipi.it), Dipartimento di Anatomia, Biochimi-
ca e Fisiologia veterinaria, Università di Pisa, viale delle Piag-
ge 2, 56100 Pisa, Italy.
Received August 22, 2005. Accepted November 30, 2005.
