Dufour glands in the hymenopterans (Apidae, Formicidae, Vespidae): a review

Abstract

Associated to the sting apparatus of the aculeate hymenopterans is found the poison gland, originated from the glands associated to the ovipositor of the non-aculeate hymenopterans and the less derived Dufour gland, homologue of the coletterial gland of other insects, and found in all hymenopteran females. The Dufour gland functions is mostly uncertain in hymenopterans but in ants it is involved with communication and defense and in non social bees with the nest building and protection. In wasps possibly with kin-recognition. Differences in morphology and chemical composition of the gland secretion were observed among species, in the same species, between the castes in the social species and among individual of the same caste playing different tasks or belonging to different nest. Its original function of egg-protective substance producing, or favoring the oviposition, appear to have been replaced or complemented in hymenopterans by the production of semiochemicals with function in communication.

Full text

Rev. Brasil. Biol., 61(1): 95-106
DUFOUR GLANDS IN HYMENOPTERANS 95
DUFOUR GLANDS IN THE HYMENOPTERANS (APIDAE,
FORMICIDAE, VESPIDAE): A REVIEW
ABDALLA, F. C. and CRUZ-LANDIM, C. da
Instituto de Biociências de Rio Claro, Departamento de Biologia, Unesp, Avenida 24A, 1515, Bela Vista,
CEP 13506-900, Rio Claro, SP, Brazil
Correspondence to: Fábio Camargo Abdalla, Departamento de Biologia, Unesp, Avenida 24A, 1515, Bela
Vista, CEP 13506-900, Rio Claro, SP, Brazil, e-mail: fabdalla@rc.unesp.br
Received June 10, 1999 – Accepted March 9, 2000 – Distributed February 28, 2001
(With 1 figure)
ABSTRACT
Associated to the sting apparatus of the aculeate hymenopterans is found the poison gland, originated
from the glands associated to the ovipositor of the non-aculeate hymenopterans and the less derived
Dufour gland, homologue of the coletterial gland of other insects, and found in all hymenopteran
females. The Dufour gland functions is mostly uncertain in hymenopterans but in ants it is involved
with communication and defense and in non social bees with the nest building and protection. In wasps
possibly with kin-recognition. Differences in morphology and chemical composition of the gland se-
cretion were observed among species, in the same species, between the castes in the social species
and among individual of the same caste playing different tasks or belonging to different nest. Its original
function of egg-protective substance producing, or favoring the oviposition, appear to have been re-
placed or complemented in hymenopterans by the production of semiochemicals with function in com-
munication.
Key words: Dufour gland, hymenopterans, morphology, pheromones, ultrastructure.
RESUMO
Glândula de Dufour nos himenópteros (Apidae, Formicidae, Vespidae): uma revisão
Anexas ao aparelho do ferrão dos himenópteros aculeados encontram-se as glândulas de veneno e as
de Dufour. A glândula de veneno é originada das glândulas associadas ao ovopositor dos himenópteros
ancestrais não aculeados, já a glândula de Dufour é menos derivada, homóloga das glândulas colateriais
dos outros insetos, sendo encontrada em todas as fêmeas dos himenópteros. Nestes insetos sua função
é, em grande parte, desconhecida, mas, em formigas, parece estar envolvida com a comunicação e a
defesa e, nas abelhas não sociais, com a construção e a proteção do ninho. Nas vespas pode estar
relacionada ao reconhecimento parental. Foram observadas diferenças morfológicas e na composição
química da secreção da glândula de Dufour entre as espécies, bem como na mesma espécie, entre as
castas dos himenópteros sociais e entre indivíduos da mesma casta desempenhando diferentes funções
ou pertencentes a ninhos diferentes. Portanto, nos himenópteros, sua função original de produzir
substâncias para proteger os ovos ou favorecer a ovoposição parece ter sido substituída ou com-
plementada com a função de produzir semioquímicos com função na comunicação.
Palavras-chave: feromônios, glândula de Dufour, himenópteros, morfologia, ultra-estrutura.
INTRODUCTION
All insects present accessory glands asso-
ciated to the female reproductive apparatus, which
are denominated colleterial glands because their
primary function is the production of substances
to fasten the laid eggs to the substrate or to protect
them during development.

Rev. Brasil. Biol., 61(1): 95-106
96 ABDALLA, F. C. and CRUZ-LANDIM, C. da
However, the pertinent literature register a
variety of functions for these glands. In Periplaneta
the eggs are laid in an ootheca consisting of tanned
material produced by the reproductive accessory
glands.
The frothy secretions which form the eggpods
of grasshoppers and the gelatinous sheath of
Chironomus eggs are also produced by the re-
productive accessory glands. In Hydrophilus, the
reproductive accessory glands produce silk which
forms the cocoon in which the eggs are laid.
THE STING GLANDS OF
HYMENOPTERANS
Female accessory glands often arise as an
invagination of the genital chamber or the vagi-
na, but some insects that developed long ovipositors
and also special methods of posture, as the Sym-
phyta and non-aculeate hymenopterans, also de-
veloped glands associated to the ovipositor, whose
products, in some way, made possible the posture
inside plants, animals or special nests.
In aculeate hymenopterans the ovipositor
became the sting and the glands previously asso-
ciated to it, changed to produce toxins used to
immobilize preys given as food to the offspring
and later, to defense. In Pompilidae and in others
hymenopterans the poison serves to paralyze preys,
but is also used in defense, to lubricate the ovi-
positor, or as via to chemical signals discharged
through the sting.
Therefore, associated to the sting apparatus
of aculeate hymenopterans there are two glands:
1. a gland corresponding to the colleterial gland,
the Dufour gland, also known as alkaline gland,
and 2. a gland corresponding to those associated
to the ovipositor of the non-aculeate hymenopte-
rans, the poison or acid gland (Carlet, 1884; Mas-
chwitz & Kloft, 1971; Hermann, 1969; Hermann
& Blum, 1967a, b, 1981).
The poison gland, as the name indicates,
produces the poison, constituted mainly by pro-
teinacious constituents in aqueous solution. In ants,
as well as in bees and wasps, the gland ends in
a poison sac that opens in the base of the sting,
allowing the poison be injected immediately with
the stinging.
The Dufour gland (Dufour, 1841) ends onto
different locals among hymenopterans: in ants it
opens in the base of the sting apparatus and in bees
and wasps, in the vagina dorsal wa1l (Billen, 1987).
However, in any case, both glands are totally inde-
pendent in production and discharge of secretion
(Maschwitz & Kloft, 1971; Hermann & Blum,
1981; Billen, 1982; Silveira, 1990).
Along evolution the original function of the
coletterial glands (production of protective subs-
tance for the eggs) changed to pheromonal function
in the Dufour gland. In Apis the Dufour gland
secretion is used to mark the eggs laid by the queen
(Katzav-Gozansky et al., 1997, 2000). This function
of the gland can be considered derived from the
original function.
MORPHOLOGY OF THE
DUFOUR’S GLAND IN
HYMENOPTERANS
The Dufour gland take different shapes in
the hymenopterans, but is often described as a
single tube or epithelial sac, involved by an
incomplete muscular envelope, tracheoles and
nerves (Bordas, 1894; Lello, 1968; Hermann &
Blum, 1967a, b; Landolt & Akre, 1979; Downing
& Jeanne, 1983; Billen, 1986; Silveira, 1990;
Abdalla, 1999; Abdalla & Cruz-Landim, 1994;
Abdalla et al., 1999a, b). The glandular epithelium
is constituted by a single layer of cells, whose
luminal surface is covered by a thick and
undifferentiated cuticle (Crouch & Smith, 1958;
Barr-Nea et al., 1976; Billen, 1986; Billen &
Gotwald Jr., 1988; Billen et al., 1984; Barrows
et al., 1986; Abdalla, 1999) secreted by the epi-
thelial cells. Therefore the glandular cells, belong
to class I glandular cells of Noirot & Quennedey
(1991) classification.
The cytoplasm of the glandular cells (Fig. 1)
presents abundant mitochondria, smooth endoplas-
mic reticulum (SER) and some Golgi complexes
(Billen, 1982, 1985, 1986, 1990; Billen & Gotwald
Jr., 1988; Barrows et al., 1986; Abdalla, 1999;
Abdalla et al., 1999a, b), hence the subcellular struc-
ture is in accordance with the nature of the secretion,
because the SER is involved with the synthesis and
transportation of lipids (main compound in the Du-
four gland secretion) and in bees, as well as, in ants,
the glandular cells present few intracellular granules
or secretion vesicles (Billen, 1982, 1985, 1986,
1990; Billen et al., 1984; Billen & Gotwald Jr.,
1988; Barrow et al., 1986; Abdalla, 1999; Abdalla
et al., 1999a, b).

Rev. Brasil. Biol., 61(1): 95-106
DUFOUR GLANDS IN HYMENOPTERANS 97
Fig. 1 — Ultrastructure of Dufour gland in Apis melifera (A, B) and Bombus terrestris (C). A) apical region showing
the circular lining (ct), subcuticular space (SS), apical invagination (iv), mitochondria (m) and B) well developed smooth
endoplasmic reticulum (SER), scar bar, 1 µm; r = polyribosomes. C) cytoplasmic detail showing multilamellar inclusions
(MLB), scale bar 1 µm.

Rev. Brasil. Biol., 61(1): 95-106
98 ABDALLA, F. C. and CRUZ-LANDIM, C. da
There are few ultrastructural studies about
the Dufour gland in bees and wasps. According
Abdalla (1999) and Abdalla et al. (1999a, b) the
cells of the Dufour’s gland in Apis mellifera and
in Bombus terrestris are morphologically similar
to Noirot & Quennedey (1991) class I glandular
insect cell classification, in the sense that they are
made by a single epithelium covered by cuticle.
However, according Noirot & Quennedey (1991)
the class I cells sinthetyses the substances they
eliminate throughtout the cuticle. In B. terrestris
the morphological evidences show that at least part
of the products of the secretion is uptaken directly
from haemolymph, descharaterizing the epithelium
as typically secretor. The way the uptaken
substances reach the lumen is not tota1ly clarified,
but they may percolate through the intercellular
space, does not passing through the epithelia1 cells,
being storaged in the subcuticular space during
a while; or may cross the cells being modified by
them.
The chemical studies about the secretion of
Bombus Dufour gland support this view. The same
hydrocarbons on the body cuticle are found in the
Dufour gland secretion (Tengö et al., 1991; Oldham
et al., 1994). The composition of the gland
secretion is different in individuals of the same
species originating from different colonies. One
explanation for this is the difference of the quality
of stored food in the colonies (Hefetz et al., 1993).
Probably stuffs absorbed by the midgut from the
food digestion are uptaken from the hemolymph
by the Dufour gland of Bombus and their quality
differences reflected in the secretion composition.
Besides as the Dufour gland products present intra
and inter colonial variations according the
substances collected and eating by the colony com-
ponents, it is clear that the epithelial cells have
a minor function, if any, in the synthesis of these
products. If they were synthesized by the cells,
as the synthetic via would be the same in a given
species of similar individual phase, the products
would not present such variation. Nevertheless,
contrary to this view, in Nannotrigona testacei-
cornis queens, the only Meliponinae bee that have
the compositon of the gland studied until know,
there are none variation between specimens
collected, as far as Brazil and Mexico (Cruz-Lopez
et al., 2000).
In Apis the cells of the distal extremity of the
queen gland are associated with oenocytes that are
secretory cells and may contribute to the secretion
composition. The epithelial cells that serves of via
to oenocytes secretion elimination belong to Noirot
& Quennedey (1991) class II glandular cells. In this
case the Dufour gland could be considerate a mixed
gland, because in the same organ there are class
I proximal cells and class II (associated to
oenocytes) distal cells. In Bombus terrestris there
are not oenocytes associated with the gland
(Abdalla et al., 1999a).
In bees and mainly ants, it is common to ob-
serve multilamellar bodies in the cytoplasm of the
glandular cells. According to Hefetz & Orion
(1982), these elements in Formicidae are a type
of secretory vesicle containing hydrocarbons, being
designated by Quennedey (1998) as myeloid se-
cretion. The possibility that those structures reflect
only reabsorption processes or cellular degene-
ration is also suggested (Gama & Cruz-Landim,
1977).
Differences in the cellular organization of
the Dufour glands can be found among subfamilies
of ants. In Myrmecinae and Ponerinae the glan-
dular epithelium does not present much variation,
but in Dorylinae the luminal surface has a cre-
nelated appearance and numerous basal invagi-
nations, and in Ecitoninae the epithelium is very
uniform with a basal layer labyrinth of plasmic
membrane infoldings. Myrmecinae, Pseudomyr-
mecinae and Dolichoderinae each, show a different
type of apical microvilli, whereas Formicidae exhi-
bit a characteristic layer of mitochondria close to
the cell luminal surface and a very thick basement
membrane (Billen, 1986).
The size of the Dufour gland in hymenop-
terans vary in different castes and in individuals
of different ages or doing different tasks. The major
workers of slave-making ant species have the
Dufour gland hypertrophied, while in other species
are the minor workers that have the gland larger
than the guardians. In the first case, the Dufour
gland secretion is used in the usurpation process
(Regnier & Wilson, 1971) and in the later the
minor, forager workers, used as trail pheromone
(Law et al., 1965). In Formica sanguinea, a slave-
making species, the active forager workers have
the Dufour gland larger than the young and old

Rev. Brasil. Biol., 61(1): 95-106
DUFOUR GLANDS IN HYMENOPTERANS 99
workers, because the first is more involved in nest
attack activity (Ali et al., 1988b). Baioco & Cunha
(1990) observed in Monomorium pharaonis that
the epithelium of the gland in virgin queens is more
developed than in mated queens. In this species
the Dufour gland produces sexual pheromones
(Hölldobler & Wüst, 1973; Buschinger, 1975).
According Lello (1968), the Dufour gland is
larger in bees situated bellow in the philogenetic
tree. In Colletidae, Halictidae and Andrenidae the
gland is large (Lello, 1968), in Megachilidae there
is a decreasing of its diameter, in Mellitidae there is
a decreasing of its length and in Anthophoridae
there is a decreasing in both dimensions, being the
gland in Apidae small and even vestigial or absent
in Meliponinae (Lello, 1968). According Kerr &
Lello (1962), in Meliponinae the virgin queens has
the Dufour gland larger then the mated queens,
being this situation inverse to that observed in Apis
(Kerr & Lello, 1962; Abdalla, 1999).
In social bees the Dufour gland development
and functioning, appear to be under juvenile
hormone (JH) control (Abdalla et al., 2001a). This
hormone show higher haemolymph titles in queens
and forager workers (Robinson & Ratnieks, 1987),
condition related to vitologenesis and etarious
polyethism respectively. In Bombus and in Apis
the Dufour gland diameter and its secretory activity
in workers increase with the increasing of oocyte
maturation in the ovary (Abdalla, 1999; Abdalla
et al., 1999a, b), condition which is under HJ con-
trol. Thefore the apparent link between vitelo-
genesis and Dufour gland development may be
mediated by the JH.
In Polistes versicolor wasps the Dufour gland
of the dominant female is more developed than
in workers. The gland of the dominant female is
deepest yellow and broad while in workers it is
transparent and slender (Nascimento & Cruz-
Landim, 1997). In some Polistes species when the
gland is inactive, its reservoir is opaque, white,
and empty (Landolt & Akre, 1979). In Polistes
queens just emerging from winter diapause the
gland is inactive, but with the eclosion of the first
workers the gland of the queens become active,
increasing in width and becoming filled with a
yellow secretion, decreasing in activity again at
the late summer (Landolt & Akre, 1979). In P.
fuscatus the gland is deeper yellow in the dominant
females of co-foundress associates during the late
pre-emergence stage. At other times this gland
show poor indications of secretory activity, regar-
dless of the rank of the individual. Glands in non-
nesting wasps, maintained in pairs, secrete more
actively than in those wasps keep solitary (Downing
& Jeanne, 1983).
FUNCTIONS AND CHEMICAL
SECRETION OF THE DUFOUR
GLAND IN HYMENOPTERANS
The main constituents of Dufour gland se-
cretion are lipids with long chains of hydrocarbons
and volatile oxygenated substances.
Because the opening of the Dufour gland in
ants is in the sting, Billen (1987) suggests that in
these hymenopterans the gland has functions asso-
ciated to communication and defense, while in
social bees, in which the gland opens in the va-
gina, may be involved mainly with reproduction.
But, in some hymenopterans it may exercise multiple
and non-specific functions according the place of
secretion discharge, as suggested by Billen (1987).
Its products may be used for reproductive,
behavioral, or other ecological proposals (Lello,
1968; Hefetz, 1987; Katzav-Gozansky et al., 1997,
2000; Abdalla & Cruz-Landim, 2001b).
One of the functions frequently attributed to
the Dufour gland in Formicidae is the production
of trail pheromone (Wilson, 1962; Walsh et al. ,
1965; Hangartner, 1969; Ritter et al. , 1977; Hefetz
& Orion, 1982), but the gland also produces sexual
pheromone (Hölldobler & Wüst, 1973) and queen
control pheromones (Edwards & Chambers, 1984).
Its contents is also used by slave-making species
in the raiding process (Ali et al., 1988b ), or as
aggregation stimulus and recruitment pheromone
(Cammaerts-Tricot, 1973; Morgan et al., 1977,
Bestmann et al., 1995).
In ants the main hydrocarbons found in the
Dufour gland are alkanes, hydrocarbons with satu-
rated chains (without couples or triple linkages).
The alkanes more frequently found are those
constituted of a main chain with 11 carbons, de-
signated n-Undecane (n-C11), succeded by n-Tride-
cane and n-Pentane. With smaller frequency, appear
alkenes and alkines (hydrocarbons with unsaturated
chains).

Rev. Brasil. Biol., 61(1): 95-106
100 ABDALLA, F. C. and CRUZ-LANDIM, C. da
According Morgan et al. (1977), hydrocar-
bons of the secretion have mainly a physical role,
they represent solely a solvent for other volatile
substances with pheromonal property. The hydor-
carbons could also provide alterations in the subli-
mation point of the pheromonal substances present
in secretion, prolonging the time of their action.
Many authors think that the n-Undecane is a phe-
romone (Regnier & Wilson, 1968, 1969; Ayre &
Blum, 1971; Bergströn & Löfqvist, 1970, 1972a,
b; Dumpert, 1972; Löfqvist, 1976) or a wetting
agent to the formic acid produced by the poison
gland (Löfqvist, 1977).
Surprisingly, most of the alkanes in pure state
are solid at the room temperature. However, the
Dufour gland secretion of the hymenopterans is
constituted by a complex mixture of saturated and
unsaturated hydrocarbons. The introduction of
double linkages in the long hydrocarbon chains
reduces the its melting point. Another strategy to
maintain the secretion in liquid or viscous state
is the introduction of double linkages with Z geo-
metry in the middle of the main hydrocarbon chain.
This linkage is much more efficient than those and
is also frequently found in the Dufour gland se-
cretion (Billen et al., 1986; Bagneres et al., 1991;
Hefetz et al., 1996).
It was verified that the secretion of the Dufour
gland varies not only with the age but with the
functional tasks done by workers of social species.
Among workers, is common that the youngest
present secretion composed by simpler mixture
of substances, generally constituted by one or few
types of hydrocarbons, and that in older ones the
secretion been incremented with more complex
substances of pheromonal action (A1i et al., 1988b;
Patrício, 1995). In slave-making ants Formica
sanguinea, the quantity of farnesene (pheromone
involved in the slave-making process) in the
secretion of the Dufour gland changes during the
life cycle of the workers. In young workers the main
components of the secretion is the n- Undecane
that is gradually substituted by two isomeric forms
of farnesene (Z-E-farnesene) in older workers that
actuate in the slave-making process (Ali et al.,
1988b).
Many functions have been described for this
gland in bees. In non-social bees the gland produces
hydrophobic lining and cementing substances for
the nest (Lello, 1968; Hefetz et al., 1979, 1982;
Heletz, 1987; A1bans et al., 1980; Cane, 1981; Cane
& Brooks, 1983; Kronenberg & Hefetz, 1984), sexual
atractants (Smith et al., 1985), recognition or nest-
marking (Bergströn & Tengö, 1974; Shimron et al.,
1985; Hefetz, 1987, 1990; Hefetz et al., 1993) or even
trail pheromones (Vinson et al., 1978). Its secretion
can serve a1so as larva1 food (Norden et al., 1980)
and food source-marking pheromones (Franckie &
Vinson, 1977).
In social bees the role of the Dufour gland
is not well known. In Apis (Snodgrass, 1956; Cruz-
Landim, 1967; Abdalla, 1999), in Bombus (Cruz-
Landim, 1967; Abdalla et al., 1999a, b) and in
meliponines (Lello, 1962) the gland is larger in
queens than in workers, besides in Apis its secretion
has caste-specific constituents (Katzav-Gozansky
et al., 1997). Due to this specificity some authors
propose that the Dufour gland in Apis queens
produces egg-marking pheromones to prevent its
eggs of being eated by workers during the posture
inspection (Ratnieks, 1993, 1995; Katzav-Go-
zansky et al., 1997).
In the Meliponinae, in spite of the sting atro-
phy, the Dufours gland is present in queens and,
sometimes, also in workers (Lello, 1968), being,
however, its function unknown.
In stingless ants, the Dufour gland is a1so
present, an additional cue to function independent
of the venom or sting gland.
Therefore, the Dufour gland, is found in all
female Hymenopterans (Bordas, 1894; Lello, 1968;
Landolt & Akre, 1979; Cruz-Landim & Saenz,
1972; Caetano et al., 1973; Billen, 1986).
In social ants as well as in bees the contents
of the secretion present variations in its quantity
and quality within species and castes (Hefetz, 1987;
Ali et al., 1988a, b, c, 1989; Billen et al., 1983;
Katzav-Gozansky et al., 1997, 2000). These varia-
tions are important for create specific, colonial
or individual labels used to produce trail, nest-
marking, nestmate recognition and egg- marking
pheromones.
In some species of social wasps it has been
hypothesized that the secretion of the Dufours gland
may be applied to the body surface during the
grooming and, becoming responsible by the kin
recognition (Dani et al., 1996). In many social
insects, as the bumble bees, is possible to found
the same hydrocarbons on the exoskeleton and in
the secretion of the Dufour gland (Tengö et al.,

Rev. Brasil. Biol., 61(1): 95-106
DUFOUR GLANDS IN HYMENOPTERANS 101
1991). In Stenogastrinae wasps the gelatinous
substance found involving the eggs and larvae of
many species was interpreted as larva1 food se-
creted by the Dufour gland (Jacobson, 1988;
Turillazzi & Pardi, 1982).
According Turillazzi (1991) the secretion
around the eggs has many other functions. It is used
as a tool in oviposition, functions as a resting
substrate for the small larvae, acts as a storage
substrate for liquid or solid food for both larvae
and adults and can serve as defense barriers against
ants.
The production of egg-marking pheromones
by queens to protect her eggs against be devoured
by subordinates during times of intense repro-
ductive competition among nestmate, also has been
speculated for wasps (Akre et al., 1976; Greene
et al., 1978; Landolt & Akre, 1979; Downing &
Jeanne, 1983). The hole of a glue-like substance
production to attach the eggs onto combs, has also
been suggested (Wigglesworth, 1972).
ln parasitic wasps the Dufour gland of queens
produces pheromones to control the nest usurpation
process (Landolt & Akre, 1979). The gland of the
parasitic queen may produce a stimulus, that makes
her to appear as pheromonally superior to the host
workers and therefore, more acceptable, than the
host queen (Jeanne, 1977; Fletcher & Blum, 1983).
The secretion could also, mask or alter the odor
of the host colony and thus confuse the host system
impairing the recognition of nest from foreign
queen, or it might alter worker behavior in such
a way that makes the usurpation process easier
(Schmidt et al., 1984)
Along the evolution of Dufour and venom
glands, not only its morphology, as its function,
have been modified and, in some cases, they took
directions that withdraw them from the function
associated to the reproduction. According Billen
(1987) in ants the loss of the roles directly linked
to the reproduction by Dufour gland was accom-
panied by the acquisition of holes related to com-
munication and defense. This condition of the
Dufour gland in ants has been favored by the
absence of brood cells (and hence the superfluous
function of producing cementing substances). The
occurrence of free ambulatory brood, which is a
genera1 but, unique aspect of ant social biology,
supports this hypothesis, argue Billen (1987).
The same substances produced by the Du-
four’s gland can play different roles, as the ma-
crocyclic lactones. In non-social bees that produce
hydrophobic lining or cementing substances for
the nest, these substances are derived from the
macrocyclic lactones. When the species make sub-
terranean nests the lactones are used to line the
nest with a hydrophobic pellicule (Hefetz et al.,
1979; Albans et al., 1980; Cane, 1981; Duffield
et al., 1981), but when the nest is made above the
soil (trees or branchs) the lactones are used as
cimenting substances mixed with other materials
(Cane, 1981; Cane & Brooks, 1983). In Lasio-
glossum zephyrum, a primitively social species of
bee, the lactones are used as sexual attractant phe-
romone (Smith et al., 1985).
A quite interesting multiple use of the Dufour
gland secretion in bees occur with the triglycerides
components. Some bees produce these substances
in the Dufour gland and use it to line the nest or
as larval food, eaten after the ending of the storaged
supplies (Norden et al., 1980).
In Apis, the secretion of the queen Dufour
gland contain wax-type esters absent from the
worker secretion. These esters, according to Ka-
tzav-Gozansky et al. (1997) serve to label the queen
eggs to prevent their elimination, during the ins-
pection activity by the workers. Besides, the same
authors verified that the secretion of the egg-laying
workers from queen-less colonies contain the same
esters, used by them to mimetize the queen eggs,
preventing they of being eaten by other non laying
workers. This fact suggests that the biosynthetic
pathway of the esters are present in both caste, but,
in some way, is inhibited in workers by the queen
presence in the colony.
According Nascimento & Cruz-Landim
(1997) in the wasp P. versicolor the Dufour gland
is deepest yellow in queens, while in workers it
is transparent and thin. The co-founddress females,
although having well developed ovaries, have the
gland smaller than the other workers. In this species
of wasps the gland may have a role in reproduction.
In wasps the wax-type esters are involved
in the kin recognition (Dani et al., 1996). The
production of these type of esters by the Dufour
gland in bees is very frequent and also must have
kin-recognition roles (Tengö et al., 1991; Oldham
et al., 1994; Abdalla & Cruz-Landim, 2001b).

Rev. Brasil. Biol., 61(1): 95-106
102 ABDALLA, F. C. and CRUZ-LANDIM, C. da
CONCLUDING REMARKS
The similarity of the Dufour gland com-
ponents among the Hymenopterans seems to indi-
cate that the biosynthetic pathways have been
conserved in this gland during the evolutive pro-
cess, once the gland synthesize the same class of
chemicals even being morpho-functionally dif-
ferent. The same conservative process happens with
the ultrastructural architecture of the glandular cells,
corroborating this hypothesis.
During the evolution, the gland may have
passed through an adaptation or modulation of the
secreted chemical components, according the eco-
logy of the species. According Abdalla (1999) and
Abdalla et al. (1999a, b) part of the content of the
secretion of the gland in A. mellifera and Bombus
terrestris is uptaken directly from the haemolymph.
This fact could explain the high conservation of
the products found in glandular secretion, because
the pathway of the lipid metabolization is simi-
lar in insects, suffering few modifications along
evolution.
In Bombus the same hydrocarbons are found
in the surface of the body and in the secretion of
the Dufour gland. Morphological evidences suggest
that the hydrocarbons could be uptake directly from
haemolymph. In fact the composition of the gland
secretion show inter-colonial variation and in bees
and wasps the cuticular hydrocarbons on the surface
body are used in the kin-recognition (the bee of
each colony have particular composition of body
surface hydrocarbons). The constancy of secretion
composition verified in N. testaceicornis by Cruz-
Lopez et al. (2000) may indicate different hole
in this bee species.
The chemical nature of the secretion, com-
posed basically of lipids with saturated and unsa-
turated long chain hydrocarbons is consistent with
the cellular organization of the gland, which has
an extensive smooth endoplasmic reticulum, Golgi
complexes and numerous mitochondria. The se-
cretion, even so, does not seem to be totally pro-
duced by the epithelial cell and was not seen to
accumulate in intracellular granules or vesicles but,
instead, is released to the glandular lumen conti-
nually. According Abda1la (1999) in social bees
the secretion activity of the queen gland can be
higher in the reproductive phases and in workers
can be stimulated by the juvenile hormone or queen
absence (Abdalla et al., 2001b).
From the exposed, may be concluded that the
Dufour gland is an example of the functional
plasticity of the insects exocrine glands, as well
as, of the possibility to use the same chemical
mixtures to signalize different activities.
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