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SYSTEMATICS, MORPHOLOGY AND PHYSIOLOGY
The Metasternal and Brindley’s Glands of Triatoma brasiliensis Neiva
(Hemiptera: Reduviidae)
ANA CRISTINA R VITTA, JOSÉ E SERRÃO, ERALDO R LIMA, EVALDO F VILELA
Depto. de Biologia Geral, Univ. Federal de Viçosa (UFV), Viçosa, MG; jeserrao@ufv.br,
mothman@insecta.ufv.br, evilela@ufv.br
Edited by Takumasa Kondo – CORPOICA, Colombia
Neotropical Entomology 38(2):231-236 (2009)
Glândulas de Brindley e Metasternal de Triatoma brasiliensis Neiva (Hemiptera: Reduviidae)
RESUMO - Triatoma brasiliensis Neiva é o principal inseto vetor da doença de Chagas no Nordeste do
Brasil. Os adultos da espécie apresentam dois pares de glândulas exócrinas, as glândulas metasternais e as
glândulas de Brindley que liberam compostos voláteis, possivelmente com função de defesa, alarme e/ou
acasalamento. O conhecimento anatômico e histológico das glândulas de Brindley e metasternal no gênero
Triatoma é escasso e, considerando a relevância dessas glândulas na sua biologia, o objetivo do presente
trabalho foi estudar e conhecer a sua morfologia. As glândulas de Brindley e metasternal de T. brasiliensis
possuem uma unidade glandular similar àquela descrita para Rhodnius prolixus Stål e Panstrongylus
megistus Burmeister, formada principalmente por um aparato secretor, sáculo e ducto coletor.
PALAVRAS-CHAVE: Doença de Chagas, triatomíneo e morfologia
ABSTRACT - Triatoma brasiliensis Neiva is the most important vector of the Chagas’ disease in
the semiarid zones of North-eastern Brazil. Adult bugs have two main pairs of exocrine glands, the
metasternal and the Brindley’s glands, which release volatiles possibly with defense, alarm and/or mating
functions. To date, anatomical and histological studies of the metasternal and the Brindley’s glands
in the genus Triatoma are scarce and, considering the relevance of these exocrine glands, the present
work aimed at studying their morphology in T. brasiliensis. The metasternal and the Brindley’s glands
of T. brasiliensis consist of glandular units similar to those described for Rhodnius prolixus Stål and
Panstrongylus megistus Burmeister, comprising a secretory apparatus, saccule and collector duct.
KEY WORDS: Chagas’ disease, triatomine, morphology
Triatoma brasiliensis Neiva is the most important vector
of the Chagas’ disease in the semiarid zones of Northeastern Brazil. Adult bugs have two main pairs of exocrine
glands, the metasternal and the Brindley’s glands, which
release volatiles possibly with defense, alarm and/or mating
functions (Manrique et al 2006, Scholfield 1979, Rossiter
& Staddon 1983).
The Brindley’s glands are simple sac-like structures
located dorsally, extending into the lateral part of the second
abdominal segment of Reduvioidae (Kälin & Barrett 1975,
Staddon 1983, Weirauch 2006). Disturbed adult triatomine
bugs release a secretion from these glands, whose main
component is isobutyric acid with putative alarm and defense
functions (Games et al 1974, Ward 1981, Manrique et al
2006). The Brindley’s glands in Rodnius prolixus Stål are
formed by saccules, secretory cells and ducts (Kalin & Barrett
1975) that resemble the dermal gland type “B” consisting
of four cell types (Wigglesworth 1933). Subsequently,
Barrett et al (1979) reported the presence of another type of
glandular unity named type “A”. In Panstrongylus megistus
Burmeister though, the Brindley’s glands consist of two cell
types (Schofield & Upton 1978).
The metasternal glands are widespread among Heteroptera
(Weirauch 2006) and lie ventrally on the metathorax, consisting
of a small pear-shaped reservoir and an unbranched secretory
tubule opening laterally to the sternal apophyseal pit. The single
known compound in Triatominae, 3-methyl-2-hexanone, is
released by the metasternal glands of Dipetalogaster maximus
Uhler (Rossiter & Staddon 1983). Alcohols and ketones are the
main compounds from these glands in Triatoma infestans Klug,
which may play a role in the sexual and alarm communication
(Manrique et al. 2006).
The present work aimed at studing the morphology of
these glands in T. brasiliensis. The anatomical and histological
studies of the metasternal and the Brindley’s glands in the
genus Triatoma will put this species in a systematic context
considering that no species in this genus have been hitherto
studied in detail.
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Material and Methods
Insects. Triatoma brasiliensis adults were maintained at 27°
+ 1°C, 64 ± 10% RH, subjected to an illumination regime
of 12:12L/D and fed on rabbit blood. Experiments were
conducted with both 30-50 day-old males and females.
Scanning electron microscope (SEM). The metasternal (n =
8) and the Brindley’s glands (n = 8) of adult males and females
were dissected in saline solution and transferred to Zamboni´s
solution (Stefanini et al 1967) for 24h at 4°C. Subsequently,
samples were washed in sodium phosphate buffer 0.1 M, pH
7.4 for 5 min, dehydrated in a graded ethanol series, transferred
to hexamethyldizilasane (HMDS) for 10 min and air dried.
Glands were then coated with a 30-nm-thick gold layer and
analyzed with a scanning electron microscope JEOL VP1430.
Some metasternal glands were transferred to distilled water for
5 min and to 1% triton 100-X during 15 min to rupture cells
and expose their ducts following fixation and the standard
procedure for SEM describe above.
Histology. After dissection, the metasternal (n = 6) and the
Brindley’s glands (n = 6) were transferred to Zamboni’s fixative
solution (Stefanini et al 1967). Glands were dehydrated in a
graded ethanol series and embedded in historesin JB4. Sections
5 μm thick were stained with hematoxyline and eosin Phloxine
stain. Ultrathin sections were contrasted with 5% uranyl acetate
and 1% lead citrate (Bancroft & Stevens 1996).
“A” cells, which are characterized by a U-shaped narrowed
saccule, whereas the type “B” cells are abundant and have
a spherical widened saccule (Fig 10).
Metasternal glands. The metasternal glands are located in
the metathoracic region, laterally to each metacoxal cavity
(Fig 3). The metasternal gland of T. brasiliensis consists of
an elongated secretory tubule that opens into a reservoir in an
elongated sac-like shape (Fig 9). Each gland, together with
its reservoir, is closely attached to an apophysis by a retractor
muscle (Fig 3). The gland opens to the exterior by means of a
small opening near to the apophysis (Fig 6). In each secretory
cell, the secretion product is collected by the collecting canal,
which dilates in a sac-like form and protrudes in the secretory
cell invagination, so that the set of collecting canals opens
independently onto the collector duct that reaches the gland
reservoir (Figs 4, 5).
The secretory portion of the metasternal glands
consists of a monolayer of columnar gland cells with
spherical nuclei (Fig 10). The cytoplasm of the gland
cells has some acidophil granules. Each gland cell has a
secretory apparatus and a receiving duct opening into the
gland lumen, which is narrowed and covered by a thick
cuticle (Figs 10, 11). The metasternal gland reservoir is
covered by a thin cuticle and surrounded by a monolayer
of epithelial cells, which are flattened as well as their
nuclei (Figs 9, 10).
Discussion
Results
Brindley’s glands. The Brindley’s glands of T. brasiliensis
are located between the abdomen and the dorsolateral part
of the metathorax. The glands possess a secretory portion
in a dilated sac-like structure opening into a collector duct
(Figs 1, 7). Attached onto the receiving duct wall, there is a
well-developed tendon connecting the duct wall to a muscular
bundle, named here retractor muscle (Figs 2, 7).
The secretory portion of the wall of the Brindley’s
gland of T. brasiliensis comprises a layer of secretory cells,
over which there is a layer of flattened cells covered by
cuticle (Figs 7, 8). The flattened cells have elongated nuclei
with condensed chromatin. A thickened cuticle over the
epithelium coats the gland lumen. The epithelium may be
folded according to the amount of secretion accumulated in
the gland (Fig 8).
The secretory unit consists of gland cells formed by
a secretory apparatus, a saccule and a collecting canal
surrounded by cuticle. The gland cells are columnar and the
well-developed nucleus has predominantly uncondensed
chromatin with an evident nucleolus (Fig 8). The cytoplasm is
characterized by the presence of granules that were negative
for either acid or alkaline staining.
The secretory apparatus is represented by a wide
extracellular cavity in which a surface folding may be seen. A
cuticular canal, the collecting canal, opens onto the secretory
apparatus and into the lumen of the gland by means of a
canalicle (Fig 8).
We found both cell types “A” and “B”. There are few type
The Brindley’s and the mestasternal glands of T.
brasiliensis reveal glandular units that are similar to those
described for both R. prolixus (Kalin & Barrett 1975) and P.
megistus (Schofield & Upton 1978, Santos-Mallet & Souza
1990), which under light microscope are mainly comprised
by a secretory apparatus, a saccule and a collecting canal.
Such gland unit resembles the dermal gland type “B”
reported by Wigglesworth (1933) and Lai-Fook (1970) for
R. prolixus. Subsequently, Barrett et al. (1979) reported the
presence of another type of glandular unit named type “A”
structurally different from type “B”. Our observations have
confirmed that the Brindley’s glands of T. brasiliensis are
formed by a set of the two glandular unit types “A” and “B”,
randomly distributed in the gland. As reported by Barret
et al (1979) the type “B” cells seem to be more numerous
than type “A”.
The retractor muscle of the Brindley’s glands of T.
brasiliensis is comprised of a well-developed tendon
directly connected to the collector duct enabling contraction
for secretion release. In R. prolixus, the retractor muscle is
connected to the collector duct through three ramifications
from the tendon (Barrett et al 1979). Although some
glands, such as those secreting terpene in Anisomorpha
buprestoides Stoll, are surrounded by a set of intrinsic
muscles that enables contraction for secretion release
(Happ et al 1966), in both R. prolixus and T. brasiliensis
a single muscle is associated with the Brindley’s glands.
Furthermore, no muscle was found surrounding either the
glandular lumen or the epithelium.
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Neotropical Entomology 38(2)
G
t
cd
rm
cd
2
1
↑
↑
AP
R
G
4
3
cd
op
cc
c
S
↑
S
5
6
Figs 1-6 Scanning electron micrographs of the Brindley’s (1-2) and metasternal (3-6) glands of Triatoma brasiliensis. 1)
Secretory portion (G) and collector duct (cd). Bar = 100 μm. 2) The tendon (t) and associated retractor muscles (rm) of the collecting
duct. Bar = 20 μm. 3) Reservoir (R) and secretory portion (G) of the metasternal gland. AP – metasternal apophysis. Bar = 100
μm. 4) Detailed view of secretory portion of the metasternal gland showing the sclerotized units (arrows). Bar = 20 μm. 5) The
collector duct (cd ) with associated saccule (s) and collecting canal (cc) of the metasternal gland. Bar = 10 μm. 6) opening (op) of
the apophysis and of the metasternal gland (arrowhead). c – body cuticle. Bar = 100 μm.
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Vitta et al - The Metasternal and Brindley’s Glands of Triatoma brasiliensis Neiva (Hemiptera: Reduviidae)
rm
bc
G
t
L
7
Fig 7 Light micrography of the section of the Bindley’s gland of Triatoma brasiliensis showing the secretory portion (G) and the
gland lumen (L). Note the collector duct (cd) associated with retractor muscles (rm) through the tendon (t). bc – body cuticle.
Bar = 20 μm.
c
L
n
s
s
sa
↑
sa
8
Fig 8 The Brindley’s gland of Triatoma brasiliensis showing
the gland epithelium. Note the secretory apparatus (sa) and the
saccule (s) of gland cells type “B” and the U-shape saccule
(arrowhead) of the gland cell type “A”. L – gland lumen; n –
nucleus; c – cuticle. Bar = 20 μm.
Strongly stained and well-distributed granules were found
in the cytoplasm of secretory cells of mestasternal glands,
suggesting that these glands produce substances different
from those secreted by the Brindley’s glands, which show
non-stained granules. Alcohols and ketones were the main
compounds produced by the metasternal glands of Triatoma
infestans (Manrique et al 2006), whereas isobutyric acid
is the major component of the Brindley’s gland (Games
et al 1974). Therefore, the presence of acidophil granules
in the metasternal glands suggest that other components
might be present in this gland, yet alcohols and ketones
may be transported to the secretory apparatus together with
substances of alkaline nature.
In both metasternal and the Brindley’s glands, the
description of the glandular cells herein presented agree with
that reported by Noirot & Quennedey (1991), showing that
they are comprised of type III cells. Hence, we suggest the use
of cellular classification into cells type III, already proposed
by Noirot & Quennedey (1991), since glandular cells from
both glands release their secretions through a collecting
canal formed by one or more cells and that such units may
be either isolated or associated to other glandular units or
accessory structures (extracellular reservoir). That general
classification into type III glands does not invalidate the
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Neotropical Entomology 38(2)
c
L
c
9
cc
cd
n
n
10
Figs 9-10 The metasternal gland of Triatoma brasiliensis. 9) The reservoir showing the enlarged lumen (L) lined by a thin
epithelium with cuticle (c). Bar = 20 μm. 10) The secretory portion showing the gland cells with well-developed nucleus (n) and
collecting canal (cc) opening in the collector duct (cd). Bar = 20 μm.
c
cc
cd
cc
cd
subdivisions of other gland types such as types “A” and “B”,
which result from particular features in the structure of the
cells forming the secretory unity. In this sense, class III glands
seem to be ubiquitous among insects, since they have been
reported in Isoptera (Noirot & Quennedey 1974), Coleoptera
(Delachambre 1975), Dictyoptera (Mercer & Brunet 1959),
Phasmatodea (Happ et al 1966), Mecoptera (Crossley &
Waterhouse 1969) and Hymenoptera (Cruz-Landim 1967,
Marques-Silva et al 2006, Azevedo et al 2007).
The present work is the first structural description of
the Brindley’s and mestasternal glands of T. brasiliensis,
which may be used as a reference for further studies on
behavior and reproduction patterns of this vector of Chagas’
disease.
Acknowledgments
11
Fig 11 The metasternal gland of Triatoma brasiliensis
showing the collecting canal (cc) opening in the conducting
duct lined by a thin cuticle (c). Bar = 20 μm.
The authors are grateful to Núcleo de Microscopia
e Microanálises from Universidade Federal de Viçosa
for technical assistance and an anonymous reviewer for
providing many insightful comments and suggestions on
drafts of this paper. To the Brazilian research agencies CNPq
and FAPEMIG for financial support.
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