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Morphology and structural organization of Gene's
organ in Argas walkerae
H . S C H OÈ L , B . E D E L M A N N , E . G OÈ B E L and R . G O T H E
Institute for Comparative Tropical Medicine and Parasitology, University of Munich, Germany
Abstract. Electron microscopy revealed that Gene's organ in females of Argas
walkerae Kaiser & Hoogstraal (Ixodida: Argasidae) is formed as a double-sac
structure consisting of an outer epithelial and an inner cuticular sac. The latter
emerges through the camerostomal aperture to the exterior in ovipositing ticks.
The epithelial sac forms the corpus and the two blind-ending horns, which pass
into the epithelium of the excretory duct of a gland at each side of Gene's
organ and envelop the cuticular sac. Both excretory ducts open into the lumen
between the epithelial and the cuticular sac. The cuticular sac is folded and
consists of a ®brous endocuticula outwards towards the lumen between the
epithelial and the cuticular sac and of a smooth epicuticula inwards. Parallel
running grooves occur over the lateral epicuticular surface turning medially into
cobble-stone pavement-like rises. Tubuli pass through the cuticular sac ending
in pores on the epicuticular surface and open into the lumen between the
epithelial and the cuticular sac. Muscle ®bres pass through the epithelial sac at
the horn tips and are inserted to the cuticular sac. In ovipositing females, the
glands are fully developed and the lumen between the epithelial and the
cuticular sac is ®lled with an amorphous mass.
Key words. Argas walkerae, Gene's organ, morphology, tick.
Introduction
The process of oviposition in Argas (Persicargas) walkerae
Kaiser & Hoogstraal is a sequence of exactly coordinated,
interlocking events independent of the age of the ticks, with an
essential functional participation of Gene's organ (Edelmann
& Gothe, 2000). Gene's organ is unique for argasid,
nuttalliellid and ixodid ticks, but in contrast to ixodids
(SchoÈl et al., 2000) its morphology in argasid species has
been almost exclusively investigated by light microscopy
(Christophers, 1906; Robinson & Davidson, 1914; Lees &
Beament, 1948; Roshdy, 1961, 1962, 1963, 1966; Balashov,
1972). Except for a species described as A. persicus (Robinson
& Davidson, 1914), its anatomical or histological structure has
been only brie¯y described using only schematic drawings.
There is only one contribution using transmission electron
microscopy which brie¯y describes the ®ne structure of Gene's
organ in unfed females of Ornithodoros (Pavlovskyella)
erraticus (Lucas) (El Shoura, 1988). However, transmission
electron microscopy (TEM) in conjunction with scanning
electron microscopical examinations (SEM) of Gene's organ,
with and without eversion of the cuticular sac alone, are
appropriate for the recognition and representation of its precise
morphology and structural organization and are particularly
conclusive for its involvement in the egg-laying process.
Accordingly, here Gene's organ was studied by TEM and
SEM, in unfed and ovipositing females of A. walkerae.
Argas walkerae is widespread in southern Africa, parasitiz-
ing domestic fowls. Wild hosts are unknown. Its documented
distribution includes the Republic of South Africa, Lesotho,
Namibia, Zimbabwe and Zambia (Kaiser & Hoogstraal, 1969;
Eastwood, 1971; Gothe & Schrecke, 1972; Colbo, 1973; Gothe
& Verhalen, 1975; Norval et al., 1985). The species occurs
commonly in peasant-type fowl runs and adjacent trees and is
the most important ectoparasite of fowl. It causes considerable
economic losses, especially where it transmits Aegyptianella
pullorum Carpano and Borrelia anserina (Sakharoff) (Gothe,
Correspondence: R. Gothe, Institute for Comparative Tropical
Medicine and Parasitology, Ludwig-Maximilians-University of
Munich, Leopoldstr. 5, 80802 Munich, Germany. Tel.: + 49
89/2180 3622; fax: + 49 89/2180 3623; e-mail: Sekretariat@
tropa.vetmed.uni-muenchen.de
422 ã 2001 Blackwell Science Ltd
Medical and Veterinary Entomology (2001) 15, 422±432Medical and Veterinary Entomology (2001) 15, 422±432
Renata
Highlight
1992a, b). In addition, larvae secrete a neurotoxin during
feeding, frequently resulting in fatal paralysis (Gothe, 1999).
Materials and Methods
The females of A. walkerae used in this study originated from a
laboratory-maintained stock, as reported previously (Edelmann
& Gothe, 2001). Virgin unfed ticks and engorged mated
females passing the ®rst genotrophic cycle were used 4 weeks
after ecdysis. Egg-laying was preceded by a mean pre-
oviposition period of 6.1 days and females were only included
in this study within 3 days after the start of oviposition. SEM
and TEM investigations were conducted according to the
methods described previously (SchoÈl et al., 2001). Brie¯y, the
ticks were killed with a scalpel blade by a transverse cut of the
body behind the second pair of legs and Gene's organ was
excised and immediately ®xed in 1% glutardialdehyde in
SoÈrensen buffer (pH 7.4). For SEM, the organs either remained
intact or were fractured with a scalpel blade. After several
rinsings in SoÈrensen buffer, the fractures and the intact organs
were dehydrated in a graded series of acetone, critical point
dried and mounted on aluminium stubs. Thereafter, the
samples were coated with gold/palladium and investigated in
a Zeiss digital scanning electron microscope (DSM 950,
Oberkochen, Germany). In addition, ticks with everted
cuticular sac of Gene's organ were killed in 10% formalin
and treated as described above. For TEM, excised intact organs
®xed in a formaldehyde-glutardialdehyde mixture were used.
After rinsing in 0.1 M cacodylate buffer (pH 7.4), the organs
were post-®xed in osmium tetroxide, washed again in
cacodylate buffer, transferred to ethanol and contrasted in 1%
uranyl acetate. Thereafter, the samples were dehydrated in
ethanol, rinsed in absolute propylene oxide, incubated in a
mixture of propylene oxide and epoxy resin, placed in
undiluted epoxy resin, embedded in a silicon mould ®lled
Fig. 1. Diagrammatic drawing of Gene's organ in unfed (a) and
ovipositing (b) tick; aperture of Gene's organ (A); corpus (C);
compound glands (CG); cuticular sac (CS); epithelial sac (ES); horn
(H); lumen between epithelial and cuticular sac (L); main efferent
duct of the glands (MD); retractor muscle (R); undeveloped glands
(UG).
Table 1. Average measurements in mm (SD) of excised Gene's
organ in unfed (n = 10) and ovipositing (n = 10) females of A.
walkerae
Unfed Ovipositing
Whole length of Gene's organ 822 (79.9) 827 (73.3)
Length of the corpus 218 (75.4) 246 (64.3)
Width of the corpus 664 (105.6) 668 (91.6)
Length of the horns 604 (69.9) 581 (58.6)
Width of the horns 203 (26.6) 251 (88.4)
Length of the glands 630 (152.3) 1269 (225.3)
Width of the glands 340 (72.2) 703 (203.8)
Fig. 2. Excised Gene's organ of unfed tick (SEM); corpus (C); horn
(H); retractor muscle (R); undeveloped glands (UG).
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Gene's organ in Argas walkerae 423Gene's organ in Argas walkerae 423
with epoxy resin and kept there at 60°C for polymerization.
Semi-thin and ultrathin sections were prepared by means of an
ultramicrotome. The semi-thin sections were put on micro-
scope slides, dried on a hotplate, covered with methylene-blue-
azur II solution and counterstained with safrine-O solution.
The ultrathin sections were mounted on copper grids and
contrasted with uranyl acetate and lead citrate solution and
investigated in a digital TEM (CM 10 TEM, Philips,
Eindhoven, The Netherlands).
Results
In unfed and ovipositing females, Gene's organ is located in
the anterodorsalregion of the body cavity immediately beneath
the dorsal integument. This organ is formed as a double-sac
structure consisting of an outer epithelial and an inner cuticular
sac; the latter emerges through the camerostomal aperture to
the exterior in egg-laying ticks. As shown (Fig. 1a), Gene's
organ in unfed ticks consists of an anterior corpus, two
posterior horns and a gland at each side, which differentiates in
ovipositing ticks (Fig. 1b) to a compound gland. The main
efferent duct of each gland opens into the lumen between the
epithelial and the cuticular sac at the height of the corpus and
the anterior part of the horns. The measurements of Gene's
organ in unfed and ovipositing females are given in Table 1.
Unfed ticks
Gene's organ in unfed ticks (Fig. 2) is smaller compared
with egg-laying females (Table 1). The epithelial sac (Fig. 3)
as the outermost part of Gene's organ is continuous with the
hypodermis of the integument, arises at the camerostomal
aperture, forms the corpus and the two blind-ending horns,
passes into the epithelium of the main excretory ducts of the
Fig. 3. Epithelial and cuticular sac of Gene's organ in unfed tick; (a) semithin section (10003); cuticular layer (CL); cuticular sac (CS);
epithelial sac (ES); (b) ultrathin section; basal lamina (BL) and cuticular layer (CL) of the epithelial sac; nucleus (N); (c) vertical fracture
(SEM); cuticular layer (CL) of the epithelial sac (ES).
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424 H. SchoÈl et al.424 H. SchoÈl et al.
glands and envelops the cuticular sac. The epithelium is single-
layered, consists of columnar cells averaging 5.8 mm in height
and rests towards the haemcoel on a basal lamina (Fig. 3b).
The epithelial cells are lined inwards by a 1.2-mm thick
cuticular layer (Fig. 3), which ends at the transition to the main
efferent duct. The cell cytoplasm contains mitochondria,
ribosomes and rough endoplasmic reticulum.
The gland cells average 5.4 mm in height and the lumenal
cell surface has a microvillar border (Fig. 4a). Towards the
haemocoel, the gland cells rest on a basal lamina (Fig. 4b).
Their cytoplasm contains vesicles, mitochondria, ribosomes
and rough endoplasmic reticulum (Fig. 4b).
The cuticular sac arises at the camerostomal aperture
passing into the cuticle of the basis capituli and the integument
and expands into the horn tips but not into the main efferent
ducts of the glands. It is folded (Figs 3a and 5) and consists of
a ®brous endocuticula outwards towards the lumen between
the epithelial and the cuticular sac (Figs 6a and 7a,c),
averaging 0.5 mm in thickness, and of a 0.3-mm thick smooth
epicuticula inwards. Parallel running grooves (Fig. 6) occur in
a mean distance of 1.9 mm over the lateral epicuticular surface
turning medially into cobble-stone pavement-like rises
(Fig. 7). Tubuli pass through the cuticular sac ending in
pores on the epicuticular surface (Figs 6a,b and 7a) and open
into the lumen between the epithelial and the cuticular sac.
Muscles originating from the dorsal integument pass through
the epithelial sac at the horn tips and are inserted to the
cuticular sac (Fig. 8).
Ovipositing ticks
Gene's organ of egg-laying females is similar in morph-
ology and structural organization to that of unfed ticks but the
cuticular sac is evertable (Fig. 9). Compared with unfed
females, however, the glands are longer and broader (Table 1),
more fully developed, and the lumen between the epithelial
and the cuticular sac is completely ®lled with an amorphous
mass (Fig. 10). Accordingly, differences in morphology and
structural organization concern the glands only. In contrast to
unfed ticks, the glands are sac-like (Figs 11 and 12) and
consist of secretory cells averaging 14 mm in height and
3.4 mm in width. Their cytoplasm (Fig. 13a±c) contains
numerous vesicles of varying size (2.7±3.7 mm), mitochondria,
ribosomes, rough endoplasmic reticulum and a Golgi network.
The lumenal cell surface has a well-developed microvillar
border (Fig. 13), which extends deeply into the intercellular
crypts (Fig. 13b) and is covered with numerous smooth ball-
like globules of different size (Fig. 13d). Towards the
haemocoel, the secretory cells rest on a basal lamina, and
their cell membranes show numerous invaginations and
evaginations forming a basal labyrinth (Fig. 13a).
Fig. 4. Gland of Gene's organ in unfed tick; (a) view (SEM) on the
microvillar border (MV) of gland cells; (b) ultrathin section; basal
lamina (BL); mitochondria (M); nucleus (N); vesicles (V).
Fig. 5. Folded cuticular sac through the main efferent duct of a
gland (unfed tick, SEM); cuticular sac (CS); epithelial sac (ES).
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Gene's organ in Argas walkerae 425Gene's organ in Argas walkerae 425
When maximally everted, the cuticular sac (Fig. 14) consists
of two cranio-ventrally orientated, kidney-like horns (Fig. 14a)
averaging 828 mm in length, 605 mm in height and 586 mm in
width. Its entire surface is covered with an amorphous mass.
Parallel grooves are arranged on the lateral surface of the horns
occupying on average a 176 mm broad area. Medially these
grooves pass into cobble-stone pavement-like rises (Fig. 14b),
which extend over a region of on average 429 mm in width.
The epithelial sac is partially everted into the evaginated
cuticular sac (Fig. 14c).
Discussion
Consideration of the results obtained for A. walkerae in this
investigation compared with studies on other argasid species
is rather unpro®table, as previously the morphology of
Gene's organ has been described only brie¯y for Argas
(Carios) vespertilionis (Latreille) (Roshdy, 1961), Argas
(Chiropterargas) boueti Roubaud & Colas-Belcour (Roshdy,
1962), Argas (Secretargas) transgariepinus (White) (Roshdy,
1963), Argas (Ogadenus) brumpti Neumann (Roshdy, 1966),
an Ornithodoros sp. (Christophers, 1906), Ornithodoros
(Ornithodoros) moubata (Murray) (Lees & Beament, 1948)
Ornithodoros (Aleveonasus) lahorensis Neumann and
Ornithodoros (Pavlovskyella) tholozani (Laboulbene &
Megnin) (Balashov, 1972). Schematic drawings have been
presented (Lees & Beament, 1948) but never any quantitative
measurements. Two further, more detailed investigations exist,
but again comparison with the present study is dif®cult because
only unfed females of a species described as Argas persicus
(Oken) (Robinson & Davidson, 1914) and of O.
(Pavlovskyella) erraticus (El Shoura, 1988) were used. In
these two studies Gene's organ was studied by light
microscopy and TEM, respectively.
A strong similarity in morphology and structural organ-
ization of Gene's organ exists between unfed females of A.
walkerae and A. persicus. In both species Gene's organ has
been shown to be formed as a double-sac structure consisting
of a `hypodermal sac', which encases a `chitinous sac', while
one gland on either side opens into the space between both sacs
(Robinson & Davidson, 1914). The hypodermal and the
Fig. 6. Unfed tick; (a) ultrathin section, endocuticula (EN) and epicuticula (EP) of the cuticular sac; tubuli (T); pores (P); (b) view (SEM) on the
epicuticula of the cuticular sac (CS); grooves (G); pores (P); (c) vertical fracture (SEM); cuticular sac (CS); grooves (G); tubuli (T).
ã 2001 Blackwell Science Ltd, Medical and Veterinary Entomology, 15, 422±432
426 H. SchoÈl et al.426 H. SchoÈl et al.
chitinous sac in A. persicus corresponds to the epithelial and
cuticular sac, respectively, in A. walkerae, but exact statements
of the structural organization of both sacs are lacking for A.
persicus, as are photographs.
In contrast to A. persicus and A. walkerae, a double-sacstructure of Gene's organ has not been reported in O. erraticus.
The short description based on TEM studies (El Shoura, 1988)
only indicates that Gene's organ in O. erraticus consists of an
anterior corpus, designated as stalk, and two posterior horns.
The stalk and the horns were described to be structurally
similar, consisting of a monolayer of columnar epithelial cells,
which are lined internally by a folded, cuticular layer and rest
on a basal lamina surrounded by muscles. However, the
statement that the epithelial cells are surrounded by a muscle
layer is not supported by the micrograph referred to.
Concurrently with A. walkerae and A. persicus, however,
muscle bundles also occur in O. erraticus originating from the
dorsal integument and passing to the two horns. These bundles
have de®nitely been demonstrated to insert to the posterior
extremity of the cuticular sac in A. walkerae, but of the
epithelial sac in A. persicus, an obvious misinterpretation
particularly if the function of these muscles is considered.
Glands associated with Gene's organ have not been described
in O. erraticus, But close examination of the micrographs
indicates that the cuticular and the epithelial layer are
separated. Furthermore, the description of cells bearing
microvilli indicates the presence of a gland. Accordingly, it
is justi®ed to assume that the structural organization of Gene's
organ in O. erraticus is also similar to that of A. walkerae and
A. persicus.
Comparing the morphology of Gene's organ in A. walkerae
with that in Dermacentor reticulatus (Fabricius), the only
ixodid species analogously investigated by SEM and TEM
(SchoÈl et al., 2001), striking differences become obvious. In
both species, Gene's organ is formed as a double-sac structure
consisting of an outer epithelial and an inner cuticular sac, but
Fig. 7. Unfed tick; (a) ultrathin section of the cuticular sac (CS) in the region of the cobble-stone pavement-like rises; endocuticula (EN);
epicuticula (EP); pores (P); (b) view (SEM) on the epicuticula (EP) of the cuticular sac; cobble-stone pavement-like rises (CSP); (c) view (SEM)
on the endocuticula (EN) of the cuticular sac in the region of cobble-stone pavement-like rises; epithelial sac (ES).
ã 2001 Blackwell Science Ltd, Medical and Veterinary Entomology, 15, 422±432
Gene's organ in Argas walkerae 427Gene's organ in Argas walkerae 427
in contrast, a pair of glands occur at each side of the organ in
D. reticulatus, which differentiates in ovipositing ticks to
compound, branched tubular glands. Furthermore, in D.
reticulatus, circular cribrate pits, ledges and cone-like struc-
tures occur on the epicuticular surface of the cuticular sac,
which are lacking in A. walkerae. The cone-like and circular
cribrate pits carrying structures, also visible in the retracted
cuticular sac, bulge balloon-like after its maximal eversion to
the exterior (SchoÈl et al., 2001).
Although the mechanism of eversion and retraction of the
cuticular sac during egg-laying is still unknown, the muscle
bundles inserting to the cuticular sac are obviously involved. In
many ixodid species (Arthur, 1953; Booth et al., 1984; El
Shoura, 1987; Booth, 1989; Kakuda et al., 1992; SchoÈl et al.,
2001) and possibly in A. walkerae, the eversion most likely is
caused by an increase in haemolymph pressure due to the
contraction of dorso-ventral muscles. The increased haemo-
lymph pressure is transmitted to Gene's organ, which even-
tually raises the pressure in the secretion-®lled lumen between
the epithelial and the cuticular sac such that the cuticular sac
turns inside out, owing to the simultaneous relaxation of the
retractor muscle originating from the dorsal integument and
inserting to the cuticular sac, and passes through the
camerostomal aperture to the exterior. During this process,
the secretion is squeezed through the tubuli and pores on the
surface of the everted cuticular sac. After laying an egg, the
everted cuticular sac is retracted into the epithelial sac through
the camerostome by the retractor muscle of Gene's organ.
The function of Gene's organ has not yet been investigated
for A. walkerae. Comparison with other tick species, however,
suggests strongly that for A. walkerae the impregnation of eggs
Fig. 8. Unfed tick; (a) view (SEM) on muscle ®bres (MF) of
retractor muscle (R) between cuticular (CS) and epithelial sac (ES)
in the horn tip; (b) semi-thin section (1000x) of muscles ®bres (MF)
of retractor muscle (R) between cuticular (CS) and epithelial sac
(ES).
Fig. 9. Diagrammatic drawing of Gene's organ with retracted (a)
and everted (b) cuticular sac in ovipositing tick; cuticular sac (CS);
dorsal integument (D); epithelial sac (ES); genital aperture (GA);
gland (GL); hypostome (HY); lumen between epithelial and cuticular
sac (L); retractor muscle (R).
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428 H. SchoÈl et al.428 H. SchoÈl et al.
by the secretion of Gene's organ is probably indispensible
(Edelmann & Gothe, 2000). After the blockage of Gene's
organ, eggs of O. moubata and Ixodes ricinus (Linnaeus) (Lees
& Beament, 1948), Haemaphysalis longicornis Neumann
(Kakuda et al., 1992) and D. reticulatus (Sieberz & Gothe,
2000) dried up quickly after deposition and were largely non-
viable. The chemical nature of the secretion of Gene's organ,
however, is still unknown.
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