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01988 The Norwegian Academy of Science and Letters
Zoologica Scripta, Vol. 17, No. 3, pp. 293-295,1988
Printed in Great Britain
The crenellate lining of the Dufour gland in the genus
Aenictus: a new character for interpreting the phylogeny of
Old World army ants (Hymenoptera, Formicidae, Dorylinae)
JOHAN P. J. BILLEN and WILLIAM H. GOTWALD JR
Accepted 7 July 1987
Billen, J. P. J. & Gotwald, W. H. Jr. 1988. The crenellate lining of the Dufour gland in the genus
Aenictus: a new character for interpreting the phylogeny of Old World army ants (Hymenoptera,
Formicidae, Dorylinae) .-Zool. Scr. 17: 293-295.
The Dufour gland epithelium in Aenictus has a crenellate appearance, a condition previously found
only in the primarily African genus Dorylus. This character, taken alone, strongly suggests that
these two genera share a common ancestry, as is presently reflected in their placement in the
subfamily Dorylinae, and that an independent, convergent origin for them, as has been proposed
in the triphyletic hypothesis for army ant evolution, is incorrect.
Johan P. J . Billen, Limburgs Universitair Centrum, Department SBM, B-3610 Diepenbeek,
Belgium. Address for correspondence: Zoological Institute, University of Leuven, Naamsestraat 59,
B-3000 Leuven, Belgium.
William H. Gotwald Jr, Utica College of Syracuse University, Department of Biology, Utica, NY
13502. U.S.A.
Introduction
Army ants are characterized by their distinct behaviour of
nomadism and group predation (Wilson 1958) and by
their pantropical distribution. Two major groups can be
clearly distinguished on the basis of zoogeographical,
morphological and ethological characteristics: the
Ecitoninae in the New World and the Dorylinae in the
Old World tropics (Gotwald 1982; Snelling 1979). The
Dorylinae comprise two tribes, with the Dorylini (single
genus Dorylus Fabricius, 1793) mainly confined to Africa
and the Aenictini (single genus Aenictus Shuckard, 1840)
best represented in tropical Asia. There are considerable
differences, however, between the members of both
tribes, especially in their external morphology. Based on
these differences and on the geological interpretation of
their actual geographical distribution the hypothesis of a
triphyletic origin for the army ants has been advanced
(Gotwald 1979). In this regard, both doryline groups have
been believed to have arisen independently from each
other and independently from the Neotropical
Ecitoninae.
Our present paper is based on the recent discovery that
the Dufour gland morphology represents a valuable
character to distinguish between the Ecitoninae and the
African Dorylini (Billen 1985). This stimulated us to
investigate the Dufour gland in Aenictus and to compare
its morphology with that of Dorylus.
Malaysia (Borneo), in June 1985 by one of us (WHG). Their posterior
abdominal halves were fixed for 2-4 h in 2% glutaraldehyde in 50 mM
sodium cacodylate buffer, pH 7.3, containing 150 mM saccharose.
Tissues were kept in buffer solution until arrival in Belgium, where they
were post-fixed for 1 h in 2% osmium tetroxide in the same buffer. After
dehydration in an acetone series, tissues were embedded in Araldite.
Double stained thin sections were examined with a Philips EM 400
electron microscope.
Results
The morphology of the Dufour gland is similar in the
workers of all three Aenictus species investigated. The
gland is a small, pyriform sac that opens in the sting base
through a slit-like duct, ventral to the opening of the
poison gland duct. As in other ants, the duct of each of
these sting glands has its own, independent muscular
supply. In the Dufour gland muscle fibres insert onto both
the dorsal and ventral duct wall. The poison gland duct,
on the other hand, only shows muscular insertion onto its
ventral side, while the dorsal wall displays a much
thickened, rigid cuticular lining (Fig. 1). The ultrastructural organization in the muscular attachment region
shows the occurrence within the duct cells of bundles of
microtubules that form the structural link between the
adhering myofilaments and the overlying cuticle, which
has a thickness of approx. 1p m (Fig. 2).
The secretory part of the Dufour gland is comprised of
a glandular epithelium that also lines the central reservoir
space (Figs. 1, 3). The epithelial thickness is fairly constant, though it may vary from 4 to 10 p m between
Material and methods
individuals. Rounded or slightly ovoid nuclei occupy a
basal position in the cells and have a diameter of between
Worker individuals of Aenictus dentatus Forel, 1911 (Utica College COIL
no. SAC-002), A . laeviceps (Fr. Smith, 1858) (SAC-009) and Aenictus 3 and 5 pm. The cytoplasm is characterized by a moderate
sp. (SAC-013) were collected at Bako National Park, Sarawak, East network of smooth endoplasmic reticulum, relatively
293
Zoologica Scripta 17
294
J . P. J . Billen & W. H . Gotwald Jr
Figs. I-5.-1-3. Aenictus dentatus.-I. Longitudinal section showing the Dufour gland (Dg)and the poison gland duct ( P d ) .DdDufour gland duct;
MFmuscle fibres.-2. Detail of the ventral wall of the Dufour gland duct, with intracellular bundles of microtubules ( M T ) and adhering muscle
fibres ( M F ) . ct cuticle.-3. Dufour gland epithelium. Note crenellate apical border and intercellular junctions mostly coinciding with intercrenellar
tops (arrows). M F muscle fibres; M mitochondria; N n u c l e u s . 4 . Crenellate Dufour gland epithelium in Doryfus nigricans.-5. Dufour gland
epithelium of uniform thickness in Eciton burcheffi.Figures 4 and 5 from Billen (1986).
numerous mitochondria in the basal region and sometimes some small electron-dense inclusions. A few electron-lucid vacuoles with a diameter of nearly 1 pm are
randomly dispersed (Fig. 3).
The epithelium has a crenellate apical border. The
lateral cell membranes are very much folded in the upper
cell half, with the most apical part of this intercellular
Zoologica Scripta 17
junction nearly always coinciding with an intercrenellar
top (Figs. 1,3). As a result, the majority of the cells show
an apical depression that corresponds with the narrow
crenel between adjacent tops.
The apical cell membrane displays a simple topography
and closely adjoins the overlying cuticle, which has a
uniform thickness between 0.20 and 0.25 pm ( 4 5 times
Dufour gland morphology in Aenictus army ants
295
thinner than in the duct region). The basal plasmalemma
shows only a very few invaginations. The gland is surrounded by a thin basement membrane (around 50 nm
thick) and a few rather thin muscle fibres (Fig. 3).
The Dufour gland epithelium in Dorylini and
Ecitoninae is shown for comparison (Billen 1986). Species
of Dorylus (and the subgenus Anomma) have a crenellate
epithelium, with a very well defined sequence of crenel
tops and depressions (Fig. 4). In Eciton, and later confirmed in Labidus and Neivamyrmex, the entirely different epithelium has a very uniform thickness and is characterized by a basal accumulation of lateral cell membrane
foldings (Fig. 5).
between the glands in Aenictus and Dorylus suggests a
common origin for these two genera. This evidence supports the current placement of both genera in the subfamily Dorylinae (see Snelling 1979; Gotwald 1982), implying
a common ancestry for all of the Old World army ants, a
group that furthermore arose independently of the New
World army ants (subfamily Ecitoninae).
The crenellate condition of the epithelial lining in both
Old World genera does not support the triphyletic
hypothesis for the army ants proposed by Gotwald (1979)
and supported by recent research on gastral exocrine
glands by Jensen (1986). Although the ancestral relationships of the Old World army ants remain unclear, the
results of this study imply a monophyletic origin.
Discussion
Acknowledgements
AS in other ants, the Dufour gland in Aenictus is formed
by a reservoir sac, lined with a secretory epithelium, and
a slit-like duct. The latter contains an extensive muscular
apparatus that allows the Dufour gland to discharge its
secretion independently from the poison gland (Billen
1982, 1986). The cytoplasmic organization of the glandular cells corresponds with that of the Dufour gland in
other ant species and is in accordance with the production
Of low
weight lipophilic substances
k
Quennedey 1974; Billen 1986). No information is available on the chemical composition of the Dufour gland in
Aenictus nor on its function. It is probably involved in
secretion of hydrocarbons with an eventual pheromonal
function, as is common among the Formicidae (Blum &
Hermann 1978).
The most obvious character of the gland in Aenictus is
the crenellate aspect of its epithelial lining and the coincidence of intercellular junctions with the intercrenellar
tops. This particular condition is all the more remarkable,
because it is most similar to that of the Dufour gland in the
other Old World army ant genus Dorylus. No other ant
species investigated thus far shows a comparable epithelial type, as was revealed by ultrastructural examination of 60 species representing the 8 major subfamilies
among the Formicidae (Billen 1986).
Given the Dufour gland’s apparent systematic importance in the ants in general (Billen 1986), and the army
ants in particular (Billen 1985), the striking similarity
We are grateful to EIS Plaum for technical assistance in sample preparation for electron microscopy. JPJB thanks the Belgian National Fund
for Scientific Research for a senior research assistantship. The research
contributions of WHG were supported by National Science Foundation
(U.S.A.) grant BSR-8403385.
References
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