Coll. and Res. (2005) 18: 1-6
1
The Ultrastructure of Compound Eye of Formosan Subterranean
Termite, Coptotermes formosanus (Isoptera: Rhinotermitidae)
Lin Chang 1*, Err-Lieh Hsu 2, Wen-Jer Wu 2
1
2
Conservation Department, National Palace Museum, Taipei, Taiwan 111, R.O.C.
Department of Entomology, National Taiwan University, Taipei, Taiwan 106, R.O.C.
(Received April 13, 2005; Accepted July 7, 2005)
Abstract. The compound eye of Coptotermes formosanus Shiraki alates is approximately round, and is
composed of 300~400 ommatidia. The compound eye of the female is larger than that of the male. Each
ommatidia with facet quadrate to hexagonal irregularly. The biconvex cornea has ~30 layers, and the outer
layer is smooth and slightly curved, whereas the inner layer is greatly curved. The crystalline cone is of the
eucone type with four cells. Retinas are of the apposition type and are positioned directly below the cones
at a distance of ~100~120 µm, and consist of eight retinular cells around the rhabdom. Many tracheae are
assembled as a tapetum near the basement membrane.
Key words: Coptotermes formosanus, Compound eye, Formosan subterranean termite, Morphology,
Isoptera.
INTRODUCTION
Sexually mature adults of termite species,
including the Formosan subterranean termite,
Coptotermes formosanus Shiraki, swarm in certain
seasons, and some are attracted to light. However,
after swarming, alates become negatively
phototaxic (Harvey, 1934), and their compound
eyes gradually degenerate during the concealed
adult life (Bremer et al., 1993). On the other hand,
the compound eyes and ocelli are absent or greatly
degenerate in soldier and worker castes or
pseudergates in most termite species (Richard,
1969; Weesner, 1969). Coptotermes formosanus is
one of the most economically important species in
Taiwan and poses a serious threat to historical
buildings and cultural properties. In a previous
study, we demonstrated that the termite alates
showed different attractiveness responses to
different light sources (Chang et al., 2001). We
were interested in the relationship between
behavior and the functional morphology of
phototaxis in C. formosanus. However,
information relevant to the morphology of the
compound eyes of C. formosanus is scarce.
*Corresponding author. E-mail: [email protected]
In this study, we examined the external
morphology and fine structures of the compound
eyes of C. formosanus. The results will be helpful
in exploring the relationship among the
ultrastructural tissues of the compound eye and
physiological mechanisms and behavioral display
to phototaxis.
MATERIALS AND METHODS
The alates of the Formosan subterranean
termite, C. formosanus, were captured while
swarming in a mountainous area near the National
Palace Museum at Wai-Hsuang Stream, Taipei,
northern Taiwan between May and June, 2001.
Scanning Electron Microscopy (SEM).
Specimens were prefixed in 2.5% glutaraldehyde
in 0.1 M phosphate buffer (pH 7.2) for 2 h at room
temperature. After washing with 0.1 M phosphate
buffer three times, specimens were postfixed in
1% OsO 4 in the same buffer for 2 h at room
temperature. The post-fixed specimens were again
triple-rinsed with 0.1 M phosphate buffer,
dehydrated in an ethanol series, and dried in a
critical point apparatus (HPC-2 Critical Point
Dryer, Hitachi, Japan). Some of the specimens
were fractured with a razor blade. All specimens
were coated with gold and observed with a Zeiss
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Coll. and Res. (2005) 18: 1-6
RESULTS
type, which was derived from four Semper cells
(Fig. 3), was directly beneath the cornea. The
diameter of the crystalline cone cell measured 13
± 1.5 µm, and the length was 12~15 µm. There
were no crystalline tracts beneath the crystalline
cone. The nucleus lay at the bottom of the
crystalline cone cell.
Light-insulating Apparatus. The lightinsulating system of C. formosanus consisted of
two kinds of pigment cells. The primary pigment
cells surrounded each crystalline cone, extending
from the cornea to the top of the retinula cells. The
irregularly shaped nucleus lay at the bottom of the
cell. The highly electron-dense and round- to oval-
The compound eye of the alate of C.
formosanus was approximately round and
composed of 300~400 ommatidia. The compound
eye of the female measured 429 ± 21 µ m in
diameter (n = 6) and was larger than that of the
male which measured 360 ± 35 µm in diameter (n
= 6). The shape of each facet varied from quadrate
to hexagonal. The facet lens surface was very
smooth, with no corneal nipples, ridges, or
interfacetal hairs (Fig. 1).
Dioptric Apparatus. The biconvex cornea of
the ommatidium was composed of approximately
30 layers, the total thickness is 17.8 ± 1.5 µm, and
the thickness of each layer decreased from the
outer one to the inner layers. In contrast, the
curvature increased from the outer to the inner
layers (Fig. 2). A crystalline cone of the eucone
Fig. 2. Transmission electron micrograph of longitudinal
DSM 950 scanning electron microscope at an
accelerating voltage of 10 kV.
Transmission Electron Microscopy (TEM).
Specimens were prefixed and postfixed with the
same procedures as for the SEM. After fixation,
specimens were washed twice with distilled water,
then block-stained in 1% uranyl acetate for 6 h at
60 . Specimens were dehydrated in an ethanol
series, then embedded in Spurr's low-viscosity
resin (Spurr, 1969). Ultrathin sections were cut at
~70~90 nm and observed with a Hitachi-7000
transmission electron microscope at 75 kV.
section of corneal lens of the compound eye of
Coptotermes formosanus. C, cornea; Cc, crystalline cone;
PPC, primary pigment cell.
Fig. 1. Scanning electron micrograph showing the surface
structure of the compound eye of Coptotermes
Fig. 3. Transmission electron micrograph of cross section
formosanus. The lower left figure shows that the surface
of four-cell crystalline cone of the compound eye of
of the inner side is more protruding than that of the outer
Coptotermes formosanus, surrounded by primary pigment
side.
cells (PPC).
Chang et al.: Compound eye of Coptotermes formosanus
3
shaped pigment granules measured 0.6~1.1 µm in
diameter. The secondary pigment cells were
located beneath the primary pigment cells and
between the two ommatidia, and extended from
the top of the retinula cells to the basement
lamina. The irregularly shaped nucleus distributed
almost anywhere inside the cell. The highly
electron-dense and round-shaped secondary
pigment granules were much smaller than the
primary ones (Fig. 4).
Fig. 5. Transmission electron micrograph of an ultrathin
cross-section of eight retinula cells of the compound eye
of Coptotermes formosanus.
Fig. 4. Transmission electron micrograph of a
longitudinal ultrathin section of the compound eye of
Coptotermes formosanus. The crystalline cone,
surrounded by primary pigment cells (PPC), is connected
with rhabdom (Rh). The rhabdom is surrounded by
secondary pigment cells (SPC).
Retinula Cells. The simple apposition-type
rhabdom extended from the bottom of the
crystalline cone to the basement lamina. The
fused-type rhabdom was formed by eight retinula
cells (Fig. 5). A rhabdom in the central part of the
eye measured 100~120 µm long and 7~12 µm in
diameter. In cross-section, the rhabdom column
was small, and the microvilli of the rhabdomere
were sparse from the top to the end (Fig. 6).
A cross-section of the top of the rhabdom
appeared round with a diameter of 10 µ m; the
middle of the rhabdom appeared star-shaped to
pentagonal with a diameter of 12~7.5 µm; and the
distal portion of the rhabdom appeared triangular
with a diameter of 3 µm (Fig. 7).
Tapetum. The basement membrane was
beneath the rhabdom. The tracheae were
condensed near the basement membrane, and
formed a layer with a width of ~15 µm in order to
reflect light (Fig. 8).
Fig. 6. Illustrative diagrams of the ommatidium of
Coptotermes formosanus showing a longitudinal section
(left) and transverse sections (right) at different levels.
DISCUSSION
Diurnal insects mostly rely on their eyes as
visual organs to distinguish direction and
objectives, thus their eyes are usually larger and
much more functional than those of nocturnal
species. Formosan subterranean termites spend
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Coll. and Res. (2005) 18: 1-6
Fig. 7. Transmission electron micrograph of a cross-section of the rhabdom of the Coptotermes formosanus alate. A to F
show the positions from the upper to deeper layers of the retina.
Fig. 8. Transmission electron micrograph of the
basement membrane of the compound eye of
Coptotermes formosanus, Many trachea (Tr) are evident.
their lives in darkness, and the reproductive alates
swarm at night. Therefore, we suspect that their
eyes tend to possess the characteristics typically of
nocturnal activity. One example could be the
smooth surface of the facet corneal of the C.
formosanus alate. This characteristic agrees with
that of nocturnal insects described by Caveney and
McIntyre (1981) who suggested that night-flying
beetles like as scarab beetles generally have large,
hemispherical eyes with smooth surface of the
facet corneal.
Exner (1988) indicated that there are two
fundamentally and anatomically established types
in the position of the retina, the superposition and
apposition images. The former one, as in most
nocturnal insects, possesses a broad clear zone
between the dioptric apparatus and retina. In
contrast, in the latter one, as in most diurnal
insects, the retina is positioned directly under the
dioptric apparatus. However, McIntyre and
Caveney (1998), who studied nine species of
onitine dung beetles, reported that superposition
optics were possessed by all species regardless of
their flying times. Similarly, Eguchi (1978)
indicated that all hesperiids possess superposition
optics despite their strictly diurnal activity pattern.
Eguchi (1982) attempted to interpret the
relationship of morphology and phylogenesis
according to the fine structure of different species
of lepidopterans with the same activity patterns.
The morphological and ultrastructural characteristics of the compound eyes of carabid beetles
and ants were shown to be coincident with their
lifestyle or behavior, even more than to their
degree of relatedness. For example, the compound
eyes of diurnal species are much larger than those
of nocturnal species, even though all of them have
about the same body size (Menzi, 1987; Bauer and
Kredler, 1993).
Chang et al.: Compound eye of Coptotermes formosanus
In previous studies on the sexually mature
adults of termites, both Neotermes jouteli and C.
formosanus were reported to have a fused-type
rhabdom. Each rhabdom of N. jouteli is formed by
six retina cells and is ~20 µm long, but that of C.
formosanus is formed by eight retina cells and is
100 µm long (Bremer and Wachmann, 1993). The
rhabdom of another primitive species, Mastotermes darwiniensis, is also formed by eight
retinal cells. The crystalline cones of all three of
these species are formed by four cone cells.
However, M. darwiniensis is of the acone type,
while the others are of the eucone type. Regardless
of whether they swarm in the day or at night, N.
jouteli, Kalotermes flavicollis and M. darwiniensis
all have the apposition type of ommatidium (von
Rosen, 1913; Horridge and Giddings, 1971;
Bremer et al., 1993), as well as is found in our
study of C. formosanus. Because termites always
live in complete concealment in the dark, we
suspect that there is no relationship between the
internal structure of their eyes and the timing of
swarming; in particular, entering the concealed life
after swarming causes a dismantling of the cone
and the rhabdom until they are completely
destroyed (Bremer et al., 1993). However,
according to our previous study, the pigment
granules accumulated around the crystalline cones
when C. formosanus was treated for 1 h of light
adaptation; whereas the pigment granules
dispersed around the rhabdom (unpublished data).
Therefore, we can confirm that the compound eyes
of termites possess a functional mechanism to
regulate light.
ACKNOWLEDGEMENTS
We are grateful to Dr. Wann-Neng Jane
(Institute of Plant and Microbial Biology,
Academia Sinica) for technical help with electron
microscopy, and also to Prof. Nan-Yao Su
(University of Florida) and Dr. Wen-Yung Lee
(retiree of Institute of Zoology, Academia Sinica)
for their review and critique of the manuscript.
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5
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(Coptotermes formosanus Shiraki)
1
2
2
1
2
300~400
30
8
100~120 µm