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Fine structure of the anteromedial eye of the liphistiid spider Heptathela kimurai.

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THE ANATOMICAL RECORD 240141-147 (1994)
Fine Structure of the Anteromedial Eye of the Liphistiid Spider,
Heptathela kimurai
AKIRA UEHARA, KIYOKO UEHARA, AND KOICHI OGAWA
Department of Biology, Faculty of Science, Kyushu University (A.U.), First Department of
Oral Anatomy, Fukuoka Dental College (K.U.), and Department of Anatomy, School of
Medicine, Fukuoka University (K.O.), Fukuoka, Japan
ABSTRACT
Background: The presence of efferent fibers in the anteromedial eye of liphistiid spiders kept in natural daily cycles of illuminance
has been reported. However, this report is limited to innervation by the
efferent fiber and daily rhabdomal changes, and there have been no detailed ultrastructural accounts of the eye.
Methods: The fine structure of this eye was examined by electron microsCOPY.
Results and conclusions: The eye consists of a cornea, a lens, a vitreous
body, and a retina. The retina contains 13or 14 receptor cells and glial cells.
The rhabdoms are distal to the nuclei of the receptor cells. In the distal
region of the receptive segment, the rhabdomeres lie in the center of the
cell. In the middle region, anisomorphic rhabdoms formed by microvilli
from adjacent cells are at the cell periphery. In the proximal region, the
rhabdomeres are situated in the center of the cell. The ocellar nerve of the
eye runs toward the protocerebrum and enters the posterior part of the
first optic ganglion of the secondary eyes. Pigmented cells and nonpigmented cells are observed. The pigmented cells are located in the most
lateral of the eye and cover the whole eye. The nonpigmented cells are
located in the receptor cell bodies and extend to the origin of the ocellar
nerve. They wind to form capillaries filled with electron-dense material.
These structures are discussed in comparison with those of other spiders
and other chelicerates. o 1994 WiIey-Liss, Inc.
Key words: Anteromedial eye, Retina, Rhabdom, Nonpigmented cells,
Capillary, Liphistiid spider, Heptathelu kimurai (Chelicerata)
The eyes of a few arthropods have been reported to be
innervated by efferent fibers; the ventral, median, and
lateral eyes of the horseshoe crab, Limulus polyphemus
(Fahrenbach, 1969, 1973), the median and lateral eye
of the scorpion, Androctonus australis (Fleissner and
Schliwa, 1977; Schliwa and Fleissner, 1980), and the
anteromedial eye of the liphistiid spider, Heptathela
k i m u r a i (Uehara et al., 1993). Fine structure and function of the eyes of Limulus (Fahrenbach, 1975; Barlow
et al., 1980; Battelle, 1991; Kass and Barlow, 1992) and
the scorpion (Fleissner and Fleissner, 1985,1988)have
been well examined. Consequently, it has been shown
that the efferent fibers contribute to the circadian sensitivity change and control of transductive membrane
turnover in these eyes. Furthermore, with regard to
the retinal anatomy and function, there are striking
similarities between the Limulus median and lateral
eyes and the scorpion median eyes (Fleissner and
Fleissner, 1985, 1988).
However, in the anteromedial eye of the liphistiid
spider, the reports in the literature (Uehara et al.,
1993) are limited to innervation by the efferent fiber
and the daily rhabdomal changes. There have been no
0 1994 WILEY-LISS, INC.
detailed ultrastructural accounts of this eye. Additionally, the liphistiid spider has vestigial segments in its
abdomen, poorly developed mandibles, two pairs of
book lungs and no tracheae, and seven or eight spinnerets. Because this spider belongs to the suborder Archaeothelae, considered to be a primitive type in the
order Araneae, their eyes are interesting subjects for
study when considered from a phylogenetic or evolutionary viewpoint. In this study, the fine structure of
the anteromedial eye of the liphistiid spider was examined by electron microscopy. The structure and possible
function of the anteromedial eye are discussed in comparison with the other eyes of Chelicerata.
Received October 4,1993;accepted February 24, 1994.
Address reprint requests to Dr. Akira Uehara, who is now at the
First Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, 814-01Japan.
Dr. Kiyoko Uehara is now at the Department of Anatomy, School of
Medicine, Fukuoka University, Jonan-ku, Fukuoka, 814-01Japan.
142
A. UEHARA ET AL.
MATERIALS AND METHODS
For Scanning Electron Microscopy
receptive segment, the receptor cells project rhabdomeral microvilli intracellularly and a rhabdom is
Adult female of liphistiid spiders, Heptathela kimu- formed in the center of the cell (Fig. 4a). In the middle
rai, were collected in the field in Southern Kyushu, region, the receptor cells extrude microvilli extracelluJapan. The spiders were kept in glass tubes stuffed larly in all directions. The microvilli from adjacent receptor cells form anisomorphic rhabdoms at the cell
with moist soil and fed small insects.
To observe the gross anatomy of the eyes, the ceph- periphery, and they abut on each other in the rhabdom
alothrace of the liphistiid spider was cut away and in various positions. Furthermore, the rhabdomeral
fixed for 2 h in 2% glutaraldehyde in 0.1 M cacodylate microvilli are directed variously and do not have a
buffer. The specimens were dehydrated in a graded se- fixed orientation. No projections of glial cells are
present in this region (Fig. 4b). In the proximal region,
ries of acetone rinses and air dried.
To examine how the ocellar nerve enters the proto- the rhabdom is situated again in the center of the recerebrum, the ocular tubercle a t the frontal region of ceptor cell. The intermediate segment between recepthe cephalothrace, with the protocerebrum still at- tive segment and receptor cell body is almost absent,
tached to the ocellar nerves of four pairs of eyes from and so the upper part of the nucleus can be seen tothe ocular tubercle, was cut away by a sharp blade and gether with the basal part of the receptive segment
a pair of microscissors. After removal of the connective (Fig. 412).
The receptor cells contain abundant cell organelles.
tissue surrounding the samples in the normal physiological saline (217 mM NaC1,5 mM KCl, 4 mM CaCl,, Especially, rough endoplasmic reticulum is well devel1.1 mM MgCl,, 3 mM NaHCO,) (Rathmayer, 1965), oped in the vicinity and inferior portion of the nucleus,
they were fixed for 2 h in 2% glutaraldehyde in 0.1 M and it is frequently filled with electron-dense material.
cacodylate buffer and postfixed for 2 h in 2%osmium At this level, they are interrupted by glial cells (Fig. 5).
tetroxide in the same buffer. After dehydration in a The receptor cell protrudes the axon from its proximal
graded series of ethanol rinses, they were immersed in end, and the 13 or 14 axons are assembled in the posisoamyl acetate, and then critical-point dried by using terior of the eye to form the ocellar nerve. The ocellar
nerve runs toward the protocerebrum away from the
liquid carbon dioxide.
These specimens were coated with platinum, and ex- other ocellar nerves of the anterolateral, posteromedial, and posterolateral eyes and enters the posterior
amined with a JSM 50-A electron microscope.
part of the first optic ganglion of these secondary eyes
(Figs. 6a, 6b).
For Transmission Electron Microscopy
The frontal parts of the cephalothraces of the liphistiid spider were cut out with a sharp blade, fixed for 2 h
in 2% glutaraldehyde in 0.1 M cacodylate buffer a t pH
7.3, and postfixed for 2 h in 2%osmium tetroxide in the
same buffer. After dehydration through ethanol rinses,
specimens were embedded in Epon. Ultrathin sections
were stained with uranyl acetate and lead tartrate and
examined with a Hitachi H-500 electron microscope.
Glial Cells
There are two kinds of glial cells in the anteromedial
eye: pigmented cells and nonpigmented cells. There are
hemocylic spaces among these glial cells. (Fig. 4c; see
also Fig. 8b).
The pigmented cells are situated in the most lateral
part of the eye and envelop the cone cells, the receptor
cells, and the nonpigmented cells from the apex of the
vitrous body to the initial region of the ocellar nerve.
RESULTS
However, they do not shield the whole eye. A part of
The anteromedial eyes are located in the top of an the receptor cell is not covered by them. Their processes
ocular tubercle at the frontal region of the cephalo- project into the receptor cells and the nonpigmented
thrace, together with the anterolateral, posteromedial, cells (Fig. 7).
and posterolateral eyes. The anteromedial eyes are the
The nonpigmented cells are situated under the resmallest of the four pairs of eyes (Fig. 1, arrow). On ceptor cell bodies and extend to the axon hillock of the
gross inspection, the live ones appear dark, whereas optic nerve, and their nuclei lie near the receptor cell
the anterolateral, posteromedial, and posterolateral bodies. Among the prolongations of the nonpigmented
eyes are pale.
cells, electron-dense material is observed in some of the
capillaries (Fig. 7). In the axon hillock of the optic
Dioptric Apparatus
nerve, two electron-dense capillaries are observed: one
The lens is biconvex, and the posterior surface is is longitudinally sectioned and the other is transmuch more convex than the anterior. It consists of sev- versely sectioned (Fig. 8a, b). Subsequent to the axon
eral parallel lamellae of whirled bundles formed by hillock of the optic nerve neither prolongation of the
numerous accumulated microfibrils (Fig. 2). Cone cells nonpigmented cell nor capillary can be found (Fig. 5a).
that comprise the vitreous body have electron-lucent
The nonpigmented cells contain abundant amount of
cytoplasm and contain electron-dense material. They filaments, endoplasmic reticulum, mitochondria, and
are interdigitated with each other and are attached numerous glycogen granules, but lack pigmented granwith septate junctions. Their intercellular spaces and ules. Their intercellular spaces are often filled with
the space between the cornea and cone cells are filled electron-dense material and expanses of the intercelluwith electron-dense material (Fig. 3).
lar spaces vary from site to site. Near the receptor cell
bodies, the extracellular spaces are narrow and the
Receptor Cells
plasma membranes are smooth (Fig. 9). Toward the
The rhabdoms are distal to the nuclei of the receptor ocellar nerve, projections of the nonpigmented cells
cells in the anteromedial eye. In the distal region of the wind to form a capillary. They extrude large numbers
ANTEROMEDIAL EYE OF THE LIPHISTIID SPIDER
Fig. 1. Scanning electron micrograph of an ocular tubercle (dorsal
view). AM, anteromedial eye. x 80. Bar: 0.1 mm.
Fig. 2. Transmission electron micrograph of a longitudinal section
through the cornea. The lens (L) is made up of concentric lamellae
filled with microfibrils. C, cornea; CC, cone cell. x 2,300. Bar: 5 pm.
143
Fig. 3. A longitudinal section of the cornea and cone cells. The cone
cells (CC) are interdigitated and attached with septate junctions (SJ).
They contain electron-dense granules and their intercellular spaces
and the space between the cornea (L) and the granules are filled with
electron-dense material. x 15,000. Bar: 1 pm.
1971; Homann, 1971; Uehara et al., 1977; Blest, 1985;
Land, 1985; Blest et al., 1990). Although considerable
intergeneric diversity is apparent from these studies,
much of it can be related phylogenetically and to various modes of life. However, the anteromedial eye of
liphistiid spider is so different from these eyes of the
DISCUSSION
other spiders in structure and the number of receptor
The structure of the anteromedial eyes of spiders has cells that it is not comparable with those of the other
been well examined for a number of species (Melamed spiders. In the liphistiid spider, the microvilli from adand Trujillo-Cen6z, 1966; Eakin and Brandenburger, jacent receptor cells form an anisomorphic rhabdo-
of microvilli into the capillary and they have coated
vesicles and microtubules (Fig. 10a). Near the capillary, the projections are attached by adherens junctions, and except for this region, they are attached by a
great number of septate junctions (Fig. lob).
144
A. UEHARA ET AL.
Figs. 4-6.
ANTEROMEDIAL EYE O F THE LIPHISTIID SPIDER
meral network in the middle region of the receptive
segment, and rhabdomeral microvilli have various orientations that are unlikely to play a role in polarized
light detection, and furthermore, the receptive segments are not always shielded by the pigmented glial
cells. Especially, this eye is comprised of only 13 or so
receptor cells, and this number is extremely small compared with that of the anteromedial eye of the other
spiders; e.g., wolf spiders, Lycosa erythrognatha and L.
thorelli, have 450 receptor cells (Melamed and Trujillo-Cen6z7 19661, jumping spiders, Phidippud johnsoni and Metaphidippus aenelous, have 800-900 receptor cells (Land, 1969; Eakin and Brandenburger, 19711,
and the orb weaver, Argiope amoena, has 400-500 receptor cells (Uehara et al., 1977).
From this structural evidence, it might be concluded
that this eye does not serve image formation, movement detection, and polarized light detection. However,
it is well known that wolf, jumping, and orb web spiders have ultraviolet and green receptors in their anteromedial eyes (DeVoe, 1972, 1975; Yamashita and
Tateda, 1978; Blest et al., 1981). Additionally, Limulus
has an ultraviolet receptor in the median eye (Wald
and Krainin, 1963), which is suggested to be the phylogenetical origin of the anteromedial eye of most spiders (Paulus, 1979). Furthermore, other chelicerates,
such as scorpions (Machan, 1968), oplionids (Carricaburu and Munoz-Cuevas, 19851,spider mites (McEnroe and Dronka, 1966), and ticks (Carroll and Pickens,
19871, also have the same receptors. Neocarus texanus,
a mite, bears the anterior and posterior ocelli consisting of 20 and 14 receptor cells, respectively, considered
to have rather low resolution from structural evidence
(Kaiser and Alberti, 1991). Since this number is very
similar to that of the anteromedial eye of the liphistiid
spider, it is conceivable that the anteromedial eye of
the liphistiid spider exhibits a spectral sensitivity to
ultraviolet and green light and plays a role in detecting
their prey like the ticks (Carroll and Pickens, 1987).
Because nonpigmented cells and some capillaries
formed by them have rarely been reported in eyes of
other spiders and other chelicerates, they are a conspicuous feature in the anteromedial eye of the liphistiid
spider. The nonpigmented cells are filamentous and
the number of spiral turns they make varies. Therefore, they seem to have features of glia. The capillaries
among the nonpigmented cells are filled with electron-
-
145
dense material and microvilli protrude into the capillaries; coated vesicles and microtubules are observed in
the cytoplasm near them. Therefore, it may be that the
capillaries are a storage site of the electron-dense material that are absorbed by the nonpigmented cells.
Furthermore, they are considered to be quite different
from eccentric and arhabdomeric cells of the eyes of
Limulus (Fahrenbach, 19751, scorpions (Schliwa and
Fleissner, 19801, harvestman (Schliwa, 19791, Acari
(Kaiser and Alberti, 19911, and whip scorpions (MeyerRochow, 1978)because the eccentric and arhabdomeric
cells bear distal dendrites that contact retinula cells
and, therefore, they are considered to play a role as
secondary neurons in the processing of visual information.
The nonpigmented cells contain endoplasmic reticulum, mitochondria, abundant free ribosomes, and a
small number of coated vesicles, so that it seems likely
that the nonpigmented cells produce and excrete secretion. However, the receptor cells overlying the nonpigmented cell contain Golgi apparatus, well-developed
endoplasmic reticulum, and expanded endoplasmic reticulum filled with electron-dense material similar to
the material in the intercellular spaces of the nonpigmented cells near them. Therefore, the receptor cells
seem to be a prominent candidate as the source of the
electron-dense material. Since the receptor cells are
innervated by efferent fibers (Uehara et al., 19931, it is
interesting to speculate that they play a role in the
regulation of neural secretion.
The apposed plasma membranes of the nonpigmented cells in the vicinity of the capillaries are attached with adherens junction and are considered to
play a role in cell attachment. The adherens junctions
might contribute to the formation of capillaries. Furthermore, a great number of septate desmosomes are
observed between nonpigmented cells and between
nonpigmented and pigment cells. Since the septa are
linear in tangential sections, this septate desmosome is
considered to be of Hydra type that is believed to be a
site of firm but flexible intercellular adhesion and have
been implicated as permeability barriers (Staehelin,
1974). The septate desmosomes in the liphistiid spider
might play a role in protecting the electron-dense material from diffusion into the hemocylic spaces and the
intercellular spaces even though the nonpigmented
cells undergo drastic changes in shape.
~
Fig. 4. Cross sections of the receptive segment of the receptor cell.
(a) Distal region. Rhabdom is located in the center of the cell.
x 11,000, Bar: 1 pm. (b) Middle region. Anisomorphic rhabdoms are
formed by microvilli from adjacent cells a t the cell periphery.
x 12,000. Bar: 1 pm. ( c ) Proximal region. Rhabdom is situated in the
center of the cell. The nucleus can be seen together with the rhabdom.
The receptor cells are surrounded by pigmented and nonpigmented
cells. x 4,700. Bar: 1pm. C, cornea; HC, hemocylic space; N, nucleus
of the receptor cell; NP, nonpigmented cell; PC, pigmented cell; RH,
rhabdom.
Fig. 5. A cross section through the lower part of the receptor cell
bodies. The receptor cell contains abundant mitochondria and a welldeveloped web of rough endoplasmic reticulum. Some part of the endoplasmic reticulum is filled with electron-dense material. NP, non-
pigmented cell; PC, pigmented cell; RC, receptor cell body. x 5,300.
Bar: 1 pm.
Fig. 6. (a)Transmission electron micrograph of a cross section of the
ocellar nerve. Thirteen receptor axons and three efferent fibers (arrow) are enveloped by the thin sheets of Schwann’s cell. Pigmented
cells, nonpigmented cells, and the capillary formed by them are almost nonexistent in this region. In the lower side of the photograph,
a part of the first optic ganglion of the secondary eyes is seen. x 4,600.
Bar: 1 pm. (b)Scanning electron micrograph of the protocerebrum
attached to the ocellar nerves. The ocellar nerve (ON) of the anteromedial eye runs away from the other ocellar nerves of the secondary
eyes and enters the posterior part (arrow)of their first optic ganglion
(OG). x 290. Bar: 50 pm.
146
A. UEHARA ET AL.
Figs. 7-1 0.
ANTEROMEDIAL EYE OF THE LIPHISTIID SPIDER
ACKNOWLEDGMENTS
We are grateful to Drs. H. Tateda and Y. Toh for
their valuable discussions.
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