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Retina and dioptric apparatus of the dung beetle Euoniticellus africanus
RETINA AND DIOPTRIC APPARATUS OF THE DUNG BEETLE EUUNiTfCELLUS AFRfCANUS V. B. ~EYE~-R~H~w Department of Biological Sciences. University of Waikato. Hamilton, New Zealand (Received
19 Apn‘t 1977)
Abstract-Retinal fine structure and optics of the eye of the dung beetle Euoniticellus africunus have been studied and compared with those of three other scarabaeid beetles: Rrpsimus manicarus. hoplognathus pal~jdjcoilis and Sericesthis geminate. The eye of E~~n~~iceilu~ in common with that of the other three species. possesses a dioptric system in which light first passes through a thick optically homogeneous cornea, and tken enters a eon-ho~geneous crystalfine cone. The lens cylinder properties of tke iatter cause the fight rays to become partially focused across the clear-zone upon tke rhabdom layer. Rays traced through a large scale drawing of the eye. with refractive indices measured for each component, predict an acceptance angle of approximately 26”. Since no significant aperture changes, lengthening of crystalline thread, cell or pigment migrations appear to be associated with dark/light adaptation. the eye may be assumed to be permanently poorly focused. In optomotor experiments the beetles did not show their characteristic antenna1 following response to black and white stripes when the Iatter had repeat periods of -CC 30”. Structurally the eye of Euoniricellus differs markedly from that of other scarabaeids. It is totally divided into dorsal and ventral eye which are of a different size (the dorsal eye is smallrf, but whose structural organization is basicahy the same. Principal pigment cells (they do not futty surround the cone) as well as accessory pigment cells (they accompany the retinula ceils in an extraordinarily regular fashion as far as to the basement membrane) exhibit some unusual features. On the proximal side of the clear-zone. at a level where all retinula cell membranes form complex meanders and convolutions. cell I is the first to possess a rhabdomere. In it, all microvilli run parallel. This rkabdomere becomes part of the rectangular proximal rhabdom over the upper 207; of its length. Below this level the rhabdom consists of 6 rhabdomeres, but throughout its length mi~ovil1~ are oriented in 2 orthogonal directions. It is thought that polarization sensitivity in dung beetles generally is related to the rhabdom organization described for E~onifjcellus. An eighth (basal) cell is present in each ommatidium. but it lacks a rhabdomere. A tracheal tapetum is not developed. Finally, the point is made not to regard al1 different eye structures in insects as per&et adaptations to a particular environment or way of living for specializations of photore~ptors may either follow, parallel or precede any ecological adaptation,
DORFand H~RRIDGE, 1973). F’maIIy, if light, entering through many facets, is accurately focused (be it by THE EYESof beetles exhibit a remarkable diversity in reflection or refraction) on a spot on the retina, we arrive at the superposition eye, a special case of the both structural organization of the retina and optical properties of the cornea and cone. Each type of eye clear-zone eye. in which acuity and sensitivity are optimal. The best known example to date is the dayis usually thought to reflect an optimum a~ptat~on to a special way of Iife or a particular environment. moth ~~ula~n~~~gs, which has an eye with a sharply but how cautious one has to be in any d~dactions focused image to which 120-150 facets contribute based on the anatomy and optics alone, is well illus(HORRIKXXet at., 1977). Examples among beeties intrated by the “superposition eye” (EXNER, 1891) or clude Lampyris (EXNER,1891) and click beetles (HOR“clear-zone eye” as it is best called (HORRIM~~E,1971). RIDGE,personal communication). This type of compound eye, commonly met with Clearly, for a nocturnal insect absolute sensitivity in the insect orders Neuroptera, Goleoptera and Lepiof its photoreceptors is of the utmost importance. but a certain degree of acuity is also desirable. Hence, doptera, is characterized by a wide clear-zone, devoid of screening pigment, between the distaf dioptric ele- ever since Exner pubfished his ideas on insect vision ments and the proximal light perceiving structures. in 3891, al1 dear-20~ eyes were called super~si~on Scarabaeid beetles were noted to possess this type eyes, and regarded as examples of a typica adap of compound eye a century ago (SCHIJI;TZ, 1868; tation of a sense organ to a nocturnal way of life GRENACHER,1879). As to the function of the clear(good resolving power combined with high sensitivity). That exceptions exist, such as the diurnal scarzone, in general, HORRILXE et al. (1972) have shown abaeid beetle Cetonia auratu, which has a clear-zone that without any ~p~st~cated optical mo~~cations eye, was known to EXNER (1891). However, the conto cornea and cone, such as lens cylinders, etc., the cept of superposition vision, hnked always to nocturclear-zone alone helps to increase the absolute sensitivity of the compound eye (but at the expense of nal ~ha~our, remained virtually unchall~ged until that the acuity). if a hmited ability exists to focus a beam of firstly HORRIDGE et al. (1972) demonstrate Skipper butterfly, an insect active in bright sunlight parallel light, entering through many facets, onto the and resting at night had an excellent superposition receptor layer, not only does the absolute fight sensitivity increase, but acuity is also improved (DIESEN- eye, and secondly MEYER-R• CHOWand HORRIDGE 165
(1975). by a variety of methods, found that the eye
af the crepuscdar scarabaeid beetle Attaplognathus was poorly focused. Because much has been learnt from beetle compound eyes in recent years, it was thou&t that a more systematic study of eye architecture within one family of beetle @carabaeidaef could be useful (a) in determining evo~~lt~ona~ trends, and (b) in discussions of the relationship between rather different structural orga~~~t~ons and iheir fundion. Few such comparative studies on optics and ultmstruct~re of eyes of phy~ogenet~~~~y closely related insects exist to date. NORRIDGEand GIDUINGS (1971) compared clear-zone eyes of various beetles. WALCXXTand HORRIDGE (1971):examined the eye of a ~~~~~opteran as an example of a relatively primitive neuropteran insect. MEYER-R• CHOW(1972) compared the retinae and optics of two species of ~~~hyli~~dae, and WADA (1974) investigated the eye structures of 29 dipteran species respresenting 13 families. The dung beetles E~~~i~~cei~as ufhwrus, intentionally introduced to Australia from South Africa in recent years (FEnRAn, f973), was chosen, be%~~~e it can be bred easily under h&oratory conditions, and differs in some aspects of visual behaviuur and external eye morphology from other scarabaeid beetles which had been studied previously (Repsimus man& carus: HORRIDGE and GI~LNN~S,1971; Anoplognathus paK;lllidicollis: MEYER-R• CHOWand HORRIDGE. 1975; and sericesf~js geminatu: ~EY~~-~~~ow, 1977). Ewriticellus does not exhibit eyeshine or a change in the optomotor response due to dark/light adaptation or time of day, and, unlike the other scarabaeid beethes studied. possesses a ~orn~on~d eye which is totaily divided into a small dorsal section and a large ventrai part.
Mature dung beetles were obtained from the C.SI.R.0. Division of Entomology in Canberra. Preparation for scanning etectron microscopy was standard (dehydration with acetone, coating with gold/palladium under vacuum). For histological examinations dark and light-adapted beetles were firstly decapitated. Then the heads were split in half and fixed for 2 hr in 1% osmium tetroxide buffered to a pW of 7.4 with a 0.1 molar solution of coliidinc-s. To reduce surface tension and help the fixative penetrate more easily. one drop of Kodak-Photo-F~o was added to the fixative, The preparations were dehydrated in a graded series of acetone and embedded in Epon 8t2. After hardening for 3 days at a tempewtine of 65°C. the specimens were sectioned with a glass knife. Goid sections were double stained with uranyl acetate (8 min) and lead citrate (4 min) and observed under the electron microscope” Refractive indices were rn~snr~d with a doublebeam interference microscope on frozen 10pm sections, using standard methods and dilute glycerol as the medium. A more detailed account of the procedure has been published earher (~EY~-R~~w, 1973). The vahres obtained were entered on scale drawings of the cornea and cone for tracings of rays in two bimensions. Azoepninee angtes for singte ommatidia were predicted from ray tracings. and
Fig. i. Diagram of an ommatidium of Erconiticellus in longitudinal section (a), and in transverse sections (b-e) at the levels indicated. Numbers alongside the drawings refer to the corresponding electron micrograpbs in this paper. This eye is rcmarkabie for the extreme rqularity by which 6 accessory pigment cells are associated with each ommatidium. and for the precise fashion in which rhabdom and rb~~omeres are otiented. Further unusual features are the 3 primary pigment ceffs which do not completely surround the cone. and rctinuta cefl I with its short rhabdomere in which all microviiti are paralfel to those of c&s 4 and 5. Abbreviations: C = cornea. Cr f 3=crystatttiine cone. Pr PC = principal pigment c&s, Ret tB = retinula c&s bodies. CZ = clear-zone. Rh = rhabdom. Bas t =i basal (eighth) reginula cetf. Ax = axons.
optomotor reactions to black and white stripes In a drum were carried out in exactly the same way as described in a paper dealing with the eye of the beetle Anoplogna#r12us (MEYER-R• CHOW and M~RRI~XX, 1975). RESULTS The ~orn~~~d eyes of ~~~~~~~~~~~s~~~~~~1~sare brown-black in cotour and he at the sides of the head, The anatomy is illustrated in Fig. I and the eiectron micrographs are taken at the levels shown by numerals in Fig. I. Each eye is eompIeteiy divided into a dorsal and a ventral part (Fig. 2a). The smaller dorsal eye consists of about 200 ommatidia which face mainly upwards (Fig. 2b). The large ventral eye is hernisphe~~~ in shape and comprises apprrrximately It?00 ommatidia which face mainly downwards and to the side (Fig. 2~). The corneae in both eyes lack surface nipples and interfacetal hairs, and there is no detectable size difference between them, both having a diameter of apFrox~~te~y 30 pm (Fig 26). Each cornea is convexly curved. The outer radius of curvature in the dorsal eye is toam whitst in the vent& eye it is 2O~m. The hexagonaf array of
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Fig. 2. (a) Scanning electron micrograph of left compound eye. The eye is totally divided into a small dorsal part and a larger ventral region. (b) The dorsal part consists of approximately 200 hexagonal ommatidia each approximately 30 pm in diameter. (c) The ventral eye is considerably larger than the dorsal area. but size and shape of ommatidia are the same. With the exception of the margin of the eye, where distorted “mini-facets” can be seen, the array of facets is extremely regular. (d) Section through ventral eye (VE) and dorsal eye (DE). The two are divided by a cuticular ridge called the canthus (Ca), below which the retinulae of both eyes almost fuse. Cornea, crystalline cone, clear-zone and rhabdom, all clearly visible, are similar in both ventral and dorsal eye.
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Fig. 3. (a) Transverse section through the crystalline cone, which is an intracellular product of the 4 cone cells (14). Each cone cell contains 5-6 layers of endoplasmic reticulum ‘near the edge of the cone plus a considerable amount of empty vesicles. The two principal pigment cells (PC, and PCJ do not fully surround the cone cells as in other insects, but leave a gap between them. They contain microtubules and pigment grains. At the distal ends of the cone cells. where their nuclei are located (inset), the pigment cells give rise to a “Star of David” pattern. (b) Size. shape and arrangement of crystalline cones as well as pigment cells are extraordinarily regular. The diameter of the pigment granules themselves, however, varies between 0.3 and 0.9 pm. (c) Longitudinal section through cone and retinula cell bodies (Ret CB) of a light-adapted photoreceptor. There is no significant migration of either cells or pigment on dark/light adaptation.
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Fig. 4. (a) Nuclei of 7 retinular cells are found on the distal side of the clear-zone. Each group of 7 cells per one ommatidium is surrounded by 6 accessory pigment cells which are easily recognizable by their “pale” appearance and clusters of what appear to be microtubules in transverse section (arrows). (b) The 4 cone cell extensions can be traced down to a level where the clear-zone begins (arrows). (c) Each group of 7 retinula cells crossing the clear-zone, is surrounded by exactly 6 clear accessory cells. devoid of screening pigment.
Fig. 5. (a) On the proximal side of the clear-zone, cell 1 is the first to produce a rhabdomere. The asymmetrical nature of this rhabdomere is seen in this light micrograph. (b) The rhabdomere of cell 1 is relatively short. In it the microvilli are oriented parallel. (c) Cell 1 contributes its rhabdomere to the rectantular shaped rhabdom. but only for a short distance (10pm. corresponding to 20:,0 of the whole rhabdom length). With regard to subcellular organization or microvillus size, cell 1 does not differ from the other retinula cells.
Fig. 6. (a) Just above the rhabdom a maze, making it impossible to follow the outline of individual retinula cells. is created by convoluted and meandering cell membranes. (b) At deeper levels retinula cell borders are more easily traceable. Six retinula cells (2-7) contribute their microvilli to the rhabdom; cell 1 no longer possesses a rhabdomere and occupies a peripheral position in each ommatidium. Six accessory pigment cells are still associated with each group of retinula cells and are easily rccognizable by their round outline and the large number of microtubules they contain (arrows). (c) Meanders of retinula cell membranes and cross section of accessory pigment cell process. containing homogeneously distributed microtubules.
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Fig. 7. Transverse sections through rhabdoms at different levels. (a) Light micrographs showrng the gradual change from a- more or less rectangular rhabdom to a square frame type a short distance above the basement membrane. Once again, the overall regularity of rhabdom shape and orientation is remarkable. (b) Over most of its length the rhabdom is composed of rhabdomeres belonging to 6 retinula cells. The microvilli of cells 3 and 6 run in the same direction but do not abut on each other. They are separated by the rhabdomeres of cells 4 and 5. and cells 2 and 7. whose microvilli run in an orthogonal direction. All retinula cells contain mitochondria and pigment granules. and form desmosomes (circles). (c) The cytoplasm of the eighth (basal) cell pushes into the rhabdom from below. and gives rise to a rhabdom which resembles a picture frame. The orthogonal arrangement of microvilli is maintained. (d) The eighth cell (8) does not have a rhabdomere of its own. The surrounding microvilli are part of retinula cells 5 and 7, and are closed off at their apices by a cell membrane (arrows).
Fig. 8. (a) All 6 accessory pigment cells can easily be traced to a level just above the basement membrane, where they show up because of their constant number and their “pale” appearance. (b) The basal retinula cell contains mitochondria and pigment granules, and its nucleus is large (N). Some accessory pigment cells (AcPC) are clearly visible. (c) Retinula cell axons of both dorsal eye (below the broken line) and ventral eye make synaptic contacts in the same common lamina. (d) Each axon bundle contains 8 retinula cell fibres. A few tracheoles (Tr) penetrate the fibrous structure of the basement membrane (BM) together with the axons.
Fig. 9. Dioptric structures of the eye under the interference microscope. (a) and (b) Longitudinal sections, 10 nm thick, through the cornea parallel to the ommatidial axis. The different degree of optical compensation in (a) and (b) clearly shows that apart from its outer and inner edge, the cornea is optically homogeneous. (c) Longitudinal 10pm thick section through crystalline cones, showing that the latter are optically non-homogeneous. (d) and (e) Interference micrographs through 10 pm transverse sections of a group of 4 cones. The stepwise compensation under green light, first for peripheral cone areas (d) and then for the centre (c) shows that a strong gradient of refractive index lies in the outer zone that the centre apart from being more homogeneous, has the higher refractive index.
The eye af the dung beetle Euaniticehs facets is regular and the interommatidial angle is 151.8” in the dorsal and 1.8-2” in the ventral eye. Ommatidia in the ventral eye have an average length of 3oO~rn but in the dorsai eye they are slightly shorter (cc_ 250 grn). Cone. pigment cells and clear-zone Below the 60 pm thick cornea, which has an inner radius of curvature of 8 pm, one finds the crystalline cone (Figs. 3a. b.c). Each cone is S0~m long and as in other insects with eucone eyes, is the result of an intracellular secretion of the so-called four Semper cells. The nuclei of these cells occupy the narrow space between cornea and crystalline cone. In cross section the crystalline cones are circular and electron opaque. As in other scarab&d beetles there are 56 concentric layers of endoplasmic reticulum surrounding each cone. The cone cell cytoplasm, compared with that of ~~z~~~~~ur~~~sis rich in empty vesicles and other subcellular components. The crystalline cone cells of insects are usually cIrcumscribed by two principal pigment cells, but in ~~on~rj~.e~~~s the situation is different. Here the two principal pigment cells are relatively small and each of them does not even surround the cone by more than 100 (Fig. 3a). The accessory pigment cells, on the other hand. are well-developed and conspicuous because of their dark pigment granules and regular arrangement (Fig. 3b). They occupy the triangular spaces left where three ommatidia meet, and in transverse section give rise to a pattern around each cone similar to a Star of David. The six accessory pigment cells. thus associated with one ommatidium. can be followed as far down in the eye as the basement membrane In spite of the presence of microtubules in both principal and accessory pigment cells, no appreciable movement of pigment or cells was seen as a consequence of dark~~~ghtadaptation, (For a more detaikd discussion of a~ptational changes and the role of microtubules see WALCOTT,1975.) Screening pigment granules in both principal and accessory pigment cells range in diameter from 0.3-0.9 pm. Euoniticeihts appeared permanently dark-adapted (Fig. 3~). even if exposed to bright light at night. Whether this apparent lack in retinomotor events is a genuine characteristic of the eye. or due to a fixation procedure which was not rapid enough to arrest cellular changes is unknown at this stage. Below the crystalline cane, groups of seven retinula cell bodies are found (Fig. 4a). Each group is surrounded by the six accessory pigment cells, which at this level no longer contain pigment granules, but appear rather empty apart from a few clusters of microtubules. The roots of the crystalline cone cells disappear shortly befare the clear-zone becomes the prominent feature of the eye (Fig. 4b). In the clear-zone the narrow retinula cell columns stain more densely than the surrounding by a variety of methods which stain proteins (Fig. 4~). In transverse section the shape of each column of 7 ceils varies, but the overall arrangement (one column always surrounded by six large accessory pigment cells. and almost always exactly equidistant from neighbouring columns by 20pm) gives this eye an extraordinary order and regularity. surpassing that of other scarabaeids.
Rhabdom
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layers
the seven retinula cells on the proximal side of the 120pm deep clear-zone in each ommatidium of both dorsal and ventral eye (Fig. 5a). gives rise to a rhabdomere, which has all its microvilli oriented in one direction (Fig. 5b). Only 10pm below this level 4 other retinula cells contribute their rhabdomeres. thus giving rise to a fused rhabdom made up of 5 rhabdomeres in which the microvilli are oriented in 2 orthogonal directions (cells 1. 4. 5 versus cells 3 and 6), and in which retinuia celt I has the largest rhabdomere (Fig. SC). There is no difference in size between microvilli belonging to ceil 1 and those which are part of the other cells; all have an average diameter of 4 pm. The cytaplasm of all retinula cells is crowded with mitochondria, and some granules of screening pigment are also present. Most unusual. however. and in strong contrast to the otherwise extreme constancy and regularity of structural elements in the eye of EuoniticeUus, are the convolutions, twists and meanderings of all retinula cell membranes in this ptane (Fig. 6a). It is impossible to outhne the peripheral boundary of retinula cells or even follow a cell membrane for a short distance. In the vicinity of each rhabdom there are still the 6 accessory pigment cells (Fig. 6b), each densely packed with microtubules of 20-25 nm diameter. but the cell borders of these cells are “‘normal”. and show no trace of any convolution (Fig. 6~). The retinula cell membranes remain rather irmgular over the entire depth of the retina without. however, affecting the consistent pattern of rhabdomercs (Fig. 7a). At a level where cell I has turned into a wide axon, the rhabdomeres of cells ?-,I rearrange to form a rectangular-shaped rhabdom (Figs. 6b. 7b). Microvilii belonging to cells 3 and 6 run in the same direction and form the shorter sides of the rectangle. Separating these two rhabdomeres are those belonging to cells 4.5 and 2.7 whose microvilli run parallel bur at right angles to those of cells 3 and 6. Alignment of microvilli and orientation of the rhabdom rectangles across the entire eye are remarkably regular. and resemble the organization described by WACHMANN and SCHR&R (1975) for the ventral eye of the whirligig beetle. Desmosomes are developed at the edge of each rhabdomere where two adjacent retinula cells meet. The rhabdom gradually changes into ti hollow square, approximately 1Sprn above the basement membrane, where the cell plasma of the 8th retinula cell projeecrs centrdiy from below into the rhabdo~~ (Fig. 7~). This basal cell. which does not appear to have a rhabdomere of its own (Fig. 7d). is surrounded by the microvilli of retinula cells 2- 7. It contains granules of screening pigment (0.6 pm in diameter1 and a large nucleus. Shortly above the basement membrane the six accessory pigment celt~ appear once more. as electron transparent, slightly swoilen cells, of circular outline (Fig. Saf. alternating in position with the seven retinula cells in one ommatidium (Fig. 8b). A few narrow tracheoles reaching the most proximal layer of the rhabdom. penetrate the 3 ~tm thick basement membrane. which is of a “‘fibrous” texture (Fig. 8d) A proper tracheaf tapeturn, howevtr, is not developed. Groups of 8 retinufa cells (one from One of
V. B. MEYER-R• CHOW
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each ommatidium) pass through the basement membrane as distinct axon bundles, which remain separate for at least 30~. They then combine with adjacent bundles to form greater aggregations (Fig. 8~). No indication was found of the existence of separate laminae, one serving the dorsal, the other the ventral eye. Dioptric apparatus and acuity Sensitivity and acuity, the two most important parameters of vision, depend to a great extent. but not entirely (visual pigment also matters) on the optical qualities and properties of the dioptric system. As in the eyes of Repsimus, Anoplognathus and Sericesthis, the cornea in Euoniticellus is relatively thick and occupies one-fifth of the ommatidial length, but in contrast to the other beetles external facets with individual convex lenses are here developed. With the exception of its outer 6pm and inner 1Opm layers the cornea is optically homogeneous (Figs. 9a, b) and has a mean refractive index of 1.534. The outer and inner edges were found to possess slightly lower values: 1.481 and 1.426 respectively. A cornea1 lens-cylinder is definitely not developed. In both transverse and longitudinal sections through the crystalline cone a radial gradient of refractive index was found (Figs. 9c, d, e). The drop of refractive index from a central value of 1.443 to a peripheral one of 1.374 was not a gradual decrease. but rather a sudden fall near the outer edge of the cone. The refractive indices of clear-zone (1.345) and rhabdom (1.353) were also measured. Encouraged by the results which were obtained from other insects by a method in which a large scale diagram of the eye was used to trace a known number of rays through cornea, crystalline cone, and clearzone, in order to determine the acceptance angle of a single ommatidium, a similar procedure was carried out on Euoniticellus. Together with the morphometric data of the various structures in the eye of Euoniticellus, the refractive index measurements provided the basis for a two-dimensional reconstruction of ray paths within the eye. A good agreement was found between theoretically predicted acceptance angle (from ray-tracing) and experimentally obtained values of the acceptance angle. In spite of its lens cylinder properties in the crystalline cone. the eye of Euconiticellus does not focus a bundle of parallel rays very well; thus, acuity cannot be very high. Ray-tracing shows that the acceptance angle of both dark and light-adapted eyes lies between 25” and 30” (Fig. 10). Animals tested in an optomotor drum at a light level of 800 lx, did indeed show that no response was obtained for black and white equally-spaced stripes with stripe repeat periods less than 30”. At higher stripe repeat periods the response of the clamped beetles did not consist of head turning movements, but of antenna1 movements, although experimental techniques and apparatus were the same throughout. DISCUSSION Although presumably phylogenetically related and, therefore placed in one family by most entomologists, the scarabaeid beetles Repsimus (HORRIDGE and GID-
Fig. 10. An acceptance angle of approximately 26” is derived from counting the number of rays which fall into sectors at the receptor level. representing individual rhabdoms. The procedure is based on measurements of refractive indices in cornea, cone and clear-zone.
1971) Anoplognathus (MEYER-R• CHOWand HORRIDGE, 1975) Sericesthis (MEYER-R• CHOW,1977) and Euoniticellus possess eyes which differ markedly from each other in their anatomy. This one family of beetles exhibits a greater variety of compound eye types than some entire orders of insects have to offer e.g. Hymenoptera (MENZEL, 1972; VARELA and PORTER, 1969; WACHMANN et al., 1973) and Diptera (representatives of 13 families, all with similar eyes, recently studied by WADA. 1974). Because Hymenoptera and Diptera are just as diverse as Scarabaeidae with regard to their requirements and ways of life, e.g. diurnal, crepuscular and nocturnal species, one wonders about the kinds of evolutionary pressure which could have led to the development of so many different types of photoreceptor organization in beetles. It is conceivable that the wide range of eye types does not reflect perfect adaptations, but that on the contrary no single photoreceptive structure has yet been evolved in beetles, capable of functioning under many different conditions. Different anatomies do not necessarily have to imply different functions, and no evolutionary pressure would have been exerted if eyes with different structure functioned equally well. DINGS,
Interspecies comparisons of eye structures Apart from the general organization of insect compound eyes into cornea, cone and retina. the only feature that the 4 species of scarab beetles have in common is the clear-zone. However, even the clearzone is not developed to the same extent in all 4 species, for in Repsimus and Anoplognathus it is very large (cu. 350 pm in depth) whilst in Sericesthis and Euoniticellus it is relatively small (cu. 110pm) even if one takes into consideration the smaller size of the latter two beetles, and their proportionate reduction in eye size. In all four beetles 7 retinula cell bodies per ommatidium are located on the distal side of the
The eye of the dung beetle Euoniticellus clear-zone. In Euoniticellus the spacing of the retinula cell columns crossing the clear-zone, and the arrangement of the surrounding accessory pigment cells, both reach maximum regularity; in the other three species the pattern is far less regular. The differences among the four beetles in rhabdom structure are most surprising, because all four, when mature. can be called “non-diurnal”, and live in an environment which is characterized by low light levels. Euoniticellus is probably the least nocturnal of the four with regard to flying time. Little published information is available on the behaviour of Euoniticellus. but from what is known, it appears that this species, unlike most other dung-beetles, e.g.. Onthophagus (which has a similar eye: MEYER-R• CHOW,unpublished observation). is a diurnal flier (FERFLAR, personal communication). When it emerges from the soil as an adult, it “spends only minutes flying to the next pad, and as soon as it arrives at the dung plunges in and starts tunnelling and shovelling, all below dung” (FERRAR.personal communication). Therefore, apart from the first few minutes of its adult life, most of the life-time of this beetle is spent below. or in. the semi-transparent cow dung, where peculiar light conditions must prevail. The eye of Euoniticellus lacks a tracheal tapetum, but possesses an eighth (basal) cell. which does not have a rhabdomere. Over most of its length the rhabdom is of rectangular shape and consists of 6 rhabdomeres. Towards its distal end the rhabdom is asymmetrical. This is the result of a large rhabdomere belonging to cell 1, in which microvilli are aligned parallel with those of cells 4 and 5. The rhabdomere/ cytoplasm ratio at mid-rhabdom level is 1:2.2. There is no difference in the dimensions of microvilli belonging to cell 1 and those which form part of the other retinula cells. Repsimus. judged by its activity, is mainly a crepuscular beetle. It possesses no basal (eighth) retinula cell, but has a tracheal tapetum which surrounds each rhabdom along its complete length. The rhabdomere/ cytoplasm ratio for one retinula cell halfway down the rhabdom. is approximately 2.5: 1. The rhabdom, cut transversely. is seven-lobed and has no apparent regularity or orientation. Behavioural observations indicate that Anoplognuthus seems to become active later in the evenings than Repsiwtus. An eighth (basal) retinula cell is usually developed, but it always lacks a rhabdomere. The tracheal tapetum reaches only halfway up the rhabdom and the rhabdomere/cytoplasm ratio per retinula cell is approximately 3: 1. The rhabdom in transverse section is seven-lobed, but otherwise has no apparent regularity. Finally, probably the most nocturnal beetle of the four. Srricesthis, also possesses no tapeturn. but has a rhabdom in three tiers. The basal cell gives rise to a small rhabdomere consisting of 9-10 parallel microvilli. At mid-rhabdom level 6 retinuia cells produce a star-shaped pattern in which the rhabdom/ cytoplasm ratio reaches at least 6:1, and the microvilli are oriented symmetrically with respect to a central point in the rhabdom, whilst towards the distal end of the rhabdom a monocellular rhabdom with larger microvilli oriented in 3 directions occupies approximately 409; of the retina.
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Evolutionary trends and photoreceptor adaptations The retention of at least the basal retinula cell if not its rhabdomere as well. the increase in rhabdom area at the expense of retinula cytoplasm, and the diversification of rhabdom organization appear to be some anatomical consequences of the evolution of scarabaeid beetles towards a more nocturnal way of life. Obviously a larger rhabdom, banked layers of rhabdomere, and a multidirectional organization of microvilli will result in an increase in sensitivity (MEYER-R• CHOW,1977). The lack of a tracheal tapeturn in Sericesthis, usually a characteristic of diurnal insects, could mean that photon capture in the rhabdom layers is so efficient that a reflecting system is not required. However. it is not known whether photoreceptor organizations evolve parallel to an ecological specialization, or whether there is a time-lag, and of what magnitude this might be. Behavioural studies lacking, it is difficult to state whether, for example. Repsimus is on the way to becoming a more diurnal insect, or whether Euoniticellus. in spite of its out-of-sight life in dung and soil, still has a photoreceptor originally developed by its ancestor to suit more diurnal needs. In Euoniticellus the orthogonal and regular microvillus orientation, the rhabdomere: cytoplasm ratio of 1:2.2 and the lack of a tapetum certainly point in this direction. Optics, sensitivity and acuity In those three species in which the dioptric apparatus has been studied the cornea is thick, but optically more or less homogeneous, with a refractive index of about 1.5. The crystalline cone. on the other hand. shows a radial gradient of refractive index with values for the central core of 1.458 (Rrpsimus: MEYERR~CHOW, 1975). 1.442 (Anoplognathus: MEYERR~CHOW and HORRIDGE, 1975) and 1.443 (Euoniticellus) and for the periphery of 1.360 (Repsimus). 1.365 (Anoplognathus). and 1.374 (Euoniticellus). Refractive indices common to all species were also found for clear-zone and rhabdom. As with the eyes of Repsimus, Anoplognathus and presumably Sericrsthis (a species for which no direct optical data are available), the compound eye of Euoniticrllus must be classed as a “partially-focused” clear-zone eye, and as such will undoubtedly exhibit an improved sensitivity at the expense of acuity (DIFSENDORFand HORRIIXE. 1973). The angular sensitivity in Euoniticellus (as inferred to from ray-tracing) is somewhat poorer than that in Anoplognathus. but that Euoniticellus in fact makes use of its visual receptors is demonstrated by its reaction to moving black and white stripes. The lack of adaptational variation in the optomotor reactions of mature Euoniticellus. is perhaps related to the way of life this beetle leads. burrowing in the ground for most of its life, so that it would rarely encounter drastic illumination changes, where adaptational measures were necessary. During the very short swarming period (a matter of minutes: FERRAR. personal communication) adaptational changes may occur, but from the moment the beetle has turned to a life in the dung, its eye appears to become permanently adapted to a low environmental brightness level. and loss of acuity is compensated for by both high absolute sensitivity and the abilitv to resoond to movements of large The - obiccts. _,
178
V. B. MEYER-R• CHOW
Because of its distal location near the top of the proximal, rectangular rhabdom, as well as because of its unidirectionally oriented microviiii, the rhabdomere of cell 1 could act as a placation filter. Polarization sensitivity of primary receptor cells not necessarily leads to a meaningful interpretation of polarization patterns; this would largely depend on the wiring of retinula cell axons in the optic ganglia, but in the simplest possible way a two-channel polarization analyzer could be formed by any two cells with rni~ro~I1~ at right angles. Such a system, whether it be a combination of cell 1 with retinufa celfs 3 or 6, or any Two other features of the eye of ~~o~~~r~~~~i~~ are pair of cells 2-7 with orthogonal microvilli, would. noteworthy: retinula cell I and its rhabdomere. and of course, depend on the regularity of its components the division of the eye into dorsal and ventral regions. and on whether the rhabdom is twisted or not. In There are a few other insects in which divided com- Euoniticellus the latter two requirements are definitely pound eyes occur e.g. male mayflies, a few dipterans. met in favour of PS. but not so in Anoplagnathus some stage beetles and whirligig beetles. Althou~ it with its irregularly shaped rhabdoms. In this latter has not been clearly established why the eye is split species MEYER-RKHOW and HORRIDGE (1975). using into two in any of these, it is generally thought that, intracellular electrophysiological recordings from at least in whirligig beetles, the ventral eye is for single retinuia cell& were unable to find any apprecivision in an aquatic environment, the dorsal for see- able polarization sensitivity. ing in air. There may, ofcourse. be additional reasonsIn conclusion, a comparison between the comand different ones for other species pound eye of ~~on~r~c~~~~sand that of three other In many insects differences between dorsal and ven- scarabaeid beetles, revealed that despite a similarity tmi fmX?tS iiir&tiOII t0 Size (EXNER. 1891). COIOtfr of dioptric systems. considerable anatomical differsensitivity (MENZEL. 1975) and fine structure (SCHINZ, ences exist. How the anatomical diversity in retina 1975) have been reported. Recently WEHNER(1976) organization can be explained in terms of adaptations to different ways of life and distinct habitats is unhas also shown that polarization sensitivity in the ant and bee may well be restricted to a small patch of known at this stage. as there are still not sufficient a few dorsal ommatidia. It is feasible that the comdata to make sensible comparative statements about bination of such differences could have led to a physifunctiona properties such as coiour and polarization cal separation into dorsal and ventral eye. Whether sensitivity, acuity range and absolute sensitivity. physiological differences exist between dorsal and ventral. facets in Euc~niticrl~us remains to be seen. for Acknowltldgpmnrts-The largest part of this research was as in the beetfe Macrogyrus striolatus (HORRIDGE and carried out at the Department of Neurobiology. Australian GIIXXMZ, f971), the anatomy of dorsal and ventral National University, Canberra. For his interest and eye is remarkably similar. fn the whirring beetles encouragement throughout this study f wish to thank Prof. G. A. HORRID~EF.R.S. (Research School of Biological Gyritws ~ril~us and G. s~hstriQtus. WACHMANN and Sciences. Department of Neurobiotogy. Canberra). For SCHX~~ER (1975) find a few structural differences such as a more highly ordered pattern of rhabdoms in the allowing me to use his Philips 200 electron microscope to finish this investigation. I thank Mr. N. H. LAW. Direcventral eye. The ventral eye further distinguishes itself tor of the Meat Industry Research Institute in Hamilton. from its dorsal counterpart by having a paraltel New Zealand. microviiius organization in rhabdomere 1, and by having a longer proximal rhabdom. Wachmann and Scbriiefs results. although seriously hampered by fixation difficulties. show that there are certain similariBIRUKOWG. (1953) Menotaxis in polarisicrtem Licht bei Georrupcs sifvaricus. ~ff~urw~sse~sc~~~en 40, 61 i -42. ties in rhabdom organ~~tion between the eyes of DIESENWRF M. 0, and HORRIDGEG. A. (1973) Two ErtonIticrlius and whirligig beetles. models of the partially focused clear-zone compound There is evidence that some scarabaeids use the eye. Prof. R. Sot. B 183. 141-158. polarization pattern of the sky as a navigational aid EXNERS. (I89f) Dip ~~~~j~~~~~~, dw ~a&~~zj$r~~ A~pn cm ~~IRUKOW, 1953, F~N~E~CH ~‘tat. 1975). In Euc~niKrrhsen und ~nsekc~}i. Franz Deuticke. Leipzig. ric&s for example. the detection of a polarization FERRERP. (1973) The CSIRO dung beetle project. Wooi pattern would be useful during the brief swarming fechnol. Shwp Breed 20. 73-75. flight. enabling the insect to fly in a straight line even FRANTSEVXHL. I., MOKRUSHOVP. A. and ZOLOTW V. V. if the sun is obstructed by a cloud. The finding of (1975) Astroorientation of tehtrus nptrrus Laxm. (Caleoptera. Scarabaeidae). Akad. Nauk SSSR 36. 61-65. a rhabdom in the dung beetle ~u~~it~ce~ius in which GRENACHER H. (1879) Unrersuchungm ii&r das Sehorgan the microvilli are consistently oriented in orthogonal dw Arthropoden insbesondrre drr Spinnen, Insekten und directions, pius the presence of a more distally located Crusraee~n. Vandenhock SCRuprecht. GMtingen. cell with microviili pointing in one direction only. HORRIDCEG. A. (1971) Alternatives to superposition imcould be significant with regard to polarization sensiages in clear-zone compound eyes. Proe. R. SOC.B 179, tivity (PS) in dung beetles. It is now generally thought 97-124. that the basis of PS lies in the paraHel alignment of HORRILXXG. A. and GIDIXNGSC. (1971) Movement on
advantage of a partially focused eye over one with a narrow acceptance angle is to increase the number of impressions summed so that important features stand out, but insistent irregularities in the visual field are smoothed (HORRIDGEand HENDERSON, 1976). Also, in Euoniticellus olfaction. to detect fresh dung, is likely to have taken over some sensory functions and may, therefore. have reduced the importance of vision (.J&scHKE. 1914).
microvilli which cause a similar alignment of visual dipole molecules in the membranes (LAUGHLIN it ai., 1975).
dark-light adaptation in beetle eyes of the neuropteran type. Pour. R. Sot. B 179, 73-85. HOHRKXXG. A.. GIWXNGSC. and STANCEG. (1972) The
The eye of the dung beetle superposition eye of skipper butterflies. Proc. R. Sor. B 182, 457495. HORRIDCEG. A. and HENDERSONI. (1976) The ommatidium of the lacewing Chrpwpa (~europtera). Proe. R, Sot. B 192, 259-27 1. HORRIDCEG. A.. NINHAM V. W. and DIESSENWRFM. (1972) Theory of the summation of scattered light in clear-zone compound eyes. Proc. R. Sot. B 175. 183-194. HORRIDGE G. A.. MCLEANM.. STANCE G. and LILLYWHITE P. G. (1977) A diurnal moth superposition eye with high resolution (Phu~a~~~jf~f~,~ rrisrjfificat. Proc. R. Sot. B (In Press ). J~RSCHKEH. (1414) Die Facettenaugen de; Orthopteren und Termiten. Z. siss. Zoo/. 61, 1533280. LALIC;HLIN S. 9.. MENZ~L R. and SNYDER A. W. (1975) Membranes. dichroism and receptor sensitivity. In Photoreceptor Optics (Ed. by SNYDERA. W. and MENZEL R.). pp. 237-258. Springer, Berlin. MEGGC;ITT S. and Mtutr+Rocnow V. 9. (1975) Two calculations on optically non-homo~cneaus lenses. In 7% Compomd Eye and I ision of fnsrcrs (Ed. by HORRIDGE G. A.). pp. 314320. Clarendon Press, Oxford. MENZEL R. (1972) Feinstruktur des Komplexanges der Roten Waldameise Formica po/Jctrna (Hymenoptera. Formicidae). Z. Zrllforsch, 127. 356-373. MT.NZELR. (1975) Colour receptors in insects. In 7%~ Compmctzd Eye and Vision qf.insrcts (Ed. by HORRI~XXG. A.). pp. 121 153. Clarendon Press. Oxford. MEYER-ROCHOW V. 9. (1972) The eyes of Creuphilus ythroccphalus F. and Sartall~rs signatus Sharp (Staphyhmdae: Coleoptera). Z. Ze//forsch. 133. 59-86. MEYI.R-ROCI~OW V. B. (1973) The dioptric system of the eye of C_vhisrrJr (Dytiscidae:Coleoptera). Proc. R. Sac. B 183. Mr~t R-ROCHOWV. 9. (1975) The dioptric system in beetle compound eyes. In The Compound Eye and Vision qf Lond.
IP 24 ?- ,
Euoniricellus
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insects (Ed. by HORRILXEG. A.). pp. 299-314. Clarendon Press, Oxford. MEYER-R• CHOW V. B. (1977) The unusual compound eye of the beetle ~~~~ic~,~r/~~s ~(~~~n~r~.Iv. 2. J. Zoo!. (In Press). MEYER-R•CHOW V. 9. and HORRI~X~ G. A. (1975) The eye of Anoplognarhus (Coleoptera. Scarabaeidae). Proc. R. Sot. Lond. B 188. I 30. SCHINZR. H. (1975) Structural specialization in the dorsal retina of the bee. Apix rnc#$v~~ Ce// Tim. RF.?. 162. 23 - 34.
SCHULTZM. S. f 11168)~Flf~~sff~h~ngn~t7 gcset~tm
Augen
der
Krrhsr
md
i&r fnsvkrrrr.
die, ~~s~‘~~~n-
Anatomische Institut. Bonn. VARELAF. G. and PORTERK. R. (1969) Fine structure of the visual system of the honey bee (.4/1is nrr//$vu). J. L’ltrastruct.
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WACHMANN E. and SCHRSERW.-D. (1975) Zur Morphologie des Dorsal und Ventraiauges des Taumelklfers GUYinus ~~~~~rriu[~~ (Steph.) (Coleoptera. Cyrinidae). Zoomorphol. 82. 43 6 1. WACHMANN E.. RIGHTERS S. and SCHRICKER 9. (1973) Feinstrukturen im Komplexauge der Blattschneiderbiene Megachilc, rotunda (F.) (Hymenoptrra. Apidaea Z. Morph. Tie-c, 76. 109. 128. WADA S. (1974) Speziellc randzonale Ommatidien der lung in den Komplexaugen. Z. ;~~r~h. Tirrv 77. 87.-125. WALCOTTB. (1975) Anatomical changes during light adaptation in insect compound eyes. In Thr Compound Eyr and Vision (Ed. by HORRIDGF G. A ). pp. 20-32. Clarendon Press. Oxford. WALCOTTB. and HORRIDT~F. G. A. (1971) The compound eye of Archzchauiiodcs (Megaloptera). Proc. R. Sot. B 179, 65-72. WEHNEK R. f 1976) Polarized-light navigation by insects. Sricvrt. ,4m 235. 106- 115.
19 Apn‘t 1977)
Abstract-Retinal fine structure and optics of the eye of the dung beetle Euoniticellus africunus have been studied and compared with those of three other scarabaeid beetles: Rrpsimus manicarus. hoplognathus pal~jdjcoilis and Sericesthis geminate. The eye of E~~n~~iceilu~ in common with that of the other three species. possesses a dioptric system in which light first passes through a thick optically homogeneous cornea, and tken enters a eon-ho~geneous crystalfine cone. The lens cylinder properties of tke iatter cause the fight rays to become partially focused across the clear-zone upon tke rhabdom layer. Rays traced through a large scale drawing of the eye. with refractive indices measured for each component, predict an acceptance angle of approximately 26”. Since no significant aperture changes, lengthening of crystalline thread, cell or pigment migrations appear to be associated with dark/light adaptation. the eye may be assumed to be permanently poorly focused. In optomotor experiments the beetles did not show their characteristic antenna1 following response to black and white stripes when the Iatter had repeat periods of -CC 30”. Structurally the eye of Euoniricellus differs markedly from that of other scarabaeids. It is totally divided into dorsal and ventral eye which are of a different size (the dorsal eye is smallrf, but whose structural organization is basicahy the same. Principal pigment cells (they do not futty surround the cone) as well as accessory pigment cells (they accompany the retinula ceils in an extraordinarily regular fashion as far as to the basement membrane) exhibit some unusual features. On the proximal side of the clear-zone. at a level where all retinula cell membranes form complex meanders and convolutions. cell I is the first to possess a rhabdomere. In it, all microvilli run parallel. This rkabdomere becomes part of the rectangular proximal rhabdom over the upper 207; of its length. Below this level the rhabdom consists of 6 rhabdomeres, but throughout its length mi~ovil1~ are oriented in 2 orthogonal directions. It is thought that polarization sensitivity in dung beetles generally is related to the rhabdom organization described for E~onifjcellus. An eighth (basal) cell is present in each ommatidium. but it lacks a rhabdomere. A tracheal tapetum is not developed. Finally, the point is made not to regard al1 different eye structures in insects as per&et adaptations to a particular environment or way of living for specializations of photore~ptors may either follow, parallel or precede any ecological adaptation,
DORFand H~RRIDGE, 1973). F’maIIy, if light, entering through many facets, is accurately focused (be it by THE EYESof beetles exhibit a remarkable diversity in reflection or refraction) on a spot on the retina, we arrive at the superposition eye, a special case of the both structural organization of the retina and optical properties of the cornea and cone. Each type of eye clear-zone eye. in which acuity and sensitivity are optimal. The best known example to date is the dayis usually thought to reflect an optimum a~ptat~on to a special way of Iife or a particular environment. moth ~~ula~n~~~gs, which has an eye with a sharply but how cautious one has to be in any d~dactions focused image to which 120-150 facets contribute based on the anatomy and optics alone, is well illus(HORRIKXXet at., 1977). Examples among beeties intrated by the “superposition eye” (EXNER, 1891) or clude Lampyris (EXNER,1891) and click beetles (HOR“clear-zone eye” as it is best called (HORRIM~~E,1971). RIDGE,personal communication). This type of compound eye, commonly met with Clearly, for a nocturnal insect absolute sensitivity in the insect orders Neuroptera, Goleoptera and Lepiof its photoreceptors is of the utmost importance. but a certain degree of acuity is also desirable. Hence, doptera, is characterized by a wide clear-zone, devoid of screening pigment, between the distaf dioptric ele- ever since Exner pubfished his ideas on insect vision ments and the proximal light perceiving structures. in 3891, al1 dear-20~ eyes were called super~si~on Scarabaeid beetles were noted to possess this type eyes, and regarded as examples of a typica adap of compound eye a century ago (SCHIJI;TZ, 1868; tation of a sense organ to a nocturnal way of life GRENACHER,1879). As to the function of the clear(good resolving power combined with high sensitivity). That exceptions exist, such as the diurnal scarzone, in general, HORRILXE et al. (1972) have shown abaeid beetle Cetonia auratu, which has a clear-zone that without any ~p~st~cated optical mo~~cations eye, was known to EXNER (1891). However, the conto cornea and cone, such as lens cylinders, etc., the cept of superposition vision, hnked always to nocturclear-zone alone helps to increase the absolute sensitivity of the compound eye (but at the expense of nal ~ha~our, remained virtually unchall~ged until that the acuity). if a hmited ability exists to focus a beam of firstly HORRIDGE et al. (1972) demonstrate Skipper butterfly, an insect active in bright sunlight parallel light, entering through many facets, onto the and resting at night had an excellent superposition receptor layer, not only does the absolute fight sensitivity increase, but acuity is also improved (DIESEN- eye, and secondly MEYER-R• CHOWand HORRIDGE 165
(1975). by a variety of methods, found that the eye
af the crepuscdar scarabaeid beetle Attaplognathus was poorly focused. Because much has been learnt from beetle compound eyes in recent years, it was thou&t that a more systematic study of eye architecture within one family of beetle @carabaeidaef could be useful (a) in determining evo~~lt~ona~ trends, and (b) in discussions of the relationship between rather different structural orga~~~t~ons and iheir fundion. Few such comparative studies on optics and ultmstruct~re of eyes of phy~ogenet~~~~y closely related insects exist to date. NORRIDGEand GIDUINGS (1971) compared clear-zone eyes of various beetles. WALCXXTand HORRIDGE (1971):examined the eye of a ~~~~~opteran as an example of a relatively primitive neuropteran insect. MEYER-R• CHOW(1972) compared the retinae and optics of two species of ~~~hyli~~dae, and WADA (1974) investigated the eye structures of 29 dipteran species respresenting 13 families. The dung beetles E~~~i~~cei~as ufhwrus, intentionally introduced to Australia from South Africa in recent years (FEnRAn, f973), was chosen, be%~~~e it can be bred easily under h&oratory conditions, and differs in some aspects of visual behaviuur and external eye morphology from other scarabaeid beetles which had been studied previously (Repsimus man& carus: HORRIDGE and GI~LNN~S,1971; Anoplognathus paK;lllidicollis: MEYER-R• CHOWand HORRIDGE. 1975; and sericesf~js geminatu: ~EY~~-~~~ow, 1977). Ewriticellus does not exhibit eyeshine or a change in the optomotor response due to dark/light adaptation or time of day, and, unlike the other scarabaeid beethes studied. possesses a ~orn~on~d eye which is totaily divided into a small dorsal section and a large ventrai part.
Mature dung beetles were obtained from the C.SI.R.0. Division of Entomology in Canberra. Preparation for scanning etectron microscopy was standard (dehydration with acetone, coating with gold/palladium under vacuum). For histological examinations dark and light-adapted beetles were firstly decapitated. Then the heads were split in half and fixed for 2 hr in 1% osmium tetroxide buffered to a pW of 7.4 with a 0.1 molar solution of coliidinc-s. To reduce surface tension and help the fixative penetrate more easily. one drop of Kodak-Photo-F~o was added to the fixative, The preparations were dehydrated in a graded series of acetone and embedded in Epon 8t2. After hardening for 3 days at a tempewtine of 65°C. the specimens were sectioned with a glass knife. Goid sections were double stained with uranyl acetate (8 min) and lead citrate (4 min) and observed under the electron microscope” Refractive indices were rn~snr~d with a doublebeam interference microscope on frozen 10pm sections, using standard methods and dilute glycerol as the medium. A more detailed account of the procedure has been published earher (~EY~-R~~w, 1973). The vahres obtained were entered on scale drawings of the cornea and cone for tracings of rays in two bimensions. Azoepninee angtes for singte ommatidia were predicted from ray tracings. and
Fig. i. Diagram of an ommatidium of Erconiticellus in longitudinal section (a), and in transverse sections (b-e) at the levels indicated. Numbers alongside the drawings refer to the corresponding electron micrograpbs in this paper. This eye is rcmarkabie for the extreme rqularity by which 6 accessory pigment cells are associated with each ommatidium. and for the precise fashion in which rhabdom and rb~~omeres are otiented. Further unusual features are the 3 primary pigment ceffs which do not completely surround the cone. and rctinuta cefl I with its short rhabdomere in which all microviiti are paralfel to those of c&s 4 and 5. Abbreviations: C = cornea. Cr f 3=crystatttiine cone. Pr PC = principal pigment c&s, Ret tB = retinula c&s bodies. CZ = clear-zone. Rh = rhabdom. Bas t =i basal (eighth) reginula cetf. Ax = axons.
optomotor reactions to black and white stripes In a drum were carried out in exactly the same way as described in a paper dealing with the eye of the beetle Anoplogna#r12us (MEYER-R• CHOW and M~RRI~XX, 1975). RESULTS The ~orn~~~d eyes of ~~~~~~~~~~~s~~~~~~1~sare brown-black in cotour and he at the sides of the head, The anatomy is illustrated in Fig. I and the eiectron micrographs are taken at the levels shown by numerals in Fig. I. Each eye is eompIeteiy divided into a dorsal and a ventral part (Fig. 2a). The smaller dorsal eye consists of about 200 ommatidia which face mainly upwards (Fig. 2b). The large ventral eye is hernisphe~~~ in shape and comprises apprrrximately It?00 ommatidia which face mainly downwards and to the side (Fig. 2~). The corneae in both eyes lack surface nipples and interfacetal hairs, and there is no detectable size difference between them, both having a diameter of apFrox~~te~y 30 pm (Fig 26). Each cornea is convexly curved. The outer radius of curvature in the dorsal eye is toam whitst in the vent& eye it is 2O~m. The hexagonaf array of
167
Fig. 2. (a) Scanning electron micrograph of left compound eye. The eye is totally divided into a small dorsal part and a larger ventral region. (b) The dorsal part consists of approximately 200 hexagonal ommatidia each approximately 30 pm in diameter. (c) The ventral eye is considerably larger than the dorsal area. but size and shape of ommatidia are the same. With the exception of the margin of the eye, where distorted “mini-facets” can be seen, the array of facets is extremely regular. (d) Section through ventral eye (VE) and dorsal eye (DE). The two are divided by a cuticular ridge called the canthus (Ca), below which the retinulae of both eyes almost fuse. Cornea, crystalline cone, clear-zone and rhabdom, all clearly visible, are similar in both ventral and dorsal eye.
168
Fig. 3. (a) Transverse section through the crystalline cone, which is an intracellular product of the 4 cone cells (14). Each cone cell contains 5-6 layers of endoplasmic reticulum ‘near the edge of the cone plus a considerable amount of empty vesicles. The two principal pigment cells (PC, and PCJ do not fully surround the cone cells as in other insects, but leave a gap between them. They contain microtubules and pigment grains. At the distal ends of the cone cells. where their nuclei are located (inset), the pigment cells give rise to a “Star of David” pattern. (b) Size. shape and arrangement of crystalline cones as well as pigment cells are extraordinarily regular. The diameter of the pigment granules themselves, however, varies between 0.3 and 0.9 pm. (c) Longitudinal section through cone and retinula cell bodies (Ret CB) of a light-adapted photoreceptor. There is no significant migration of either cells or pigment on dark/light adaptation.
169
Fig. 4. (a) Nuclei of 7 retinular cells are found on the distal side of the clear-zone. Each group of 7 cells per one ommatidium is surrounded by 6 accessory pigment cells which are easily recognizable by their “pale” appearance and clusters of what appear to be microtubules in transverse section (arrows). (b) The 4 cone cell extensions can be traced down to a level where the clear-zone begins (arrows). (c) Each group of 7 retinula cells crossing the clear-zone, is surrounded by exactly 6 clear accessory cells. devoid of screening pigment.
Fig. 5. (a) On the proximal side of the clear-zone, cell 1 is the first to produce a rhabdomere. The asymmetrical nature of this rhabdomere is seen in this light micrograph. (b) The rhabdomere of cell 1 is relatively short. In it the microvilli are oriented parallel. (c) Cell 1 contributes its rhabdomere to the rectantular shaped rhabdom. but only for a short distance (10pm. corresponding to 20:,0 of the whole rhabdom length). With regard to subcellular organization or microvillus size, cell 1 does not differ from the other retinula cells.
Fig. 6. (a) Just above the rhabdom a maze, making it impossible to follow the outline of individual retinula cells. is created by convoluted and meandering cell membranes. (b) At deeper levels retinula cell borders are more easily traceable. Six retinula cells (2-7) contribute their microvilli to the rhabdom; cell 1 no longer possesses a rhabdomere and occupies a peripheral position in each ommatidium. Six accessory pigment cells are still associated with each group of retinula cells and are easily rccognizable by their round outline and the large number of microtubules they contain (arrows). (c) Meanders of retinula cell membranes and cross section of accessory pigment cell process. containing homogeneously distributed microtubules.
172
Fig. 7. Transverse sections through rhabdoms at different levels. (a) Light micrographs showrng the gradual change from a- more or less rectangular rhabdom to a square frame type a short distance above the basement membrane. Once again, the overall regularity of rhabdom shape and orientation is remarkable. (b) Over most of its length the rhabdom is composed of rhabdomeres belonging to 6 retinula cells. The microvilli of cells 3 and 6 run in the same direction but do not abut on each other. They are separated by the rhabdomeres of cells 4 and 5. and cells 2 and 7. whose microvilli run in an orthogonal direction. All retinula cells contain mitochondria and pigment granules. and form desmosomes (circles). (c) The cytoplasm of the eighth (basal) cell pushes into the rhabdom from below. and gives rise to a rhabdom which resembles a picture frame. The orthogonal arrangement of microvilli is maintained. (d) The eighth cell (8) does not have a rhabdomere of its own. The surrounding microvilli are part of retinula cells 5 and 7, and are closed off at their apices by a cell membrane (arrows).
Fig. 8. (a) All 6 accessory pigment cells can easily be traced to a level just above the basement membrane, where they show up because of their constant number and their “pale” appearance. (b) The basal retinula cell contains mitochondria and pigment granules, and its nucleus is large (N). Some accessory pigment cells (AcPC) are clearly visible. (c) Retinula cell axons of both dorsal eye (below the broken line) and ventral eye make synaptic contacts in the same common lamina. (d) Each axon bundle contains 8 retinula cell fibres. A few tracheoles (Tr) penetrate the fibrous structure of the basement membrane (BM) together with the axons.
Fig. 9. Dioptric structures of the eye under the interference microscope. (a) and (b) Longitudinal sections, 10 nm thick, through the cornea parallel to the ommatidial axis. The different degree of optical compensation in (a) and (b) clearly shows that apart from its outer and inner edge, the cornea is optically homogeneous. (c) Longitudinal 10pm thick section through crystalline cones, showing that the latter are optically non-homogeneous. (d) and (e) Interference micrographs through 10 pm transverse sections of a group of 4 cones. The stepwise compensation under green light, first for peripheral cone areas (d) and then for the centre (c) shows that a strong gradient of refractive index lies in the outer zone that the centre apart from being more homogeneous, has the higher refractive index.
The eye af the dung beetle Euaniticehs facets is regular and the interommatidial angle is 151.8” in the dorsal and 1.8-2” in the ventral eye. Ommatidia in the ventral eye have an average length of 3oO~rn but in the dorsai eye they are slightly shorter (cc_ 250 grn). Cone. pigment cells and clear-zone Below the 60 pm thick cornea, which has an inner radius of curvature of 8 pm, one finds the crystalline cone (Figs. 3a. b.c). Each cone is S0~m long and as in other insects with eucone eyes, is the result of an intracellular secretion of the so-called four Semper cells. The nuclei of these cells occupy the narrow space between cornea and crystalline cone. In cross section the crystalline cones are circular and electron opaque. As in other scarab&d beetles there are 56 concentric layers of endoplasmic reticulum surrounding each cone. The cone cell cytoplasm, compared with that of ~~z~~~~~ur~~~sis rich in empty vesicles and other subcellular components. The crystalline cone cells of insects are usually cIrcumscribed by two principal pigment cells, but in ~~on~rj~.e~~~s the situation is different. Here the two principal pigment cells are relatively small and each of them does not even surround the cone by more than 100 (Fig. 3a). The accessory pigment cells, on the other hand. are well-developed and conspicuous because of their dark pigment granules and regular arrangement (Fig. 3b). They occupy the triangular spaces left where three ommatidia meet, and in transverse section give rise to a pattern around each cone similar to a Star of David. The six accessory pigment cells. thus associated with one ommatidium. can be followed as far down in the eye as the basement membrane In spite of the presence of microtubules in both principal and accessory pigment cells, no appreciable movement of pigment or cells was seen as a consequence of dark~~~ghtadaptation, (For a more detaikd discussion of a~ptational changes and the role of microtubules see WALCOTT,1975.) Screening pigment granules in both principal and accessory pigment cells range in diameter from 0.3-0.9 pm. Euoniticeihts appeared permanently dark-adapted (Fig. 3~). even if exposed to bright light at night. Whether this apparent lack in retinomotor events is a genuine characteristic of the eye. or due to a fixation procedure which was not rapid enough to arrest cellular changes is unknown at this stage. Below the crystalline cane, groups of seven retinula cell bodies are found (Fig. 4a). Each group is surrounded by the six accessory pigment cells, which at this level no longer contain pigment granules, but appear rather empty apart from a few clusters of microtubules. The roots of the crystalline cone cells disappear shortly befare the clear-zone becomes the prominent feature of the eye (Fig. 4b). In the clear-zone the narrow retinula cell columns stain more densely than the surrounding by a variety of methods which stain proteins (Fig. 4~). In transverse section the shape of each column of 7 ceils varies, but the overall arrangement (one column always surrounded by six large accessory pigment cells. and almost always exactly equidistant from neighbouring columns by 20pm) gives this eye an extraordinary order and regularity. surpassing that of other scarabaeids.
Rhabdom
175
layers
the seven retinula cells on the proximal side of the 120pm deep clear-zone in each ommatidium of both dorsal and ventral eye (Fig. 5a). gives rise to a rhabdomere, which has all its microvilli oriented in one direction (Fig. 5b). Only 10pm below this level 4 other retinula cells contribute their rhabdomeres. thus giving rise to a fused rhabdom made up of 5 rhabdomeres in which the microvilli are oriented in 2 orthogonal directions (cells 1. 4. 5 versus cells 3 and 6), and in which retinuia celt I has the largest rhabdomere (Fig. SC). There is no difference in size between microvilli belonging to ceil 1 and those which are part of the other cells; all have an average diameter of 4 pm. The cytaplasm of all retinula cells is crowded with mitochondria, and some granules of screening pigment are also present. Most unusual. however. and in strong contrast to the otherwise extreme constancy and regularity of structural elements in the eye of EuoniticeUus, are the convolutions, twists and meanderings of all retinula cell membranes in this ptane (Fig. 6a). It is impossible to outhne the peripheral boundary of retinula cells or even follow a cell membrane for a short distance. In the vicinity of each rhabdom there are still the 6 accessory pigment cells (Fig. 6b), each densely packed with microtubules of 20-25 nm diameter. but the cell borders of these cells are “‘normal”. and show no trace of any convolution (Fig. 6~). The retinula cell membranes remain rather irmgular over the entire depth of the retina without. however, affecting the consistent pattern of rhabdomercs (Fig. 7a). At a level where cell I has turned into a wide axon, the rhabdomeres of cells ?-,I rearrange to form a rectangular-shaped rhabdom (Figs. 6b. 7b). Microvilii belonging to cells 3 and 6 run in the same direction and form the shorter sides of the rectangle. Separating these two rhabdomeres are those belonging to cells 4.5 and 2.7 whose microvilli run parallel bur at right angles to those of cells 3 and 6. Alignment of microvilli and orientation of the rhabdom rectangles across the entire eye are remarkably regular. and resemble the organization described by WACHMANN and SCHR&R (1975) for the ventral eye of the whirligig beetle. Desmosomes are developed at the edge of each rhabdomere where two adjacent retinula cells meet. The rhabdom gradually changes into ti hollow square, approximately 1Sprn above the basement membrane, where the cell plasma of the 8th retinula cell projeecrs centrdiy from below into the rhabdo~~ (Fig. 7~). This basal cell. which does not appear to have a rhabdomere of its own (Fig. 7d). is surrounded by the microvilli of retinula cells 2- 7. It contains granules of screening pigment (0.6 pm in diameter1 and a large nucleus. Shortly above the basement membrane the six accessory pigment celt~ appear once more. as electron transparent, slightly swoilen cells, of circular outline (Fig. Saf. alternating in position with the seven retinula cells in one ommatidium (Fig. 8b). A few narrow tracheoles reaching the most proximal layer of the rhabdom. penetrate the 3 ~tm thick basement membrane. which is of a “‘fibrous” texture (Fig. 8d) A proper tracheaf tapeturn, howevtr, is not developed. Groups of 8 retinufa cells (one from One of
V. B. MEYER-R• CHOW
176
each ommatidium) pass through the basement membrane as distinct axon bundles, which remain separate for at least 30~. They then combine with adjacent bundles to form greater aggregations (Fig. 8~). No indication was found of the existence of separate laminae, one serving the dorsal, the other the ventral eye. Dioptric apparatus and acuity Sensitivity and acuity, the two most important parameters of vision, depend to a great extent. but not entirely (visual pigment also matters) on the optical qualities and properties of the dioptric system. As in the eyes of Repsimus, Anoplognathus and Sericesthis, the cornea in Euoniticellus is relatively thick and occupies one-fifth of the ommatidial length, but in contrast to the other beetles external facets with individual convex lenses are here developed. With the exception of its outer 6pm and inner 1Opm layers the cornea is optically homogeneous (Figs. 9a, b) and has a mean refractive index of 1.534. The outer and inner edges were found to possess slightly lower values: 1.481 and 1.426 respectively. A cornea1 lens-cylinder is definitely not developed. In both transverse and longitudinal sections through the crystalline cone a radial gradient of refractive index was found (Figs. 9c, d, e). The drop of refractive index from a central value of 1.443 to a peripheral one of 1.374 was not a gradual decrease. but rather a sudden fall near the outer edge of the cone. The refractive indices of clear-zone (1.345) and rhabdom (1.353) were also measured. Encouraged by the results which were obtained from other insects by a method in which a large scale diagram of the eye was used to trace a known number of rays through cornea, crystalline cone, and clearzone, in order to determine the acceptance angle of a single ommatidium, a similar procedure was carried out on Euoniticellus. Together with the morphometric data of the various structures in the eye of Euoniticellus, the refractive index measurements provided the basis for a two-dimensional reconstruction of ray paths within the eye. A good agreement was found between theoretically predicted acceptance angle (from ray-tracing) and experimentally obtained values of the acceptance angle. In spite of its lens cylinder properties in the crystalline cone. the eye of Euconiticellus does not focus a bundle of parallel rays very well; thus, acuity cannot be very high. Ray-tracing shows that the acceptance angle of both dark and light-adapted eyes lies between 25” and 30” (Fig. 10). Animals tested in an optomotor drum at a light level of 800 lx, did indeed show that no response was obtained for black and white equally-spaced stripes with stripe repeat periods less than 30”. At higher stripe repeat periods the response of the clamped beetles did not consist of head turning movements, but of antenna1 movements, although experimental techniques and apparatus were the same throughout. DISCUSSION Although presumably phylogenetically related and, therefore placed in one family by most entomologists, the scarabaeid beetles Repsimus (HORRIDGE and GID-
Fig. 10. An acceptance angle of approximately 26” is derived from counting the number of rays which fall into sectors at the receptor level. representing individual rhabdoms. The procedure is based on measurements of refractive indices in cornea, cone and clear-zone.
1971) Anoplognathus (MEYER-R• CHOWand HORRIDGE, 1975) Sericesthis (MEYER-R• CHOW,1977) and Euoniticellus possess eyes which differ markedly from each other in their anatomy. This one family of beetles exhibits a greater variety of compound eye types than some entire orders of insects have to offer e.g. Hymenoptera (MENZEL, 1972; VARELA and PORTER, 1969; WACHMANN et al., 1973) and Diptera (representatives of 13 families, all with similar eyes, recently studied by WADA. 1974). Because Hymenoptera and Diptera are just as diverse as Scarabaeidae with regard to their requirements and ways of life, e.g. diurnal, crepuscular and nocturnal species, one wonders about the kinds of evolutionary pressure which could have led to the development of so many different types of photoreceptor organization in beetles. It is conceivable that the wide range of eye types does not reflect perfect adaptations, but that on the contrary no single photoreceptive structure has yet been evolved in beetles, capable of functioning under many different conditions. Different anatomies do not necessarily have to imply different functions, and no evolutionary pressure would have been exerted if eyes with different structure functioned equally well. DINGS,
Interspecies comparisons of eye structures Apart from the general organization of insect compound eyes into cornea, cone and retina. the only feature that the 4 species of scarab beetles have in common is the clear-zone. However, even the clearzone is not developed to the same extent in all 4 species, for in Repsimus and Anoplognathus it is very large (cu. 350 pm in depth) whilst in Sericesthis and Euoniticellus it is relatively small (cu. 110pm) even if one takes into consideration the smaller size of the latter two beetles, and their proportionate reduction in eye size. In all four beetles 7 retinula cell bodies per ommatidium are located on the distal side of the
The eye of the dung beetle Euoniticellus clear-zone. In Euoniticellus the spacing of the retinula cell columns crossing the clear-zone, and the arrangement of the surrounding accessory pigment cells, both reach maximum regularity; in the other three species the pattern is far less regular. The differences among the four beetles in rhabdom structure are most surprising, because all four, when mature. can be called “non-diurnal”, and live in an environment which is characterized by low light levels. Euoniticellus is probably the least nocturnal of the four with regard to flying time. Little published information is available on the behaviour of Euoniticellus. but from what is known, it appears that this species, unlike most other dung-beetles, e.g.. Onthophagus (which has a similar eye: MEYER-R• CHOW,unpublished observation). is a diurnal flier (FERFLAR, personal communication). When it emerges from the soil as an adult, it “spends only minutes flying to the next pad, and as soon as it arrives at the dung plunges in and starts tunnelling and shovelling, all below dung” (FERRAR.personal communication). Therefore, apart from the first few minutes of its adult life, most of the life-time of this beetle is spent below. or in. the semi-transparent cow dung, where peculiar light conditions must prevail. The eye of Euoniticellus lacks a tracheal tapetum, but possesses an eighth (basal) cell. which does not have a rhabdomere. Over most of its length the rhabdom is of rectangular shape and consists of 6 rhabdomeres. Towards its distal end the rhabdom is asymmetrical. This is the result of a large rhabdomere belonging to cell 1, in which microvilli are aligned parallel with those of cells 4 and 5. The rhabdomere/ cytoplasm ratio at mid-rhabdom level is 1:2.2. There is no difference in the dimensions of microvilli belonging to cell 1 and those which form part of the other retinula cells. Repsimus. judged by its activity, is mainly a crepuscular beetle. It possesses no basal (eighth) retinula cell, but has a tracheal tapetum which surrounds each rhabdom along its complete length. The rhabdomere/ cytoplasm ratio for one retinula cell halfway down the rhabdom. is approximately 2.5: 1. The rhabdom, cut transversely. is seven-lobed and has no apparent regularity or orientation. Behavioural observations indicate that Anoplognuthus seems to become active later in the evenings than Repsiwtus. An eighth (basal) retinula cell is usually developed, but it always lacks a rhabdomere. The tracheal tapetum reaches only halfway up the rhabdom and the rhabdomere/cytoplasm ratio per retinula cell is approximately 3: 1. The rhabdom in transverse section is seven-lobed, but otherwise has no apparent regularity. Finally, probably the most nocturnal beetle of the four. Srricesthis, also possesses no tapeturn. but has a rhabdom in three tiers. The basal cell gives rise to a small rhabdomere consisting of 9-10 parallel microvilli. At mid-rhabdom level 6 retinuia cells produce a star-shaped pattern in which the rhabdom/ cytoplasm ratio reaches at least 6:1, and the microvilli are oriented symmetrically with respect to a central point in the rhabdom, whilst towards the distal end of the rhabdom a monocellular rhabdom with larger microvilli oriented in 3 directions occupies approximately 409; of the retina.
177
Evolutionary trends and photoreceptor adaptations The retention of at least the basal retinula cell if not its rhabdomere as well. the increase in rhabdom area at the expense of retinula cytoplasm, and the diversification of rhabdom organization appear to be some anatomical consequences of the evolution of scarabaeid beetles towards a more nocturnal way of life. Obviously a larger rhabdom, banked layers of rhabdomere, and a multidirectional organization of microvilli will result in an increase in sensitivity (MEYER-R• CHOW,1977). The lack of a tracheal tapeturn in Sericesthis, usually a characteristic of diurnal insects, could mean that photon capture in the rhabdom layers is so efficient that a reflecting system is not required. However. it is not known whether photoreceptor organizations evolve parallel to an ecological specialization, or whether there is a time-lag, and of what magnitude this might be. Behavioural studies lacking, it is difficult to state whether, for example. Repsimus is on the way to becoming a more diurnal insect, or whether Euoniticellus. in spite of its out-of-sight life in dung and soil, still has a photoreceptor originally developed by its ancestor to suit more diurnal needs. In Euoniticellus the orthogonal and regular microvillus orientation, the rhabdomere: cytoplasm ratio of 1:2.2 and the lack of a tapetum certainly point in this direction. Optics, sensitivity and acuity In those three species in which the dioptric apparatus has been studied the cornea is thick, but optically more or less homogeneous, with a refractive index of about 1.5. The crystalline cone. on the other hand. shows a radial gradient of refractive index with values for the central core of 1.458 (Rrpsimus: MEYERR~CHOW, 1975). 1.442 (Anoplognathus: MEYERR~CHOW and HORRIDGE, 1975) and 1.443 (Euoniticellus) and for the periphery of 1.360 (Repsimus). 1.365 (Anoplognathus). and 1.374 (Euoniticellus). Refractive indices common to all species were also found for clear-zone and rhabdom. As with the eyes of Repsimus, Anoplognathus and presumably Sericrsthis (a species for which no direct optical data are available), the compound eye of Euoniticrllus must be classed as a “partially-focused” clear-zone eye, and as such will undoubtedly exhibit an improved sensitivity at the expense of acuity (DIFSENDORFand HORRIIXE. 1973). The angular sensitivity in Euoniticellus (as inferred to from ray-tracing) is somewhat poorer than that in Anoplognathus. but that Euoniticellus in fact makes use of its visual receptors is demonstrated by its reaction to moving black and white stripes. The lack of adaptational variation in the optomotor reactions of mature Euoniticellus. is perhaps related to the way of life this beetle leads. burrowing in the ground for most of its life, so that it would rarely encounter drastic illumination changes, where adaptational measures were necessary. During the very short swarming period (a matter of minutes: FERRAR. personal communication) adaptational changes may occur, but from the moment the beetle has turned to a life in the dung, its eye appears to become permanently adapted to a low environmental brightness level. and loss of acuity is compensated for by both high absolute sensitivity and the abilitv to resoond to movements of large The - obiccts. _,
178
V. B. MEYER-R• CHOW
Because of its distal location near the top of the proximal, rectangular rhabdom, as well as because of its unidirectionally oriented microviiii, the rhabdomere of cell 1 could act as a placation filter. Polarization sensitivity of primary receptor cells not necessarily leads to a meaningful interpretation of polarization patterns; this would largely depend on the wiring of retinula cell axons in the optic ganglia, but in the simplest possible way a two-channel polarization analyzer could be formed by any two cells with rni~ro~I1~ at right angles. Such a system, whether it be a combination of cell 1 with retinufa celfs 3 or 6, or any Two other features of the eye of ~~o~~~r~~~~i~~ are pair of cells 2-7 with orthogonal microvilli, would. noteworthy: retinula cell I and its rhabdomere. and of course, depend on the regularity of its components the division of the eye into dorsal and ventral regions. and on whether the rhabdom is twisted or not. In There are a few other insects in which divided com- Euoniticellus the latter two requirements are definitely pound eyes occur e.g. male mayflies, a few dipterans. met in favour of PS. but not so in Anoplagnathus some stage beetles and whirligig beetles. Althou~ it with its irregularly shaped rhabdoms. In this latter has not been clearly established why the eye is split species MEYER-RKHOW and HORRIDGE (1975). using into two in any of these, it is generally thought that, intracellular electrophysiological recordings from at least in whirligig beetles, the ventral eye is for single retinuia cell& were unable to find any apprecivision in an aquatic environment, the dorsal for see- able polarization sensitivity. ing in air. There may, ofcourse. be additional reasonsIn conclusion, a comparison between the comand different ones for other species pound eye of ~~on~r~c~~~~sand that of three other In many insects differences between dorsal and ven- scarabaeid beetles, revealed that despite a similarity tmi fmX?tS iiir&tiOII t0 Size (EXNER. 1891). COIOtfr of dioptric systems. considerable anatomical differsensitivity (MENZEL. 1975) and fine structure (SCHINZ, ences exist. How the anatomical diversity in retina 1975) have been reported. Recently WEHNER(1976) organization can be explained in terms of adaptations to different ways of life and distinct habitats is unhas also shown that polarization sensitivity in the ant and bee may well be restricted to a small patch of known at this stage. as there are still not sufficient a few dorsal ommatidia. It is feasible that the comdata to make sensible comparative statements about bination of such differences could have led to a physifunctiona properties such as coiour and polarization cal separation into dorsal and ventral eye. Whether sensitivity, acuity range and absolute sensitivity. physiological differences exist between dorsal and ventral. facets in Euc~niticrl~us remains to be seen. for Acknowltldgpmnrts-The largest part of this research was as in the beetfe Macrogyrus striolatus (HORRIDGE and carried out at the Department of Neurobiology. Australian GIIXXMZ, f971), the anatomy of dorsal and ventral National University, Canberra. For his interest and eye is remarkably similar. fn the whirring beetles encouragement throughout this study f wish to thank Prof. G. A. HORRID~EF.R.S. (Research School of Biological Gyritws ~ril~us and G. s~hstriQtus. WACHMANN and Sciences. Department of Neurobiotogy. Canberra). For SCHX~~ER (1975) find a few structural differences such as a more highly ordered pattern of rhabdoms in the allowing me to use his Philips 200 electron microscope to finish this investigation. I thank Mr. N. H. LAW. Direcventral eye. The ventral eye further distinguishes itself tor of the Meat Industry Research Institute in Hamilton. from its dorsal counterpart by having a paraltel New Zealand. microviiius organization in rhabdomere 1, and by having a longer proximal rhabdom. Wachmann and Scbriiefs results. although seriously hampered by fixation difficulties. show that there are certain similariBIRUKOWG. (1953) Menotaxis in polarisicrtem Licht bei Georrupcs sifvaricus. ~ff~urw~sse~sc~~~en 40, 61 i -42. ties in rhabdom organ~~tion between the eyes of DIESENWRF M. 0, and HORRIDGEG. A. (1973) Two ErtonIticrlius and whirligig beetles. models of the partially focused clear-zone compound There is evidence that some scarabaeids use the eye. Prof. R. Sot. B 183. 141-158. polarization pattern of the sky as a navigational aid EXNERS. (I89f) Dip ~~~~j~~~~~~, dw ~a&~~zj$r~~ A~pn cm ~~IRUKOW, 1953, F~N~E~CH ~‘tat. 1975). In Euc~niKrrhsen und ~nsekc~}i. Franz Deuticke. Leipzig. ric&s for example. the detection of a polarization FERRERP. (1973) The CSIRO dung beetle project. Wooi pattern would be useful during the brief swarming fechnol. Shwp Breed 20. 73-75. flight. enabling the insect to fly in a straight line even FRANTSEVXHL. I., MOKRUSHOVP. A. and ZOLOTW V. V. if the sun is obstructed by a cloud. The finding of (1975) Astroorientation of tehtrus nptrrus Laxm. (Caleoptera. Scarabaeidae). Akad. Nauk SSSR 36. 61-65. a rhabdom in the dung beetle ~u~~it~ce~ius in which GRENACHER H. (1879) Unrersuchungm ii&r das Sehorgan the microvilli are consistently oriented in orthogonal dw Arthropoden insbesondrre drr Spinnen, Insekten und directions, pius the presence of a more distally located Crusraee~n. Vandenhock SCRuprecht. GMtingen. cell with microviili pointing in one direction only. HORRIDCEG. A. (1971) Alternatives to superposition imcould be significant with regard to polarization sensiages in clear-zone compound eyes. Proe. R. SOC.B 179, tivity (PS) in dung beetles. It is now generally thought 97-124. that the basis of PS lies in the paraHel alignment of HORRILXXG. A. and GIDIXNGSC. (1971) Movement on
advantage of a partially focused eye over one with a narrow acceptance angle is to increase the number of impressions summed so that important features stand out, but insistent irregularities in the visual field are smoothed (HORRIDGEand HENDERSON, 1976). Also, in Euoniticellus olfaction. to detect fresh dung, is likely to have taken over some sensory functions and may, therefore. have reduced the importance of vision (.J&scHKE. 1914).
microvilli which cause a similar alignment of visual dipole molecules in the membranes (LAUGHLIN it ai., 1975).
dark-light adaptation in beetle eyes of the neuropteran type. Pour. R. Sot. B 179, 73-85. HOHRKXXG. A.. GIWXNGSC. and STANCEG. (1972) The
The eye of the dung beetle superposition eye of skipper butterflies. Proc. R. Sor. B 182, 457495. HORRIDCEG. A. and HENDERSONI. (1976) The ommatidium of the lacewing Chrpwpa (~europtera). Proe. R, Sot. B 192, 259-27 1. HORRIDCEG. A.. NINHAM V. W. and DIESSENWRFM. (1972) Theory of the summation of scattered light in clear-zone compound eyes. Proc. R. Sot. B 175. 183-194. HORRIDGE G. A.. MCLEANM.. STANCE G. and LILLYWHITE P. G. (1977) A diurnal moth superposition eye with high resolution (Phu~a~~~jf~f~,~ rrisrjfificat. Proc. R. Sot. B (In Press ). J~RSCHKEH. (1414) Die Facettenaugen de; Orthopteren und Termiten. Z. siss. Zoo/. 61, 1533280. LALIC;HLIN S. 9.. MENZ~L R. and SNYDER A. W. (1975) Membranes. dichroism and receptor sensitivity. In Photoreceptor Optics (Ed. by SNYDERA. W. and MENZEL R.). pp. 237-258. Springer, Berlin. MEGGC;ITT S. and Mtutr+Rocnow V. 9. (1975) Two calculations on optically non-homo~cneaus lenses. In 7% Compomd Eye and I ision of fnsrcrs (Ed. by HORRIDGE G. A.). pp. 314320. Clarendon Press, Oxford. MENZEL R. (1972) Feinstruktur des Komplexanges der Roten Waldameise Formica po/Jctrna (Hymenoptera. Formicidae). Z. Zrllforsch, 127. 356-373. MT.NZELR. (1975) Colour receptors in insects. In 7%~ Compmctzd Eye and Vision qf.insrcts (Ed. by HORRI~XXG. A.). pp. 121 153. Clarendon Press. Oxford. MEYER-ROCHOW V. 9. (1972) The eyes of Creuphilus ythroccphalus F. and Sartall~rs signatus Sharp (Staphyhmdae: Coleoptera). Z. Ze//forsch. 133. 59-86. MEYI.R-ROCI~OW V. B. (1973) The dioptric system of the eye of C_vhisrrJr (Dytiscidae:Coleoptera). Proc. R. Sac. B 183. Mr~t R-ROCHOWV. 9. (1975) The dioptric system in beetle compound eyes. In The Compound Eye and Vision qf Lond.
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SCHULTZM. S. f 11168)~Flf~~sff~h~ngn~t7 gcset~tm
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WACHMANN E. and SCHRSERW.-D. (1975) Zur Morphologie des Dorsal und Ventraiauges des Taumelklfers GUYinus ~~~~~rriu[~~ (Steph.) (Coleoptera. Cyrinidae). Zoomorphol. 82. 43 6 1. WACHMANN E.. RIGHTERS S. and SCHRICKER 9. (1973) Feinstrukturen im Komplexauge der Blattschneiderbiene Megachilc, rotunda (F.) (Hymenoptrra. Apidaea Z. Morph. Tie-c, 76. 109. 128. WADA S. (1974) Speziellc randzonale Ommatidien der lung in den Komplexaugen. Z. ;~~r~h. Tirrv 77. 87.-125. WALCOTTB. (1975) Anatomical changes during light adaptation in insect compound eyes. In Thr Compound Eyr and Vision (Ed. by HORRIDGF G. A ). pp. 20-32. Clarendon Press. Oxford. WALCOTTB. and HORRIDT~F. G. A. (1971) The compound eye of Archzchauiiodcs (Megaloptera). Proc. R. Sot. B 179, 65-72. WEHNEK R. f 1976) Polarized-light navigation by insects. Sricvrt. ,4m 235. 106- 115.