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Fine structural description of the compound eye of the Madagascar ‘hissing cockroach’Gromphadorhina portentosa (Dictyoptera... Article in Insect Science · April 2008 DOI: 10.1111/j.1744-7917.2008.00199.x
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-192, of DOI Insect Science (2008)Fine 15, 179 structure the10.1111/j.1744-7917.2008.00199.x eye of hissing cockroach 179
Fine structural description of the compound eye of the Madagascar ‘hissing cockroach’ Gromphadorhina portentosa (Dictyoptera: Blaberidae) Monalisa Mishra1 and Victor Benno Meyer-Rochow1,2 1
Faculty of Engineering and Sciences, Jacobs University (formerly known as International University Bremen), Bremen, Germany, and Department of Biology (Eläinmuseo), University of Oulu, Oulu, Finland
2
Abstract The compound eyes of the wingless adults of the Madagascar‘hissing cockroach’ Gromphadorhina portentosa Sachum, 1853 were examined by light and electron microscopy. Each eye contains 2 400-2 500 mostly hexagonal facets. However, irregularities affecting both shape and size of the ommatidia are relatively common, especially towards the margins of the eye. An individual ommatidium of this eucone type of apposition eye contains eight retinula cells, which give rise to a centrally-fused, tiered rhabdom. The distal end of the latter is funnel-shaped and accommodates the proximal end of the cone in its midst. Further below, the rhabdom (then formed by the rhabdomeres of four retinula cells) assumes a squarish profile with microvilli aligned in two directions at right-angle to each other. Cross sections through the proximal regions of the rhabdom display triangular rhabdom outlines and microvilli (belonging to 3-4 retinula cells different from those involved in the squarish more distal rhabdom) that run in three directions inclined to one another by 120° . Overall the organization of the eye conforms to the orthopteroid pattern and particularly closely resembles that of the American cockroach Periplaneta americana. However, since G. portentosa possesses fewer ommatidia, this could be a consequence of its inability to fly. On the other hand, the large size of the facets and the voluminous rhabdoms suggest considerable absolute sensitivity and an ability to detect the plane of linearly polarized light. Based on the pattern of microvillus orientations in combination with the crepuscular lifestyle G. portentosa leads and the habitat it occurs in, the prediction is made that this insect uses its green receptors for e-vector discrimination in the environment of down-welling light that reaches the forest floor. Key words apposition, blattodea, closed rhabdom, ommatidium, polarization, vision
Introduction If the number of species is used as a criterion, then cockroaches reached their evolutionary climax approximately 250 million years ago in the Upper Carboniferous.
Correspondence: Victor B. Meyer-Rochow, Faculty of Engineering and Sciences, Jacobs University (formerly known as International University Bremen), P.O. Box 750561, D-28725 Bremen, Germany. Tel: +49 421 2003242; email:
[email protected]
Their numbers have declined ever since (Carpenter, 1930), but in spite of this decline cockroaches must still be regarded a highly successful group of insects, having adapted to almost every conceivable type of terrestrial ecological niche (Roth & Willis, 1960). There are 4 000 to 5 000 described species of cockroaches today (Roth, 1970), placed into 440 genera (Princis, 1960). The family Blaberidae, originally established by McKittrick (1964), contains 11 subfamilies (Grandcolas, 1997). All members of this family are commonly known as giant cockroaches. The Madagascar hissing cockroach (Gromphadorhina portentosa Schaum, 1853) is a member of the family Blaberidae.
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Both males and females of G. portentosa are wingless and can reach a total body length of around 5 cm. Sound production in this insect is associated with aggressive (Clark & Moore, 1994; Clark & Moore, 1995) and courtship behavior (Clark et al., 1995). This cockroach has recently been gaining importance as a pet and entertainment insect in museums and insect exhibitions and as a laboratory animal for behavioral and physiological studies (Carrel & Tanner, 2002). It is now also widely being used in insect anatomy classes. Besides its considerable popularity, little attention has been paid to the structure and function of its compound eye. Photoreceptor studies in cockroaches are of interest for several reasons. First, these evolutionarily old insects can be expected to possess features that in more‘modern’insects have become lost or modified during evolution. Second, since large cockroach species with wings (e.g., Periplaneta americana) and without wings (e.g., G. portentosa) exist, one could investigate through inter-species comparisons whether an inability to fly resulted in modifications to eye anatomy and ultrastructure as has been shown for wingless mutants of Drosophila (Lin et al., 2004). Third, all cockroaches investigated to date, possess apposition eyes, which are photoreceptors most commonly encountered in daytimeactive insects. Yet, most cockroach species are nocturnal or darkness-loving creatures. G. portentosa is no exception, and therefore, a study of its eyes ought to provide us with clues as to how apposition eyes can be designed to function well under dim environmental conditions. With their millions of years of selection behind them, cockroaches ought to be prime candidates for such an enquiry. Finally, a point of interest in this kind of study is, furthermore, the large body size of G. portentosa. The optical properties of a compound eye are largely dependent on the dimensions of the eye and its structural components (Nilsson, 1990; Rutowski, 2000). Insect eyes are generally both within (Zöllikofer et al., 1995) and across species (Jander & Jander, 2002) scaled to body size (Land, 1981), so that bigger insects tend to have more ommatidia per eye, larger facets (and hence greater overall sensitivity), but smaller interommatidial angles (and hence improved visual resolution: Wehner, 1981; Zöllikofer et al., 1995; Jander & Jander, 2002). As the Madagascar hissing cockroach is large as well as wingless and nocturnal as well, it seemed an interesting undertaking to examine its eye’ s organization and ultrastructure.
Materials and methods Ten adult specimens of Gromphadorhina portentosa Schaum, 1853, ranging from 4.2 to 4.5 cm in total body size
were used in this study. The individuals were decapitated during the day at around 12.00 h. Their severed heads were split in half along the eye’s sagittal plane and fixed for 1 day in a cold mixture of 2% paraformaldehyde and 2.5% glutaraldehyde, buffered in 0.1 mol/L cacodylate to a pH of 7.4. Following two washes in 0.1 mol/L cacodylate buffer, the specimens were then fixed for 1 h in 2% cacodylatebuffered OsO4. After three brief rinses in the same buffer and two in distilled water, the specimens were passed through a graded series of ethanol, before becoming immersed in acetone/Epon mixture (50:50) for 1 day. Finally, the specimens were embedded in pure Epon resin and hardened for 3 days at a temperature of 60 oC. Semi-thin sections for light microscopy were cut on an ultramicrotome (RMC) with a glass knife and stained with 0.5% aqueous solution of toluidine blue on a hot plate for a few seconds. Ultrathin sections were cut with glass or diamond knives and picked up on uncoated 300-mesh copper grids. The ultrathin sections were stained with Reynolds’ lead citrate for 20 minutes and 2% aqueous uranyl acetate for 15 minutes and finally observed under a Zeiss EM 10 transmission electron microscope, operated at 60 KV. For observations by scanning electron microscopy (SEM), eyes were removed from freshly-killed cockroaches with a razor blade and afixed on sticky cellotape. The eyes were then air-dried, coated with a thin layer of gold-palladium and viewed under a scanning electron microscope. On the SEM photo, a 1 mm2 area of the eye was marked and all ommatidia inside this area were counted. Facet diameters (i.e., corner to corner distances of the hexagonal lenses) were determined from 15 randomly selected ommatidia. Photos of each eye were scanned into a computer in order to measure eye surface areas with an imaging programme (Image J). The total number of ommatidia per eye was extrapolated from the count of the 1 mm2 area. The error due to minor variations in facet sizes and shapes was regarded as negligible.
Results External features The two large compound eyes of G. portentosa occupy dorso-lateral positions on the head with most of the posterior edge of the eye running parallel to the posterior wall of the head capsule. As with Periplaneta americana (Butler, 1973a), the opisthognathous resting position of the head in G. portentosa results in a tilt of the main axis of the eye of approximately 55°from the longitudinal axis of the animal. An‘equator’that separates, dorsal-ventral mirror image patterns of facets as, for example, in fly eyes (Meinertzhagen,
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Fig. 1 Scanning electron micrographs of the compound eye of G. portentosa. A. Whole eye with facets not well aligned in definitive rows. B. Hexagonal facets and randomly distributed peg-like protrusions on the eye’ s surface. C. Marginal ommatidia with less regularly arranged facets. D. Interommatidial protrusion at higher magnification, showing absence of any hair-like features and possibly representing a waxy secretion.
1972), was not developed, but left and right eyes were mirror images of each other. The compound eyes of 4.2 to 4.5 cm-long specimens of G. portentosa have a maximum extension (dorso-ventral axis) of approximately 3.4 mm, contain 2 400-2 500 ommatidia, and are‘hatchet’-shaped with the‘handle’ pointing ventrally (Fig. 1A). Differences between male and female antennae were described by Slifer (1968), but with regard to the eyes no evidence for a gender difference was found. The cuticular corneal lenses are biconvex throughout, but considerably less curved externally than internally (Fig.1A). SEM observations reveal that in the
apical, ventral region of the eye the ommatidia are hexagonal (Fig. 1B) with centre to centre distances of at least 45 μm. Although facet sizes do not seem to vary greatly between the wider dorsal and the narrower, ventral eye region, laterally facets with pentagonal or irregular outlines are common (Fig. 1C). The ommatidia are arranged in rows, but owing to the curvature of the eye and its unusual non-spherical shape, the rows are not always regular and sometimes two adjacent rows may accommodate a new row of facets in their midst. High magnification micrographs show that the corneal surfaces are smooth and without corneal nipples (Fig. 1C). However, a few
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interommatidial featureless protrusions (arrow in Fig. 1B), developed as short pegs of approximately 3.5-4.5 μm height (Fig. 1D) and in P. americana interpreted by Butler (1973a) as corneal hairs, are present. It is possible that these protrusions and the associated holes in the cuticle represent interommatidial exocrine glands, recently described by Müller et al. (2003a) from the compound eyes of Chilopoda. The curvature of the eye surface, and, thus, the interommatidial angles between the facets, vary depending on where and how the measurements are taken. The longest ommatidia are present in the centre of the wide dorsal eye region and the shortest near the ventral apex of the eye. Inter-ommatidial angles are much narrower when determined from facets along the eye’ s dorso-ventral axis than if the measurements stem from adjacent ommatidia in an anterio-posterior direction, irrespective of whether one chooses the dorsal bulkier or the narrower ventral region of the eye. The overlapping visual fields of individual ommatidia, therefore cannot be circular, but must be oval. Internal organization Ommatidial units consist of the dioptric apparatus (made up of the cornea and four crystalline cone cells) and the light-perceiving structures, that is, the photoreceptive cells. Furthermore, each ommatidium contains a pair of primary pigment cells as well as some secondary pigment cells. A longitudinal section through an ommatidium is shown as a semi-schematic sketch in Figure 2 and as a light micrograph in Figure 3A with transverse sections at various levels indicated in Figures 3B-K. Cornea The biconvex cornea, thought to be the secretary product of the two primary pigment cells, possesses a diameter of approximately 45 μm and outer and inner radii of curvature of >100 μm and 20 μm, respectively. Numerous layers of chitin lamellae (Fig. 4A), varying in thickness from 80 nm in the centre of the cornea to 70 nm in the interommatidial regions, are discernable. In longitudinal sections the laminations appear strongly curved, resembling a series of parabolas ca. 0.15 μm apart. In sections prepared for light microscopy the distal layers of the cornea stain less intensely than the proximal ones. Crystalline cone and cone cells The inner surface of the cornea is developed into a short but strongly bulging corneal cone that is separated from the underlying four cone cells by some thin, distal extensions of the two primary pigment cells that surround the cone
Fig. 2 Semi-schematic drawings of G. portentosa ommatidium: longitudinally sectioned on the left and in transverse sections on the right. Abbreviations: c = cornea; cc = cone cells; ppc = primary pigment cells; spc = secondary pigment cells; rh = rhabdom; rcn = retinula cell nuclei; bm = basement membrane; ax = axons.
cells. The cone cells, whose bean-shaped, almost 15 μmlong nuclei with dark karyoplasm are placed distally (Fig. 4B), give rise to a composite crystalline cone with characteristics that approach the eucone condition (cf. Grenacher, 1879). The cone lies below the corneal cuticle and shows some cytoplasmic variation from the distal to proximal end. Although circular in cross section and made up of four cells throughout, distally not all four cone cells contribute equally (Fig. 4B). Further proximal, the cones are made up of four quarters, with each cone cell contributing an equal share (Fig. 4C). Although poorly endowed with organelles, the cones are more electron dense than the surrounding cytoplasm of the cone cells, which contains microtubules, microfilaments and some cisternae of rough endoplasmic reticulum. Quite
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Fig. 3 Light micrographs of an ommatidium of G. portentosa in A. longitudinal perspective with representations of transverse sections at different levels labeled B-K on the left side and abbreviations of the structural elements on the right side of Fig. 3A. The dioptric apparatus consists of cornea (c) and crystalline cone (cc), the latter being surrounded by two primary pigment cells (ppc). Each primary pigment is surrounded by 12 secondary pigment cells. Towards the proximal end of the cone the rhabdomeres of four distal retinula cells form an open rhabdom (rh) around the cone. Below the cone a centrally fused rhabdom of square outline in transverse section appears at the level of some retinula cell bodies with nuclei (rcb). Proximally the square rhabdom turns into a triangularly shaped rhabdom, formed by the remaining retinula cells. Four narrow cone cell extensions (cce) run from the crystalline cone to the proximal retina, where they widen again. Axon bundles, originating from the eight retinula cells of an ommatidium, pass through perforations in the basement membrane.
frequently one or two of the four cone segments stains more intensely than the others. The reason for this phenomenon (which has also been reported from other apposition eyes: Skrzipek & Skrizipek, 1971) remains unknown.
The cones measure approximately 26-30 μm in diameter at their widest part and have a length of approximately 40 μm. As with corneal thickness, cone lengths depend on ommatidial size. Before the proximal tip of the cone is
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Fig. 4 Transmission electron micrographs of sections through the dioptric apparatus of the eye of G. portentosa. A. Longitudinal section showing part of the cornea (c) and cone (cc). The cone is surrounded by the primary pigment cells (ppc). B. Transverse section of the cone (cc) showing unequal contribution of the cone cells surrounded by the nuclei of the primary (nppc) and accessory (napc) pigment cells. C. Distal region of the cone (cc) showing quadri-partite cone surrounded by primary and secondary pigment cells with their granules. D. One (of four) cone cell extensions (cce), containing microtubules, at higher magnification between two retinula cells. Desmosomes (des) near the junction with the rhabdom (rh) between neighbouring retinula cells and pigment granules (pg) are visible.
reached, each cone cell splits and sends a thin‘cone cell root’as far down as to the basement membrane, passing in the narrow inter-cellular gaps between the retinula cells (Fig. 4D). Four of the latter have their distal ends push into the spaces between the primary pigment cells and the cone (Fig. 5A). Surrounding the cone in this way on four sides, these four distally-placed photoreceptive cells develop a square rhabdom fringe around the cone (Figs. 5B,C). In this kind of‘open rhabdom’the centre space is occupied by the proximal end of the cone and the microvilli on the
outside of it are arranged in orthogonal directions. At their terminations near the basement membrane the cone cell roots enlarge again and their cytoplasm becomes electron dense, and containing screening pigment granules as well as microtubules (Fig. 5D). Primary and secondary pigment cells The two primary pigment cells, which are in direct contact with the underside of the corneal cuticle (Fig. 3C),
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Fig. 5 Transmission electron micrographs through transition zone between cone and rhabdom. A. The first sign of the rhabdom appears around the periphery of the cone (arrows). Note the size difference between pigment granules of primary (ppc) and retinula pigment cells (rpc). B. Transverse section showing rhabdom microvilli (rh) on the outside of the cone (cc) on four sides. C. Transverse section through proximal region of the cone (cc) showing formation of an open rhabdom that envelopes the cone. Laterally displaced cone cell roots (arrow) are noticeable. D. Cone cell processes re-unite below the rhabdom and form a cap-like structure at the proximal end of the rhabdom. The size difference between the grains of retinal pigment cells and secondary screening pigment cells is obvious.
form a sleeve around the distalmost two-thirds of the four cone cells (Fig. 4B,C). Small osmiophilic aggregations within the first endocuticular lamella strengthen the connection between the cornea and the underlying corneogenous cytoplasm. Numerous screening pigment granules are present in both primary and secondary pigment cells, but the grains of the primary pigment cells, measuring 0.8-1.7 μm in diameter (Fig. 4A-C), are slightly larger than those of the secondary pigment cells and more than twice as large as those of the retinula cells (Fig. 5A).
An average of 12 secondary (also known as accessory) pigment cells, shared between neighboring ommatidia, can be counted around the cone cells of a typical hexagonal ommatidium (Fig. 4C). The small nuclei of these cells are positioned in the distalmost region of the cell. The electron-opaque screening pigment granules of the secondary pigment cells are only marginally smaller than those of the primary pigment cells, but noticeably larger than those of the retinula cells, which measure only 0.50.9 μm in diameter (Fig. 5A,D). Whether all or just some
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Fig. 6 Transmission electron micrographs through the rhabdom of G. portentosa. A. Transverse section through nuclei (n) of some of the retinula cells. All eight retinula cells contain retinal screening pigment granules at this level. B. Higher magnification of the rhabdom showing that mostly four rhabdomeres make up the rhabdom with microvilli neatly arranged in two orthogonal directions. C. Transverse section through mid-rhabdom region, where the rhabdom changes its shape from square to triangular. D. Higher magnification of rhabdom, showing microvilli arranged in several directions, because of the contributions of the rhabdomeres of the remaining retinula cells. Note the desmosomes (arrows) between neighboring retinula cells.
of the secondary pigment cells reach the basement membrane could not be determined, but there is no doubt that some screening pigment cells were present just above the basement membrane (Fig. 5D). Based on the size of their pigment grains, these cells do not seem to be identical with the secondary screening pigment cells further distal and thus appear to represent a special type of secondary pigment cell, occurring just above the basement membrane.
Retinula cells and rhabdom Altogether eight retinula cells per ommatidium, arranged in two tiers of four each, are present. Transversely sectioned rhabdoms exhibit three distinct shapes: in the distalmost region the rhabdoms resemble a square pictureframe, surrounding the centrally-placed cones (Fig. 5C). Deeper into the retina, the rhabdoms then turn into square columns with microvilli filling the entire cross section and
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Fig. 7 Transmission electron micrographs through the proximal region of the retina, showing in A. the nuclei of the proximal retinula cells and the triangularly shaped rhabdom that the latter form in their midst. B. Higher magnification of the rhabdom with typical orientation of the microvilli. C. Longitudinal section through most proximal retinal region, showing basement membrane (bm), absence of rhabdom and axons (ax). Some tracheoles (tr) are present. A nucleus (n) seen at this level may belong to a supporting/glial cell. D. Transverse section through axon bundle, containing eight axons (ax) with neurotubules (n), some mitochondria (mt) and the occasional pigment granule.
further proximally rhabdom outlines become triangular. The distal retinula Distally only four retinula cells are involved in surrounding the proximal two-thirds of the cones to form a square, picture-frame-like rhabdom around them (Fig. 5C). The highly regular microvilli of the contributing rhabdomeres are arranged in such a way that those of the retinula cells on
opposite directions have microvilli oriented in the same direction, but at right-angle to the microvilli of the other contributing cells (Fig. 6A,B). Thus, a rhabdom is created that at its most distal end appears“open” , although further proximally the rhabdomeres first begin to touch each other, and then ultimately create a centrally-fused rhabdom. Nowhere in the eye of G. portentosa a truly “open” rhabdom, in the way it occurs in the eyes of most Diptera (Trujillo-Cenoz & Melamed, 1966) or cucujoid beetles
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(Wachmann, 1977), is present. At the same time over a considerable distance the rhabdoms are also not solidly fused like those of numerous beetles (Gokan & MeyerRochow, 2000). As the centrally located cone diminishes in size and eventually disappears completely from the centre of the rhabdom, the microvilli gradually increase in length from approximately 0.7-0.9 μm near the rhabdom’ s distalmost end to maximally 2.5 μm further proximally, where the rhabdomeres unite to create a fused rhabdom that can have a diameter of up to 6.50 μm. The cytoplasm of the distally placed retinula cell is rich in multivesicular, lysosomal, and numerous residual bodies. Besides these organelles, numerous pigment granules and endoplasmic reticulum (ER) are found in the retinular cell cytoplasm. The smooth ER occurs either as a hardly visible system of submicrovillar cisternae (smER after Bedini, 1968) and perirhabdomeric ER or as a so-called “sunsurface ER”(ssER after Bähr, 1971) whose channels are arranged along the peripheral plasmalemma (Fig. 6A, C). Easily identifiable perirhabdomeric maculae adherentes (also known as‘desmosomes’) ensure stable cohesion between neighbouring retinula cells (Fig. 6D). The proximal retinula More proximally, that is, below the cones, the rhabdom is fused (Fig. 6A-D) and, still being formed mostly by the same four retinula cells that were first seen around the proximal ends of the cones, it now has a diameter of 6.50 μm. In transverse sections the rhabdoms have square outlines and their microvillar orientations remain the same as seen further distally (Fig. 6A,B). Rhabdom diameters and microvillar orientations only begin to change when in the mid-rhabdom transition zone the remaining rhabdomeres begin to participate in the formation of the rhabdom (Fig. 6C,D). Eventually the remaining four and in the end only three retinula cells take over and between them produce a fused triangular-shaped rhabdom with maximum sidelengths of 4.5 μm and maximum microvillar lengths of 2.3 μm (Fig. 7A,B). Both distal and proximal microvilli are of the same diameter (80 nm) and stain equally intensively with toluidine blue (for light microscopy) and lead citrate (for electron microscopy). Perirhabdomeric ER is more frequent around the edges of the proximal rhabdomeres, but generally the same organelles, known already from the cytoplasm of the distal retinula cells, are present in the proximal cells. The number of pigment granules in them increases towards the basement membrane. Throughout their lengths the retinula cells are accompanied by: (i) the thin cone tracts of the cone cells, which occupy the narrow inter-retinular spaces; and (ii) the thin sheaths of secondary, accessory pigment cells. As the
rhabdoms approach the basement membrane, they decrease progressively and 4-6 μm above the basement membrane the rhabdoms disappear completely (Fig. 7C). At this level the eight retinula cells turn into axons and, becoming embedded between the widening terminations of basal or interommatidial pigment cells, penetrate the basement membrane in distinct bundles of eight (Fig. 7D). The basement membrane separates the region of the eye from the adjacent neuropil and other non-optical tissues of the head capsule (Fig. 7C). It represents the most proximal surface of an ommatidium to which retinal and dioptric elements can be attached. It consists of an extracellular and cellular portion and contains the swollen proximal processes of the cone and secondary pigment cells. Apart from the axon bundles, some underlying muscle fibres and possibly basal or glial cells as well as the occasional tracheole are visible. The entire basal lamina is approximately 4 μm thick and apparently made up of a dense mat of collagen fibers and microfilaments.
Discussion Our study of the eye of the giant Madagascar ‘hissing cockroach’Gromphadorhina portentosa has to be seen in the context of photoreceptor studies of other orthopteroid insects and in particular other Blattodean species. Our ultrastructural investigation of the eye of G. portentosa provides further evidence for the view that phylogenetically ancient insects, like orthopteroids, share a basic compound eye organization, which, for example, is to some extent even preserved in the compound eye of Scutigera coleoptrata (Müller et al., 2003b), representing a different branch of tracheate lineage. On the basis of earlier reports on the eyes of Blattodea (Butler, 1973a,b; Nowel, 1981), Isoptera (Horridge & Giddings, 1971), Embioptera (Nagashima & MeyerRochow, 1993), Notoptera (Grylloblattodea: Gokan et al., 1979), Dermaptera (McLean & Horridge, 1977), Plecoptera (Gokan & Nagashima, 1979; Nagashima & Meyer-Rochow, 1995), Orthoptera (Horridge, 1966; Wachmann, 1970; Burghause, 1979; Horridge et al., 1981; Hoff, 1985), and Phasmida (Meyer-Rochow & Keskinen, 2003), we are now in a position to list some compound eye features that are shared between all of them and G. portentosa. These features include the presence of: (i) mostly hexagonal facets, but irregularly shaped ones, especially along the anterior, dorsal and ventral edges of the eye; (ii) an apposition type of eye with eight retinula cells per ommatidium; (iii) a centrally fused, tiered rhabdom (whose distal,
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funnel-shaped end accommodates in its midst the proximal end of the cone), which then changes into a rhabdom of squarish cross-sectional profile (made up by four or five rhabdomeres of corresponding retinula cells), and further proximally assumes a triangular profile (created by mainly three or four rhabdomeres belonging to retinula cells different from those involved in the more distal, squarish rhabdom), in which the microvilli are offset to one another by 120° ; (iv) two primary pigment cells that surround the tetrapartite cones and with some distal pigment-free cytoplasmic extensions that may squeeze into the narrow space between cornea and cone; (v) numerous accessory pigment cells with pigment granules of somewhat smaller diameter than those of the primary pigment cells; (vi) cone cell roots that branch off distally from the cone cell bodies (usually one per cell) and then run along towards the basement membrane in the intercellular spaces between adjacent retinula cells; and (vii) separate bundles of eight axons, which pass out of the retina through distinct perforations of the basement membrane. A tracheal tapetum or extensive tracheal sheaths around the retinula cells like those often seen in the eyes of nocturnal Neuroptera, Lepidoptera and Coleoptera (Seitz, 1978; Carlson & Chi, 1979; Ribi, 1979; Gokan & MeyerRochow, 2000) are not developed. Likewise, corneal nipples, known to help absorb up to 4% more light in photon-starved insects by acting as an impedance-matching system (Greiner et al., 2004; Stavenga et al., 2006), are absent. The features listed above, being characteristic of the eyes of orthopteroid insects, can be expected to have accompanied the evolution of the various orthopteroid insect groups from the times of their origins and, having thus been preserved since ancient times, to provide us with an idea of how the compound eyes of the first terrestrial arthropods must have looked. The next question to be answered is how the eye of G. portentosa serves this large and wingless species and how it differs from that of other insects, in particular fully winged species. The only other species of cockroach, whose eyes have been examined in detail, is a species that does have wings and can fly: the American cockroach Periplaneta americana (Butler, 1973a, b; Nowel, 1981). The latter species reaches an average length of 4 cm and is therefore only marginally shorter than the average G. portentosa. However, the eye of an adult P. americana can contain over 3 500 ommatidia (Nowel, 1981), while an almost 5 cm-long G. portentosa merely reaches a figure of 2 500 ommatidia (this paper). Moreover, if we compare the ommatidial addition ratio between first instar and adult, we
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find a 35-fold increase in the number of ommatidia in P. americana, an approximately 10-fold increase in G. portentosa, but only a 3-fold increase in the stick insect Carausius morosus (Meyer-Rochow & Keskinen, 2003), the latter admittedly not a cockroach, but a large orthopteroid, nevertheless. Another large orthopteroid, the praying mantis, appears to have even more ommatidia in its eye than any of the aforementioned species (Barros-Pita & Maldonado, 1970). What does this tell us? It suggests that a large predatory, flying insect (like the praying mantis) needs more ommatidia than the flying, but non-predatory P. americana. However, the latter has more ommatidia than the flightless G. portentosa, a nocturnal scavenger. Thus, vision seems least important (if one uses the number of ommatidia as a criterion and, by extension, the overall size of the compound eye) to a slow-moving, wingless leaf-eater like the stick insect. However, not only the total number of the ommatidia is important: sizes and shapes also matter and the ommatidia in G. portentosa adults clearly reach a larger size than those in the P. americana eye. Functionally, the eye of P. americana belongs to the group with“slow type responses”, based on Autrum’ s (1950) original hypothesis that in“slow type”eyes the cells of the lamina are too far away from the retina to contribute to the electroretinogramme. Although retina-lamina distances in G. portentosa were not investigated, it would be extremely unlikely to expect retina-lamina distances in G. portentosa to be smaller than those of P. americana. In fact, because of the larger body size of G. portentosa retina-lamina distances are more likely to be larger as well. In species with apposition eyes and identical ommatidial structures and interommatidial angles, those that look for prey in dim light need larger corneal lenses to provide more efficient contrast transfer than those that hunt in bright light (Bauer & Kredler, 1992). Although ommatidial diameters are generally larger in nocturnal insects (Horridge, 1978; Land, 1989; Jander & Jander, 2002), one must also not forget the well-known phenomenon of isometric corneal diameter increases in arthropod eyes in relation to body size (Eguchi et al., 1989; Meyer-Rochow & Keskinen, 2003; Keskinen & Meyer-Rochow, 2004). Thus, the presence of wider facets alone in G. portentosa cannot tell us conclusively whether or not this insect has an eye of higher sensitivity than, for example, the American cockroach with its smaller but more numerous facets. On the other hand, it is known that a regular array of facets is, generally speaking, advantageous for vision (French et al., 1977). Yet, in both cockroach species under discussion facet irregularities are surprisingly common, which has recently prompted Heimonen et al. (2006) to search for possible benefits of this facet variability, assuming that insect eye morpholo-
© 2008 The Authors Journal compilation © Institute of Zoology, Chinese Academy of Science, Insect Science, 15, 179-192
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gies must have been shaped by evolution to match behavior and lifestyle (Mosler et al., 2004). In mosquitoes, nocturnally active species possess ommatidia, which are larger than those of diurnal species (Land et al., 1999; Kawada et al., 2006), but in addition to the ommatidial size difference, other modifications that improve the function of the compound eye at night have been described. These include rhabdomeres that envelope the proximal ends of the cones (seen also in the nocturnal apposition eye of Scutigera coleoptrata: Müller et al., 2003) and rhabdoms of wider diameters than those seen in apposition eyes of diurnal insects. Since these criteria are met in the eye of G. portentosa to a greater degree than in the eye of P. americana, we can conclude that an individual facet of the eye of G. portentosa would have a greater lightgathering capacity than one in the P. americana eye. On the other hand, the smaller ommatidia in P. americana ought to be able to provide this species with somewhat better resolving power (Warrant & McIntyre, 1993), a feature more useful to a flying insect than a wingless species. The greater number of ommatidia, furthermore, should offset the disadvantage of their smaller size, and thus, provide the eye as a whole with adequate sensitivity. In both species, shape and position of the eyes on the head are nearly identical. For this reason, the calculations by Butler (1973a) of the visual overlap between left and right eyes and the geometrically determined composite fields of view can be regarded to apply equally to the two species under discussion. However, another feature common to both species, which to date has not adequately been explained, is the relatively regular arrangement of the rhabdom microvilli, namely in orthogonal directions across the distal region of the rhabdom and in three directions, offset by 120°to one another, more proximally. This regular alignment is so striking that it must have some fundamental function. An essential requirement for polarization sensitivity is an arrangement of microvilli, in which the latter run either in orthogonal directions or in directions offset to one another by 120°(Horvath & Varju, 2003). In order to unambiguously determine the orientation of the e-vector, microvilli had better be aligned in three directions of 120° difference from one another (Kirschfeld, 1972). However, to optimize polarization sensitivity throughout the day and under different environmental conditions, spectrally different photoreceptors would be needed. For example, perception of polarization under cloudy skies would be most advantageous in the UV-blue range of the spectrum, but green sensitivity of polarization detectors would be a more useful asset in an environment dominated by downwelling light under canopies during sunset (Hegedüs et al., 2006).
Since it has been known for a long time that cockroaches possess green and UV receptors in their eyes (Mote & Goldsmith, 1971; Butler, 1971), it would seem that in the eyes of these insects both cell types are involved in e-vector detection, but at different times of the day. It also suggests that polarization sensitivity is an archaic trait, not necessarily linked to orientation flights of flower-seeking insects in sunlight (like, for example, bees and other diurnal insects: Wehner, 1981; Horvath & Varju, 2003), but equally useful for scavenging insects that live on the forest floor and become active when it gets dark.
Acknowledgments We wish to thank Dr. H. Schikora for advice on rearing of the insects and we wish to express our gratitude to the Electron Microscopy Unit, run by Prof. W. Heyser of the University of Bremen, for access to their facilities. Finally, we would like to thank Stanley Ting Fan Lau and Iikka Salmela for fruitful discussions on cockroach eyes and visual properties.
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Accepted October 8, 2007
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