Compound Eye Miniaturization in Lepidoptera: a comparative morphological analysis

Superposition and apposition compound eyes are commonly associated with moths and butterflies, respectively. However, recently intermediate eye designs, combining features of both apposition and superposition eyes were found in tiny insects. Here, we examine the eyes of 12 species of moth, ranging from 1.88 to 6.03 mm body size, by scanning and transmission electron microscopy. Correlations between body and eye sizes are discussed with regard to the eyes' functionality. Although all of the species shared an ommatidial organization characteristic of pterygote insects, three optical designs were found: (a) an apposition eye, (b) an eye resembling apposition eyes, but with a unique crystalline cone, and (c) an eye intermediate in structure between apposition and superposition eyes. Our comparisons also revealed a new type of basal matrix for the Lepidoptera. The results show that in most of the examined compound eyes (with the exception of the apposition eye of Micropterix aruncella), a clear distinction between apposition and superposition eyes is not feasible. Due to functional morphological constraints as a consequence of miniaturization, evolutionary transformations from superposition into apposition optics may have occurred several times independently in various ‘microlepidopteran’ taxa. The Phyllonorycter medicaginella eye appears to illustrate this evolutionary scenario best.     

Neither apposition nor superposition: the compound eyes of the Chestnut Leafminer Cameraria ohridella

The two lemon-shaped compound eyes of the moth Cameraria ohridella measure in dorsal–ventral direction 263.0 μm in male and 238.9 μm in female individuals. In anterior–posterior direction no significant differences were found between the sexes, eye length being about 194.6 μm. The eyes of males consist of ca. 417 hexagonal facets, while those of females contain 367. In both sexes facet diameters are approximately 11.5 μm. Despite the size differences of the eyes in the two sexes, ultrastructurally they are identical and both possess ommatidia of 80 μm mean length. The ultrastructure of the eye is described and compared with that of other compound eyes of Lepidoptera. Anatomically the eyes represent a type intermediate between apposition and refractive superposition kind. A distal rhabdom is present in the space that in the eyes of larger moths with superposition optics is occupied by the so-called clear zone. A tracheal tapetum and longitudinal screening pigment migrations, typical of superposition but not apposition eyes are present despite the lack of a clear zone. Thus, our results support an earlier calculated minimal theoretical limit for superposition eyes.     

Ontogeny and optics of the eyes of the common prawn Palaemon (Palaemon) serratus (Pennant, 1777)

A brief review of the work on crustacean compound eyes is given. Two main types of eye have been recognized: apposition and superposition. The ontogeny of the eyes of the common prawn Palaemon serratus is examined using a variety of methods: photography of live specimens, histological sections, SEM and TEM. In common with other decapod larvae, the common prawn hatches with apposition eyes having circular lenses packed hexagonally. After metamorphosis the gradual squaring of the eye facets, begun during the larval phase, is completed. This is an essential prerequisite for the functioning of the facultative superposition reflecting optics found in long-bodied decapods (e.g. shrimps, prawns and lobsters) and some Anomura. The possible phylogenetical significance of superposition, reflecting optics is also discussed.     

Geometrical optics of a galatheid compound eye

The eyes of galatheid squat lobsters (Munida rugosa) are shown to be of the reflecting superposition type. In the dark-adapted state corneal lenses focus light at the level of the rhabdoms and light from more than 1000 facets is redirected to the superposition focus by the reflecting surfaces of the crystalline cones. When the eye is light adapted, apposition optics are used. In this state paraxial light is focused by the corneal lens and the parabolic proximal end of the cone onto the distal end of a rhabdomeric lightguide. The latter transmits light across the clear zone to the rhabdom layer. In the dorsal part of the eye the individual ommatidia become progressively shorter until the cones and rhabdoms are no longer separated by a clear zone. Although formerly considered to be developing ommatidia, they are shown to be retained specifically for scanning the downwelling irradiance.Abbreviations RI refractive index - SEM scanning electron microscope     

Compound eyes of insects and crustaceans: Some examples that show there is still a lot of work left to be done

Similarities and differences between the 2 main kinds of compound eye (apposition and superposition) are briefly explained before several promising topics for research on compound eyes are being introduced. Research on the embryology and molecular control of the development of the insect clear‐zone eye with superposition optics is one of the suggestions, because almost all of the developmental work on insect eyes in the past has focused on eyes with apposition optics. Age‐ and habitat‐related ultrastructural studies of the retinal organization are another suggestion and the deer cad Lipoptena cervi, which has an aerial phase during which it is winged followed by a several months long parasitic phase during which it is wingless, is mentioned as a candidate species. Sexual dimorphism expressing itself in many species as a difference in eye structure and function provides another promising field for compound eye researchers and so is a focus on compound eye miniaturization in very small insects, especially those that are aquatic and belong to species, in which clear‐zone eyes are diagnostic or are tiny insects that are not aquatic, but belong to taxa like the Diptera for instance, in which open rather than closed rhabdoms are the rule. Structures like interommatidial hairs and glands as well as corneal microridges are yet another field that could yield interesting results and in the past has received insufficient consideration. Finally, the dearth of information on distance vision and depth perception is mentioned and a plea is made to examine the photic environment inside the foam shelters of spittle bugs, chrysales of pupae and other structures shielding insects and crustaceans.     

Challenging limits: Ultrastructure and size‐related functional constraints of the compound eye of Stigmella microtheriella (Lepidoptera: Nepticulidae)

With a body length of only 2 mm, the nepticulid Stigmella microtheriella (Stainton, 1854) is one of the smallest moths known to date. We investigated the optical design of its lemon‐shaped compound eyes, which measure 83.60 μm in anterior–posterior and 119.77 μm in dorso‐ventral direction. The eyes consist of about 123 facets, each of the latter just 9.9 μm in diameter. Transmission electron microscopy reveals an optical design with features intermediate between apposition and superposition optics similar to that known from two other small species of moths (one Nepticulid and one Gracillarid). Size‐related evolutionary adaptations of the ommatidial organization include (1) the involvement of only five rhabdomeres in the formation of the distal rhabdom (2) the complete absence of a rhabdomere of the eighth (= basal) retinula cell, (3) the “hourglass” shape of the rhabdom with a characteristic narrow waist separating distal from proximal portion, and (4) the reduction to one single layer of tracheoles as an adaptation to the overall restricted space available in this minute eye. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

Retinal and optical adaptations for nocturnal vision in the halictid bee<Emphasis Type="Italic"> Megalopta genalis</Emphasis>

The apposition compound eye of a nocturnal bee, the halictid Megalopta genalis, is described for the first time. Compared to the compound eye of the worker honeybee Apis mellifera and the diurnal halictid bee Lasioglossum leucozonium, the eye of M. genalis shows specific retinal and optical adaptations for vision in dim light. The major anatomical adaptations within the eye of the nocturnal bee are (1) nearly twofold larger ommatidial facets and (2) a 4–5 times wider rhabdom diameter than found in the diurnal bees studied. Optically, the apposition eye of M. genalis is 27 times more sensitive to light than the eyes of the diurnal bees. This increased optical sensitivity represents a clear optical adaptation to low light intensities. Although this unique nocturnal apposition eye has a greatly improved ability to catch light, a 27-fold increase in sensitivity alone cannot account for nocturnal vision at light intensities that are 8 log units dimmer than during daytime. New evidence suggests that additional neuronal spatial summation within the first optic ganglion, the lamina, is involved.B.G. is thankful for travel awards from the Royal Physiographic Society, the Per Westlings Fond, the Foundation of Dagny and Eilert Ekvall and the Royal Swedish Academy of Sciences. E.J.W. is grateful for the support of a Smithsonian Short-Term Research Fellowship, the Swedish Research Council, the Crafoord Foundation, the Wenner-Gren Foundation and the Royal Physiographic Society of Lund for their ongoing support     

To the Question of Eyes in Primitive Crustaceans

Based on a review of studies of functional and comparative anatomy of crustacean eyes, a hypothesis is formed on eyes in primitive crustaceans. It is suggested that they were similar to present-day frontal eyes of the malacostracan type. Neuronal architecture suggests that the development to apposition compound eye followed two main routes, one seen in malacostracans and the other in non-malacostracans. Within the two subgroups different and separate lines have been followed to form specialized apposition types and, within the Malacostraca, superposition eyes as pointed out by Nilsson (Nilsson, D. E. 1989. Facets of vision, pp. 30–73).     

Structure of the dorsal eye region of the moth,Adoxophyes reticulana Hb. (Lepidoptera : Tortricidae)

Ommatidia of the eucon compound eye of Adoxophyes reticulana (Lepidoptera : Tortricidae) were investigated elect ronmicroscopically. The dorsofrontal part and the dorsal rim region were examined in serial sections. Seven radially arranged retinula cells RC₁₋₇ form the rhabdom from distal to proximal region (Fig. 1). The 8th retinula cell RC₈ joins the first 7 at their bases; this cell enlarges proximally (Fig. 1C, D). In the dorsofrontal region, 2 types of rhabdoms are distinguished; Type II (Figs. 1B₂;3b) outnumbers Type I (Figs. 1B₁;3a by a ratio of 4 : l. In the dorsal rim area, the first 2 rows are occupied exclusively by Type 11-rhabdoms; beyond this, the rhabdom of the dorsal rim area is characterized by the fact that its middle and proximal parts are considerably larger in diameter than in the dorsofrontal part; in this region, the microvilli of the horizontally oriented rhabdomeres are also parallel to the ;,-axis of the eye (Figs. 1B₃;3d). Thus, this small eye region meets the structural requirements for the detection of polarized light. The eye is interpreted as an intermediate between apposition and superposition eyes, because the rhabdom begins at the tip of the crystalline tract and the retinula cells are pigmented like those of an apposition eye. On the other hand, the structure of the dioptric apparatus and the tracheal system corresponds to those of superposition eyes. Parallels with the Ephestia eye in basic structural features are discussed in regard to the possible function of this eye and to the systematic position of A. reticulana.     

Visual ecology of Indian carpenter bees II: adaptations of eyes and ocelli to nocturnal and diurnal lifestyles

Most bees are diurnal, with behaviour that is largely visually mediated, but several groups have made evolutionary shifts to nocturnality, despite having apposition compound eyes unsuited to vision in dim light. We compared the anatomy and optics of the apposition eyes and the ocelli of the nocturnal carpenter bee, Xylocopa tranquebarica, with two sympatric species, the strictly diurnal X. leucothorax and the occasionally crepuscular X. tenuiscapa. The ocelli of the nocturnal X. tranquebarica are unusually large (diameter ca. 1 mm) and poorly focussed. Moreover, their apposition eyes show specific visual adaptations for vision in dim light, including large size, large facets and very wide rhabdoms, which together make these eyes 9 times more sensitive than those of X. tenuiscapa and 27 times more sensitive than those of X. leucothorax. These differences in optical sensitivity are surprisingly small considering that X. tranquebarica can fly on moonless nights when background luminance is as low as 10⁻⁵ cd m⁻², implying that this bee must employ additional visual strategies to forage and find its way back to the nest. These strategies may include photoreceptors with longer integration times and higher contrast gains as well as higher neural summation mechanisms for increasing visual reliability in dim light.     

The ontogeny of facultative superposition optics in a shrimp eye: hatching through metamorphosis

Summary Compound eyes of larval and first postlarval grass shrimp (Palaemonetes pugio Holthuis) were studied with light and electron microscopy following adaptation to darkness or bright light. Larvae have well-developed apposition eyes, including 3 main types of accessory screening and reflecting pigments and a fourth class of putatively reflective granules recently described in adult shrimps. Rhabdoms contain orthogonally layered microvilli, and by the last larval stage, 8 retinular cells. Ocular accessory pigments in both light- and dark-adapted larvae are distributed much like those of light-adapted adults, but the distal mass of reflecting pigment is concentrated dorsally in larvae and ventrally in adults. Since larvae swim upside-down, reflecting pigment is oriented downward in all developmental stages and may function for countershading. Light and dark adaptational migrations of all 3 major accessory pigments commence abruptly at metamorphosis to the first postlarva. Upon dark adaptation in postlarvae, superposition optics remain impossible because (1) distal screening pigment migrates only slightly, (2) no clear zone has developed, and (3) the crystalline cones remain circular in cross section. Nevertheless, a slight improvement in photon catch is expected due to extensive redistributions of reflecting pigment and retinular cell screening pigment granules.

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Exceptionally well‐preserved isolated eyes from Cambrian ‘Orsten’ fossil assemblages of Sweden

Abstract: Eyes other than those of trilobites are rarely preserved in the fossil record. We describe here a set of six tiny, isolated, three‐dimensionally preserved compound eyes. These secondarily phosphatized eyes were etched from ‘Orsten’ limestone nodules dated to the Agnostus pisiformis Biozone from the Cambrian Alum Shale Formation of Sweden. The ovoid eyes arise from an elongated stalk, their surface being covered by a mosaic of regular and hexagonal‐shaped facets representing the surface of ommatidia. Facet size and pattern change within the same specimen from the posterior to the anterior end. With regard to some morphological criteria, we grouped the material in two different morphotypes, type A and B, the first being represented by specimens of two different developmental stages. From stage to stage, mostly growth in overall size and addition of new ommatidia was noticed. Among the meiobenthic ‘Orsten’ arthropods, only the crustacean Henningsmoenicaris scutula has been described as possessing stalked eyes, but the eyes of the largest specimen with preserved eyes of this species are much smaller than the new eyes and do not display any kind of ommatidia on their visual surface. However, fragments of larger specimens of H. scutula and the co‐occurrence of this species with the new isolated eyes in the sieving residues make it likely that the latter belong to this species but belong to more advanced stages than those described previously of H. scutula. Ontogenetically, the eye stalks of this fossil crustacean elongate progressively, while the regular hexagonal facets, lacking in early stages, appear later on.     

Optics of the butterfly eye

The afocal apposition optics of butterfly eyes was examined from both a geometrical optics and a wave optics point of view. We used several different species of butterfly but put special emphasis on a common Australian nymphalid,Heteronympha merope. From the anatomy of the retina, the optics of isolated components of the eye and the ophthalmoscopy of the intact living eye we derived the following.

Sexual Dimorphism in the Compound Eye of Rhagophthalmus ohbai (Coleoptera: Rhagophthalmidae): I. Morphology and Ultrastructure

The eyes of the winged males and larvi-form, wingless females of the firefly Rhagophthalmus ohbai differ from each other in several respects. Compared with the eyes of the males, those of the females contain fewer (35 versus ca. 3500) and smaller (20 μm versus 24-31 μm) facets and anatomically they are of the apposition type. Their main function appears to be to detect light intensity changes from day to nighttime; resolving power of the female eye must be poor and e-vector discrimination would be absent. The eyes of the males consist of a smaller, dorsal region of ca. 500 om-matidia of about 250 μm length and a larger, ventral region of ca. 2000 ommatidia of about 640 urn length. The microvilli of the dorsal eye region are somewhat wider than those of the ventral region (55 nm versus 45 nm) and are less regularly arranged. A tapetal reflecting layer is only present in the dorsal eye region. The small clear-zone between dioptric apparatus and retina in the dorsal eye region would not allow as good a superposition image to be produced as in the ventral eye region with its 5 times wider clear-zone. The regular orientations of the microvilli in the rhabdoms and the lack of a proper tapetum in the ventral eye region suggest that e-vector discrimination should be possible.     

The zoeal development of Platymaia wyvillethomsoni Miers, 1886 (Crustacea: Decapoda: Majoidea: Inachidae) described from laboratory reared material

The spider crab Platymaia wyvillethomsoni was reared in the laboratory, from hatching to the megalopal stage at 20°C. The larval development comprises two zoeal stages and a megalopa. The zoeal stages are described for the first time and compared with those of the four known species of the family Inachidae from the northern Pacific. The zoeal characters (carapace spines, antenna, mouthpart appendages, pleon and telson fork) of P. wyvillethomsoni are significantly different from those of two Achaeus species from northern Pacific and other inachid genera (Inachus and Macropodia) from the Atlantic. Therefore, this species should not be placed in the family Inachidae based on zoeal morphology. A provisional key for the identification of known zoeae of the family from the northern Pacific is provided.     

Larval development of the subantarctic king crabs<Emphasis Type="Italic"> Lithodes santolla</Emphasis> and<Emphasis Type="Italic"> Paralomis granulosa</Emphasis> reared in the laboratory

The larval development and survival in the two subantarctic lithodid crabs Lithodes santolla (Jaquinot) and Paralomis granulosa (Molina) from the Argentine Beagle Channel were studied in laboratory cultures. In L. santolla, larval development lasted about 70 days, passing through three zoeal stages and the megalopa stage, with a duration of approximately 4, 7, 11 and 48 days, respectively. The larval development in P. granulosa is more abbreviated, comprising only two zoeal stages and the megalopa stage, with 6, 11 and 43 days' duration, respectively. In both species, we tested for effects of presence versus absence of food (Artemia nauplii) on larval development duration and survival rate. In P. granulosa, we also studied effects of different rearing conditions, such as individual versus mass cultures, as well as aerated versus unaerated cultures. No differences in larval development duration and survival were observed between animals subjected to those different rearing conditions. The lack of response to the presence or absence of potential food confirms, in both species, a complete lecithotrophic mode of larval development. Since lithodid crabs are of high economic importance in the artisanal fishery in the southernmost parts of South America, the knowledge of optimal rearing conditions for lithodid larvae is essential for future attempts at repopulating the collapsing natural stocks off Tierra del Fuego.Communicated by H.-D. Franke     

Butterfly optics exceed the theoretical limits of conventional apposition eyes

Optical experiments on butterfly compound eyes show that they have angular sensitivities narrower than expected from conventional apposition eyes. This superior performance is explained by a theoretical model where the cone stalk is considered as a modecoupling device. In this model the Airy diffraction pattern of the corneal facet excites a combination of the two waveguide modes LP₀₁ and LP₀₂. When the two modes propagate through the cone stalk the power of LP₀₂ is transferred to LP₀₁ alone which is supported by the rhabdom. This mechanism produces a higher on-axis sensitivity and a narrower angular sensitivity than conventional apposition optics. Several predictions of the model were confirmed experimentally.