Visual fields and eye morphology support color vision in a color-changing crab-spider

Vision plays a major role in many spiders, being involved in prey hunting, orientation or substrate choice, among others. In Misumena vatia, which experiences morphological color changes, vision has been reported to be involved in substrate color matching. Electrophysiological evidence reveals that at least two types of photoreceptors are present in this species, but these data are not backed up by morphological evidence. This work analyzes the functional structure of the eyes of this spider and relates it to its color-changing abilities. A broad superposition of the visual field of the different eyes was observed, even between binocular regions of principal and secondary eyes. The frontal space is simultaneously analyzed by four eyes. This superposition supports the integration of the visual information provided by the different eye types. The mobile retina of the principal eyes of this spider is organized in three layers of three different types of rhabdoms. The third and deepest layer is composed by just one large rhabdom surrounded by dark screening pigments that limit the light entry. The three pairs of secondary eyes have all a single layer of rhabdoms. Our findings provide strong support for an involvement of the visual system in color matching in this spider.     

The eyes of Macrosoma sp. (Lepidoptera: Hedyloidea): a nocturnal butterfly with superposition optics

The visual system of nocturnal Hedyloidea butterflies was investigated for the first time, using light and electron microscopy. This study was undertaken to determine whether hedylids possess the classic superposition eye design characteristic of most moths, or apposition eyes of true butterflies (Papilionoidea), and, to gain insights into the sensory ecology of the Hedyloidea. We show that Macrosoma heliconiaria possesses a superposition-type visual mechanism, characterized by long cylindrical crystalline cones, a lack of corneal processes, 8 constricted retinular sense cells, rhabdoms separated from the crystalline cones forming a translucent 'clear zone', and tight networks of trachea that form a tapetum proximal to the retina and which also surround the rhabdoms to form a tracheal sheath. Dark-adapted individuals of M. heliconiaria, M. conifera, and M. rubidinarea exhibited distal retinular pigment migration, forming an eye glow. Correspondingly, light-exposure induced pigment to migrate proximally, causing the eye glow to be replaced by a dark pseudopupil. Other characteristics of the visual system, including relative eye size, facet size, and external morphology of the optic lobes, are mostly 'moth like' and correlate with an active, nocturnal lifestyle. The results are discussed in relation to the evolution of lepidopteran eyes, and the sensory ecology of this poorly understood butterfly superfamily.     

Visual field structure in the Empress Leilia, Asterocampa leilia (Lepidoptera, Nymphalidae): dimensions and regional variation in acuity

Male Empress Leilia butterflies ( Asterocampa leilia) use a sit-and-wait tactic to locate mates. To see how vision might influence male behavior, we studied the morphology, optics, and receptor physiology of their eyes and found the following. (1) Each eye's visual field is approximately hemispherical with at most a 10 degrees overlap in the fields of the eyes. There are no large sexual differences in visual field dimensions. (2) In both sexes, rhabdoms in the frontal and dorsal ommatidia are longer than those in other eye regions. (3) Interommatidial angles are smallest frontally and around the equator of the eye. Minimum interommatidial angles are 0.9-1 degrees in males and 1.3-1.4 degrees in females. (4) Acceptance angles of ommatidia closely match interommatidial angles in the frontal region of the eye. We conclude that vision in these butterflies is mostly monocular and that males have more acute vision than females, especially in the frontal region (large facets, small interommatidial angles, small acceptance angles, long rhabdoms, and a close match between interommatidial angles and acceptance angles). This study also suggests that perched males direct their most acute vision where females are likely to appear but show no eye modifications that appear clearly related to a mate-locating tactic.     

Vision in the deep sea

The deep sea is the largest habitat on earth. Its three great faunal environments--the twilight mesopelagic zone, the dark bathypelagic zone and the vast flat expanses of the benthic habitat--are home to a rich fauna of vertebrates and invertebrates. In the mesopelagic zone (150-1000 m), the down-welling daylight creates an extended scene that becomes increasingly dimmer and bluer with depth. The available daylight also originates increasingly from vertically above, and bioluminescent point-source flashes, well contrasted against the dim background daylight, become increasingly visible. In the bathypelagic zone below 1000 m no daylight remains, and the scene becomes entirely dominated by point-like bioluminescence. This changing nature of visual scenes with depth--from extended source to point source--has had a profound effect on the designs of deep-sea eyes, both optically and neurally, a fact that until recently was not fully appreciated. Recent measurements of the sensitivity and spatial resolution of deep-sea eyes--particularly from the camera eyes of fishes and cephalopods and the compound eyes of crustaceans--reveal that ocular designs are well matched to the nature of the visual scene at any given depth. This match between eye design and visual scene is the subject of this review. The greatest variation in eye design is found in the mesopelagic zone, where dim down-welling daylight and bio-luminescent point sources may be visible simultaneously. Some mesopelagic eyes rely on spatial and temporal summation to increase sensitivity to a dim extended scene, while others sacrifice this sensitivity to localise pinpoints of bright bioluminescence. Yet other eyes have retinal regions separately specialised for each type of light. In the bathypelagic zone, eyes generally get smaller and therefore less sensitive to point sources with increasing depth. In fishes, this insensitivity, combined with surprisingly high spatial resolution, is very well adapted to the detection and localisation of point-source bioluminescence at ecologically meaningful distances. At all depths, the eyes of animals active on and over the nutrient-rich sea floor are generally larger than the eyes of pelagic species. In fishes, the retinal ganglion cells are also frequently arranged in a horizontal visual streak, an adaptation for viewing the wide flat horizon of the sea floor, and all animals living there. These and many other aspects of light and vision in the deep sea are reviewed in support of the following conclusion: it is not only the intensity of light at different depths, but also its distribution in space, which has been a major force in the evolution of deep-sea vision.     

Optical parameters of the eyes of some benthic decapods as a function of habitat depth (Crustacea,Decapoda)

Summary Eye diameter relative to body length, and interommatidial angle, rhabdom length and rhabdom width as a function of eye size, were determined for specimens of 19 benthic macruran decapod species in 8 genera and 5 families, spanning a wide range of habitat depths. For these species, eye diameter relative to body length tends to increase with adult habitat. In addition, rate of eye growth relative to body growth increases with habitat depth, a trend opposite to that of pelagic crustaceans previously investigated. Interommatidial angle decreases with increasing eye diameter, and therefore with depth for an individual of a particular size. Rhabdom length and width tend to increase with eye diameter. Visual sensitivity may increase with depth among these species as a result of both larger eyes and the associated increase in rhabdom dimensions. Differences in energetic limitations and visual environments might produce the difference in trends of eye size relative to body size between benthic and pelagic crustaceans.     

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.     

Fundamental differences in the optical structure of the eyes of nocturnal and diurnal mosquitoes

We have studied the anatomy and optics of the eyes of a range of mosquito species from the wholly dark-active blood-feeding Anopheles gambiae to the diurnal plant-feeder Toxorhynchites brevipalpis. Consistent with studies by Satô in the 1950s, we find that dark-active and crepuscular species have short fused rhabdoms with a conical construction. This maximises the amount of light the rhabdoms receive from the almost hemispherical wide-aperture lenses. Toxorhynchites, on the other hand, has long narrow rhabdomeres that are separated from each other over their entire length, and so resemble the open rhabdoms of advanced flies (Brachycera and Cyclorrhapha). These findings are confirmed by studies of the pseudopupil, whose form indicates the layout of the rhabdomere tips in the focal plane of each ommatidial lens. In anopheline species the pseudopupil is a single undivided ellipse, indicating a fused rhabdom structure, whereas in Toxorhynchites there is a ring of six outer elements surrounding a central one. This means that each rhabdomere views a separate direction in space, and our measurements indicate that, as in higher Diptera, adjacent rhabdomeres share their fields of view with one of the rhabdomeres in the immediately adjacent ommatidia. This in turn means that in the diurnal type of mosquito eye there is a basis for neural superposition, but the fused construction of anopheline rhabdoms precludes this. The Aedes species studied were similar to Anopheles but with lenses of less extreme aperture, and Sabethes cyaneus, a diurnal blood-feeder, was intermediate in structure, with fused conical rhabdoms in the centre of the eye and unfused rhabdomeres around the periphery.     

Modelling the visual world of a velvet worm

In many animal phyla, eyes are small and provide only low-resolution vision for general orientation in the environment. Because these primitive eyes rarely have a defined image plane, traditional visual-optics principles cannot be applied. To assess the functional capacity of such eyes we have developed modelling principles based on ray tracing in 3D reconstructions of eye morphology, where refraction on the way to the photoreceptors and absorption in the photopigment are calculated incrementally for ray bundles from all angles within the visual field. From the ray tracing, we calculate the complete angular acceptance function of each photoreceptor in the eye, revealing the visual acuity for all parts of the visual field. We then use this information to generate visual filters that can be applied to high resolution images or videos to convert them to accurate representations of the spatial information seen by the animal. The method is here applied to the 0.1 mm eyes of the velvet worm Euperipatoides rowelli (Onychophora). These eyes of these terrestrial invertebrates consist of a curved cornea covering an irregular but optically homogeneous lens directly joining a retina packed with photoreceptive rhabdoms. 3D reconstruction from histological sections revealed an asymmetric eye, where the retina is deeper in the forward-pointing direction. The calculated visual acuity also reveals performance differences across the visual field, with a maximum acuity of about 0.11 cycles/deg in the forward direction despite laterally pointing eyes. The results agree with previous behavioural measurements of visual acuity, and suggest that velvet worm vision is adequate for orientation and positioning within the habitat.     

Interspecific variations in the morphology and ultrastructure of the rhabdoms of oplophorid shrimps

Interspecific variations in rhabdom structure between various oplophorid shrimps are described and the differences are related to the light environment at different depths within the mesopelagic zone. The ultrastructure of the distal rhabdom in these species is described for the first time. Quantitative measurements show that the proportion of the rhabdom layer occupied by the distal rhabdom varies from 3.5-25% in the dorsoventral plane of the eye of Systellaspis debilis. The distal rhabdom occupies less than 1% of the rhabdoms in the eye of Acanthephyra pelagica, where it can only be seen by using the electron microscope. It is suggested that the rhabdoms of those species that remain within the photic zone (such as S. debilis) are adapted to maximize contrast, whereas in those whose depth ranges extend into the aphotic zone (such as A. pelagica) they are adapted for maximum sensitivity.     

Fine structure of the eyes of orb-weavers,Argiope amoena L. Koch (Aranea: Argiopidae)

The anterolateral eye, the posterolateral eye and the posteromedial eye of the web-building spider, Argiope amoena have been examined by light and electron microscopy. The dioptric apparatus of all three eyes is similar in structure, and consists of a cornea, a lens and a vitreous body. The retina contains monopolar receptor cells, the cell bodies of which are present beneath the vitreous body in all three eyes. Proximal processes of the receptor cells form rhabdoms beneath the cell body layer and then extend toward the first optic glomerulus as an ocellar nerve. Two distinct patterns of retinal organization are present in the three eyes. In one type the rhabdomic layer of the retina is backed by a pigmented layer. In the other type the rhabdomic layer is backed by a tapetal reflecting layer. Rhabdomic structure and cytoplasmic inclusions of the receptor cells differ greatly between the two types. The anterolateral eye possesses a single type of retina with the rhabdoms backed by the tapetum. Both the posterolateral and the posteromedial eye are similar in structure, each possessing beneath the common dioptric apparatus retinae of both types.     

黑翅土白蚁有翅成虫复眼的形态结构

采用组织切片法光镜下观察黑翅土白蚁Odontotermes formosanus(Shiraki)有翅成虫的复眼形态结构及光、暗适应条件下色素颗粒移动的规律。结果如下:(1)头正前方观,复眼外部形态略呈圆形。(2)有翅成虫复眼类型属于并列像眼,每只复眼约由360个小眼组成。(3)每个小眼是由1套屈光器(1个角膜和1个晶锥)、小网膜色素细胞、视杆和基细胞等几部分组成。小网膜色素细胞内均含有丰富的色素颗粒。(4)在光适应条件状态下,屈光器及视杆周围的色素颗粒主要分布在视杆部位的上侧,暗度适应条件状态时则较均匀地分布于视杆两侧上下;性别对色素颗粒分布无明显影响。     

The sophisticated visual system of a tiny Cambrian crustacean: analysis of a stalked fossil compound eye

Fossilized compound eyes from the Cambrian, isolated and three-dimensionally preserved, provide remarkable insights into the lifestyle and habitat of their owners. The tiny stalked compound eyes described here probably possessed too few facets to form a proper image, but they represent a sophisticated system for detecting moving objects. The eyes are preserved as almost solid, mace-shaped blocks of phosphate, in which the original positions of the rhabdoms in one specimen are retained as deep cavities. Analysis of the optical axes reveals four visual areas, each with different properties in acuity of vision. They are surveyed by lenses directed forwards, laterally, backwards and inwards, respectively. The most intriguing of these is the putatively inwardly orientated zone, where the optical axes, like those orientated to the front, interfere with axes of the other eye of the contralateral side. The result is a three-dimensional visual net that covers not only the front, but extends also far laterally to either side. Thus, a moving object could be perceived by a two-dimensional coordinate (which is formed by two axes of those facets, one of the left and one of the right eye, which are orientated towards the moving object) in a wide three-dimensional space. This compound eye system enables small arthropods equipped with an eye of low acuity to estimate velocity, size or distance of possible food items efficiently. The eyes are interpreted as having been derived from individuals of the early crustacean Henningsmoenicaris scutula pointing to the existence of highly efficiently developed eyes in the early evolutionary lineage leading towards the modern Crustacea.     

Visual-optical characteristics of caged and semifree-ranging monkeys

Five species of macaques and one species of mangabey comprising a total of 324 monkeys (132 males and 192 females) were given visual examinations which included measures of corneal curvature, depth of the anterior chamber, thickness of the lens, depth of the vitreous chamber, total axial length, total power of the eye and intraocular pressure as well as the refractive error of eye under cycloplegia in the anesthetized monkey. Cercocebus and Macaca mulatta demonstrated the greatest amount of myopia and Macaca fascicularis the least, with M. speciosa, M. fuscata, and M. nemestrina in order between these extremes. The M. nemestrina eye approximates that of the chimpanzee in size and relationship of the components. The findings indicate that males have larger eyes than females, the curvature of the cornea decreases as the axial length increases, and there is a close relationship between the length of the eye and the amount of myopic refractive error. There is some evidence that amount of myopia and the percentage of animals showing a myopic refractive error are related to the visual conditions and the behavior patterns of the different species.     

亲土苔蛾成虫复眼超微结构

【目的】重叠型眼在昆虫复眼演化中起着重要作用。本研究旨在阐明夜出型亲土苔蛾Manulea affineola复眼类型及结构特征,以期填补灯蛾亚科昆虫复眼研究的空白,扩充夜出型昆虫复眼的特征数据,为探讨重叠型眼的变异趋势及复眼演化提供依据。【方法】运用光学和透射电子显微技术观察亲土苔蛾成虫复眼的超微结构。【结果】亲土苔蛾成虫复眼具有一个透明区,由6个次级色素细胞的透明胞质构成。小眼具8个视网膜细胞,其中1个视网膜细胞较短,仅位于小眼基部。在透明区内,7个视网膜细胞聚集成一束,其远端与晶体束末端相接,但并不形成视杆。在透明区下方,这7个视网膜细胞形成一个中心融合的视杆。在复眼背缘区的小眼的视杆具有近似矩形的横截面,而其余小眼的视杆具多分支状截面。【结论】亲土苔蛾成虫复眼属于重叠型眼;复眼背缘区的矩形视杆很可能与昆虫的偏振敏感性有关。     

Compound Eyes of Some Deep-Sea and Fiord Mysid Crustaceans

The compound eyes of the deep-sea mysid Boreomysis scyphops and the two mysid species Amblyops abbreviata and Pseudomma affine, which are indigenous to deep fiords in Norway, have been investigated. The eye stalks are greatly transformed, but contain hypertrophied retinas. The ommatidia of all three species lack a dioptric apparatus, possessing only retinular cells, which are arranged in a cylinder-like fashion. Folds from the retinular cells project into the “cylinder” and are covered with microvilli. The arrangement is explained functionally by an increase in the photopigment-bearing surface as an adaptation to low-light intensities. The orderly arrangement of microvilli in most arthropod compound eyes has been lost, and the arrangement is thus multidirectional in these mysids. With the photopigment dipoles arranged along the microvillar axis, the disorderly arrangement of microvilli signifies a more efficient capture of non-polarized light. It is concluded that the mysid compound eyes show adaptations to low-light intensities probably acquired during the species' evolutionary descent into deep-sea habitats. Amblyops abbreviata and Pseudomma affine, belonging to genera with entirely transformed eyes and with an ultrastructure less “normal” than that of Boreomysis scyphops are believed to be earlier descendants into the deep-sea habitats than the latter species, which belongs to a genus in which most of the species have well-developed eyes.     

Circadian Structural Changes in the Retina of Lycosa tarentula (Araneae: Lycosidae)

Daily structural changes of the rhabdoms are described in the four eye types of a lycosid spider submitted to laboratory conditions: LD 12:12 (light on at 08.00, 100 lux). From a study of animals submitted to constant darkness during fourteen days, rhabdom turnover was shown to be circadian. Each type of retina exhibits its own rhythmic turnover of rhabdoms. Anterior-lateral, posterior-median and lateral eyes are mostly diurnal; anterior-median retinae comprise 300 receptors with mainly nocturnal functioning and 150 receptors with mainly diurnal functioning. A correlation was found between rhythms of locomotor activity, other activity, and rhabdom turnover in L. tarentula suggesting that the same pacemaker controls these different rhythms.     

龟纹瓢虫成虫的复眼形态及其显微结构

利用光镜、组织切片法观察了龟纹瓢虫Propylaea japonica(Thunberg)成虫的复眼形态及其显微结构。结果如下:(1)头正前方观,复眼外形似半球,且后方稍向内合拢。每个复眼约包括630个小眼。(2)每个小眼是由1套屈光器(1个角膜和1个晶锥)、6至8个小网膜细胞及其特化产生的视杆和基细胞等几部分组成。晶体周围及小网膜色素细胞内均含有丰富的色素颗粒。(3)小眼整体纵切显示,其上、下段色素颗粒分布相对较多,中段分布较少。(4)明、暗适应状态对小眼的色素颗粒分布有影响,性别对其分布无明显影响。明适应状态下,其色素颗粒较均匀地分布于视杆两侧上下,暗适应状态时色素颗粒则主要分布在视杆部位的上侧,显示其具有一定的重叠眼性质;而在相同的明、暗适应状态下其雌、雄成虫复眼的色素颗粒分布间无明显差异。     

Circadian Structural Changes in the Retina of Lycosa tarentula (Araneae: Lycosidae)

Daily structural changes of the rhabdoms are described in the four eye types of a lycosid spider submitted to laboratory conditions: LD 12:12 (light on at 08.00, 100 lux). From a study of animals submitted to constant darkness during fourteen days, rhabdom turnover was shown to be circadian. Each type of retina exhibits its own rhythmic turnover of rhabdoms. Anterior-lateral, posterior-median and lateral eyes are mostly diurnal; anterior-median retinae comprise 300 receptors with mainly nocturnal functioning and 150 receptors with mainly diurnal functioning. A correlation was found between rhythms of locomotor activity, other activity, and rhabdom turnover in L. tarentula suggesting that the same pacemaker controls these different rhythms.     

The vitamin A of the lobster

In many crustacea, including the lobster, the bulk of the vitamin A of the whole animal is concentrated in the eyes. Recently Fisher, Kon, and Thompson found that vitamin A extracted from the eyes of euphausiid crustacea has only about one half the biological potency of the same amount of the all-trans acetate or fish liver vitamin A. In the present experiments the vitamin A of the lobster eye is found to consist almost entirely of the hindered cis isomer, neo-b, the precursor in the vertebrate retina of the visual pigments rhodopsin and iodopsin. This isomer is known to have a low biological potency in the rat, only about one quarter that of all-trans vitamin A. In the lobster eye it is virtually all extractable with petroleum ether, about 30 per cent in the form of free alcohol, about 70 per cent in the form of esters. It was identified by its absorption spectrum, as derived from measurements on crude extracts, and measured directly in purified preparations; the changes in absorption which accompany isomerization; oxidation to the corresponding retinene; and synthesis from the latter of rhodopsin. The examination of an extract of euphausiid eyes, provided by Dr. Kon, also revealed the presence of neo-b vitamin A virtually alone. This may be the characteristic condition in the eyes of Eucarid crustacea. It is peculiar in that the neo-b isomer, being a sterically hindered form, is ordinarily expected to be represented in any equilibrium mixture of geometric isomers in very small amount. Apparently certain crustacea have ways of circumventing the difficulties implicit in producing and retaining this isomer, and store it in the eye virtually alone.     

Vision in elasmobranchs and their relatives: 21st century advances

This review identifies a number of exciting new developments in the understanding of vision in cartilaginous fishes that have been made since the turn of the century. These include the results of studies on various aspects of the visual system including eye size, visual fields, eye design and the optical system, retinal topography and spatial resolving power, visual pigments, spectral sensitivity and the potential for colour vision. A number of these studies have covered a broad range of species, thereby providing valuable information on how the visual systems of these fishes are adapted to different environmental conditions. For example, oceanic and deep-sea sharks have the largest eyes amongst elasmobranchs and presumably rely more heavily on vision than coastal and benthic species, while interspecific variation in the ratio of rod and cone photoreceptors, the topographic distribution of the photoreceptors and retinal ganglion cells in the retina and the spatial resolving power of the eye all appear to be closely related to differences in habitat and lifestyle. Multiple, spectrally distinct cone photoreceptor visual pigments have been found in some batoid species, raising the possibility that at least some elasmobranchs are capable of seeing colour, and there is some evidence that multiple cone visual pigments may also be present in holocephalans. In contrast, sharks appear to have only one cone visual pigment. There is evidence that ontogenetic changes in the visual system, such as changes in the spectral transmission properties of the lens, lens shape, focal ratio, visual pigments and spatial resolving power, allow elasmobranchs to adapt to environmental changes imposed by habitat shifts and niche expansion. There are, however, many aspects of vision in these fishes that are not well understood, particularly in the holocephalans. Therefore, this review also serves to highlight and stimulate new research in areas that still require significant attention.