Open Access
How to translate text using browser tools
1 December 2001 The Crustacean Eye: Dark/ Light Adaptation, Polarization Sensitivity, Flicker Fusion Frequency, and Photoreceptor Damage
V. Benno Meyer-Rochow
Author Affiliations +

Compound eyes, nauplius eyes, frontal organs, intracerebral ocelli, and caudal photoreceptors are the main light and darkness detectors in crustaceans, but they need not be present all at once in an individual and in some crustaceans no photoreceptors whatsoever are known. Compound eye designs reflect on their functions and have evolved to allow the eye to operate optimally under a variety of environmental conditions. Dark-light-adaptational changes manifest themselves in pigment granule translocations, cell movements, and optical adjustments which fine-tune an eye's performance to rapid and unpredictable fluctuations in ambient light intensities as well as to the slower and predictable light level changes associated with day and night oscillations. Recycling of photoreceptive membrane and light-induced membrane collapse are superficially similar events that involve the transduction cascade, intracellular calcium, and membrane fatty acid composition, but which differ in aetiology and longterm consequence. Responses to intermittant illumination and linearly polarized light evoke in the eye of many crustaceans characteristic responses that appear to be attuned to each species' special needs. How the visual responses are processed more centrally and to what extent a crustacean makes behavioural use of e-vector discrimination and flickering lights are questions, however, that still have not been satisfactorily answered for the vast majority of all crustacean species. The degree of light-induced photoreceptor damage depends on a large number of variables, but once manifest, it tends to be progressive and irreversible. Concomittant temperature stress aggravates the situation and there is evidence that free radicals and lipid hydroperoxides are involved.


Despite numerous thorough investigations important gaps still exist in our understanding of how exactly crustaceans detect light, process visual information, and adjust their photoreceptors to the changing ambient thermal and photic conditions caused (a) by shifts in cloud cover and/or the animal's entry into shaded or illuminated areas and (b) by the regular exposure to a daily dark/light rhythm (Meyer-Rochow, 1999a).

Another area of crustacean vision in which our understanding is still incomplete concerns polarization sensitivity and the perception of flickering lights. This review provides an introductory survey of crustacean photoreceptors before addressing some of the above issues in more detail. It will end with a brief discussion on light-induced photoreceptor damage in the crustacean eye.

Crustacean Photoreceptors

Amongst the crustaceans, a variety of structures may be involved in the perception of light. The most conspicuous and best-studied organs are the compound eyes (Fig. 1a). They reach their highest degree of sophistication in the stomatopod (Cronin, et al., 1994), euphausiid (Land, 1981), and decapod crustaceans (Herring and Roe, 1988), but are absent from the Copepoda, Mystacocarida, Cephalocarida, and some smaller groups with very few species (see further below). In Cirripedia they still occur in the last larval stage and amongst the Ostracoda they are known from the Myodocopa.

Fig. 1

(a): Sector of crayfish compound eye with facets (Fac.) to the left and major internal layers, i.e. dioptric structures (Diop.), clear-zone (Cl. Zone), and retina (Ret.), visible in the longitudinal section (parallel to the ommatidial axes). Scale=0.1 mm. (b): Section through nauplius eye of the Antarctic ostracode Acetabulastoma sp., showing optic nerve (O.N.), photoreceptor cell nuclei (N.), visual membranes (Rh.), crystalline tapetum (Tap.), and screening pigment grains (P.). The direction of the light is from the left. Scale=1 μm.


Another kind of crustacean photoreceptor (Fig. 1b) are the nauplius eyes (Elofsson, 1965; 1966), which are usually present in the earliest larval stages, but may persist throughout adulthood (except in Leptostraca, Mysidacea, Cumacea, Isopoda, and Amphipoda). In some crustacean taxa (e.g., Copepoda, Mystacocarida, Cephalocarida, and Cirripedia) they represent the only photoreceptors. For ultrastructural details see, for example, Fahrenbach (1964), Dudley (1969), Ong (1970) and Meyer-Rochow (1999b).

The frontal organs, present in a large number of crustaceans, are clearly photoreceptors that are usually not homologous with the nauplius eye and which form the third category of crustacean light detectors (Elofsson, 1965, 1966). Examinations of individual cases are required before any statement concerning a specific frontal organ's ontogeny can be given and homology with the nauplius eye, or perhaps intracerebral ocelli (see below), can even be suggested. Incidentally, the term ‘median eye’, sometimes found in the literature to describe either nauplius eyes or frontal organs, is ambiguous and, henceforth, had better be avoided.

The fourth type of photoreceptive structure in crustacea is represented by the intra-cerebral ocelli, which are usually not visible from the outside of an intact animal and occur in the brain as clusters (or cluster) of a few photoreceptive cells (Martin, 1976; Sandeman et al., 1990; Martin et al., 1995; Frelon-Raimond et al., 2001). The tail (or caudal) photoreceptor, known from the sixth abdominal ganglion of some decapods, forms the fifth and last group of light and darkness detectors in crustacea (reviewed in Wilkens, 1988).

In certain crustacean taxa eyes occur that cannot be immediately and easily categorized and assigned to, for instance, the compound eyes or the nauplius eyes; yet they probably represent modified, but already known types of eyes rather than completely new classes of photoreceptor structures. Included in this group of “aberrant” or “non-typical” eyes are the single-lens eyes of the ampeliscid amphipods (Hallberg et al., 1980), the “accessory eyes” of shrimps (Itaya, 1976; Ugolini and Borgioli, 1993), the unusual eyes of cumacea (Meyer-Rochow, 1989) and the facet- as well as cone-less eyes of hydrothermal vent shrimps (O'Neill et al., 1995; Lakin et al., 1997). All four kinds of eye are interpreted, by most researchers, as modified compound eyes. Equally unusual and somewhat difficult to classify phylogenetically as well as physiologically are the single-lens nauplius eyes of certain copepods, e.g. Copilia, Corycaeus, and Sapphirina (Vaissière, 1961; Elofsson, 1969) whose retinas have been likened in function by Gregory et al. (1964) to the electron beam and screen of the television tube.

This brief introductory survey of photoreceptors in the crustacea does not rule out the possibility that other sense organs might also possess some sensitivity to light (crustacean integumental chromatophores and the ‘organ of Bellonci’ come to mind) or that as yet undiscovered light-sensors might exist (cf. Edwards, 1984). All the crustacean taxa considered to consist of individuals that have not evolved any eyes whatsoever (e.g., Remipedia, Thermosbaenacea, Spelaeogriphacea, Mictacea), ought to be re-examined just like some other so-called “eyeless” cave species (e.g., mysids, amphipoda, isopoda, shrimps, and crabs) in view of the fact that (a) not all photoreceptors are compound or nauplius eyes and (b) retinula cells can exist under the cuticle even when externally no eye can be seen (an example from the insects would be the eyeless grylloblattid Galloisiana nipponensis: Nagashima, 1990, an example from the decapods Typhlatya garciai: Meyer-Rochow and Juberthie-Jupeau, 1983).

With the exception of the nauplius eye of the adult barnacle, for which considerable physiological data exist (Stuart, 1983), and excluding the compound eye, which will be dealt with in more detail further below, very little is known about adaptational processes in any of the other kinds of photoreceptors or the extent to which they influence each other (e.g., the caudal photoreceptor's role in phase-shifting ERG-amplitude in juvenile crayfish: Bernal-Moreno et al., 1996). Changes in sensitivity thresholds have been documented in several extraocular photoreceptors by electrophysiological methods (Wilkens, 1988; Sandeman et al., 1990) and apparently light-induced structural and behavioural changes can occur in nauplius eyes, if not frontal organs as well (Debaisieux, 1944; Meyer-Rochow and Keskinen, unpublished). Whether, however, also intracerebral ocelli respond structurally and not only functionally (Hariyama et al., 1982) to variations in ambient light intensity and, as with the compound eye, undergo regular cyclic daily changes regarding volume of photoreceptive membranes and variety and density of cell organelles, are still open questions.

Crustacean Compound Eye: Basic Structure

The overall uniformity of the crustacean compound eye and its similarity in basic design with the compound eyes of xiphosuran chelicerates (e.g., Limulus) and insects had been noticed more than a hundred years ago (Exner, 1891). Melzer et al. (1997) give reasons and summarize arguments for a common evolutionary origin of the insect and crustacean ommatidium. A typical crustacean compound eye (for instance, Figs. 1a, 2a) consists of a number of similar anatomical units known as ommatidia, which are covered on the outside by a faceted, transparent, and multilayered cornea. The cornea is secreted by two corneagenous cells per ommatidium and forms, together with usually four cone cells, the dioptric apparatus of the eye. On the proximal side of the cone cells lies a group of retinula cells (frequently eight, but depending on the taxon also seven, six, or even five) with membrane specializations termed rhabdomeres which are the light-receptive elements of the ommatidium and contain the photopigment. Axons from the retinula cells penetrate the basement membrane in distinct bundles and terminate in the lamina from where second-order neurons link up with cells of the medulla. A variety of distal and proximal screening pigment cells (Hallberg and Elofsson, 1989) completes the basic structure of the crustacean compound eye. An eye conforming to the anatomy thus outlined, would be called an “apposition eye” and can be considered to represent the original archaic principle of the compound eye (Richter, 1999).

One modification of this basic arrangement is so characteristic that it has led to the establishment of a separate type of crustacean compound eye: an eye which can easily be distinguished from the apposition eye by the presence of a clear-zone, i.e., a region devoid of pigment (at least under dark-adapted conditions) between dioptric and receptor layers (Fig. 2b). The clear-zone may be formed by the elongated proximal ends of the cone cells or some narrow distal projections of the retinula cells. It was originally thought that amongst the crustaceans, clear-zone eyes occurred only in some malacostraca (e.g., Euphausiaceae, Mysidaceae, and Decapoda) and that this anatomical design was an adaptation to improve vision in dimly lit environments through superposition either by refraction or reflection (Land, 1981; Cronin, 1986). However, additional designs and mechanisms have been described in recent years (Cronin, 1986; Nilsson, 1989). Also, some species with this kind of eye (e.g., the hermit crab Dardanus and the syncarid Anaspides tasmaniae) were discovered in groups not previously expected to harbour species operating with superposition (Nilsson, 1990). It could also be shown that some apposition eyes can be as sensitive as superposition eyes (Land and Nilsson, 1990) or possess long and narrow cones which act as light-guides (Meyer-Rochow, 1978; Land, 1981b). Additional and more detailed information on functional differences between apposition and superposition eyes can be obtained in a recent publication by Warrant (1999).

Fig. 2

(after Hardie 1988 and Nilsson 1989). (a): Pathway of the light and structural elements in a model crustacean apposition compound eye (C=cornea, Co=cones, P=screening pigment, Rh=rhabdoms, BM=basement membrane, Ax=axons). (b): Pathway of the light and structural organization of a model crustacean superposition compound eye (C=cornea, Co=crystalline cones, DP=distal screening pigment, CZ=clear zone, Rh=rhabdoms, PP=proximal screeining pigment, Ax=axons).


Both apposition (Hallberg et al., 1980; Schiff et al., 1986; Cronin et al., 1994) and superposition eyes (Elofsson and Hallberg, 1977; Hiller-Adams and Case, 1988; Gaten et al., 1992; Richter, 1999) probably as an evolutionary consequence of environmental pressures, may display further structural and functional modifications. Forms, for instance, that flourish in extreme environments (mesopelagic and deep-sea crustaceans, and species adapted to a life underground or in caves) frequently exhibit morphologies that differ from the basic design (Meyer-Rochow and Nilsson, 1999). Within the genetic confines of the taxon such changes may affect primarily the optical components of the crustacean compound eye, the retina, or both. With regard to the eye's optics, for example, reflecting, refracting, and parabolic superposition eyes as well as apposition eyes with and without light guides and with and without screening or tapetal structures are now known (Nilsson, 1989). On the retinal side, long and thin, short and fat, solid or multilobed as well as fused or open rhabdoms may occur (Elofsson, 1976) and the nuclei of the retinula cells may be positioned above or below the basement membrane of the eye (Debaisieux, 1944). Yet, despite the variations in design, all compound eyes that display dark/light adaptational changes, exhibit these changes for the same purpose, namely to optimize the function of the eye under particular photic conditions. Photomechanical changes may affect the positions and shapes of whole cells, the amounts and distributions of organelles, and the chemical compositions of membranes, photopigments and intracellular messengers (cf. Meyer-Rochow, 1999a) so that firstly, the crustacean's requirements for light sensitivity and acuity are met and secondly, the constituent cells of the eye derive maximum protection against potentially damaging radiation.

Although specific environmental adaptations have been described from the compound eyes of a large number of species covering all the major taxa and it has been possible to formulate generalizations (see below), the crustacean compound eye can undergo changes within an animal's life span: in some species the eyes turn from apposition into superposition eyes as the animal grows (Meyer-Rochow, 1975; Hafner et al., 1982a; Nilsson et al., 1986), microvillar dimensions can change (Meyer-Rochow and Reid, 1996), and in others the eyes may develop an extremely high degree of asymmetry as, for instance, in some mesopelagic species with totally different dorsal and lateral ommatidia (Land et al., 1979; Land, 1981a; Gaten et al., 1992). What is more, new findings have shown that regional differences are present in the eyes of many crustaceans and not just those adapted to extreme environments (Odselius and Nilsson, 1983; Tokarski and Hafner, 1984; Cronin et al., 1992; Zeil and Zanker, 1997), highlighting the need for additional research into how the various regions of a compound eye behave (and perhaps influence each other) and how, more generally, post-embryonic eye differentiation occurs (cf., Meyer-Rochow et al., 1990; Ziedins and Meyer-Rochow, 1990; Hafner and Tokarski, 1998, 2001).

A further complicating factor in qualitative and quantitative studies of eyes and vision in crustaceans is that structural (Fig. 3), and functional (Fig. 4), responses of the eye depend on the time of day as well as on the previous photic exposure history of an individual. For example, the well-documented long-term damaging effect of bright light on the structural integrity and performance of the lobster compound eye (Fig. 5) is very much dependent on the depth, i.e., the ambient light intensity and the adaptational state to which the animals had been adjusted prior to the experimental exposure (Gaten, 1988; Gaten et al., 1990), a conclusion earlier reached also by Lindström and Nilsson (1984) on the basis of observations on light-induced photoreceptor damage and recovery in the oppossum shrimp Mysis relicta. Furthermore, photoreceptor membrane recycling, a diurnally modulated phenomenon, can result in very different profiles of rhabdoms and retinula cells at different times of day (see below).

Fig. 3

(after Bryceson and McIntyre 1983). Schematic illustration of the anatomy of an ommatidium of the crayfish Cherax destructor under three conditions of adaptation (LA=light adapted, DA=dark adapted). The small retinula cell R8 has been omitted for the sake of clarity.


Fig. 4

(after Meyer-Rochow and Tiang 1984). Stimulus/response curves (standard deviations indicated) based on ERG-recordings from the eyes of 10 rock lobsters (Jasus edwardsii) at night (left curve) and during the day (right curve). At night the eyes are at least 100 times more sensitive.


Fig. 5

(after Meyer-Rochow and Tiang 1984). (a): Bisected eye of rock lobster kept under normal 12h dark/light conditions, but exposed to white light of approx. 60000 lux from a xenon arc lamp for ca. 3 sec one week previously. Damage to cones and retina (arrows) is evident. (b): Bisected eye of rock lobster kept under normal conditions for two months, but prior to that exposed to sunlight for 420 min accumulated over a period of 7 days. Increased damage to dioptric structures and retina is obvious. (c): Bisected eye of rock lobster kept under normal conditions for almost 3 months, but with exposures to sunlight of 240 min on day 1, 240 min on day 2, 30 min on day 35, and 150 min on day 48. The damage to the eye is severe. Scale=0.5 mm.



Excellent descriptions of photomechanical changes affecting the crustacean compound eye and their underlying possible causes can be found in Autrum's (1981) review, which, furthermore, provides very useful definitions for the various kinds of sensitivity (e.g., absolute-, increment-, detection-, range-, and polarization sensitivity) and also deals with membrane dynamics during adaptations. An updated view on compound eye pigment and cell migrations as well as other micro-anatomical changes upon dark/light adaptation has recently been published by Meyer-Rochow (1999a). This review will, therefore, focus on new and perhaps little-known aspects of adaptation.

Although any component of the crustacean compound eye can be affected by dark/light adaptational changes (Meyer-Rochow, 1999a), the two most obvious involve (a) the position of the screening pigment granules (Fig. 6) and (b) the position, size, and shape of the rhabdom (Figs. 7, 8). The main purpose of these and other adjustments is to allow more light under dim conditions to enter the eye in order to improve the ‘photon-capture-rate’ through interceptions by the molecules of the photopigment (Struwe et al., 1975; Frixione et al., 1979; Land, 1981; Hallberg and Elofsson, 1989; Meyer-Rochow et al., 1990). This explains why at night in many species of crustaceans the apertures of the dioptric apparatus are frequently enlarged and screening pigments are withdrawn to regions outside the path of the light within the eye (Fig. 9), why often a reflecting tapetum at the back of the retina or around the retinula cells becomes exposed (Fig. 10), and why the rhabdom volume may dramatically increase (Fig. 11). In cases where adaptational changes of these kinds occur, there is usually a trade-of between sensitivity and acuity: one gains, the other loses. The gap between the two can be considerable as in the crayfish Cherax (Walcott, 1974) or it may be rather small as in Ligia exotica (Hariyama et al., 2001).

Fig. 6

(a): Cross section through retina of crayfish Procambarus clarkii, kept for 3 weeks in total darkness at 10°C; dark screening pigment granules are almost totally absent. Scale=10 μm. (b): Cross section through retina of crayfish Procambarus clarkii, kept for 3 weeks in the light at 10°C; dark screening pigment granules are abundant and insulate adjacent rhabdoms. Scale=10 μm.


Fig. 7

(after Meyer-Rochow and Tiang 1984). (a) and (b): Cross sections through light- and dark-adapted distal rhabdoms of the rock lobster Jasus edwardsii, showing difference in screening pigment distribution, rhabdom size and shape. Scale=1 μm. (c) and (d): Cross sections through part of light- and dark-adapted proximal rhabdoms of the rock lobster Jasus edwardsii, showing difference in screening pigment distribution, microvillar sizes and shapes. Scale=2 μm. Cone cell processes are denoted by asterisks.


Fig. 8

(after Meyer-Rochow and Tiang 1979). Diagrammatic representation of dark (DA) and light adaptational (LA) changes in the eye of the Antarctic amphipod Orchomene plebs (Cor.=cornea, Dist. P.=distal pigment, Rh.=rhabdom, Bm=basement membrane, Ret.C.=retinula cell bodies).


Fig. 9

Bisected, unfixed eye of Jasus edwardsii at night (a) and during the day (b), showing clear zone (CZ) and migration of screening pigments (P) to either below or above the reflecting layer (Tap) and the photoreceptive elements of the retina (Rh). Scale=0.1 mm.


Fig. 10

Longitudinal section through the centre of a dark-adapted (a) or light-adapted (b) Jasus edwardsii eye, showing extent of clear zone (CZ) and position of proximal screening pigment (PP) either below the basement membrane (exposing the reflecting layer=Tap), or above (shielding it). Migration of distal pigments into the clear zone (arrow) is also obvious. Scale=0.3 mm.


Fig. 11

Transverse section of the eye of the shrimp Macrobrachium heterochirus, fixed instantaneously (a) at night, showing rhabdom enlargement (Rh) and (b) during the day, showing diminution of rhabdom. Scale=50 μm.


Photomechanical changes involving screening pigments (both distal and proximal) can be observed in the living animal (Fig. 12) by examining its eye-glow (Arechiga et al., 1973; Frixione et al., 1979) or pseudopupil (Cronin, 1992). In species with “glowing eyes”, the animal is given a second chance to make use of the light that on its inward direction has first passed through the retina without being absorbed and then has undergone reflection at the tapetum behind the retina, reversing its path and directing it through the retina for a second time. Ommatidial ‘sleeves’ of reflecting granules or a zone of lower refractive index (frequently referred to as ‘palisade’) are also often involved in the enhancement of the rhabdom's photon capture efficiency. The screening pigment granules inside the receptor cell may move toward or away from the edge of the rhabdom (=radial migration), thereby altering the diameter of the pseudopupil (Cronin, 1992). Many of the known screening pigment translocations and changes in cell shape position upon adaptation can be generated at any time of day. However, exposing a crustacean to a light at night, for example, may produce additional adaptational changes that differ significantly from those seen during the day (Henkes, 1952; Bryceson and McIntyre, 1983; Meyer-Rochow et al., 2001). The same holds true for dark adaptation (Fig. 3). In insects (Nilsson et al., 1989), pupil control mechanisms vary between apposition (control over screening pigment position entirely retinal) and superposition eyes (independent distal and retinal control); in crustaceans, although less well-studied than insects, the situation seems to be somewhat more complicated with pigmentory effectors responding directly to the light (Frixione et al., 1979), but also to neurohormones (see below).

Fig. 12

Eyeglow of the eye of a dark adapted rock lobster (a) immediately and (b) 8 minutes after the first photographic flash of light. Scale=1.5 mm.


There is, first of all, usually a difference in the speed with which light and dark adaptations proceed (light adaptation is generally faster and often requires no more than a few minutes, whereas total dark adaptation can take hours: Meyer-Rochow, 1999a). Pigment granules involved in longitudinal migrations may cover a distance of up to 200 μm in 7–8 minutes, but after an initial fast translocation, pigment grains slow down progressively (Hallberg et al., 1980). Therefore, a value of 0.38 μm/sec for granule translocations in the crayfish given by Frixione et al., (1979) has to be an average. Radial pigment migrations may be as fast (King and Cronin, 1994), but cover shorter distances. Different cytoskeletal structures seem involved in radial and longitudinal pigment translocations (King and Cronin, 1993). Irrespective of time of day, the influence of light tends to supersede all other influences and can push the proximal pigment of the dark-adapted crayfish eye more rapidly into the light adapted position than it can the distal pigment. According to Bryceson (1986), the reverse holds true for dark adaptation. That the daily changes in morphology do not depend on the geographic latitude was shown in studies by Rosenberg and Langer (2001) with four species of Ocypode.

Much work (e.g. DeBruin and Crisp, 1957; Bryceson and McIntyre, 1983; Shelton et al., 1986) has been devoted to elucidate circadian effects on the responsiveness of distal, proximal, and reflecting pigments (Fig. 13), and considerable excitement was generated in the 70s and 80s after the discovery was made that photoreceptor turnover processes are diurnally modulated (Nässel and Waterman, 1979; Stowe, 1980; Toh and Waterman, 1982). Numerous intracellular changes, associated with rhabdom degradation (Hafner et al., 1982b) and up to 20 fold differences in rhabdom volume between day and night conditions were recorded in some species (Nässel and Waterman, 1979). It is possible that the circadian changes in the detectability of the microvillar actin core-filaments, reported by Hevers and Stieve (1995) for the crayfish Orconectes limosus, are related to the recent finding that in the crab Hemigrapsus sanguineus vesicles containing opsin are increasing in number in the retinula cell bodies towards dusk (Matsushita et al., 1999). The same vesicles are then thought to be incorporated into the rhabdom, thus causing its well-documented nocturnal enlargement (Arikawa et al., 1987). However, membrane recycling and adaptational phenomena are two separate issues and despite progress, some fundamental questions remain unanswered. How, for example, do different species cope, on the one hand, with the need for an immediate readiness to respond to changes in ambient light levels and, on the other, with the requirement to prepare the eye for the predictable and recurring cyclic luminosity oscillations between day and night? There is evidence that proximal retinal screening pigments, at least in crayfish, operate independently from distal screening pigments and that the latter obey a biphasic movement pattern (Frixione and Perez-Olvera, 1991).

Fig. 13

Ommatidial pigment shield (after Hallberg and Elofsson 1989), COR=cornea, CUT=cuticle, COR C=corneagenous cells, DP/DRP=distal screening pigment/distal reflecting pigment cells, IOP/IORP=interommatidial screening pigment/interommatidial reflecting pigment cells, RET C=retinula cell, RET P=retinula cell pigment, RH=rhabdom, PP/PRP=proximal screening pigment/proximal reflecting pigment, CP=cone cell process, BM=basement membrane, BP/BRP=basal screening pigment/basal reflecting pigment, AX=axon.


Humoral control has been implicated in some screening pigment displacements, especially those affecting the distal pigments (Kulkarni and Fingerman, 1987; Nordtug and Krekling, 1989) and ERG-amplitudes in the crayfish Orconectes were shown to rise and fall in response to certain neuropeptides: for example RPCH (=red pigment-concentrating hormone) increased, PDH (=pigment dispersing hormone) decreased ERG-amplitudes (Gaus and Stieve, 1992). A host of chemicals, some like colchicine affecting microtubules (e.g., Schraermeyer, 1992), others like oxygen and CO2 being involved in respiration and metabolism (Henkes 1952; Fanjul-Moles et al., 1998) or, like Ca2+, Na+, K+, etc. (Frixione and Arechiga, 1981), being part of the excitation cascade and the generation of the bioelectrical response, are known to interfere with adaptational processes. Ambient temperature (Meyer-Rochow and Tiang, 1979, 1982; King and Cronin, 1994) and pH (Delpiano et al., 1992; Coles et al. 1996) also apparently have a role to play, but an efferent control system, passing signals from brain to eye as in Limulus (Kier and Chamberlain, 1990; Chamberlain, 1998) has never been convincingly demonstrated to occur in the crustacea. This, despite the fact that Nagano (1986) was able to show that serotonin, now known to be present in the crustacean brain (Sandemann et al., 1995) and in fibres of the vicinity of photo-receptor axons (Arechiga et al., 1990), affected the circadian changes in pseudopupil size, presumably via its action on the sinus gland.

Moreno-Saenz et al. (1987), furthermore, demonstrated an effect of serotonin, which is the precursor of melatonin, on the size of the crayfish ERG and Meyer-Rochow (unpublished), through radioimmunological surveys, explored melatonin concentrations of severed eyes in dark and light adapted Astacus crayfish and the isopod Saduria entomon. In some preliminary tests, melatonin levels in the heads of immature, juvenile isopods were elevated when compared with those of adult, light- adapted day animals (Meyer-Rochow, unpublished), and occasionally dark- and light-adapted mature individuals also possessed different melatonin concentrations. Yet, in fully-grown crayfish no statistically significant differences in melatonin levels of eyes of dark- and light-adapted animals were ever noticed. On the other hand, towards winter crayfish eye melatonin concentrations, generally, tended to increase and a seasonal effect, therefore, cannot be ruled out. Since Withyachumnarnkul et al. (1995) were also unable to detect significant day/night fluctuations in melatonin levels in the optic lobes of the shrimp Penaeus monodon, most likely a single melatonin/serotonin-based control system of adaptational events in the crustacean eye does not exist and, just like different eye anatomies have evolved to meet different environmental challenges, different adaptational control mechanisms may have evolved. It is interesting in this context to note that deep-sea species frequently do not display any obvious photomechanical responses to light whatsoever (e.g. Gennadas sp.: Nilsson, 1990) and apparently lack membrane cycling (Chamberlain, 1998).

Turning our attention now back to those species that do display photomechanical adjustments, what do the structural changes really mean in terms of function? Behavioural observations on animals under different photic conditions have given us some answers (DeBruin and Crisp, 1957), as have biochemical (Barnes and Goldsmith, 1977; Kong and Goldsmith, 1977) and electrophysiological studies (Arechiga et al., 1973; Walcott, 1974; Meyer-Rochow and Tiang, 1984; Bryceson and McIntyre, 1983; Bryceson, 1986; Lindström et al., 1988). There is no doubt that fully dark adapted animals possess eyes of greater absolute sensitivity to light than specimens with light-adapted eyes, i.e. animals kept in the light and/or studied during the day (Fig. 4). There is also no question that in most cases in which photomechanical changes occur, acuity (=degree of resolution) improves at the expense of sensitivity as the eye becomes light adapted. This is reflected in a narrower acceptance angle during the day and/or upon light adaptation (Bryceson and McIntyre, 1983). Juvenile individuals with eyes differing from those of the adults in structure and function frequently also display movement patterns and behaviours that are different (Meyer-Rochow, 1975; Hines et al., 1995). Likewise, individuals in which significant changes in eye organization accompany the daily light cycle, display very different behaviours at night and during the hours of daylight. It was noticed that rock lobsters with imbalanced visual inputs due to unilateral light adaptation or damage to the eye acquired a lop-sided stance (Meyer-Rochow and Tiang, 1984) and that bilaterally-blinded individuals instead of remaining concealed during the day, tended to expose themselves far more frequently than normal individuals (Meyer-Rochow, 1988). Electrophysiologically a correlation between ERG and locomotor activity was shown by Fuentes-Pardo and Inclan-Rubio (1981) for the crayfish. However, a consensus on whether the adaptational state in one eye of a crustacean influences that of the other (Barrera-Mera and Berdeja-Garcia, 1979) or whether the two eyes operate independently of each other (Meyer-Rochow, 1982) may not be possible, as more than one control system could exist.

All kinds of known superposition eyes are generally interpreted as an attempt by Nature to come up with a compromise between the demands for optimal sensitivity and optimal acuity. There are, however, apposition eyes that possess identical sensitivities to eyes that operate on the superposition principle, but the latter do outperform the former by a factor of three with regard to resolution (Land and Nilsson, 1990). Theoretically, in addition to the various possible optical improvements of vision under dim conditions, crustacea that make large vertical migrations could improve photon capture by widening the spectral sensitivity window as they get closer to the surface and by ‘narrowing’ it to wavelengths that are maximally transmitted to greater depths as they swim downward. Shifts in spectral sensitivity as a consequence of the migrations of screening pigment granules in the day- and night-eye have been reported from the isopod Ligia exotica by Hariyama et al. (1986) as well as the crayfish Procambarus (Fanjul-Moles and Fuentes-Pardo, 1988) and may be more common than is presently realized.

Additional and apparently much greater gains could be achieved by neural means: neighbouring visual channels could be summed (=spatial summation) or be allowed increased periods (=temporal summation) over which they could count“a sample of photons” (Warrant, 1999). But while visual processing at higher level has been studied relatively well in some insects (Strausfeld, 1989), crustacean compound eye research despite some excellent studies in relation to polarization sensitivity by, to name but a few, Legget (1976), Glantz and Bartels (1984), and Wang-Bennett and Glantz (1987), has lagged somewhat behind in this respect. Circadian anatomical changes affecting lamina cells have not been described yet from any crustacean eye, but are known to occur in, for example, the fly (Pyza and Meinertzhagen, 1995). Cyclic variations in ERG amplitude of several crustacean eyes have, however, been well documented (e.g., Arechiga et al., 1973; Barrera-Mera and Abaster, 1978; Meyer-Rochow and Tiang, 1984) and now lead us to examine the events that occur right at the onset of photoreception and culminate in a signal being sent from the receptor cell to the brain.


The chain of events starts with the photopigment molecules (they are visible on freeze-fracture electron micrographs as intramembraneous ca. 10 nm particles that most likely represent aggregates of 4 molecules: Eguchi et al., 1989) in the microvilli of the crustacean rhabdom (Eguchi and Waterman, 1976; Meyer-Rochow and Eguchi, 1984). The microvilli are hollow, fingerlike tubes of usually 60-80 nm in diameter and variable length that are oriented perpendicular to the light path. Their membranes, apart from the photopigment, contain a variety of phospholipids as well as very fine fibrilar links to the core-filament (identified as actin: Hafner et al., 1992; Hevers and Stieve 1995) in the centre of each microvillus (Fig. 14).

Fig. 14

(a): Deep-etched crayfish rhabdom, showing microvilli in transverse section and core filaments (arrows). Scale=0.1 μm. (Courtesy of E.Eguchi). (b): Freeze-fractured crayfish rhabdom, showing photopigment molecules in microvillar membranes. Scale=0.1 μm (after Meyer-Rochow and Eguchi 1984). (c): High power electron micrograph of transversely sectioned microvilli from the dark adapted crayfish eye, showing core filament (arrows). Scale=50 nm.


The spaces between the microvilli, which are connected to one another by glycoproteins, leave little room for extracellular lacunae. Retinal (vitamin A1) is the major chromophore in the crustacean eye, but 3-dehydroretinal (porphyropsin) can also be present (Suzuki and Eguchi, 1987; Zeiger and Goldsmith, 1993). Through the action of a single photon the chromophore changes from the 11-cis to the all-trans molecular configuration. The resulting conformational change of the apoprotein (the opsin) to the photoactivated state can cause G-proteins to initiate the downstream phototransduction cascade. Perhaps better studied in the insect eye (Suzuki, 1999), but probably not very different in the crustacean photoreceptor, the ensuing process sees photoactivated metarhodopsin activate phospholipase-C to hydrolyze phosphatidylinositol 1,4-biphosphate, producing phosphatidylinositol triphosphate (IP3) and diacylglycerol (DG). Ca2+-ions are then liberated (most likely from intracellular stores) by IP3, consequently exerting their influence on calcium-release-activated channel proteins. A comprehensive review on the role of calcium in the phototransduction cascade of Limulus has recently been published by Dorlöchter and Stieve (1997).

Since G-proteins, known to become released in the cray-fish retina by photo-regeneration (Terakita et al., 1993), appear to play a pivotal role in the phototransduction cascade they have also come under considerable scrutiny. One G-protein, known as Gq(alpha), was localized in the rhabdoms of dark-adapted crayfish as the membrane-bound form, but as the soluble form in the cytoplasm following light adaptation. What this means is that the amount of Gq that can be activated by rhodopsin is light-modulated and, at least in vitro, regulated by the fatty-acid modification of Gq(alpha) (Terakita et al., 1996). Clearly this has ramifications for the integrity of the microvillus since the often reported light-dependent reduction of rhabdom diameters in the crustacean eye is probably affected by light-activated phospholipases (Trowell et al., 1991). When the phospholipase inhibitor manoalide was applied to the retina of the crab Leptograpsus variegatus, the rhabdoms failed to exhibit the light-dependent reductions in diameter (Blest and Stowe, 1997). G-proteins, therefore, not only play a role in the phototransduction cascade, but also influence amount and structural integrity of the visual membranes.

Very recently the concept that cation-selective channels in the compound eye might be regulated by polyunsaturated fatty acids (PUFA) has been introduced (Chyb et al., 1999; Kiselyov and Muallem, 1999) and this concept may be applicable to the crayfish retina. When, as shown for example in Fig. 15, crayfish eyes are exposed to bright light, they react with marked decreases in phosphatidylcholine and PUFA-levels, but, when exposed in the presence of phospholipase-A2 inhibitors, like DMDA or manoalide, no such decreases occur (Kashiwagi et al., 1999). PUFA-mediated effects of light other than changes in membrane fluidity alone (e.g., intracellular Ca-concentration) may, therefore, be involved in photic damage (Meyer-Rochow, 2000).

Fig. 15

(a): Changes in the retinal lipids of the eye of the crayfish Procambarus clarkii following exposure to light of approx. 5000 lux. Phosphatidylcholine amounts decrease sharply (after Kashiwagi et al. 1997). (b): Effect of phospholipase inhibators on phosphatidylcholine changes in the retina of the crayfish Procambarus clarkii, following exposure to light of approx. 5000 lux. Manoalide and DMDA prevent the light-induced decrease of PC in the light (after Kashiwagi et al., 2000).



The overwhelming majority of all crustacean species live in the water. Those not concealed and close to the surface are almost constantly exposed to wave-induced flicker frequencies, which are most intense and far-reaching when the sun is at its zenith during midday and least obvious at night during new moon. In clear tropical seas at least down to 5 m from the surface the power spectrum of flickers from downwelling light was dominated (i.e., >50%) by frequencies below 15 Hz, but even at 5 m some power was present above 50 Hz (McFarland and Loew, 1983). The boundary frequencies for 50% of the total power spectrum amounted to 14.5 Hz, 6 Hz, and 4 Hz for depths of 0.25 m, 2.5 m, and 4.5 m, respectively (McFarland and Loew, 1983). As waves can also produce fluctuating patterns of spatial frequencies underwater, it has been suggested by the same authors that body markings like reticulations and gratings, common in surface water fishes, have been an evolutionary consequence of the sunlight-wave interactions. It would be interesting to examine to what extent that argument is applicable to crustaceans and crustacean vision.

It would certainly seem plausible that eyes of crustaceans subjected to these naturally-generated underwater flickers should possess temporal characteristics that match the flicker rates created by the surface waves. Given the fact that crustaceans are not known to produce flickering light signals themselves by blinking or to be able to rapidly switch on and off their photoreceptor cells (as had once been suggested for Limulus: Fuortes and Hodgkin, 1964), the crustacean eye has to cope with the rapid successions of light and dark inherent to flickers in other ways. With regard to the structural organization of the eye, flickering lights usually lead to light adaptation and, if excessive, to photoreceptor damage (see below).

As a measure of the eye's physiological performance in the presence of flickers, i.e. its temporal resolution, the so-called ‘flicker fusion frequency’ (defined as the critical frequency at which discrete individual responses to a flickering stimulus become fused to a continuous response), has proved useful. The signals to generate flickers in connection with electrophysiological recordings can be of two kinds: (a) the periods between low and bright phases of the oscillations are of equal duration and, by necessity, become shorter as the frequency of the flickers increases or (b) the flash of light used as the stimulus is very brief, e.g. 1 ms, and remains of the same duration as the number of flashes per second delivered to the eye is increased. Most commonly the first kind of stimulation is used. Both depend on the eye's, or better, the visual cell's ability to ‘recover’ and to reach an excitable state each time again the bright phases of the flickers are followed by a light-trough.

From the small amount of data available (Table 1), the following generalizations seem possible: in comparison with insects (and especially flying species: Nakagawa and Eguchi, 1994), crustaceans with the exception of some semi-terrestrial species like Ligia, which does not avoid bright sunshine, possess much lower FFFs (Table 1). As with insects, however, FFF values increase as the intensity of the flashes used in the flickering lights increases. Whether the exceptionally low FFF of the Antarctic isopod Glyptonotus antarcticus (Fig. 16) has something to do with the subzero temperatures of the water in which the animal lives (Meyer-Rochow and Laughlin, 1997) or is a reflection of the fact that flickering lights are of no importance in that animal's habitat, remains an open question for the time being.

Table 1

Flicker fusion frequencies (FFFs) of the eyes of some crustacean species


Fig. 16

Flicker fusion frequency to flashes of white light in the Antarctic isopod Glyptonotus antarcticus (after Meyer-Rochow and Laughlin 1997).



Many crustaceans possess eyes with photoreceptor cells that respond to linearly polarized light. Depending on whether the e-vector of the polarized light excites the photopigment maximally or minimally, up to an at least tenfold sensitivity difference may be recorded intracellularly from a retinula cell under these two situations (Shaw, 1969). A crustacean, which turns its body or rotates its eyes in a polarized photic environment must therefore experience changes in ambient luminosity that cannot be too unlike fluctuations in absolute or spectral light intensities. Indeed, selective adaptations of those retinula cells maximally sensitive to a given e-vector should result in pigment distributions and other signs typical of receptor cells exposed to bright light.

While Waterman's (1981) review of polarization sensitivity is still timely and relevant especially with regard to the crustacean compound eye, considerable progress has been made in elucidating the physical details, the degree and direction of linear polarization, the “transmissivity and the shape of the refraction-polarization oval” of underwater polarization patterns (Horvath and Varju, 1995). To what extent the bright eye-glow seen in many dark adapted crustacean eyes is polarized remains to be measured. The molecular basis of crustacean polarization sensitivity has been revisited by Eguchi (1999), who reiterates, and provides further evidence, for the view that the orthogonal orientation of microvilli in separate retinula cells is the anatomical manifestation of e-vector discrimination. In other words, twisted crustacean rhabdoms (Meyer-Rochow, 1978) and retinula cells with multidirectional microvilli (e.g., retinula cell R8 in Libinia and other decapods: Eguchi and Waterman, 1967) cannot adequately convey information on the e-vector to the optic ganglia, whereas layered (or ‘banded’) rhabdoms, in which perpendicularly oriented plates of microvilli belonging to different cell groups apparently terminate as two separate channels in the lamina (Nässel and Waterman, 1977), can. Thus, ultrastructural analyses of crustacean rhabdoms may be used to make predictions on whether or not a given crustacean eye has the potential of being polarization sensitive. On the basis of retinal symmetries and microvillar directions, the compound eyes of mantis shrimps (Stomatopoda) ought to possess the most complicated polarization vision of any crustacean (Marshall et al., 1991).

In the crayfish eye, neurons of the lamina exhibit polarization sensitivities that are not directionally sensitive to e-vector rotations and are generally comparable to those of the receptor cells (Glantz and Bartels, 1984). However, medullary neurons of both the crab (Leggett, 1976) and the crayfish eye (Glantz, 1996, 2001) possess neurons that are highly sensitive to a rotating polarizer. It has been postulated by Glantz (1996) that this may be of importance to the animal in its natural environment as it has to respond to changing e-vectors due to rotations of the head, and that the tangential neurons responsible for the response may exploit the local variations in the e-vector to enhance motion detection at low contrasts. Other functions suggested by a variety of investigators over the years for underwater polarization sensitivity include contrast enhancement, maintenance of body position, navigational aid in (vertical) migration and orientation (Goddard and Forward, 1991). In the cephalopod Sepia officinalis, moreover, polarization vision plays a role in intraspecific communication (Shashar et al., 1996), but for crustaceans a similar role has yet to be demonstrated.


Obviously, crustacean photoreceptors can be damaged in a variety of ways. There is mechanical damage, perhaps due to (a) physical (wave action, water currents, collisions with inanimate objects, etc.) or (b) biological effects (attacks by predators, disease, incomplete moulting, etc.) and there is damage that is due to radiation (ionic, photic, thermal). This section will not deal with damage of a mechanical origin, but will focus instead on the other causes of damage. Crustaceans with one eye or both eyes painted or blinded (Fraenkel and Gunn, 1960) provide us with information on the role(s) the eyes play in the intact, undamaged animal. It has become clear that visually impaired crustaceans frequently display abnormal reactions (Meyer-Rochow and Tiang, 1984; Attramadal et al., 1985; Meyer-Rochow, 1988).

Light-induced photoreceptor damage (Fig. 17) in crustaceans results in suppressed visual sensitivity and has recently been reviewed (Meyer-Rochow, 1994). Unlike regular light-adaptation, which tends to result in a parallel shift of the V/log I curve so that brighter lights are required to produce the same receptor potential of the eye or receptor cell, damage manifests itself in a flattening of the V/log I curve, i.e., in a reduction of the slope of the V/log I relationship (Fig. 18). Like the less well-studied damage caused by prolonged darkness (reviewed by Eguchi, 1986), light-induced damage is undoubtedly multifactorial. The effects of ionizing radiation and X-rays, known to damage the vertebrate photoreceptor (e.g., Brunst, 1967), have not yet been examined in the crustacean eye. What we do know about light-induced damage in the crustacean eye deals almost entirely with the receptor cells and the rhabdom; much less is known about the effects of bright light on the dioptric structures cornea and crystalline cone (Meyer-Rochow, 1981; Meyer-Rochow and Tiang, 1984: Gaten, 1988). A total lack of information exists in relation to the question of whether and how the damage seen in the retinula cells affects the second-order neurons.

Fig. 17

Longitudinal section through normal (undamaged) rhabdom of the crayfish eye (a) and rhabdom that displays obvious light-induced membrane damage (b). Scale=1 μm (courtesy of E. Eguchi).


Fig. 18

Diagram showing differences between response/stimulus intensity curves of eyes from rock lobsters at night (curve on the left), during the day (curve in the centre), and following an exposure of 1 hr to sunlight (curve on the right).


Obviously, what constitutes light-induced damage has to be distinguishable from normal light-induced adaptations as well as membrane shedding and re-cycling, and that is not always easy (cf. Figs. 7 and 17). Another good example comes from the eye of the amphipod Pontoporeia affinis (Rosenberg and Langer, 1995). Taking, for instance microvillar diameter and ultrastructure, there are many reports of crustacean eyes that exhibit wider microvilli (Meyer-Rochow, 1999a) and fragmentation, or even loss, of the core filament during the day (Hevers and Stieve, 1995). An increase in free cellular Ca2+ has been linked to this lability of core filament architecture (Blest et al., 1982), but greater calcium concentrations are an inevitable consequence of photoreception in arthropods, generally (Dorlöchter and Stieve, 1997). Whether or not the retinula cell runs into problems and begins to destroy the photoreceptive membranes and, thereafter, itself (in that order: Meyer-Rochow and Järvilehto, 1997), depends on a variety of factors.

Clearly, photopigment concentration in the visual membranes and amount of opsin precursors in the cytoplasm are important, but so are G-proteins and lipid composition of the membranes. In fact, since it could be shown that, in Antarctica, crustacean eyes, containing predominantly long-chain polyunsaturated fatty acids (Meyer-Rochow and Pyle, 1980), were easily damageable by elevated temperature (Meyer-Rochow and Tiang, 1979; Meyer-Rochow, 1982), research was initiated to investigate the role lipids played in membrane maintenance. Differences in retinal lipid compositions were found in crayfish that came from high-latitude and medium-latitude environments (Meyer-Rochow et al., 1999a), providing further evidence for the view that ambient light levels and temperature influence membrane biochemistry. Elevated temperature alone can adversely affect membrane ultrastructure (Meyer-Rochow and Eguchi, 1984), but the most severe membrane disintegrations (Fig. 19) occur as a result of a combined bright light/elevated temperature assault (Lindström et al., 1988; Kashiwagi et al., 1997).

Fig. 19

(after Lindström et al. 1988). (a): Normal microvilli of the rhabdom of the opossum shrimp Mysis relicta, kept at 4°C. (b): Swollen microvilli of an individual of M. relicta, exposed to white light of 4000 lux for one hr, but subsequently kept in darkness for 5 days at 4°C. (c): Microvilli of M. relicta individual, kept in darkness and water at 14°C for 5 days, following an exposure to white light of 4000 lux for one hour. The damage exceeds that of (b). Scale (a,b,c)=0.5 μm.


Thermal and photic stress cause an increase in fatty acid 18:0 and decreases in acids 16:1, 20:1, and 22:6 (Kashiwagi et al., 1997), but that alone is insufficient to cause visible membrane damage. The latter is likely to occur when dormant lipoxygenases, present in all animal cells, get activated (Hölzel and Spiteller, 1995). They oxidize unsaturated membrane fatty acids, a process that does not as tacitly assumed involve only arachidonic acid, but also others (Hölzel and Spiteller, 1995). The oxidized fatty acids are then decomposed to chemically highly reactive species that further interfere with cellular organelles and their functions, leading to additional damage. The discovery of peroxidase activity (Fig. 20), e.g. in secondary lysosomes that degrade photosensory membrane (Schraermeyer and Stieve, 1991), fits this scenario, but a reported midday rhabdom enlargement paralleled by a decrease in multivesicular bodies (Piekos, 1989) seems difficult to reconcile with it and suggests that multivesicular body production and rhabdom diminution “are not causally related in the manner predicted by the lysosome-related-body hypothesis of rhabdom cycling”. However, membrane damage due to excessive light is likely to result in a disruption of normal membrane cycling and, therefore, may follow a different path.

Fig. 20

Immuno-gold-labelled active peroxisomes in the retinula cells of the eye of the crab Ucides sp. Scale=0.17 μm (courtesy Silvana Allodi and Ahmed Yagi).


Bright illumination of the retina can lead to the production of singlet oxygen and this can lead to membrane damage involving oxidation of either proteins or lipids or both, ultimately increasing fluidity of the membrane (Delmelle, 1977). Increases in the amount of peroxidated retinal fatty acids following an exposure to light in crayfish kept in the dark prior to irradiation were, indeed, recorded, but not until at least 2 hours after the exposure (Kashiwagi et al., 1997). This is consistent with the electron microscopical findings and means that sensitivity loss (very rapid) and membrane damage (delayed) are linked, but separate phenomena (Lindström et al., 1988). The key question is “What activates the dormant lipoxygenases?”. Hölzel and Spiteller (1995) list a variety of diseases in humans that qualify, diseases that have in common a tendency to weaken or injure cell membranes. Heat, in particular, is singled out as a potent liberator of the dormant lipoxygenases. Could, therefore, screening pigment granules, closely approaching the rhabdom in order to protect it against excessive radiation, aggravate the situation by absorbing light and slowly dissipating the gained energy as heat?

This is supported by the recent discovery by Meyer-Rochow et al. (1999b) that, in the crayfish retina, the eighth, distally placed retinula cell R8 (which has the rhabdomere most at risk due to its position) escapes damage and remains totally normal, while proximal rhabdomeres become almost unrecognizable due to the light-induced degradation (Fig. 21). Significantly, R8 is also the only retinula cell without screening pigment granules. However, other explanations cannot be ruled out and R8 membranes may be chemically different, contain another visual pigment, or are synthesized in a cell that does not operate on the same metabolic principle as the other retinula cells. Observations by Hafner et al. (1982) on white-eyed, pigmentless crayfish that also exhibit more damage in the proximal than in the distal rhabdom point into the same direction. Perhaps the total volume of visual mebrane in R8 is so small that it never gets in danger of receiving excessive amounts of damaging radiation. Membrane damage is a complex problem and in some species may continue in darkness after a brief, but very intense exposure (Shelton et al., 1985), more or less ruling out any prolonged heat effects. Damage is often more pronounced following exposure to shorter wavelengths (Meyer-Rochow and Tiang, 1984; Rapp and Smith, 1992), and can depend on the pre-exposure state of eye-adaptation (Nilsson and Lindström, 1983; Lindström et al., 1988), on population differences regarding tolerance to light (Meyer-Rochow and Lindström, 1998), depth at which the animals were caught (Gaten et al., 1990), dietary history (Tschugunoff, 1913), perhaps season (Suzuki et al., 1985), and time of day at which the exposure is carried out.

Fig. 21

(after Meyer-Rochow et al., 1999b) Proximal rhabdomeres of crayfish (a) exposed for 3 days to 5000 lux bright, white flashes of light, flickering at a rate of 3 Hz, exhibit considerbable damage, but the same treatment has virtually no effect on the microvilli of the distal rhabdomere R8 (b). Scale (a,b)=1 μm.


In conclusion, we have to admit that we have yet to establish whether or not the various manifestations of light-(and perhaps temperature-) induced damages to receptor cells and dioptric elements have a common origin. Regular adaptational phenomena such as pigment translocations and cell kinetics complicate the picture further and the occurrence of diurnally modulated membrane recycling makes it almost impossible to examine one effect in isolation from the others. Tissue cultures and lines of selected cell types from the crustacean eye could help, but in the absence of such material, the use of specific mutants is one promising avenue, the selection of species lacking, for instance, membrane recycling or dioptric elements like hydrothermal vent shrimps, is another.


[1] This paper is dedicated to my good friend Dr. Yukitomo Morita, formerly Professor of Physiolgy at Hamamatsu University, Medical School, who passed away on September 27th, 2001.


The author is indebted to Prof. Juhani Leppäluoto of the Physiology Department of Oulu University for generously providing space and facilities to accomplish this review; he also wishes to thank the staff of the photography unit of the School of Dentistry for their help with the illustrations and Prof. E. Eguchi (Yokohama City University, Japan) for having made available those micrographs credited to him in the appropriate figure legends. Finally, the author gratefully acknowledges permission given to him by Prof. K. Wiese to withdraw this manuscript from Wiese's book on the crustacean nervous system, so that it conld be published independently.



H. Arechiga, E. Bañuelos, E. Frixione, A. Picones, and L. Rodriguez-Sosa . 1990. Modulation of crayfish retinal sensitivity by 5-hydroxytryptamine. J Exp Biol 150:123–143. Google Scholar


R. H. Arechiga, B. Fuentes-Pardo, and B. Barrera-Mera . 1973. Circadian rhythm of responsiveness in the visual system of the crayfish. In F. Salanky ed. Neurobiology of invertebrates. Tihany. Budapest. pp. 403–421. Google Scholar


K. Arikawa, K. Kawamata, T. Suzuki, and E. Eguchi . 1987. Daily changes of structure, function and rhodopsin content in the compound eye of the crab Hemigrapsus sanguineus. J Comp Physiol A 161:161–174. Google Scholar


J. G. Attramadal, J. H. Fossa, and H. L. Nilsson . 1985. Changes in behaviour and eye morphology in Boreomysis megalops Sars (Crustacea; Mysidacea) following exposure to short periods of artificial and natural daylight. J Exp Mar Biol Ecol 85:135–148. Google Scholar


H. Autrum 1981. Light and dark adaptation in invertebrates. In H. Autrum ed. Handbook of sensory physiology, vol VII/6C, Comparative physiology and evolution of vision in invertebrates. Springer. Berlin, Heidelberg, New York. pp. 1–91. Google Scholar


S. N. Barnes and T. H. Goldsmith . 1977. Dark adaptation sensitivity and rhodopsin level in the eye of the lobster Homarus. J Comp Physiol 120:143–159. Google Scholar


B. Barrera-Mera and E. M. Abaster . 1978. Electrophysiological evidences of mutual modulating influences on the retinal activity of the cray-fish Procambarus bouvieri. Brain Res Bull 3:101–106. Google Scholar


B. Barrera-Mera and G. Y. Berdeja-Garcia . 1979. Bilateral effects of retinal shielding pigments during monocular photostimulation in Procambarus. J Exp Biol 79:163–168. Google Scholar


J. A. Bernal-Moreno, M. Miranda-Anaya, and M. L. Fanjul-Moles . 1996. Phase shifting the ERG amplitude circadian rhythm of juvenile crayfish by caudal monochromatic illumination. Biol Rhythm Res 27:299–301. Google Scholar


A. D. Blest and S. Stowe . 1997. A phospholipase inhibitor, manoalide, and a G-protein activator, Mas-7, both affect the turnover of photo-transductive membranes by crab retinas in darkness. J Comp Physiol A 180:347–355. Google Scholar


A. D. Blest, S. Stowe, and W. Eddey . 1982. A labile Ca2+-dependent cytoskeleton in the rhabdomeral microvilli of blowflies. Cell Tissue Res 223:553–573. Google Scholar


V. V. Brunst 1967. Acute radiation injury to the eye in the adult axolotl (Siredon mexicanum). Am J Roentgenol 100:948–955. Google Scholar


K. P. Bryceson 1986. Diurnal changes in photoreceptor sensitivity in a reflecting superposition eye. J Comp Physiol A 158:573–582. Google Scholar


K. P. Bryceson and P. McIntyre . 1983. Image quality and acceptance angle in a reflecting superposition eye. J Comp Physiol A 151:367–380. Google Scholar


S. C. Chamberlain 1998. Circadian rhythms in the horseshoe crab lateral eye: signal transduction and photostasis. Bioelectrochem Bioenergetics 45:111–121. Google Scholar


S. Chyb, P. Raghu, and R. C. Hardie . 1999. PUFAs activate Drosophila light-sensitive channels TRP and TRPL. Nature 397:255–259. Google Scholar


J. A. Coles, P. Marcaggi, C. Vega, and N. Cotillon . 1996. Effects of photoreceptor metabolism on interstitial and glial cell pH in bee retina: evidence of a role for NH4+. J Physiol 495:305–318. Google Scholar


T. W. Cronin 1986. Optical design and evolutionary adaptation in crustacean compound eyes. J Crust Biol 6:1–23. Google Scholar


T. W. Cronin 1992. Visual rhythms in stomatopod crustaceans observed in the pseudopupil. Biol Bull 182:278–287. Google Scholar


T. W. Cronin, N. J. Marshall, and R. L. Caldwell . 1994. The retinas of mantis shrimps from low-light environments (Crustacea; Stomatopoda; Gonodactylidae). J Comp Physiol A 174:607–619. Google Scholar


P. Debaisieux 1944. Les yeux des crustacés: structure, développement, réactions à l'éclairement. Cellule 50:9–122. Google Scholar


G. H. P. DeBruin and D. J. Crisp . 1957. The influence of pigment migration on vision of higher crustacea. J Exp Biol 34:447–462. Google Scholar


M. Delmelle 1977. Retinal damage by light: possible implication of singlet oxygen. Biophys Struct Mechanism 3:195–198. Google Scholar


M. A. Delpiano, U. Knollmann, H. Acker, and H. Langer . 1992. PO2 and pH changes in the retina of the crab Ocypode ryderi: evidence for aerobic glycolysis. J Comp Physiol B 162:502–507. Google Scholar


M. Dorlˆchter and H. Stieve . 1997. The Limulus ventral photoreceptor: light response and the role of calcium in a classic preparation. Progr Neurobiol 53:451–515. Google Scholar


P. Dudley 1969. The fine structure and development of the nauplius eye of the copepod Doropygus seclusus Illg. Cellule 68:7–35. Google Scholar


D. H. Edwards 1984. Crayfish extraretinal photoreception: behavioural and motoneuronal responses to abdominal illumination. J Exp Biol 109:291–306. Google Scholar


E. Eguchi 1986. Eye and darkness–Evolutionary and adaptational aspects. Zool Sci 3:931–943. Google Scholar


E. Eguchi 1999. Polarized light vision and rhabdom. In Ed by E. Eguchi and Y. Tominaga . Atlas of arthropod sensory receptors. Springer. Tokyo, Berlin, New York. pp. 33–46. Google Scholar


E. Eguchi and T. H. Waterman . 1967. Changes in retinal fine structure induced in the crab Libinia by light and dark adaptation. Z Zellforsch 79:209–229. Google Scholar


E. Eguchi and T. H. Waterman . 1976. Freeze-etch and histochemical evidence for cycling in crayfish photoreceptor membranes. Cell Tissue Res 169:419–434. Google Scholar


E. Eguchi, T. Seki, and T. Suzuki . 1989. Comparative studies of chromophore contents inside and outside the rhabdoms of arthropod compound eyes. J Comp Physiol A 165:589–604. Google Scholar


R. Elofsson 1965. The nauplius eye and frontal organs in Malacostraca (Crustacea). Sarsia 19:1–54. Google Scholar


R. Elofsson 1966. The nauplius eye and frontal organs of the nonmalacostraca (Crustacea). Sarsia 25:1–128. Google Scholar


R. Elofsson 1969. The ultrastructure of the nauplius eye of Sapphirina (Crustacea: Copepoda). Z Zellforsch 100:376–401. Google Scholar


R. Elofsson 1976. Rhabdom adaptation and its phylogenetic significance. Zool Scripta 5:97–101. Google Scholar


R. Elofsson and E. Hallberg . 1977. Compound eyes of some deep-sea and fjord mysid crustaceans. Acta Zool 58:169–177. Google Scholar


S. Exner 1891. Die Physiologie der facettirten Augen von Krebsen und Insekten. Deuticke. Leipzig. Google Scholar


W. H. Fahrenbach 1964. The fine structure of a nauplius eye. Z Zellforsch 62:182–197. Google Scholar


M. L. Fanjul-Moles and B. Fuentes-Pardo . 1988. Spectral sensitivity in the course of the ontogeny of the crayfish Procambarus clarkii. Comp Biochem Physiol 91A:61–66. Google Scholar


M. L. Fanjul-Moles, T. Bosques-Tistler, J. Prieto-Sagredo, O. Castañón-Cervantes, and L. Fernández-Rivera-Río . 1998. Effect of variation in photopreiod and light intensity on oxygen consumption, lac-tate concentration and behaviour in crayfish Procambarus clarkii and P. diguetti. Comp Biochem Physiol 119A:263–269. Google Scholar


G. S. Fraenkel and D. L. Gunn . 1960. The orientation of animals. Dover. New York. Google Scholar


T. M. Frank 1999. Comparative study of temporal resolutions in mesopelagic crustaceans. Biol Bull 196:137–144. Google Scholar


M. Frelon-Raimond, V. B. Meyer-Rochow, A. Ugolini, and G. Martin . 2001. First cytological description of intracerebral ocelli in an amphipod: the extraretinal photoreceptors of the sandhopper Talitrus saltator (Crustacea; Amphipoda). Invert Biol in press. Google Scholar


E. Frixione and H. Arechiga . 1981. Ionic dependence of screening pigment migrations in crayfish retinal photoreceptors. J Comp Physiol A 144:35–43. Google Scholar


E. Frixione and O. Perez-Olvera . 1991. Light-adapting migration of the screening-pigment in crayfish photoreceptors is a two-stage movement comprising an all-or-nothing initial phase. J Neurobiol 22:238–248. Google Scholar


E. Frixione, H. Arechiga, and V. Tsutsumi . 1979. Photomechanical migrations of pigment granules along the retinula cells of the crayfish. J Neurobiol 10:573–590. Google Scholar


B. Fuentes-Pardo and V. Inclan-Rubio . 1981. Correlation between motor and electroretonographic circadian rhythms in the crayfish Procambarus bouvieri (Ortmann). Comp Biochem Physiol 68A:477–485. Google Scholar


M. G. Fuortes and A. L. Hodgkin . 1964. Changes in time scale and sensitivity in the ommatidia of Limulus. J Physiol 171:239–263. Google Scholar


E. Gaten 1988. Light-induced damage to dioptric apparatus of Nephrops norvegicus(L.) and the quantitative assessment of the damage. Mar Behav Physiol 13:169–183. Google Scholar


E. Gaten, P. M. J. Shelton, C. J. Chapman, and A. M. Shanks . 1990. Depth related variation in the structure and functioning of the compound eye of the Norway lobster Nephrops norvegicus. J Mar Biol Ass UK 70:343–355. Google Scholar


E. Gaten, P. M. J. Shelton, and P. J. Herring . 1992. Regional morphological variations in the compound eyes of certain mesopelagic shrimps in relation to their habitat. J Mar Biol Ass UK 72:61–75. Google Scholar


G. Gaus and H. Stieve . 1992. The effect of neuropeptides on the ERG of the crayfish Orconectes limosus. Z Naturforsch 47c:300–303. Google Scholar


R. M. Glantz 1996. Polarization sensitivity in the crayfish optic lobe: peripheral contributions to opponency and directionally selective motion detection. J Neurophysiol 76:3404–3414. Google Scholar


R. M. Glantz 2001. Polarization analysis in crayfishl visual system. J-Exp Biol 204:2383–2390. Google Scholar


R. M. Glantz and A. Bartels . 1984. The spatiotemporal transfer function of crayfish lamina monopolar neurons. J Neurophysiol 71:2168–2182. Google Scholar


S. Goddard and R. B. Forward . 1991. The role of the underwater polarized light pattern, in sun compass navigation of Palaemonetes vulgaris. J Comp Physiol A 169:479–491. Google Scholar


R. L. Gregory, H. E. Ross, and N. Morey . 1964. The curious eye of Copilia. Nature (Lond) 201:1166–1169. Google Scholar


G. S. Hafner and T. R. Tokarski . 1998. Morphogenesis and pattern formation in the retina of the crayfish Procambarus clarkii. Cell Tiss Res 293:535–550. Google Scholar


G. S. Hafner and T. R. Tokarski . 2001. Retinal development in the lobster Homarus americanus : comparison with compound eyes of insects and other crustaceans. Cell Tiss Res 305:147–158. Google Scholar


G. S. Hafner, T. Tokarski, and G. Hammond-Soltis . 1982a. Development of crayfish retina: a light and electron microscopic study. J Morphol 173:101–118. Google Scholar


G. S. Hafner, T. Tokarski, C. Jones, and R. Martin . 1982b. Rhabdom degradation in white-eyed and wild-type crayfish after long term dark adaptation. J Comp Physiol A 148:419–429. Google Scholar


G. S. Hafner, T. R. Tokarski, and J. Kipp . 1992. Localization of actin in the retina of the crayfish Procambarus clarkii. J Neurocytol 21:94–104. Google Scholar


E. Hallberg and R. Elofsson . 1989. Construction of the pigment shield of the crustacean compound eye: a review. J Crust Biol 9:359–372. Google Scholar


E. Hallberg, M. Andersson, and D-E. Nilsson . 1980. Responses of the screening pigments in the compound eye of Neomysis integer (Crustacea: Mysidacea). J Exp Zool 212:397–402. Google Scholar


E. Hallberg, H. L. Nilsson, and E. Elofsson . 1980. Classification of amphipod compound eyes–the fine structure of ommatidial units (Crustacea, Amphipoda). Zoomorphol 94:279–306. Google Scholar


R. C. Hardie 1988. The physiology of the compound eyes of insects and crustaceans: S Exner, translated and annotated by RC Hardie. Springer. Heidelberg Berlin New York. Google Scholar


T. Hariyama, V. B. Meyer-Rochow, and E. Eguchi . 1986. Diurnal changes in structure and function of the compound eye of Ligia exotica. J Exp Biol 123:1–26. Google Scholar


T. Hariyama, V. B. Meyer-Rochow, T. Kawauchi, Y. Takaku, and Y. Tsukahara . 2001. Diurnal changes in retinula cell sensitivities and receptive fields (two-dimensional angular sensitivity functions) in the apposition eyes of Ligia exotica (Crustacea, Isopoda). J Exp Biol 204:239–248. Google Scholar


T. Hariyama, M. Yoshida, E. Eguchi, and V. B. Meyer-Rochow . 1982. Effect of circadian rhythm on spectral sensitivity and eye structure in Ligia exotica (Isop.). XVII Scand Congr Physiol Pharmacol (Reykjavik), Acta Physiol Scand Suppl 50837. Google Scholar


H. E. Henkes 1952. Retinomotor and diurnal rhythm in crustaceans. J Exp Biol 29:178–191. Google Scholar


P. J. Herring and H. S. J. Roe . 1988. The photoecology of pelagic oceanic decapods. Symp Zool Soc Lond 59:263–290. Google Scholar


W. Hevers and H. Stieve . 1995. Ultrastructural changes of the microvillar cytoskeleton in the photoreceptor of the crayfish Orconectes limosus related to different adaptation conditions. Tissue Cell 27:405–419. Google Scholar


P. Hiller-Adams and J. F. Case . 1988. Eye size of pelagic crustaceans as a function of habitat depth and possession of photophores. Vision Res 28:667–680. Google Scholar


A. H. Hines, T. G. Wolcott, E. Gonzalez-Gurriaran, J. L. Gonzales-Escalante, and J. Freire . 1995. Movement patterns and migrations in crabs: telemetry of juvenile and adult behaviour in Callinectes sapidus and Maja squinado. J Mar Biol Ass UK 75:27–42. Google Scholar


C. Hölzel and G. Spiteller . 1995. Zellschädigäng als Ursache für die Bildung von Hydroperoxiden ungesättigter Fettsäuren. Naturwissenschaften 82:452–460. Google Scholar


S. K. Itaya 1976. Light and dark adaptation in the accessory eye of the shrimp Palaemonetes. Tissue Cell 8:583–590. Google Scholar


G. Horvath and D. Varju . 1995. Underwater refraction-polarization patterns of skylight perceived by aquatic animals through Snell's window of the flat surface. Vission Res 35:1651–1666. Google Scholar


T. Kashiwagi, V. B. Meyer-Rochow, K. Nishimura, and E. Eguchi . 1997. Fatty acid composition and ultrastructure of photoreceptive membrane in Procambarus clarkii under conbditions of thermal and photic stress. J Comp Physiol B 167:1–8. Google Scholar


T. Kashiwagi, V. B. Meyer-Rochow, K. Nishimura, and E. Eguchi . 2000. Light activation of phospholipase A2 in the photoreceptor of the cray-fish (Procambarus clarkii). Acta Neurobiol Exp 60:9–16. Google Scholar


C. K. Kier and S. C. Chamberlain . 1990. Dual controls for screening pigment movement in photoreceptors of the Limulus lateral eye: circa-dian efferent input and light. Vis Neurosci 4:237–255. Google Scholar


C. A. King and T. W. Cronin . 1993. Cytoskeleton of retinular cells from the stomatopod Gonodactylus oerstedii : possible roles in pigment granule migration. Cell Tiss Res 274:315–328. Google Scholar


C. A. King and T. W. Cronin . 1994. Investigations of pigment granule transport systems in Gonodactylus oerstedii (Crustacea: Hoplocarida: Stomatopoda) II. Effects of low temperature on pigment granule position and microtubule populations in retinular cells. J Comp Physiol A 175:331–342. Google Scholar


K. Kiselyov and S. Muallem . 1999. Fatty acids, diacylglycerol, Ins(1,4,5) P3 receptors and Ca2+ influx. Trends Neurosci 22:334–337. Google Scholar


K. L. Kong and T. H. Goldsmith . 1977. Photosensitivity of retinular cells in white-eyed crayfish (Procambarus clarkii). J Comp Physiol 122:273–288. Google Scholar


G. K. Kulkarni and M. Fingerman . 1987. Distal retinal pigment of the fiddler crab, Uca pugilator : release of the dark-adapting hormone by methionine enkephalin and FMRFamide. Pigment Cell Res 1:51–56. Google Scholar


R. C. Lakin, R. N. Jinks, B. A. Battelle, E. D. Herzog, L. Kass, G. H. Renninger, and S. C. Chamberlain . 1997. Retinal anatomy of Chorocaris chacei, a deep-sea hydrothermal vent shrimp from the mid-Atlantic ridge. J Comp Neurol 385:503–514. Google Scholar


M. F. Land 1981a. Optics and vision in invertebrates. In H. Autrum ed. Handbook of sensory physiology. vol VII/6B:Springer. Berlin, Heidelberg, New York. pp. 471–592. Google Scholar


M. F. Land 1981b. Optics of the eyes of Phronima and other deep-sea amphipods. J Comp Physiol A 145:209–226. Google Scholar


M. F. Land 1984. Crustacea. In M. A. Ali ed. Photoreception and vision in invertebrates. Plenum. New York. pp. 401–438. Google Scholar


M. F. Land and D-E. Nilsson . 1990. Observations on the compound eyes of the deep-sea ostracod Macrocypridina castanea. J Exp Biol 148:221–233. Google Scholar


M. F. Land, F. A. Burton, and V. B. Meyer-Rochow . 1979. The optical geometry of euphausiid eyes. J Comp Physiol 130:49–62. Google Scholar


L. M. Leggett 1976. Polarized light-sensitive interneurons in a swimming crab. Nature (Lond) 262:709–711. Google Scholar


M. Lindström and H. Nilsson . 1984. Synförmagan hos pungrökan Mysis relicta I olika ljusmiljör. Mem Soc Fauna Flora Fenn 60:35–38. Google Scholar


M. Lindström, H. Nilsson, and V. B. Meyer-Rochow . 1988. Recovery from light-induced sensitivity loss in the eye of the crustacean Mysis relicta in relation to temperature increase: a study of ERG-determined V/log I relationships and morphology at 4°C and 14°C. Zool Sci 5:743–757. Google Scholar


N. J. Marshall, M. F. Land, C. A. King, and T. W. Cronin . 1991. The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda): 1. Compound eye structure: the detection of polarized light. Phil Trans Roy Soc Lond B 334:33–56. Google Scholar


G. Martin 1976. Mise en évidence et étude ultrastructurale des ocelles médians chez les crustacés isopodes. Annls Sci nat 18:405–436. Google Scholar


G. Martin, P. P. Jaros, J. Chaigneau, and V. B. Meyer-Rochow . 1995. Intracerebral ocelli in the giant Antarctic slater Glyptonotus antarcticus (Crustacea; Isopoda; Valvifera). J Crust Biol 15:228–236. Google Scholar


A. Matsushita, K. Arikawa, and E. Eguchi . 1999. Appearance of opsin-containing vesicles as rhabdomeric precursors and their incorporation into the rhabdom around dusk in the compound eye of the crab, Hemigrapsus sanguineus. Zool Sci 16:25–34. Google Scholar


W. N. McFarland and E. R. Loew . 1983. Wave-produced changes in underwater light and their relations to vision. In D. L. G. Noakes, et al eds. Predators and prey in fishes. Junk. The Hague. pp. 11–21. Google Scholar


R. R. Melzer, R. Diersch, D. Nicastro, and U. Smola . 1997. Compound eye evolution: highly conserved retinula and cone cell patterns indicate a common origin of the insect and crustacean ommatidium. Naturwissenschaften 84:542–544. Google Scholar


V. B. Meyer-Rochow 1975. Larval and adult eye of the western rock lobster (Panulirus longipes). Cell Tissue Res 162:439–457. Google Scholar


V. B. Meyer-Rochow 1978. The eye of mesopelagic crustaceans II: Streetsia challengeri (Amphipoda). Cell Tissue Res 186:337–350. Google Scholar


V. B. Meyer-Rochow 1981. The eye of Orchomene sp. cf. O. rossi, an amphipod living under the Ross Ice Shelf (Antarctica). Proc Roy Soc. Lond B 212:93–111. Google Scholar


V. B. Meyer-Rochow 1982. The divided eye of isopod Glyptonotus antarcticus : effects of unilateral dark adaptation and temperature. Proc Roy Soc Lond B 215:433–450. Google Scholar


V. B. Meyer-Rochow 1988. Spatial distribution and behaviour in bilaterally-blinded juveniles of the rock lobster Panulirus longipes. Res Crust 17:1–6. Google Scholar


V. B. Meyer-Rochow 1989. A re-investigation and re-interpretation of the cumacean photoreceptor. Zool Scripta 18:283–288. Google Scholar


V. B. Meyer-Rochow 1994. Light-induced damage to photoreceptors of spiny lobsters and other crustaceans. Crustaceana 67:97–111. Google Scholar


V. B. Meyer-Rochow 1999a. Compound eye: circadian rhythmicity, illumination, and obscurity. In ed by E. Eguchi and Y. Tominaga . Atlas of arthropod sensory receptors. Springer. Tokyo, Berlin, New York. pp. 97–124. Google Scholar


V. B. Meyer-Rochow 1999b. Photoreceptor ultrastructure in the Antarctic mussel shrimp Acetabulastoma (Crustacea; Ostracoda), a parasite of Glyptonotus antarcticus (Crustacea; Isopoda). Polar Biol 21:166–170. Google Scholar


V. B. Meyer-Rochow 2000. Visual membrane vulnerability: the fatty acid connection. Trends Neurosci 23:14–15. Google Scholar


V. B. Meyer-Rochow, D. Au, and E. Keskinen . 2001. Photoreception in fishlice (Branchiura): The eyes of Argulus foliaceus Linné 1758 and A. coregoni Thorell 1865. Acta Parasitol in press. Google Scholar


V. B. Meyer-Rochow and E. Eguchi . 1984. The effects of temperature and light on particles associated with crayfish visual membrane: a freeze-fracture analysis and electrophysiological study. J Neurocytol 13:935–959. Google Scholar


V. B. Meyer-Rochow and M. Järvilehto . 1997. Cytological postmoretm changes in highly specialized cells subjected to different causes of necrosis. Cytologia 62:41–46. Google Scholar


V. B. Meyer-Rochow and L. Juberthie-Jupeau . 1984. An open rhabdom in a decapod photoreceptor: structure and possible function of the eye of Typhlatya. Biol Cell 49:278–282. Google Scholar


V. B. Meyer-Rochow, T. Kashiwagi, K. Nishimura, and E. Eguchi . 1999a. Eye phospholipids and fatty acids from taxonomically related Finnish and Japanese crayfish of similar habitats, but separated by 25° of latitude. Comp Biochem Physiol B 123:47–52. Google Scholar


V. B. Meyer-Rochow, T. Kashiwagi, and E. Eguchi . 1999b. Effects of photic and thermal stress on distal and proximal rhabdomeres in cray-fish eye. Protoplasma 210:156–163. Google Scholar


V. B. Meyer-Rochow and S. B. Laughlin . 1997. Intracellular recordings from photoreceptors of the Antarctic isopod Glyptonotus antarcticus. In. 3rd Int Congr Physiol Sci (St Petersburg) p. P071.01. Google Scholar


V. B. Meyer-Rochow and M. Lindström . 1997. Light-induced photoreceptor sensitivity loss and recovery at 4∫C and 14°C in Mysis relicta Loven (Crustacea: Peracarida) from Pojoviken Bay (Finland). Annls Limnol 33:45–51. Google Scholar


V. B. Meyer-Rochow and H. L. Nilsson . 1999. Compound eyes in polar regions, caves, and the deep-sea. In ed by E. Eguchi and Y. Tominaga . Atlas of arthropod sensory receptors. Springer. Tokyo, Berlin, New York. pp. 125–142. Google Scholar


V. B. Meyer-Rochow and C. A. Pyle . 1980. Fatty acid analysis of lens and retina of two Antarctic fishes and the head and body of the Antarctic amphipod Orchomene plebs. Comp Biochem Physiol 65B:395–398. Google Scholar


V. B. Meyer-Rochow and W. A. Reid . 1996. Does age matter in studying the crustacean eye? J Comp Physiol B 166:319–324. Google Scholar


V. B. Meyer-Rochow and K. M. Tiang . 1979. The effects of light and temperature on the structural organization of the eye of the Antarctic amphipod Orchomene plebs (Crustacea). Proc Roy Soc Lond B 206:353–368. Google Scholar


V. B. Meyer-Rochow and K. M. Tiang . 1982. Comparison between temperature-induced changes and effects caused by dark/light adaptation in the eyes of two species of Antarctic crustaceans. Cell Tissue Res 221:625–632. Google Scholar


V. B. Meyer-Rochow and K. M. Tiang . 1984. The eye of Jasus edwardsii (Crustacea, Decapoda): electrophysiology, histology, and behaviour. Zoologica 45/134:1–61. Google Scholar


V. B. Meyer-Rochow, D. Towers, and I. Ziedins . 1990. Growth patterns in the eye of Petrolisthes elongatus. Exp Biol 48:329–340. Google Scholar


E. Moreno-Saenz, J. Hernandez-Falcon, and B. Fuentes-Pardo . 1987. Role of the sinus gland in crayfish rhythmicity: II. ERG circadian rhythm. Comp Biochem Physiol 87A:119–125. Google Scholar


M. Nagano 1986. Regional inhibitory effects of 5HT and GABA on the spontaneous electrical activity of a crab neurosecretory system. Biomed Res 7:267–277. Google Scholar


T. Nagashima 1990. Eye structure of externally eyeless grylloblattids (Insecta, Notoptera). Bull Sugadaira Mntane Res Ctr 11:89–93. Google Scholar


T. Nakagawa and E. Eguchi . 1994. Differences in flicker fusion frequencies of the five spectral photoreceptor types in the swallowtail butterfly's compound eye. Zool Sci 11:759–762. Google Scholar


D. R. Nässel and T. H. Waterman . 1977. Golgi EM evidence for visual information channelling in the crayfish lamina ganglionaris. Brain Res 130:556–563. Google Scholar


D. R. Nässel and T. H. Waterman . 1979. Massive diurnally modulated photoreceptor membrane turnover in crab light and dark adaptation. J Comp Physiol A 131:205–216. Google Scholar


D-E. Nilsson 1983. Refractive index gradients subserve optical isolation in a light-adapted reflecting superposition eye. J Exp Zool 225:161–165. Google Scholar


D-E. Nilsson 1989. Optics and evolution of the compound eye. In D. G. Stavenga and R. C. Hardie . eds. Facets of vision. Springer. Berlin. pp. 30–73. Google Scholar


D-E. Nilsson 1990. Three unexpected cases of refracting superposition eyes in crustaceans. J Comp Physiol A 167:71–78. Google Scholar


D-E. Nilsson, E. Hallberg, and R. Elofsson . 1986. The ontogenetic development of refracting superposition eyes in crustaceans: transformation of optical design. Tissue Cell 18:509–519. Google Scholar


D-E. Nilsson, I. Henrekson, and A-C. Järemo . 1989. Pupil control in compound eyes: more than one mechanism in moths. In ed by N. Singh and N. J. Strausfeld . Neurobiology of sensory systems. Plenum. New York. pp. 17–22. Google Scholar


H. L. Nilsson and M. Lindström . 1983. Retinal damage and sensitivity loss of a light-sensitive crustacean compound eye (Cirolana borealis): electron microscopy and electrophysiology. J Exp Biol 107:277–292. Google Scholar


T. Nordtug and S. Krekling . 1989. Steady-state and dynamic properties of photomechanical light and dark adaptation in the eye of the shrimp Eualus gaimardii (Crustacea, Natantia). J Exp Zool 250:117–127. Google Scholar


R. Odselius and D-E. Nilsson . 1983. Regionally different ommatidial structure in the compound eye of the waterflea Polyphemus. Proc Roy Soc London B 217:177–189. Google Scholar


P. J. O'Neill, R. N. Jinks, E. D. Herzog, B. A. Battelle, L. Kass, G. H. Renninger, and S. C. Chamberlain . 1995. The morphology of the dorsal eye of the hydrothermal vent shrimp, Rimicaris exoculata. Vis Neurosci 12:861–875. Google Scholar


J. E. Ong 1970. The micromorphology of the nauplius eye of the estuarine calanoid copepod, Sulcanus conflictus Nicholls (Crustacea). Tissue Cell 2:589–610. Google Scholar


W. B. Piekos 1989. Temporal separation of rhabdom shrinkage and MVB formation in the light-adapting crayfish retina. J Exp Zool 250:17–21. Google Scholar


E. Pyza and I. A. Meinertzhagen . 1995. Monopolar cell axons in the first optic neuropil of the housefly, Musca domestica L. undergo daily fluctuations in diameter that have a circadian basis. J Neurosci 15:407–418. Google Scholar


L. M. Rapp and S. C. Smith . 1992. Morphologic comparisons between rhodopsin-mediated and short-wavelength classes of retinal damage. Invest Ophthalmol Visual Sci 33:3367–3377. Google Scholar


S. Richter 1999. The structure of the ommatidia of the malacostraca (Crustacea)–a phylogenetic approach. Verh Naturwiss Ver Hamburg NF 38:161–204. Google Scholar


J. Rosenberg and H. Langer . 1995. Ultrastructure of the compound eyes of Pontoporeia affinis (Crustacea, Amphipoda) and effects of light on their fine structure. Zoology 99:138–150. Google Scholar


J. Rosenberg and H. Langer . 2001. Ultrastructural changes of rhabdoms of the eyes of Ocypode species in relation to different regimes of light and dark adaptation. J Crust Biol 21:345–353. Google Scholar


P. Ruck and T. L. Jahn . 1954. Electrical studies on the compound eye of Ligia occidentalis. J Gen Physiol 37:825–849. Google Scholar


D. C. Sandeman, R. E. Sandeman, and H. G. DeCouet . 1990. Extraretinal photoreceptors in the brain of the crayfish Cherax destructor. J Neurobiol 21:619–629. Google Scholar


R. E. Sandeman, A. H. D. Watson, and D. C. Sandeman . 1995. Ultrastructure of the synaptic terminals of thye dorsal giant serotonin-IR neuron and deutocerebral commissure interneurons in the accessory and olfactory lobes of the crayfish. J Comp Neurol 361:617–632. Google Scholar


H. Schiff, R. B. Manning, and B. C. Abbott . 1986. Structure and optics of ommatidia from eyes of stomatopod crustacea from different luminous habitats. Biol Bull 170:461–480. Google Scholar


U. Schraermeyer 1992. Effects of chloroquine on the photosensory membrane turnover and the ultrastructure of lysosome-related bodies of the crayfish photoreceptor. Z Naturforsch 47c:420–428. Google Scholar


U. Schraermeyer and H. Stieve . 1991. Peroxidase and tyrosinase are present in secondary lysosomes that degrade photosensory membranes of the crayfish photoreceptor: possible role in pigment granule formation. Pigment Cell Res 4:163–171. Google Scholar


N. Shashar, P. R. Rutledge, and T. W. Cronin . 1996. Polarization vision in cuttlefish–a concealed communication channel? J Exp Biol 199:2077–2084. Google Scholar


S. R. Shaw 1969. Sense-cell structures and interspecies comparisons of polarized light absorption in arthropod eyes. Vision Res 9:1031–1040. Google Scholar


P. M. J. Shelton, E. Gaten, and C. J. Chapman . 1985. Light and retinal damage in Nephrops norvegicus(L.) (Crustacea). Proc Roy Soc Lond B 226:217–236. Google Scholar


P. M. J. Shelton, E. Gaten, and C. J. Chapman . 1986. Accessory pigment distribution and migration in the compound eye of Nephrops norvegicus(L.) (Crustacea: Decapoda). J Exp Mar Biol Ecol 98:185–198. Google Scholar


S. Stowe 1980. Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk. Cell Tissue Res 211:419–440. Google Scholar


N. J. Strausfeld 1989. Beneath the compound eye: neuroanatomical analysis and physiological correlates in the study of insect vision. In D. G. Stavenga and R. C. Hardie . eds. Facets of vision. Springer. Berlin. pp. 317–359. Google Scholar


G. Struwe, E. Hallberg, and R. Elofsson . 1975. The physical and morphological properties of the pigment screen in the compound eye of a shrimp (Crustacea). J Comp Physiol A 97:257–270. Google Scholar


A. E. Stuart 1983. Vision in barnacle. Trends Neurosci 6:137–140. Google Scholar


E. Suzuki 1999. Photoreceptive membrane and phototransduction. In E. Eguchi and Y. Tominaga . eds. Atlas of arthropod sensory receptors. Springer. Tokyo. pp. 13–22. Google Scholar


T. Suzuki and E. Eguchi . 1987. Survey of 3-dehydroretinal as a visual pigment chromophore in various species of crayfish and other freshwater crustaceans. Experientia 43:1111–1113. Google Scholar


T. Suzuki, K. Arikawa, and E. Eguchi . 1985. The effects of light and temperature on the rhodopsin-porphyropsin visual system of the cray-fish, Procambarus clarkii. Zool Sci 2:455–461. Google Scholar


A. Terakita, H. Takahama, S. Tamotsu, T. Suzuki, T. Hariyama, and Y. Tsukahara . 1996. Light-modulated subcellular localization of the alpha-subunit of GTP-binding protein Gq in crayfish photoreceptors. Vis Neurosci 13:539–547. Google Scholar


A. Terakita, Y. Tsukahara, T. Hariyama, T. Seki, and H. Tashiro . 1993. Light-induced binding of proteins to rhabdomeric membranes in the retina of crayfish (Procambarus clarkii). Vision Res 33:2421–2426. Google Scholar


Y. Toh and T. H. Waterman . 1982. Diurnal changes in compound eye fine structure in the blue crab Callinectes. J Ultrastruct Res 78:40–59. Google Scholar


T. R. Tokarski and G. S. Hafner . 1984. Regional morphological variations within the crayfish eye. Cell Tissue Res 235:387–392. Google Scholar


S. C. Trowell, J. A. Clausen, and D. Blest . 1991. The principal light-phosphorylated protein of crab retina is a phosphatase. Comp Biochem Physiol 99B:785–792. Google Scholar


V. N. Tschugunoff 1913. Über die Veränderungen des Auges bei Leptodora kindtii (Focke) unter dem Einfluss von Nahrungsentziehung. Biol Centralbl 33:351–361. Google Scholar


A. Ugolini and G. Borgioli . 1993. On the “accessory eye” of shrimps (Decapoda, Natantia). Crustaceana 65:112–115. Google Scholar


R. Vaissière 1961. Morphologie et histologie compareés des yeux des crustacés copèpodes. Arch Zool Expér Genét 100:1–125. Google Scholar


B. Walcott 1974. Unit studies on light adaptation in the retina of the crayfish Cherax destructor. J Comp Physiol 94:207–218. Google Scholar


L. Wang-Bennett and R. M. Glantz . 1987. The functional organization of the crayfish lamina ganglionaris. 1.Nonspiking monopolar cells. J Comp Physiol 161:131–145. Google Scholar


E. J. Warrant 1999. Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation. Vision Res 39:1611–1630. Google Scholar


T. H. Waterman 1961. Light sensitivity and vision. In ed by T. H. Waterman The physiology of crustacea. vol 2:Academic Press. New York. pp. 1–64. Google Scholar


T. H. Waterman 1981. Polarization sensitivity. In H. Autrum ed. Handbook of sensory physiology. vol VII/6C:Springer. Berlin. pp. 281–469. Google Scholar


L. A. Wilkens 1988. The crayfish caudal photoreceptor: advances and questions after the first half century. Comp Biochem Physiol 91C:61–68. Google Scholar


B. Withyachumnarnkul, P. Pongtippatee, and S. Ajpru . 1995. N-acetyltransferase, hydroxyindole-O-methyltransferase and melatonin in the optic lobes of the giant tiger shrimp Penaeus monodon. J Pineal Res 18:217–221. Google Scholar


J. Zeiger and T. H. Goldsmith . 1993. Packaging of rhodopsin and porphyropsin in the compound eye of the crayfish. Vis Neurosci 10:193–202. Google Scholar


J. Zeil and J. M. Zanker . 1997. A glimpse into crabworld. Vision Res 37:3417–3426. Google Scholar


I. P. Ziedins and V. B. Meyer-Rochow . 1990. ERG-determined spectral and absolute sensitivities in relation to eye size in the half crab Petrolisthes elongatus. Exp Biol 48:319–328. Google Scholar
V. Benno Meyer-Rochow "The Crustacean Eye: Dark/ Light Adaptation, Polarization Sensitivity, Flicker Fusion Frequency, and Photoreceptor Damage," Zoological Science 18(9), 1175-1197, (1 December 2001).
Received: 25 September 2001; Published: 1 December 2001
vision, eye
Back to Top