N. Justin Marshall

Multiple spectral classes of photoreceptors in the retinas of gonodactyloid stomatopod crustaceans

Summary1.We examined the compound eyes of 2 species of gonodactyloid stomatopods, Gonodactylus oerstedii and Pseudosquilla ciliata, using end-on microspectrophotometry of frozen sections of dark-adapted retinas.2.The cornea and crystalline cones of both species were virtually transparent from 350 to 700 nm. Primary screening pigment granules in the retinular cells had the broad absorption spectra typical of ommochromes. Colored vesicles, of unknown function, also were found in the cytoplasm of the retinular cells. The intrarhabdomal filters appeared to act as long-pass spectral filters, and had maximum optical densities in situ of 0.94 to 11.1.3.A variety of visual pigments were found in both species, each in a specific retinal region. Their maximum absorption peaked at wavelengths from 400 nm to well beyond 530 nm.4.Spectral sensitivity functions of all retinal regions were estimated. In both species, each of the 4 most dorsal ommatidial rows of the central band had a pair of narrow spectral sensitivitity curves, usually separated by 50 to 75 nm. These 4 pairs covered the spectrum from below 400 to beyond 650 nm. The other 2 rows of the central band had identical, broad sensitivity functions. Spectral sensitivities of all peripheral ommatidia in each species were identical, but different from any region of the central band.5.These stomatopod species have retained the typical crustacean layered rhabdoms in the peripheral retina and the 2 most ventral rows of the central band, but have converted the photoreceptors of the 4 dorsal rows of the central band into as many as 8 narrowly tuned spectral classes. This design could serve a high-quality hue discrimination system.

Specialization of retinal function in the compound eyes of mantis shrimps

Visual function and its specialization at the level of the retina were studied in 13 species of stomatopod crustaceans, representing three superfamilies: Gonodactyloidea, Lysiosquilloidea, and Squilloidea. We measured attenuation and irradiance spectra in the environment of each species, at the actual depths and times of activity where we observed individuals. We also characterized the intrahabdomal filters of all study species and determined the absolute spectral sensitivity functions and approximate photon capture rates of all photoreceptor classes below the level of the 8th retinular cell in seven of these species. Shallow-water gonodactyloid species have four distinct classes of intrarhabdomal filters, producing photoreceptors that are relatively insensitive but which have the broadest spectral coverage of all. Deep-water gonodactyloids and all lysiosquilloids have filters that are spectrally less diverse. These species often discard the proximal filter classes of one or more receptor types. As a result, their retinas are more sensitive but have reduced spectral range or diversity. The single squilloid species has the most sensitive photoreceptors of any we observed, due to the lack both of intrarhabdomal filters and tiered photoreceptors. Photon absorption rates, at the times of animal activity, were similar in most photoreceptor classes of all species, whether the receptors were tiered or untiered, or filtered or unfiltered. Thus, the retinas of stomatopods are specialized to operate at similar levels of stimulation at the times and depths of actual use, while evidently maintaining the greatest possible potential for spectral coverage and discrimination.

Stomatopod photoreceptor spectral tuning as an adaptation for colour constancy in water

Where colour is used in communication absolute judgement of signalling spectra is important, and failures of colour constancy may limit performance. Stomatopod crustaceans have unusual eyes in which the midband contains ten or more classes of photoreceptor. For constancy based on receptor adaptation to a fixed background, elementary theory predicts and we confirm by modelling, that stomatopods narrow-band receptors outperform more broadly tuned receptors. Similar considerations could account for the small spectral separation of receptors in each midband row. Thus, stomatopods seem to trade-off sensitivity and signal-to-noise ratio for increased colour constancy.

Ultraviolet photoreception in mantis shrimp.

An UV-sensitive class of photoreceptors exists in all regions of the retinas of mantis shrimps. UV photosensitivity apparently resides in rhabdomeres of the eighth retinular cell (R8) that lies atop each rhabdom; and in ommatidia where the R8 rhabdomere consists of microvilli parallel in a single direction, sensitivity is maximal when the e-vector of plane-polarized light is parallel to the microvilli. Spectral sensitivity of the UV photoreceptor peaks at 345 nm and is best explained by the presence of a photopigment with lambda max near 325 nm overlain by material that absorbs UV light at wavelengths below approximately 350 nm. Rhabdomeres of R8 cells in several different retinal regions of a variety of species examined contain a photopigment absorbing maximally below 340 nm. Under appropriate conditions, a metapigment with lambda max near 460 nm can be formed. UV vision may be useful for enhancing the visual contrast of midwater predators or prey.

The intrarhabdomal filters in the retinas of mantis shrimps.

The intrarhabdomal filters in the photoreceptors of compounds eyes of 32 species of mantis shrimps (Crustacea: Stomatopoda), representing seven families within the superfamilies Lysiosquilloidea and Gonodactyloidea, were surveyed by microspectrophotometry of filters in fresh cryosections of the retina. A total of up to four classes of filters exist in stomatopods: two each in Rows 2 and 3 of the midband. All lysiosquilloid species lacked the proximal filter in Row 3; a few also lacked the proximal Row 2 class. While most gonodactyloid species had all four possible classes, in some species the proximal filters of Row 3 and (in one case) Row 2 were missing. In all, at least 11 distinct spectral classes of pigments were found. Absorption spectra suggested that the filter pigments were probably carotenoids or carotenoproteins, although the distal filter of Row 3 was often exceptional, appearing to contain a mixture of pigments. While the types of pigments found in the filters of the various species generally followed taxonomic lines, numerous exceptions were found that were apparently related to the ecological requirements of the various species.

COMPOUND EYES AND OCULAR PIGMENTS OF CRUSTACEAN LARVAE (STOMATOPODA AND DECAPODA, BRACHYURA)

Larvae of decapod and stomatopod crustaceans possess paired compound eyes not unlike those of adult crustaceans. However, the visual demands of larval and adult life differ considerably. Furthermore, the eyes of adult stomatopods appear to be far more specialized than those of the larvae. We examined eyes of several stomatopod species just before and after larval metamorphosis. At this time, the entire larval retina is joined by a new, adult-type retinal array which gradually replaces the remnants of the larval retina. The new retina of the postlarva is anatomically similar to that of the full-grown adult, and has virtually identical assemblages of intrarhabdomal filters. We determined the photopigments of Gonodactylus aloha, the only species for which we were able to obtain both larval and adult specimens, using microspectrophotometry. The single middle-wavelength larval rhodopsin (λmax= 499 nm) disappears at metamorphosis; none of the 10 classes of adult rhodopsins has λmax between 473 and 510 nm. This metamorphic change of visual pigment does not occur in a comparison species of decapod crustacean, the blue crab Callinectes sapidus. Here, rhodopsins both of the megalops larva and the adult had λmax at 503-504 nm. The difference between these two species can be explained by the varying ecological requirements of their larvae and adults, and more study of visual pigments in retinas of larval and adult crustaceans is warranted.

Optokinesis in gonodactyloid mantis shrimps (Crustacea; Stomatopoda; Gonodactylidae)

Summary1.We investigated optokinetic eye movements in 3 species of stomatopod crustaceans (Odontodactylus scyllarus, Pseudosquilla ciliata, and Gonodactylus oer stedii), all of which are members of the superfamily Gonodactyloidea, by making video recordings of their behavior when placed at the center of a rotating striped drum. Results from these species were sufficiently similar to permit a general description of optokinesis in gono dactyloid stomatopods.2.Within the range of drum speeds tested (0.40 to 33.6° s-1), the eyes frequently moved smoothly in the direction of the drums rotation. The movements of the 2 eyes were only weakly coordinated, and optokinesis occurred with an irregular and intermittent time course.3.Closed-loop gains varied with the drums speed of rotation, ranging from 0.4 to near 1.0. The gain did not depend on the orientation of the eye in space, remaining relatively constant as the eye swung on its point of at tachment to the anterior end of the animal or rotated on the eyestalk axis.4.In O. scyllarus (the only species tested), optokinetic eye movements in the animals vertical, dorsoventral plane occurred with characteristics similar to those in the horizontal plane.