The use of different eye regions in the mantis shrimp Hemisquilla californiensis Stephenson, 1967 (Crustacea: Stomatopoda) for detecting objects

Abstract

A behavioral assay was used to assess the ability of the stomatopod Hemisquilla californiensis to perceive and respond to a moving target under different wavelengths and intensities of light illumination. Subjects responded to targets rotating horizontally across their visual field by a brief startle response of their eyes or antennules but did not track the targets. Under white light responses were elicited down to a light intensity of 0.9 μW cm^− 2. Responses were seen in blue light at intensities as low as 0.5 μW cm^− 2, and in green light down to 1.0 μW cm^− 2. The animals were less sensitive to red light, with no responses seen at intensities below 3.0 μW cm^− 2. Subjects did not respond to the targets at all under infrared light. This response pattern mirrors the computed sensitivity spectrum of ommatidia in the species' peripheral hemispheres but not that in most of the central bands. We conclude that this species uses the monochromatic vision in the peripheral hemispheres of its eyes to recognize objects and that the sharply tuned color receptors of the central band serve to add supplemental information if light conditions allow.

Introduction

The eyes of stomatopods are structurally and functionally more complex than those of most other crustaceans (Cronin et al., 1988, Cronin et al., 2000, Marshall, 1988). In crustaceans such as crabs the ommatidia in different eye regions are similar in structure and contain only 2–3 different types of pigment (Cronin and Forward, 1988, Sakamoto et al., 1996). Stomatopod eyes, in contrast, are divided into several different morphological regions, each with its own ommatidial structure as well as its own type of pigments and characteristic spectral sensitivity. The stomatopod eye is usually elliptical rather than spherical. It has two peripheral hemispheres composed of many rows of ommatidia (Fig. 1). These hemispheres provide a wide angle of vision in both the vertical and horizontal dimensions and probably allow stereoscopic vision in each eye (Milne and Milne, 1961, Marshall and Land, 1993). Except in the deep-sea Bathysquilloidea, the hemispheres are separated by a midband which usually contains 6 rows of ommatidia. The ommatidia in these 6 central rows are parallel to one another and directed at the same area as are the nearby ommatidia in the peripheral hemispheres. Hence, the central part of the visual field for each eye is viewed simultaneously by three different sets of ommatidia (Marshall, 1988, Cronin et al., 1988).

The pigments and spectral sensitivities in the different regions of stomatopod eyes have been well characterized. Stomatopods have as many as 11 different visual pigments, which through a combination of receptor stacking and screening pigments may have as many as 16 different patterns of absorbance, each with its own maximum spectral sensitivity (S_max) (Marshall et al., 1999). In the peripheral hemispheres, rhabdoms are similar to those seen in other crustaceans, with a short R8 cell distally placed over a longer R1–7 rhabdom tier (Marshall et al., 1999). These ommatidia have a single broad peak of spectral sensitivity, mostly in the blue and blue-green (Fig. 2). The 6 rows of midband ommatidia have a much more complex structure and sensitivity. The first 4 rows seem to be specialized for color vision (Marshall et al., 1999). In a pattern unusual for crustaceans, the photoreceptor segments are two-tiered within the rhabdoms, with different visual pigments in each tier, plus have colored intrarhabdomal filters between the two tiers. This arrangement results in a very sharp spectral tuning of each retinal area, which may allow sensitive discrimination of colors. The maximum sensitivity of each row and tier is different from that of the others. Together they are sensitive to an unusually wide spectrum of colors for aquatic species, especially in the Gonodactyloids in which S_max in these rows ranges from 400 to nearly 700 nm (Cronin et al., 1994b, Cronin et al., 2000, Marshall et al., 1999). The bottom two rows of ommatidia appear to be specialized for polarization vision (Marshall, 1988, Marshall et al., 1991, Marshall et al., 1999, Cronin et al., 2000, Cronin et al., 2002, Cronin et al., 2003). In addition, the R8 cells in several different regions of the eye are sensitive to ultraviolet light (Marshall et al., 1999).

Stomatopods are highly visually oriented and are primarily tropical species. Many species, especially Gonodactyloids, inhabit shallow water and are exposed to a broad spectrum of light (Cronin and Marshall, 1989, Cronin et al., 1994b). Many species rely on colored spots on their exoskeleton for intraspecific signaling (Caldwell and Dingle, 1975, Caldwell and Dingle, 1976, Hazlett, 1979, Marshall et al., 1996, Chiao et al., 2000). They can learn to discriminate different colors in response to a food reward (Marshall et al., 1996). Their specialized eyes, sensitivity to a broad spectrum of color, and obvious visually influenced behavior make them appropriate models for investigating the correlation between their behavior and the visual inputs from different regions of their eyes.

Hemisquilla californiensis is a deep-living gonodactyloid stomatopod found off the coast of California and the Pacific coast of Central America. It is often found in relatively turbid warm temperate water, and may be found down to 114 m depth (Schiff and Hendrickx, 1997). Its preferred habitat is silty sand, in which it digs a home burrow (Basch and Engle, 1989). At these depths and in warm temperate water, light is much more attenuated than at the surface and spectrally narrowed into blues and greens. Nevertheless, the animals have well-developed eyes and visual interactions with their surroundings are very important. The animals are brightly colored, including pink, yellow, red, and iridescent blue. Their eyes, although the absorbance peaks are shifted more toward blue and green than in most gonodactyloids, still have a broad range of maximum sensitivities ranging from below 400 nm to beyond 650 nm (Cronin et al., 1994a, Cronin et al., 2000). As in other stomatopods, different portions of the eye have quite different color sensitivities (Fig. 2). Assuming that rhabdoms may generate a usable signal at all wavelengths for which sensitivity is at least 10% of their maximum sensitivity, and using the data from Cronin et al. (1994a), the peripheral hemispheres of this species have a broad peak of sensitivity from 400 to nearly 600 nm and are still useful up to about 625 nm. This would allow them to perceive blue, green, yellow, and even some orange with the peripheral hemispheres. In the midband, row 1 has a sensitivity range from below 400 to about 550, and could perceive blue and green. Row 2 has sensitivity from about 510 to 650 and could perceive green, yellow, orange, and some red. Row 3 has sensitivity from 600 to 675 and can only perceive orange and red, nearly to the infrared range. Row 4 is sensitive from 475 to 590 and perceives blue, green, yellow, and orange. Rows 5 and 6 have similar sensitivity as do the peripheral hemispheres and perceive blue to orange. Various portions of their eyes, then, are sensitive to different portions of the spectrum from nearly ultraviolet to the edge of infrared, in addition to their R8 receptors which are sensitive to ultraviolet. At the same time, no portion of the eye can see all the colors the animal may be exposed to.

In this paper we used a behavioral assay to determine which wavelengths of light among the many this species is sensitive to are used in perceiving and recognizing objects, and infer which regions of the eye must be used for this process based on spectral sensitivity.