Ontogeny of vision in marine crustaceans

Ontogeny of Vision in Marine Crustaceans1

SYNOPSIS. Marine crustaceans present an extremely interesting set of examples in which to examine visual development and metamorphosis. Larvae of these animals are almost always planktonic, living in the light field of open waters. The presence of a simple, predictable photic environment, the relatively basic visual requirements of larvae, and the need to remain transparent to reduce predation lead to the use of a single eye type throughout all marine crustacean larvae. Adult crustaceans, on the other hand, use a greater diversity of optical designs than all other animals combined, occupy habitats from the deep sea to mountaintops, and have very complex visual systems and behaviors. Thus, visual development varies tremendously among modern Crustacea. In this brief review, we consider the structure and development of marine crustacean eyes, focusing on optics, retinal design, and metamorphosis of the visual pigments.

INTRODUCTION

When animals live in very different environments during different stages of their development, and their sensory requirements change, their sensory systems are obligated to undergo considerable reorganization as ontogeny proceeds. Such is the case with the great majority of marine crustacean species, which almost always pass through a planktonic larval existence before metamorphosing to benthic or nektonic adult forms. Frequently, the habitats of larvae and adults differ greatly from each other in the structure of the visual world, as well as in the intensity and spectral distribution of the illumination.

Perhaps even more significantly, the visual tasks of larvae and adults rarely have much in common. Larval vision is primarily concerned with orientation in the water column, vertical migration, and avoidance of predators (Forward et al., 1984; Tankersley et al., 1995). Adult vision is employed for far more elaborate tasks in addition to these: navigation, prey recognition and capture, spatial vision, mate selection, and communication (see reviews of Wehner, 1981; Cronin, 1986). Consequently, adult eyes are often quite unlike those of the larvae (for an example drawn from the stomatopods, see Fig. 1). Even when adult and larval crustaceans inhabit the same environments (as in the case of mesopelagic shrimps, such as the oplophorids), the adult visual system is far more complex than what exists in the larval stages and demands specialized ocular adaptations.

In this review, we will focus primarily on crustacean taxa that include large, powerful marine animals as adults: decapods and stomatopods. Less is known of larval sensory development in other crustaceans, many of which undergo direct development and thereby avoid the challenge of metamorphosis in any case. Our focus will be on the structure and function of the eyes of planktonic crustacean larvae, as these seem to be similar throughout the group, and on some of the changes that must occur as the eye takes on the structure and functions required by the adult.

STRUCTURE OF CRUSTACEAN LARVAL EYES

Throughout the euphausiids, decapods, and stomatopods, larvae invariably possess compound eyes, which are naturally complicated structures. Making such an eye presents a planktonic crustacean larva with an impossible dilemma: the primary passive defense of plankton is transparency, but photoreceptors by definition must absorb light and thereby sacrifice transparency (see Nilsson, 1996 for discussion). The problem is compounded by the need to shield the independent optical units of the eye to preserve some level of optical independence between them and to reduce off-axis stimulation. This screening requires additional light-absorbing material, decreasing transparency yet further. Crustacean larvae respond in the simplest possible way to this challenge; they condense their retinas to a tiny clump in the eye's center, packing the visual and screening pigments into a compact mass. The optical design of a compound eye that permits the smallest retinal radius is the apposition type, so it is not surprising that this is the optical plan used in all larval crustacean compound eyes (Fincham, 1984; Nilsson, 1983; Nilsson et al., 1986; Cronin, 1986; Douglas and Forward, 1989; Gaten, 1998).

Each photoreceptor unit in an apposition compound eye receives input through a single optical system. With proper design (Nilsson, 1983), the optics can be isolated in each ommatidium without shielding and thus remain transparent, as their function is only to refract light onto the receptors. In crustacean larval eyes, the receptor array is tightly bunched into a sphere surrounding the geometrical center of the eye. This array consists of radially oriented photoreceptors (rhabdoms) separated by screening pigment. As mentioned above, the screening pigment is essential; otherwise, the rhabdoms would receive light from all directions, destroying any spatial information. The pigment must lie not only alongside receptors, but also underneath them to prevent light entering from the "wrong" end.