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Marine Biological Laboratory, Woods Hole, Massachusetts 02543
When a trilobite larval Limulus hatches from an egg, it begins to forage with the locomotor abilities of an adult but not with the vision of an adult. Its lateral eyes have fewer than 2% of the photoreceptors possessed by an adult. Our understanding of the way an adult horseshoe crab sees its environment is now sufficiently advanced that its visual processes can be mathematically modeled (1). Guided by this model, we have set out to examine how the lateral eye and visually guided behavior develop. Here we report on how photoreceptors, or ommatidia, are added during development, and how the eyes of juvenile crabs sample visual space.
We collected eggs from nests on tidal flats of Cape Cod, Massachusetts, from June 4 to 12, 2001 and maintained them under natural diurnal lighting in Petri dishes in the laboratory. In 3–4 weeks the eggs hatched into trilobite larvae, or Stage I crabs (3 mm wide), and 4 weeks later the larvae molted into Stage II crabs (5.5 mm wide). To analyze the ommatidial array at both stages, we photographed the eyes with a Zeiss Axiocam attached to an Axioplan II compound microscope. The array is clearly distinguishable in some parts of the eye but is partially obscured in others by retinal pigmentation. We analyzed photographs taken at various eye orientations to resolve and reconstruct the arrays of lateral eyes in Stage I and II crabs.
Lateral eyes of trilobite larvae (Stage I) approximate an equilateral triangle (100–120 µm on a side) containing 14 to 17 ommatidia (Fig. 1). We observed a gradient of ommatidial diameters within the array, with the largest ommatidium at the posterior apex, and the smallest at the base. In the larval eye in Figure 1 (left), the diameters of the largest and smallest ommatidia are 26 µm and 15 µm, respectively.
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Juvenile horseshoe crabs (stages VI [16 mm wide] to X [40 mm]) were also collected on tidal flats of Cape Cod from June 4 to 12, 2001. We maintained them under diurnal lighting in shallow troughs in the laboratory. They were fed, and their water was changed weekly. To assess the growth of their lateral eyes, we placed five scars along the anterior and ventral edges of the cornea with a sharp metallic needle (diameter 50 µm). Using a Zeiss SV11 stereoscope, we photographed the scarred eyes before and after each animal molted. We also photographed their molted shells to supplement the original records of their eyes.
To assess the visual field of the juvenile eye, we adapted the method of Herzog and Barlow (2). With the high magnification of a stereomicroscope, we identified the ommatidium whose optic axis was aligned with that of the microscope. By changing the orientation of the molt, we measured the optic axes of numerous ommatidia and determined the visual field of the eye as well as its resolution in various parts of the visual field. We analyzed the growth of the lateral eye at various stages and found, as others have, that the eye adds ommatidia at each molt (3,4).
When a Stage IX crab (30 mm wide) molted to a Stage X crab (38 mm), its right lateral eye increased from 1.8 to 2.2 mm along the anterioposterior axis, adding approximately 90 ommatidia (490 to 580) in agreement with morphometric data of Waterman (3). The diameter of ommatidia in the medial and posterior regions of the eye increased from 64 µm to 78 µm. Scars along the anterior edge shifted posteriorly, revealing the addition of 5 columns of about 90 small ommatidia (52 µm in diameter). This result supports previous observations that the lateral eye grows by adding new photoreceptors at its anterior edge (4). A similar result was reported for the dragonfly eye using the same scarring technique (5). Curiously, the ventral scars moved dorsally by about 5 ommatidial diameters. This movement is not associated with the addition of new ommatidia because the number of ommatidia medial and posterior to the scars was the same in both the molt and the crab. Apparently the outer scarred cornea of the Stage X crab had not grown as much as the underlying matrix of lens facets.
A juvenile crab has about the same visual field as an adult, but samples it differently. This can be demonstrated by locating the unique "index" ommatidium, which is the ommatidium with its optic axis horizontal and normal to the body axis of the crab. It is located near the center of the adult eye, but in a more posterior position in juveniles. The younger the crab, the more posterior is the location of the index ommatidium. For example, 22% of ommatidia in a Stage VIII eye lie posterior to the index ommatidium, whereas 35% do in a Stage XII eye. Consequently, juveniles sample the anterior region of visual space with a greater proportion of ommatidia than an adult eye. However, they do so with about half the horizontal resolution (0.05 cycles/deg, Ref. 2) of an adult because they possess fewer columns of ommatidia. On the other hand, juveniles have about the same vertical resolution as an adult (0.1 cycles/deg above, and 0.2 cycles/deg below the horizon) because they possess vertical columns with about the same number of ommatidia (23 to 26) as an adult.
Pulsatile growth of the eye at the anterior edge modifies its view of the world after each molt. That is, ommatidia viewing the most anterior region of the animal’s visual space now sample a more lateral region of visual space. As a consequence, the retinotopic map in the brain must undergo comparable rearrangements to accommodate inputs from new ommatidia sampling visual space in front of the animal. The retinotopic map has been determined for adult animals at the first two synaptic layers in the brain (6), but that of the juvenile remains to be studied. The retinotopic map must be plastic to accommodate the changing retinal mosaic as the eye grows.
Supported by grants from the National Science Foundation, National Eye Institute, and the National Institutes of Mental Health. C. McGuiness and S. Meadors received REU Fellowships from the National Science Foundation. We thank the Monomoy National Wildlife Refuge, Morris Island, Chatham, Massachusetts.
Footnotes
1 University of South Carolina. 
3 SUNY Upstate Medical University.
Literature Cited
This article has been cited by other articles:
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  K. Smith, C. Ridings, F. A. Dodge, and R. B. Barlow Development of the Lateral Eye of Juvenile Limulus Biol. Bull., October 1, 2002; 203(2): 222 - 223. [Full Text] [PDF]
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