Stomatopod Vision: A More Delightful Vision by Peter A. Ensminger
The article below is taken with permission from parts of Chapter 6 of Peter A. Ensminger's book "Life Under the Sun", a very interesting collection of essays on the many ways light affects the lives of various plants, animals and other organisms. Thanks to Peter for re-introducing me to the the cellular slime molds, an extremely interesting group of critters that I used to hunt for in the tropics.
The colors we see depend on the wavelength sensitivities of the visual receptors within our eyes as well as the wavelengths of light that enter our eyes. In color vision, light excites different classes of photoreceptor cells, containing different visual pigments, and the brain compares their differential light absorption. Thus, in bright light, we humans see a colorful world because the cone cells in our retinas have three visual pigments, with maximal sensitivities in the blue (~425 nm), green (~530 nm), and red (~560 nm) regions of the spectrum and the differential responses of these cells enables color vision (1a). But our own colorful world pales in comparison to the world of the mantis shrimps. These Crustaceans must be considered the champions of color vision, since their eyes have more than ten different classes of visual pigments.
The eyes of these Crustaceans have eight classes of visual pigments for detection of color, as well as additional classes of visual pigments for sensing the polarization and distribution of light. In addition, they have the ability of depth perception with a single eye, and sample their environment with many intricately coordinated eye movements.
How do its compound eyes work?
The human eye works like a camera, in that it uses a large light refractive lens to focus light onto a large photosensitive retina at the back of the eyeball. In contrast, the eyes of mantis shrimps and many other Crustaceans are classified as "apposition compound eyes", very different from the "simple camera eyes" of humans. Apposition compound eyes are composed of many tiny optical elements (ommatidia), each with its own cornea and crystalline cone. Light rays must be aimed directly into an individual element to be sensed by the underlying visual pigments; the responses of the thousands of these elements are integrated to form an image. In the other major type of eye found in Arthropods, "superposition compound eyes", a cluster of nearby optical elements direct their light rays onto the same patch of visual pigment. Superposition eyes perform better at low light levels, but the apposition eyes of mantis shrimps have better resolution than many types of superposition eyes.
A truly remarkable feature of the compound eyes of mantis shrimps is that a single location in space can be seen by optical elements in three different parts of the same eye - the upper hemisphere, midband, and lower hemisphere. Thus, each individual eye of the mantis shrimp has depth perception and trinocular vision. In contrast, we humans require both of our eyes for depth perception and binocular vision.
Aside from their roles in trinocular vision, the upper and lower hemispheres of the mantis shrimp compound eye are rather unremarkable. The optical elements in these regions are used primarily for recognition of forms, not color vision. The upper and lower hemispheres have elements with one type of rhodopsin in the upper part that is sensitive to short wavelengths of light (such as blue), and another type of rhodopsin in the lower part that is sensitive to long wavelengths of light (such as red). This is similar to the compound eyes of many other Crustaceans.
Sensation of colors
The midband region, which consists of six rows of optical elements in the Gonodactyloids and Lysiosquillids, is the most remarkable region of the mantis shrimp's eyes. The elements of midband rows 1-4 are particularly important for color vision. Each of these has eight different classes of visual pigments that vary in maximal sensitivity from about 400 nm (deep violet) to about 550 nm (green). Since the receptor cells that contain these pigments have special wavelength filters, the wavelength range of the different receptor cells is even greater, from about 400 nm (deep violet) to about 650 nm (ruby-red). All these visual pigments use a vitamin A analog (11-cis retinal) as the light-absorbing compound that is attached to a protein called opsin (see Figure A1 in Appendix), so their wavelength sensitivities presumably differ because they are coded by different opsin genes.
In addition to having a diversity of visual pigments, each optical element in midband rows 1-4 is segregated into 3 tiers. The elements of rows 2 and 3 have two rows of color filters that separate the three tiers, so that the color of light changes as it passes through these elements. These color filters are mostly carotenoid compounds whose colors are purple, blue, red, orange, or yellow (depending on the species) and function in tuning and sharpening the wavelength range of light that reaches the visual pigments beneath.
The color filters of the midband region, like sunglasses, markedly reduce the level of light that reaches the visual pigments, so mantis shrimps require bright light to use their sophisticated color vision systems. This may explain why they are so successful in the well-lit waters of coral reefs. The few Gonodactyloids and Lysiosquilloids that do live in deep or murky water generally lack certain types of color filters and some of the other adaptations for color vision.
Sensation of light polarization
While the optical elements in midband rows 1-4 are used for color vision, those in rows 5 and 6 are used for detection of light polarization. Our own eyes are poor at sensing light polarization (see Sidebar 3), but very good at sensing its color and brightness; however, sensation of light polarization is not at all unusual in the animal kingdom. It is found in some insects, crustaceans, fish, birds, and particularly in cephalopods, a class of mollusks that includes squids, octopuses and cuttlefish. In analogy to color vision, a key requirement for polarization sensitivity is the excitation of two or more classes of visual pigments that have different alignments in the eye (technically, different axes of maximal excitation). In the mantis shrimp, the visual pigments of the different tiers of optical elements in rows 5 and 6 have different alignments. Comparison of the neural inputs from these two rows allows the mantis shrimp to sense polarized light.
The subtlety of polarization vision in humans makes it difficult for us to appreciate that polarized light signals are widespread throughout nature, including the shallow tropical waters inhabited by mantis shrimps. In general, polarization sensitivity enhances contrast vision, and this is particularly important for the mantis shrimp, since underwater objects generally have lower contrast. The mantis shrimp's polarization sensitivity allows it to better see many of the fish upon which it preys, since the silvery sides of many fish species strongly polarize light.
Clearly, the most sophisticated region of the mantis shrimp's eye is the midband. However, the midband only views a small area (about 5-10 degrees) of the visual field at any given instant. Optical elements in the upper and lower hemispheres, which lack the specializations for color and polarization vision, can only sense forms and motion. Thus, it might seem that the mantis shrimp senses the color and polarization of light in only a very narrow range of its visual field.
But this is not quite correct. In fact, the eyes of the mantis shrimp are mounted on mobile stalks and are constantly moving about, apparently independent of one another. These eye movements are controlled by eight individual eyecup muscles that have been divided into six functional groups. Slow scanning movements of the eyes allow the mantis shrimp to "paint" color and polarization information onto the forms that are seen by optical elements in the upper and lower hemispheres of its eyes. In addition, mantis shrimp eyes, like those of humans, also have "saccadic" movements. These rapid eye movements facilitate rapid redirection of a gaze, without blurring the visual image, just as readers of this essay are doing right now, moving from one line to the next. A third type of eye movement in the mantis shrimp is "tracking", which is used in following moving objects, such as prey. Tracking involves large, rapid eye movements, in which the two eyes appear to move independently, often up to 70 degrees, at an instant.
The eye of the mantis shrimp, with its trinocular vision, its multitude of visual pigments, its polarization sensitivity, and its intricate movements, is truly among the most specialized and most sophisticated eye in the animal kingdom. How can we humans possibly know what the mantis shrimp sees and what kind of world it lives in?
Alas, because of widespread variation in human visual pigment genes, we do not even share the same color perception with one another, so we can only imagine what the mantis shrimp sees. The sophisticated eyes of the mantis shrimp should teach us that visual perception is only relative and that our own view of the world is not necessarily the best view.
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Site Created February 3, 1998