Photobehavior of marine invertebrates: Extraocular photoreception

How do animals sense light? What are their responses? The researches into photobehavior of animals has had a long and exciting history. In the 1930s John H. Welsh began a series of researches on the photobehavior of invertebrate animals that he continued to pursue into the 1960s. Welsh’s studies, to cite a few, included the effects of light on locomotor muscles, on the reactions of their tentacles, on rhythmic behavior, and on neurohormones (Welsh, 1932, 1933a.b, 1934a,b, 1961). These photobehavioral studies bear directly on our understanding of the mechanisms of neurosensory and visual systems of animals, but how these behavioral responses are carried out via their receptors is not completely understood. Invertebrates exhibit a variety of photobehaviors; that is, they move, orient or swim to or away from the light source. The movement may be in the bending or contraction of part or all of the body. Other photobehavioral responses are migration and circadian rhythms. These photobehavioral responses, or a set of responses that are not initiated via the eye but through photoreceptors closely bound to dermal and neural cells, including the brain, are defined as extraocular or are referred to as the extraretinal photoreceptor system. The search into extraocular photoreception was pioneered by the investigations of Steven (1963) and Millott (1968). Their studies and more recent investigations are reviewed by Menaker (1976, 1977), Millott (1978) Yoshida (1979) Wolken (1986) and Wolken and Mogus (1979, 1981). In attempts to understand the mechanisms of extraocular photoreception and behavior, questions arise as to where are the photoreceptors located, and what are the photoreceptor molecules? How are the photoreceptors structured, and are they similar to or do they differ from the visual photoreceptors? Extraocular photoreceptors are widely distributed throughout the animal, and their function is to inform the animal of the presence or absence of light, monitor the light intensity, measure the duration of light, and select specific wavelengths of light. In some animals, the extraocular photoreceptor analyzes the plane of vibration of polarized light for orientation and navigation. A brief review of some behavioral responses of marine invertebrates will be illustrative of extraocular photosensitivity. For example, many invertebrates respond to a sudden change in light intensity by a withdrawal reaction, which is observed for numerous marine animals and is referred to as the shadow response. Steven (1963) attributed such photobehavior to a dermal light sense, but Millott (1968) preferred the all-inclusive term extraocular for all types of photobehavior that was not initiated through the eye. The shadow response of the sea urchin Diadema exhibits a withdrawal from the light and is accompanied by a complex spine waving reaction (Millott, 1968). In annelids, there is withdrawal of the tail. In Nereis diuersicolor, the photosensitive area is located on the parapodia and proand peristromium (Gwilliam, 1969). In nematodes, there is a similar phototactic response to light (Croll et al., 1975). The marine worm GolJingia gouldii reacts to light by retraction of the proboscis (O’Benar and Matsumoto, 1976). The burrowing sea anemone Calamactis praelongus bends toward the light (Marks, 1976). The adult sea squirt Ciona intestinalis orients in the direction of the light, accompanied by the opening and closing of its siphons (Dilly and Wolken, 1973). The Ciona body surface is also sensitive to changes in light intensity, and the most light-sensitive area is found in the region of the ganglion cells. The response to changes in light intensity are localized contractions or a total contraction of the body. These contractions and elongations continue in Ciona even when the siphons are removed. Migration is a behavioral response for many marine animals that is associated with extraocular photosensitivity. Migrating rhythms have been studied in the squid Todurodes sagittatus and in the tubellarian flatworm Convoiuta roscoffensis. Convoluta lives in the sand at night and during high tides, and emerges onto the surface at low tides during the daytime. If the animals are brought into the laboratory and exposed to a constant light source, vertical migration continues for up to seven days in synchronization with the tides. The migratory rhythm persists in continuous light but ceases in continuous darkness (Palmer, 1974; Wolken, 1975; Naylor, 1985). However, if they are subjected to a flash of light in their dark world, they will resynchronize their rhythm. The extraocular system is also involved in the entrainment of circadian rhythms (Bennett, 1979; Hisano et al., 1972a). The daily rhythmic behavior can directly mediate the response, or entrainment, of the circadian oscillator, via the sixth abdominal