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Information Feedback from Photophores and Ventral Pacific Science (1973), Vol. 27, No.1, p. 1-7 Printed in Great Britain Information Feedback from Photophores and Ventral Countershading in Mid-Water SquidI RICHARD EDWARD YOUNG2 ABSTRACT: The arrangement ofphotosensitive vesicles and photophores in two species of mid-water squid suggests that the vesicles function in detecting the in­ tensity ofdownward-directed surface light and the intensity oflight from their own photophores. This information is precisely what is required for an animal to eliminate its ventral shadow by the production ofa ventral bioluminescent glow. This arrangement, therefore, offers strong support for the theory of ventral countershading in mid-water animals. CEPHALOPODS have photoreceptive structures The function of the photosensitive vesicles other than the eyes. In octopods these organs beyond their photosensitive capacity is un­ have been called epistellar bodies (Young, known. One probable function, however, has 1929); in squid and cuttlefish they have been recently emerged during the course of a study labeled the parolfactory vesicles (Boycott and which is attempting to correlate modifications Young, 1956). In both instances the names are of the photosensitive vesicles with certain as­ associated with the location of the organs: in pects of the ecology of mid-water cephalopods octopods, on the stellate ganglia; and in squid off Hawaii. and cuttlefish, near the olfactory lobe on the op­ I would like to thank J. Z. Young, University tic stalk of the brain. In spite of the different College London; N. B. Marshall, British Mu­ locations of these organs, they are probably seum (Natural History); C. F. E. Roper, Smith­ homologous structures (Nishioka, Hagadorn, sonian Institution; J. M. Arnold, Pacific Bio­ and Bern, 1962; Nishioka et aI., 1966, and per­ medical Research Center; T. Okutani, Tokai sonal observations). It is, therefore, no longer Regional Fisheries Research Laboratory; and desirable to maintain a separate terminology in J. Walters and S. Amesbury, University of the different groups. Since neither ofthe present Hawaii, for reading and commenting on the names is appropriate to all cephalopod groups, manuscript. I also thank T. Clarke, University it becomes necessary to rename the organs. ofHawaii, for providing some of the specimens Since these organs are photoreceptors (Nishioka examined. et aI., 1966; Mauro and Baumann, 1968; Mauro and Sten-Knudsen, 1972), it is suggested that RESULTS the epistellar bodies andtheparolfactoryvesicles be called the photosensitive vesicles. 3 Pelagic cephalopods living below the epi­ pelagic zone during the daytime (i.e., in the mid-water environment) have photosensitive I. This work was supported by grant GB 20993 from the National Science Foundation. Manuscript received vesicles which exhibit many variations; these 10 May 1972. often involve hypertrophy of the organs. Two 2 DepartmentofOceanography, University ofHawaii, such variations have already been reported Honolulu, Hawaii 96822. (Messenger, 1967; Baumann et aI., 1970). The 3 An abstract, treating the modifications ofthe photo­ sensitive vesicles in mid-water squid, was published in most striking modifications that I have observ­ the Proceedings of the Joint Oceanographic Assembly, ed occur in some members of the squid family Tokyo, 1971. In this abstract I used the term "photic Enoploteuthidae. Although the arrangement vesicles." J. Z. Young has since informed me that this varies somewhat between the species examined, term had already been used for certain light-sensitive most basic elements of the general pattern re­ structures in gastropods. Following his suggestion, I now adopt the term "photosensitive vesicles." main constant. The animals studied in most 1 1-2 2 PACIFIC SCIENCE, Volume 27, January 1973 .OP. 5T. E5. CE. CART. .......~"lt-- ........(T P. PHOTo VE5.--t-ihH!r~ NER.---+l:-\<f----'-:¥; FIG. 1. Lateral dissection of the head of Abraliopsis Sp. SYMBOLS: A. V. PHOTo VES., anterior ventral photosensitive vesicles; CEo CART., cephalic cartilage; D. FU. PHOT., dorsal funnel photophores; D. PHOTo VES., dorsal photosensitive vesicles; L. FU. PHOT., lateral funnel photophores; M. V. PHOTo VES., mid-ventral photosensitive vesicles; NER., nerve; OP. ST., optic stalk; P. PHOTo VES., posterior photosensitive vesicles; V. FU. PHOT., ventral funnel photophores. detail belong to two undescribed species of stalks of the brain. All of the vesicles lie within Abraliopsis (Burgess, in manuscript). Both of the head adjacent to the inner wall of the ce­ these species are commonly captured in mid­ phalic cartilage. One set is situated dorsally; water trawls off Hawaii. Although the data are two are ventrally located; and the fourth, which rather sparse, these species seem to occupy is absent in one species, occupies a posterior depths during the daytime around 600 meters position within the head (Fig. 1). Each member, and at night they migrate into the upper hun­ or lobe, ofa set consists of a number ofindivi­ dred meters. dual vesicles, each with a lining of cell bodies The structure and arrangement of the photo­ that have photosensitive processes extending sensitive vesicles in these species of Abraliopsis into a central lumen. differ greatly from those found in neritic or Each lobe of the dorsal set of vesicles lies epipelagic squid. The unusual arrangement of close to the dorsal surface of the head and pro­ vesicles is described in the following paragraphs trudes into a concavity in the cephalic cartilage. and provides the basis for the subsequent As a result, the cartilage above each lobe is very discussion. thin. Muscle tissue, although present on all sur­ Squid occupying near-surface waters gener­ rounding areas, is absent from most of the area ally have a single, small set ofvesicles. In con­ immediately above the dorsal vesicles. There­ trast, these deeper living species of Abraliopsis fore, between the vesicles and the surface lie have three to four greatly enlarged sets, all well only the thin cephalic cartilage and the integu­ removed from the usual position on the optic ment. The integument over most ofthe surface Photophores and Ventral Countershading in Squid-YoUNG 3 FIG. 2. A, dorsal view ofhead ofAbraliopsis sp. B, ventral view ofhead ofAbraliopsis sp. with the funnel adductor muscles cut and the funnel reflected posteriorly. Shaded portion indicates areas covered by chromatophores. C, lateral view of Abraliopsis sp. showing ventral predominance of photophores. SYMBOLS: CHR., chromatophore; CUT. FU ADD. MUSe., cut funnel adductor muscle; D. FU. PHOT., dorsal funnel photophores; D. WIN., dorsal window; FU., funnel; NOR. POS. FU., normal position of the funnel; PHOT., photophores; POS. A. V. PHOTo VES., position of the anterior ventral photosensitive vesicles; POS. M. V. PHOTo VES., position of the mid-ventral photosensitive vesicles; V. WIN., ventral window. of the head contains two layers of chromato­ extend ventrally along the inner surface of the phores. The innermost layer is absent from the cephalic cartilage and enter the brain in the re­ integument immediately above the vesicles and gion of the peduncle lobe. the other layer is usually observed with all The ventral sets of vesicles are shaped quite chromatophores contracted. This arrangement differently from the dorsal one. The most an­ provides a distinctive"window" on the surface terior of the two ventral sets consists of some­ of the head through which light has easy access what flattened, sausage-shaped structures with to the dorsal vesicles (Fig. 2A). Viewed dor­ thickened and laterally curved anterior ends sally, each lobe has a nearly circular shape except (Fig. 1). Each lobe of this anteroventral set lies for a V-shaped indentation on its lateral margin. in a depression in the floor of the cartilage ex­ The dorsal surface of the lobe is smooth and cept for a small medial projection which par­ convex while the ventral surface is approxi­ tially lies in a foramen in the cartilage. Each lobe mately flat but rather irregular. seems to consist ofa single layer ofvesicles. At Each dorsal lobe appears to consist of a the thickened anterior end, the vesicles are single layer of elongate vesicles oriented per­ elongate and have their long axes approximately pendicular to the dorsal surface ofthe lobe. The perpendicular to the convex ventral surface of cross sections ofindividual vesicles are approxi­ the organ. The flatter, posterior portions of mately circular. Cell bodies of the photosensi­ each lobe have somewhat irregular elongate tive cells are found primarily along the sides and vesicles which lie parallel to the ventral surface dorsal ends of the individual vesicles, and the of the organ. Cell bodies of the photosensitive photosensitive processes, in general, are aligned cells occur in a compact layer on all surfaces of with the long axis of each vesicle. Large flat­ the individual vesicles but predominate on the tened bundles of nerves from each dorsal lobe side and ventral margins of the vesicles. Each 4 PACIFIC SCIENCE, Volume 27, January 1973 anteroventral lobe is in contact with another In order to interpret the probable functions lobe, the mid-ventral lobe, via a narrow strand of the dorsal and ventral sets of vesicles, it is of vesicles. necessary to examine the arrangements of In contrast to the anteroventral lobes, the photophores in these squid. These species of mid-ventral lobes are very irregular in outline Abraliopsispossess numerous photophores over and are extraordinarily thin (Fig. 1). Individual the surfaces
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