View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by OceanRep Marine Biology 51, 371-380 (1979) MARINE BIOLOGY by Springer-Verlag 1979 Eyes and Extraocular Photoreceptors in Midwater Cephalopods and Fishes: Their Roles in Detecting Downwelling Light for Counterillumination R.E. Young ], C.F.E. Roper 2 and J.F. Waiters3 ]Department of Oceanography, University of Hawaii at Manoa; Honolulu, Hawaii, USA 2Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution; Washington, D.C., USA and 3Maui Community College; Hawaii, USA Abstract The means of detecting downwelling light for counterillumination in several midwa- ter animals has been examined. Eyes and extraocular photoreceptors (dorsal photo- sensitive vesicles in the enoploteuthid squid Abraliopsis sp. B and pineal organs in the myctophid fish Mgctophum spinosum) were alternately exposed to overhead light or covered by a small opaque shield above the animal and the bioluminescent response of the animal was monitored. Covering either the eyes or the extraocular photore- ceptors resulted in a reduction in the intensity of counterillumination. Prelimi- nary experiments examining the bioluminescent feedback mechanism for monitoring intensity of bioluminescence during counterillumination in the midwater squid Abra- lia trigonura indicated that the ventral photosensitive vesicles are responsible for bioluminescent feedback. Introduction range of about 16,OO0-fold which corre- sponds to light changes that occur in Faint but highly directional daylight in clear oceanic waters over a depth range midwaters of the open ocean silhouettes of nearly 300 m (Young et al., in prepa- an opaque animal which could be visible, ration). therefore, to predators below. Many ani- To counterilluminate properly, an mals, however, can use their own bio- animal must be able to determine the in- luminescence to eliminate their silhou- tensity of the downwelling light and ettes. The idea that photophores are must have some means to insure that its used for counterillumination (biolumi- photophores respond appropriately. Young nescent countershading) in midwater ani- (1973) suggested that midwater squids mals has been suggested, apparently in- utilize extraocular photoreceptors (dor- dependently, by a number of biologists sal photosensitive vesicles) to detect (e.g. Dahlgren, 1916; Rauther, 1927; downwelling light. He also suggested Jermanska, 1960; Fraser, 1962; Clarke, that other extraocular photoreceptors 1963); evidence for counterillumination (ventral photosensitive vesicles) detect from living midwater animals has accumu- light from the animal's own photophores, lated rapidly in recent years. The radi- thereby providing a feedback mechanism ance pattern of artificially induced lu- for adjusting the intensity of the light minescence in several midwater fishes from their photophores relative to the (Denton et al., 1972) and shrimps (Herring, downwelling light. 1976) closely matched that of ambient sunlight. Midwater squid in an aquarium Lawry (1974) suggested that the eyes viewed from below by an observer became of myctophid fishes detect downwelling invisible when the squids' luminescence light. Midwater fishes, however, have a matched the overhead light intensity prominent extraocular photoreceptor, the (Young and Roper, 1976). Cephalopods, pineal organ, often lying beneath an un- fishes and shrimp in an aquarium regu- pigmented cutaneous window, which could lated the intensity of their lumines- be important in detecting downwelling cence to match changes in the intensity light (McNulty and Nafpaktitis, 1976, of the overhead light (Case et al., 1977; 1977). In various midwater fishes, Nicol Young and Roper, 1977). One squid varied (1967), Young (1973), and Lawry (1974) the intensity of its luminescence over a suggested that photophores directed into 0025-3162/79/0051/0371/S02.00 372 R.E. Young et al. : Roles of Photoreceptors in Counterillumination the eyes provide feedback information to injury. Fishes were placed in flexible regulate luminescence, tubes made from clear vinyl film through The dorsal photosensitive vesicles in which water flowed continuously. many midwater squids consist of a pair The squid studied were Abraliopsis spp. of organs located posterior to the eyes (2 undescribed species), Abralia trigonura near the dorsal surface of the head (Fig. Berry, 1913, Enoploteuthis sp. (unde- IB). The paired ventral photosensitive scribed species), and Pyroteuthis addolux vesicles are located near the ventral Young, 1972. One species of fish was surface of the head, dorsal to the fun- examined: the myctophid Myctophum spinosum nel. The funnel has numerous photophores (Steindachner). directed at the ventral vesicles (see The experimental apparatus (Fig. I) Young, 1973, 1978). The photoreceptive was mounted in a box-like housing lo- nature of these vesicles is well estab- cated on a vibration dampener. The spec- lished (see review by Mauro, 1977). imen to be examined was placed in a ta- The pineal organ in myctophid fishes pered, transparent, flexible tube (clear lies in the dorsal midline of the head, vinyl film) with slowly flowing water. between the eyes (Fig. IB). Evidence The taper provided a means of closely that supports the photoreceptive nature fitting the size of the tube to the size of this organ has been reviewed by Mc- of the animal. A tube with an animal in- Nulty and Nafpaktitis (1977). side was placed on a clear acrylic plat- We now present behavioral data on the form that contained a small hole into roles of the dorsal photosensitive vesi- which a fiber optic probe was inserted. cles and the eyes as detectors of down- Squid were positioned with the fiber op- welling light in squids, as well as the tic probe beneath the photophore-covered roles of the pineal organ and the eyes head; fish were positioned with the as detectors of downwelling light in probe beneath several photophores just myctophid fishes. We also present pre- posterior to the pectoral girdle. A liminary data on the role of the ventral 3.2 mm diameter fiber optic probe trans- photosensitive vesicles in squid as a mitted light from the animal's photo- photoreceptor for bioluminescent feed- phores to an EMI 9789 photomultiplier back of information for counterillumina- tube 1, and ligh t values were recorded on tion. a Hewlett Packard 2-channel strip chart recorder. The light above the animals was provided by a 250 W slide projector Materials and Methods located in the adjacent room. A diffuser placed in front of the projector bulb Most data were collected during a cruise eliminated the image of the filament. off leeward Oahu, Hawaii, aboard the Focused light from the projector passed University of Hawaii's research vessel through a series of neutral-density fil- "Kana Keoki" in April, 1978. Preliminary ters and an interference filter (trans- data were accumulated during cruises in mission peak = 476 nm, full width half June and September, 1977. maximum = 10 nm), and was then deflected Squids were captured in a shortened onto the animal by a 45 ~ mirror located 3 m Isaacs-Kidd midwater trawl with a about 20 cm above the specimen. The fine mesh liner (13 mm stretch mesh), a overhead light was thus a small source, 505 ~m plankton net cod-end, and a coni- with a gradually spreading beam located cal cod-end bucket shielded against ex- about 1.3 m from the animal. ternal light. Upon retrieval, the bucket The intensity of the overhead light was immediately wrapped in black plastic was monitored via a 1.6 mm diameter fi- during the day or handled under red ber optic probe positioned beside the light at night to protect the animals' specimen and attached to an EMI 9789 photoreceptors. Myctophid fishes were photomultiplier tube; it was recorded in captured under a night-light with a dip parallel on the same strip chart as the net. animal's luminescence. The intensity of Living animals were placed in running overhead light was held at approximately seawater tanks in the totally dark 8.2 x 10 -4 ~W cm-2. Previous work (Young aquarium-laboratory. Water temperatures et al., in preparation) demonstrated that were regulated to correspond approximate- this value is well within the range of ly to temperatures normally encountered light levels over which these animals by these vertically migrating animals can counterilluminate. (about 7 ~ to 9~ during the day and 15 ~ Opaque shields, made to size for each to 18~ during the night). Prior to ex- specimen, were used to shade the animal's perimentation, squid were maintained in photoreceptors from the overhead light. aquaria in small, screened, plastic vials which allowed water circulation iMenti0n of a company name does not imply prod- but restricted their movements to avoid uct endorsement. R.E. Young et al.: Roles of Photoreceptors in Counterillumination 373 (~ | Fiber optic probe ~..I /to overhead light I / " " /~-- -- XI Turn m z_~ ..-~-~ ~ Handle Shield H~20 ~ //~ _L ~Ir'v" I Fiber optic probe to photophores : f~l---E ye Sh{eld ~-J.i;ll~l-n k~'_j~Pineal Shield Eye Shield---~, A/~ ~ I F-- ~-]- .... --,- I ~/i ~:'~ LK I ~lr-Pinea Organ vesoc'e ~ I /~ i Dorsal /. / "1 / /// /\ Photosensitive / / //I / / Vesicles ~ ~ Fig. I. (A) Experimental apparatus. Tube containing squid has been drawn to one side to show posi- tion of the fiber optic probe; PMT: photomultiplier tube. (B) Abraliopsis sp. B (left) and Mycto- phum spinosum (right). Outline drawings of the two species examined, showing approximate position of shields when covering photoreceptors The shields consisted of heavy aluminum interfering with light reception from tape covered with black tape on one side the edges of the diffuser by these and white tape on the other. The black photoreceptors. As a result, this system tape prevented reflections from disturb- was abandoned and replaced with the more ing the animal during the lowering of directional lighting system described the shield and the white surface aided above. the experimenter in correctly position- To test the role of the eyes and ex- ing the shield.