Eyes and Extraocular Photoreceptors in Midwater Cephalopods and Fishes: Their Roles in Detecting Downwelling Light for Counterillumination

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Marine Biology 51, 371-380 (1979) MARINE BIOLOGY by Springer-Verlag 1979

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 midwater animals has been examined. Eyes and extraocular photoreceptors (dorsal photosensitive 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 photoreceptors 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 position 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. The shields were at- traocular photoreceptors in detecting tached to slender rods and could be ro- overhead light, the animals were placed tated to a horizontal position dorsal to under the light regime and allowed to the organ being tested, thus cutting off counterilluminate; then one or the other the overhead illumination, or to a ver- organ was shielded and the animal's lu- tical position to allow light to enter minescent response recorded. Experiments the organs. The shields were positioned on squids consisted of trials with (I) initially with the aid of dim red light. the dorsal vesicles covered, (2) the Initial experiments were carried out eyes covered, or, (3) both the eyes and with a broad overhead diffuser located dorsal vesicles covered. Each trial con- immediately beneath the 45 ~ mirror. This sisted of a 5 min exposure of the eyes system closely duplicates the radiance and vesicles to overhead light, and the pattern of light in the ocean; however, resulting luminescence gave the "initial the broad acceptance angle of the extra- value" against which later values were ocular photoreceptors made shielding the compared. This was followed by 5 min eyes difficult without simultaneously with one or both sets of organs covered 374 R.E. Young et al. : Roles of Photoreceptors in Counterillumination with the opaque shield(s). At the end of oblique light that bears a constant ra- each series of trials the overhead light tio in intensity to the vertical compo- was turned off for 5 min. Since fishes nent of the downwelling light apparently exhibited a more rapid response, trials is sufficient. were reduced to 2 min with eyes and pi- We were able to conduct a few prelim- neal organ exposed to overhead illumina- inary experiments on the feedback function followed by 2 min with one or both tion of the ventral photosensitive vesi- organs covered. cles of squid. The experimental proce- The animals were confined in the dure consisted of placing the squid in tubes, but they could not be completely the vinyl tube under a constant source immobilized. The luminescence of a total- of diffuse overhead light to stimulate ly immobilized squid becomes erratic, counterillumination. The ventral surface probably due to impairment of respira- of the head and the ventral vesicles were tory movements. A fish usually behaves illuminated via one branch of a fiber similarly if its swimming movements are optic light probe located 2 cm from the totally inhibited. ventral surface of the head. The ven- Animals in this confined system often tral light passed through a Wratten No. required considerable time to adjust so 45 blue filter (peak at 487 nm) from a that raising and lowering the shield, small light source regulated by a vari- ship's vibrations, etc. did not disturb able transformer. The other branch of them. A disturbance is easily detected the fiber optic probe passed from the on the strip chart records as broadly same light source onto a photomultiplier fluctuating light intensities. Most tube. Light produced by the squid was specimens were tested over a period of detected by a separate photomultiplier about 6 to 12 h until the experiment was tube via a separate fiber optic probe. completed or until the animal's behavior The intensity of the ventral light was became erratic. increased gradually until the squid re- While the light beam projected onto sponded by lowering its luminescence. In the experimental platform was highly di- the range of response, several light in- rectional, light received by the animal tensities were examined. In each case was less directional. The refraction of the squid was given 5 min to adjust to light at the curved sides of the tube in the light values, at which time a read- which the animal was located introduced ing was made. This system thus far has some light to its eyes at oblique angles proven impossible to calibrate, since over a rather broad angular range. This neither the percent of the ventral pho- oblique lightwas essential to the suc- tosensitive vesicles illuminated, nor cess of our experiments, since we dis- the loss of light prior to reaching the covered that squids, at least, can not vesicles due to absorption by chromoto- detect exclusively vertical overhead phores and photophores on the funnel, light. We examined a squid in the fol- could be determined. lowing way. A small squid was positioned head-down in an aquarium, and the narrow beam from a high-intensity microscope Results lamp was directed at the dorsal surface of the animal. Light from the lamp hit The data are presented as relative val- the lens of the eye and was focused on ues. A counterilluminating animal can the retina. The spot on the retina was maintain a constant level of lumines- bright enough to be seen through the cence for long periods of time. If the pigment-covered eye and the head. When animal is disturbed, however, this level the light was centered over the dorsal may alter slightly. In addition, the surface of the head to simulate vertical animal may not always return to precise- light no image was formed on the retina. ly the former level of luminescence when However, when the light was moved slight- it recovers from a dark period. This in- ly to one side but pointed at the squid, consistency appears to be caused partly a distinct spot could be seen on the by the excitable condition of a confined retina of the eye of that side. Measure- animal and partly to slight movements ments of the distances involved indicate the animal may make relative to the that light will strike the retina on a fiber optic probe. Movement of the ani- horizontally oriented squid, if the mal over the probe slightly changes the light is at least 10 ~ to 12 ~ from the position of the photophores "viewed" by vertical. While we did not examine the the probe and may affect the recorded fish in the same way, inspection sug- light value. For this reason, the data gests that they also may not be able to for any trial with an organ covered by a detect vertical light with their eyes. shield are presented as a percent of the If eyes are used to help regulate coun- initial level of luminescence when all terillumination, their detection of photoreceptors were exposed at the be- R.E. Young et al.: Roles of Photoreceptors in Counterillumination 375

100 . Specimen No. I

1- ~ I ~ I ,-:. i_oT io.L o Male, 21 mm mantle length; captured at night; experiments began 4 h after capture and continued for another 12 h. This squid was extremely irritable and frequently became erratic, forcing many i - trials to be aborted and restarted. .E When only the dorsal photosensitive _.1 vesicles were covered by the opaque 60~- . shield the squid decreased its lumines-

c cence to an average of 13% of its ini- o . tial intensity when the vesicles were exposed. On the average, half of the decrease occurred in 18 sec. While the a 40~ squid decreased its luminescence greatly with the vesicles covered, its decrease was even greater when both eyes and vesicles were covered. In these latter tests the squid's luminescence dropped to an average of 4% of its initial value, ._.1~ 20 ,--, and half the decrease took place in about 5 sec. When only the eyes were covered the t t squid's luminescence decreased to an 0 I I il average of 74% of its initial intensity. Abraliopsis sp. Myctophum spinosurn Half the total decrease in luminescence occurred in 3 to 6 sec. The variation in Fig. 2. Abraliopsis sp. B and Myctophum spino- response was considerable and changed in sum. Summary of test data indicating the extent a consistent manner: each successive of decrease in bioluminescence when photorecep- trial gave a greater decrease than the tors are covered. Bars indicate range and sym- previous one. This pattern is reflected bols indicate means for a particular test. Cir- in progressive increases in the intensi- cles: tests of extraocular photoreceptor(s); ty of luminescence during periods when squares: tests of eyes; triangles: test of ex- no organs were covered. In several cases traocular photoreceptor(s) and eyes. n = 4-10 an initial drop in luminescence after the eyes were covered was followed by a gradual increase, resulting in the final recorded value being less than the maximum decrease.

ginning of that trial. A summary of the data is presented in Fig. 2. Specimen No. 2 Female, 16.5 mm mantle length; captured during the evening. Experiments began Abraliopsis sp. B I h after capture and continued for an additional 10 h. This specimen was doc- This squid is undescribed. The designa- ile and not readily disturbed. tion B was adopted for this species by When only the dorsal photosensitive Young (1978). This short, stocky squid vesicles were covered, the squid's lumi- bears a dense array of small photophores nescence dropped to an average of 8.0% on its ventral surfaces. Accounts of its of its initial intensity when the vesi- counterilluminating abilities have been cles were exposed (Fig. 3A). The lumi- presented in earlier papers (Young and nescence dropped to half its final value Roper, 1976, 1977). A transparent window in an average of about 16 sec. When both above each dorsal photosensitive vesicle eyes and vesicles were covered the allows easy location of these organs and squid's luminescence dropped to an aver- thus accurate positioning of the shield. age of 0.6% of its intensity when both During the day this species primarily organs were exposed (Fig. 3C), and half occupies depths of 500 to 650 m, and at of the decrease took place in about 5 night it occurs primarily in the upper sec. 100 m (Young, 1978). Therefore, during When only the eyes were covered the both day and night the animal is exposed squid's luminescence dropped to an aver- to light levels at which counterillumi- age of 89% of its former level (Fig. 3B). nation could be of value. Half of the decrease occurred in about 376 R.E. Young et al.: Roles of Photoreceptors in Counterillumination

Fig. 3. Abraliopsis sp. B, Specimen No. 2. (A) Test of dorsal photosensitive vesicles; (B) test of eyes; (C) test of both dorsal vesicles and eyes. Upward pointing arrows indicate shield covering photoreceptor raised, downward pointing arrows indicate shield lowered to cover photoreceptor

2 to 6 sec. In all trials the initial ered with many large but rather broadly drop after the eyes were covered was spaced photophores. The skin above the greater than the final value recorded at pineal organ lacks chromatophores, al- the end of 5 min. Indeed, in one trial lowing easy location of the organ and the gradual increase following the ini- accurate positioning of the shield. The tial drop resulted in a level of lumi- organ lies over a heavily pigmented epi- nescence equal to that before the eyes thelium which provides a light shield were covered. If the magnitude of the from below. Clarke (1973) captured this initial drop is considered and not that species at 600 m during the day, but at the 5-min point, the average decrease suggested that it may occur in shallower would be to 82%. well lighted depths where it can detect and avoid the trawl. At night he cap- Myctophum spinosum tured it from O to 15 m, but again noted that it probably can avoid capture by The ventral surface of this fish is cov- the trawl. R.E. Young et al. : Roles of Photoreceptors in Counterillumination 377

of its former intensity when both photoreceptors were exposed.

Specimen No. 2

Female, 87 mm standard length; dip- netted at the night-light. Experiments began 3 h after capture and continued for an additional 5 h. The head of this specimen was firmly wedged into the tube, eliminating all side movement. When the pineal organ was covered, the fish's luminescence decreased to an average of 31% of its initial intensity before the organ was covered (Fig. 4A) . The decrease was gradual: half of the decrease occurred in an average of about 12 sec. The range of values during trials was broad (13 to 49%). When the eyes were Fig. 4. Myctophum spinosum. Specimen No. 2. (A) covered the fish's luminescence de- Test of pineal organ; (B) test of eyes. Upward creasedI to an average of 26% of its in- pointing arrows indicate shield covering photo- tensity prior to covering the eyes (Fig. receptor raised; downward pointing arrows indi- 4B). The decrease was rapid: half of the cate shield lowered to cover photoreceptor. total decrease took between I and 2 sec. Zero indicates overhead light turned off Before tests could be run with both the eyes and the pineal organ covered, the fish's luminescence became erratic and all attempts to stabilize its behavior were unsuccessful. No further data were Specimen No. I obtained.

Male; 78 mm standard length; dip-netted at the night-light. Experiments began Comparisons between Squid and Fish 3 h after capture and continued for an additional 6 h. Myctophids placed in The responses of the squid and fish to tubes with flowing water tended to move covering the photoreceptors were some- their heads from side to side as part of what different. The squid with dorsal their swimming movements. In this speci- photosensitive vesicles covered reduced men, movement was greatly restrained but its luminescence by about 90%. With the not totally eliminated. Therefore, in eyes covered, however, it decreased its placing shields over the head allowance luminescence by only about 20%. Mycto- had to be made for this movement, which phids reduced their luminescence with resulted in shields being less than op- the pineal organ covered by an average timum size. of about 25% in one specimen and 70% in When the pineal organ was covered the the other, while covering the eyes luminescence dropped to an average of caused an average reduction of about 70% 73% of its former intensity when the or- of the uncovered value. Therefore, cov- gan was exposed. The range of values ering the eyes in these fish elicited a during trials was narrow (71 to 80%). response of greater magnitude than in The drop in intensity was gradual: half these squid. the decrease occurred in 10 to 11 sec. When the eyes of fish were covered, When the overhead light was extinguished their luminescence reached half its to- at the end of this series, which elimi- tal decrease in about I sec, while cov- nated the visual response, a more rapid ering the pineal organ resulted in half drop ensued. When the eyes were covered, the total decrease (which was usually the fish's luminescence dropped to an less extensive) occurring in 10 to 12 average of 35% of its former level. This sec. The differences with squid were not drop in intensity was extremely rapid: as dramatic and were less consistent. half of the decrease occurred in about With the eyes covered, the squid's lumi- I sec. When the overhead light was ex- nescence usually reached half its total tinguished at the end of this series, decrease in 3 to 6 sec; however, the ex- which eliminated the pineal response, a tent of the drop was small, about 20%. gradual drop ensued. When both eyes and With the vesicles covered, half the to- pineal organ were covered the fish's tal decrease took 16 to 18 sec, but the luminescence dropped to an average of 5% drop was much more extensive, about 90%. 378 R.E. Young et al.: Roles of Photoreceptors in Counterillumination

the light projected onto the ventral o ~ I~176I surface of the head resulted in a decrease in luminescence by a correspond- ~~.~ 8~I ing amount; and conversely, when the ~E60 - light was decreased, the squid increased its luminescence to a corresponding de- ~-~ 40 - gree (Fig. 5). Since the exact amount of light that reached the vesicles could ~ 20 - not be determined, a regression line through the data points in this region 0; 20' 40' 60' 80' "100 120' 140' "1 '6o- 300 320 was extrapolated to the X-axis. At the intercept (i.e., the point at which bio- Illumination of Ventral Vesicles as a % of luminescence would be zero) it was as- Standard Luminescence sumed that light received by the vesicles from the fiber optic probe was ex- Fig. 5. Abralia trigonura. Effect on squid ven- actly that normally received from the tral luminescence of artificially illuminating funnel photophores by an unmolested in- the ventral photosensitive vesicles during dividual during counterillumination. counterillumination. Dashed line: predicted That is, at this point all the light for relationship; continuous line: regression line feedback is artificial, bioluminescence of data points excluding the two values on the having decreased to the zero point as far right (see text). Standard luminescence = artificial light increased. A comparison ventral luminescence prior to experiment of the slope of the regression line through the data points with the slope of a predicted line reveals little dif- ference (Fig. 5). Fig. 5 also shows two data points that were not included in However, when both the eyes and vesicles the regression calculation. These points were covered, half the total decrease represent light values approximately 1.5 took place in about 5 sec. This indi- and 3.0 times brighter than the pro- cates that in squid, as in fish, the re- jected "turn-off" point. At these values sponse to the eyes being covered is the squid's luminescence was not extin- faster than the response to the extra- guished. Indeed, the greater illumina- ocular photoreceptors being covered. tion of the head at these two values resulted in brighter luminescence. Since the light was bright at this point and Abralia trigonura directed vertically upward, some light may have passed throughthe head to the Female, 20 mm mantle length. Experiments dorsal vesicles, which complicated the began I h after capture during the day squid's response. and continued for an additional 11 h. This squid generally occupies depths of 450 to 650 m during the day and oc- Discussion curs primarily in the upper 1OO m at night (Young, 1978). It therefore occu- The data demonstrate that when an opaque pies depths where counterillumination shield is placed above the dorsal photo- should be of value. This squid's ability sensitive vesicles of the squid or the to counterilluminate has been reported pineal organ of the myctophid fish or previously (Young and Roper, 1977). The above the eyes of the squid and fish feedback mechanism that involves the when these animals are exposed to over- ventral photosensitive vesicles was ex- head illumination, the counterillumi- amined in the present study. nating animals respond by decreasing Abralia trigonura has a large number of their luminescence. Clearly, the ani- photophores on the dorsal surface of the mal's mechanism for detecting downwel- funnel directed toward the ventral ling light was interfered with. Presum- photosensitive vesicles and is, in this ably the mechanism involves the organs respect, similar to Abraliopsis sp. de- shielded, although control experiments scribed by Young (1973). When light with involving severing nerves to these or- sufficient intensity to interfere with gans were not performed. the feedback mechanism was projected on Although we present data on detection the ventral vesicles, the squid re- of downwelling light for only two mycto- sponded by lowering its luminescence. phids (Mgctophum spinosum)and two squid Six different light intensities within (Abraliopsis sp. B), we obtained data on the range of response were projected on- an additional 8 squids (Abralia trigonura, to the posteroventral surface of the 5 individuals; Abraliopsis sp. A, I indi- head. Within this range, an increase in vidual; Enoploteuthis sp. , I individual; R.E. Young et al. : Roles of Photoreceptors in Counterillumination 379

Pyroteuthis addolux, I individual). A large to tilt slightly and, when tilted, to diffuse overhead light source was used fix on a prey below the body axis, the with these individuals. While these data animal's view of the downwelling light are less reliable than those obtained would be further reduced. The extraocu- with the more directional illumination lar photoreceptors face vertically up- (see "Materials and Methods"), they are ward and, with their broad angle of ac- consistent with the data presented here. ceptance, their "view" of downwelling The two myctophids gave quite differ- light would be little affected by the ent responses when the pineal organ was animal's tilting. The dual mechanism in- covered. The smaller individual, which volving eyes and extraocular photorecep- was able to move its head slightly from tors, therefore, may allow these animals side to side, may have received some to separate downwelling light from bio- light via the pineal organ during the luminescent light, while being unaf- tests; this would account for the lesser fected by changes in body attitude or response, in this fish. tilt of the eyes. Our examination of the bioluminescent Apparently, both the eyes and extra- feedback mechanism for counterillumina- ocular photoreceptors in squids and tion in squid indicated that artificial fishes are involved in detecting down- illumination of the region of the ven- welling light for counterillumination. tral vesicles within a certain range of These two organs are very different types values reduced the squid's biolumines- of photoreceptors. The eyes are designed cence. Within this range, a given in- to detect images, while the extraocular crease or decrease in artificial illumi- photoreceptors presumably act as simple nation resulted in a decrease or in- photometers. Neither organ by itself can crease of corresponding magnitude in give the animal all the information it luminescence. These results suggest that requires for proper counterillumination. the squid was attempting to maintain its As simple photoreceptors, extraocular luminescence at a constant level by re- organs presumably cannot distinguish be- lying on information received by the ven- tween downwelling light and biolumines- tral vesicles and, therefore, that the cent light; they simply record the total ventral photosensitive vesicles of squid radiation falling on them. However, the do indeed provide the bioluminescent midwater predator with image-forming eyes feedback mechanism for controlling coun- can detect "bright" luminescent spots terillumination. and flashes against the fainter, uniform background of downwelling sunlight. The Acknowledgements. We thank the officers and prey, therefore, must match only the in- crew of the R.V. "Kana Keoki" and the numerous tensity of the downwelling light if it students of the University of Hawaii for their is to be concealed by its luminescence. assistance aboard ship. We are especially grate- If the intensity of ambient bioluminescence ful to S. Maynard Who managed the trawling pro- approaches that of the downwelling light, gram and provided other logistic support. B. a counterilluminating animal that relies Nafpaktitis, K. Mangold, S. Maynard, F. Mencher only on extraocular photoreceptors would and J. Walsh reviewed the manuscript. This ma- produce a ventral glow correspondingly terial is based on research supported by the brighter than the downwelling light, mak- National Science Foundation under Grant No. ing it vulnerable to detection. However, OCE76-81030 and the Smithsonian Institution. if this animal also relies on its own Hawaii Institute of Geophysics Contribution No. eyes to gauge the contribution of the am- 932. blent bioluminescence, it should get an accurate measure of the intensity of the downwelling light, titerature Cited

The eyes also have limitations as de- Case, J.F., J. Warner, A.T. Barnes and M. Lowen- tectors of downwelling light. The later- stine: Bioluminescence of lanternfish (Mycto- ally-directed eyes detect a strong ver- phidae) in response to changes in the light tical gradient in background illumina- intensity. Nature, Lond. 265, 176-181 (1977) tion (downWelling light) across their Clarke, W.D.: Function of bioluminescence in visual field. In both squids and fishes mesopelagic organisms. Nature, Lond. 198, the eyes have a slight forward tilt. 1244-1246 (1963) Therefore, when an animal is tilted Clarke, T.: Some aspects of the ecology of lan- downward the maximum intensity within ternfishes (Myctophidae) in the Pacific Ocean the visual field will be reduced com- near Hawaii. Fish Bull., U.S. 71, 401-434 pared with that of an animal in a hori- (1973) zontal position (upward tilting animals Dahlgren, U.: The production of light by animals. would further compound the problem). In Light production in cephalopods. J. Franklin addition, the eyes themselves are able Inst. 81, 525-556 (1916) 380 R.E. Young et al.: Roles of Photoreceptors in Counterillumination

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- - Morphology of the pineal complex in seven University of Hawaii at Manoa species of lanternfishes (Pisces: Myctophi- Honolulu, Hawaii 96822 dae). Am. J. Anat. 150, 509-530 (1977) USA

Date of final manuscript acceptance: December 15, 1978. Communicated by N.D. Holland, La Jolla