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Visual pigments and visual range underwater
Vision Res. Vol. 8, pp. 997-1011.
VISUAL
Pergamon Press 1968. Printed in Great Brimn.
PIGMENTS AND VISUAL UNDERWATER
RANGE
J. N. LYTHGOE M.R.C. VisionResearch Unit, institute of Ophthalmology, Judd Street, London, W.C.1 (Received 24 April 1968)
VISIONunderwater is severely limited by the optical properties of the water itself. Even in the clear waters of the Mediterranean it is rare for a diver to see any object at a range greater than 40 m and for British inshore waters a visual range of 5 m is considered good. Yet fishes appear to make good use of their surprisingly well developed eyes and it is possible that some of the special features of these eyes may be “adaptive” ones enabling the fish to see further through the water. The possibility that the visual pigments found in fishes might be adapted to render them most sensitive to the prevailing light conditions where they live was suggested by CLARKE (1936) and BAYLISSctal. (1936). The discovery, made almost simultaneously by DENTONand WARREN(1957) and by MUNZ (1957), that deep-sea fishes have visual pigments that are most sensitive to the pr~o~nantly blue light of abyssal depths strongly supported this suggestion. More recently MUNZ (1958, 1964) has shown that fishes living in the yellow-stained waters found close inshore tend to have visual pigments more sensitive to long wavelength light than do those living in the bluer waters of the open sea. Thus there is general support of the view that fishes possess visual pigments with maximum absorption at wavelengths (&,,3 more or less coincidental with the wavelength of maximum transmission of the water. However disparities between the properties of visual pigments actually extracted from the eye and those expected on this “Sensitivity hypothesis” are sufficiently frequent and consistent to suggest that this is not the whole story (LYTHGOE, 1966). These disparities may arise because the consideration of sensitivity alone is the wrong way to approach the problem. A fish needs to be able to see its prey, predators, companions and food from as far away as possible, and greater sensitivity to the incident daylight does not necessarily bring this about. The situation is similar to a man driving through fog at night. An increase in the brilliance of the headlights does not increase his visual range because there is also an increase in the light scattered back into the eye from the water droplets in the fog. But if the eye could be made more sensitive to the optical contrast between the distant objects on the road and their foggy background, these objects would become visible at a greater range. Usually underwater objects are seen because they appear to be either slightly brighter or slightly darker than the water background, but as the visual range between the object and the eye increases so the apparent contrast between it and its background decreases. 997
998
J.N. LYTHGOE
When the apparent contrast reaches a value too low for the eye to detect, the object becomes invisible. The possibility that some visual pigments may be more suitable than others to detect contrasts underwater springs from the fact that the further light travefs underwater the more monochromatic it becomes (TYLER, 1958, 1965). Thus daylight that has travelled the direct path from the surface to the object and from thence into the eye will have travelled a shorter path than light scattered into the eye from the water behind the object. The water background spacelight is therefore more monochromatic than that from the object unless, of course, the object is itself coloured. From Fig. 1 it becomes obvious that
WAVELENGTH
(nm)
FOG.I. The relative speetrai radiance of the water background (heavy line) just below the water surface, and the apparent spectral radiances of two matt grey targets, one slightly brighter (curves above heavy line) and the other slightly darker (curves below heavy line) than the background at various ranges (M = metres). Note that both families of curves approach the water background radiance as the distance increases. a visual pigment that has its maximum absorption offset from the wavelength of light that is best transmitted through the water will absorb less light from both the object and the background spacelight, but that relatively more light wiil be absorbed from the object than from the water background. The object will thus become brighter relative to the water background against which it is seen. The aim of this paper is to assess the advantages, in terms of visual range, to be expected from the use of various visual pigments in one type of coastal Mediterranean water. The investiga~on fell naturally into two parts: (1) The underwater measurement of the way in which the spectral contrast between a white object and its water background decreased as the visual range increased. (2) The use of these measurements in the computation of the visibility of white or grey objects (viewed horizontally in shallow water) as a function of visual pigment A,,,.
Visual Pigments and Visual Range Underwater
999
THEORY The image-forming light proceeding from an object to the eye underwater is reduced in intensity partly by absorption in the water mass and partly by loss through scattering. Simultaneously there is an increase in intensity due to light from other directions being scattered into the eye. In the simplest case where the path of sight is horizontal relative to the penetrating daylight the spectral radiance of the light JV, from the direction of the target changes with path length (r) through the water according to equation 1 (DUNTLEY, 1962). rN,. = rNoPr+ gN(l-e-Or) (1)
where the first term on the right represents the loss by absorption and scatter of imageforming light and the second term the gain of non-image forming light from scattering into the eye. a is the total spectral attenuation coefficient of a collimated beam of light passing through the water, rN,, is the spectral radiance of the target when r = o, gN is the spectral radiance of the water background and is independent of r. An object is visible only when the contrast between it and its background is large enough to detect. The apparent spectral contrast is defined by the equation:
cr=INrBLBN C, is a quantity depending on the two radiances rNr and eN and can be measured by physical means independent of the eye. By substituting the defining function for rNr (equation 1) for rN, in equation 2 it is apparent that for horizontal paths of sight C, is reduced as r increases, thus: C, = COe-m
(3)
(This equation has also been derived, but by another method, by LE GRANDE(1936)). Now if for a white target, i.e. when TN, > sN, rN, is reduced by a known factor, F, sothat:
.N,F= BN
(4)
then :
and similarly for a black target, where TN, < sN, the background a factor, F,sothat:
.NF=.N,
is similarly reduced by
(6)
and hence,
c, =
,,NF--,N gN
=-
F-l 1
(7)
From equation 3 it is evident that the inherent spectral contrast, CO(the contrast when I’ = o), can be calculated. CO is independent of depth because both gN and rN,, are reduced by the same factor as the depth increases. When the target is just beneath the surface the differential attenD
J. N.
1000
LYTHGOE
uation of daylight passing through the very thin water layer is insignificant, and ,N, is chiefly governed by the spectral reflectance of the target (if it has a matt surface) and the spectral irradiance of the daylight. In point of fact the spectral quality of daylight seems to have very little influence on the perception of underwater contrasts (LYTHGOE, 1966) and the daylight is here assumed to contain the same number of quanta at each frequency interval throughout the spectrum. Using equation 2 and assuming that TN, is approximately proportional to the diffuse spectral reflectance of the target at the very shallow depth under consideration here, the relative spectral energy distribution of ,N can be obtained. If C, is known for two or more values of r, a can be calculated from equation 3. Using these values of a and BN relative to *No it is possible to obtain rN, relative to ,N for any value of r. rN, and ,N are actual radiances, which can be measured at the plane of the eye with a photocell. However, the light reaching the front of the eye has then to pass into the eye and become absorbed by the visual pigment before it has any relevance to the visual capability of the animal. What is calculated here is the relative number of quanta that are absorbed by the visual pigment in the eye .N,. and BN and the visual contrast (,i,C,-) can be defined thus: .
.
J
rNr. Vp. P. dA -
viaCr
=
,N. Vp. P. dh
il
J
,N. Vp. P. dA
where Vp is the absorption curve of the visual pigment of known A,,,. and optical density, and P is the absorption of the pre-retinal media. METHODS The design of the instrument (Fig. 2) used to measure the apparent spectral contrast between the target. T,V~,and the water background spacelight, BN, is based on equations 4 and 6 for white and black targets respectively. A field derived from TN, is displayed against one derived from BN in a split-field fashion and this split field is viewed through one of a series of eight interference filters. One of a series of neutral density fikers is held by a magnet in the position indicated in Fig. 2. The transmission of this filter together with the refly factor of the two mirrors repizsents the factor, F. The neutral density iiiter is selected so that TN~F> ~$4 when r = o, and TN*F< fl when r is stightly leas than the visibk distance of the target or available measuring scale, whichever is the shorter. The instrument is then held to the eye so that the target fills the appropriate half of the split-field and the distance between the target and the diver is then varied until the two fields are of equal brightness. The distance between the neutral density filter and the target is then measured and recorded. The design of the instrument is governed by the important requirements that it should work immersed in water, and that it should be sufficiently robust to resist the inevitably rough treatment it receives in prolonged diving use. The neutral density filters were made by mounting Ilford gelatine filters between a microscope slide and a cover glass using the clear mounting cement “Depex.” The spectral transmission of the mounted filters was measured in an S.P. 600 Unican spectrophotometer and a calculated correction applied to allow for the decreased reflectance loss at the two glass surfaces when the filters are immersed in water. The spectral transmissions of the eight l-in. Balzer interference filters were measured in an S.P. 500 spectraphotometer. They had a ha-~ndwidth varying between 7 and 10 nm and a maximum transmission varying between O-37 and 0.59. They were protected by the manufacturer on both faces by coverglasses, and were mounted on a wheel so that they could be used in sequence. The split-field block was made of a 90” glass prism, half-silvered on one face, cemented to a glass rhomb whose outer long face was also silvered and protected from the sea water by a glass cover-slip cemented
Visual Pigments and Visual Range Underwater
FIG. 2. The diver-operated imtrumen t used to find the between a target and the water background spacelight of 8 interference filters allows these measurements to mode of operation is shown
1001
range at which the spectral contrast falls to aome known level. A series be made on a spectral basis. The in Fig. 3.
over it. The two long faces of the rhomb were not quite parallel so that the fields to be compared were separated by 5” 40’. It is essential that the eye should be able to focus on the plane of the @Meld and the collection angle of the instrument should allow the target to till the appropriate half of the 6eld compktely. For this reason a tube of machined perspex, 13 in. long, was used to separate the eye from the split-fkld. Perspex was used because it is colourless and because, having nearly the same refractive index as water, it is optically inert and scarcely interferes with the passage of light through it. When a uniformly illuminated field is viewed through the split-field block the ditference in brightness between the two fields due to reflection losses at the two aluminised surfaces on one side is very evident.
J. N. Lv,rsrc+ofi
1002
This light loss was estimated in two ways: (1) A uniformly ill~ted field was viewed through the instrument in the normal way using a 513 nm interference filter. Various combinations of finely graded neutral density filters were placed before the
brighter Geld until such a combination of l%ers was found that there was a visually exact match between the two fields. This indicated a reflectance factor of @617. (2) An S.E.I. spot photometer was used to obtain a series of measurements of each field. In this case the ilIuminated Seld was placed where the eye is usually positioned and the pempex tube and interference filter was removed. The measurements were made through the front of the instrument. Repeated measurements showed that the retleetance light loss was 0624 with a standard deviation of +0*021. The reflectance factor used in the calculations was O-621. The use of interferenoa Illtens means that the brightness of the two fields is greatly reduced relative to the surrounding daylight. Careful precautions have therefore to be taken to exclude all unwanted light. All surfaces were painted black and the perspex tube was shrouded in black plastic tape. The face plate was blacked out with felt except for a small aperture in front of one eye. A black rubber eyepiece attached to the end of the perspex tube was pressed against the face plate and thus an e%ctive light seal was made. &cause the two iields were viewed ~~~~y through the same interference filter, their spectral dlstrlbutlons were almost identical and the target range at which they appeared equally bright was the same irreape&ve of the adaptation state of the eye. However, because the contrast perception of the eye falls at low luminances the precision of the measurements was reduced at low intensities. Unakrwater sighting range The arrangement of apparatus to measure the decrease in contrast between a target and its water background is shown in Fig. 3. The measurements (off Marfa Quay on the North West Comer of Malta)
FIG. 3. The sighting range used to measure the spectral contrast between a target and its water background. The diver is holding the device shown in Fig. 2. The target and the measuring tape (which the diver is holding) are held up by inverted buckets filled with air. were made as near to noon as possible, but the target was down-sun from the observer in the afternoon.
The water background behind the target was unobscured by visible rocks or by obstructions of any kind. The target was made of a rigid square board of “perspex” with sides of I m. An adhesive sheet of white matt-surfaced plastic was applied to the visible face of the board and a sheet of black cotton velvet was applied to the back face. The diffuse spectral re&ctance of the white face is shown in Fig. 4. The target board was anchored to the bottom by cords attached to its two lower comers and held upright in the water by two cords tied to inverted air-Shed buckets. During all the experiments described the water was calm and there was no perceptible ground swell. To the base of the target was attached a wire-reinfomed surveyors’ tape, which was stretched out in a dire&on norm& to the plane of the target and held at a convenient height above the bottom by inverted air-filled buckets. The sighting range, being only 24 ft deep, was u~o~u~tely well within grappling range and indeed was entirely removed-preauma bly by fishermen-on one occasion. The whole set-up had therefore to be laid and taken up each day-a procees that took about 30 min. For the measurements described here the instrument was held to the eye as if it were a telescope with a diver steadying himself by grasping the measuring tape with his free hand. The instrument was then aligned on the target so that light from the target or from the background (whichever was the brighter) passed through the neutral density Iilter side of the instrument. Care was taken that the target completely filled the appropriate half of the split-field, and the iIIStNIl!Cnt was held so that the two fields from the same horizontal plane were compared. The diver then moved back and forth along the tape until the two fields were of equal brightness, whereupon the distance from the target (r) was read from the measuring tape and was recorded on a writing slate. The process was repeated using another neutral density filter until all available filters had
1003
Visual Pigments and Visual Range Underwater
WAVELENGTH
(nm)
FIG. 4. The diffuse reflectance (in air) of the white matt plastic target used in the measurements shown in Fig. 5. been tried. Both black and white targets were used, all the white target measurements being done first and the target was then reversed for the black target measurements. For the measurements of spectra1 contrast the white face of the target was used. Measurements of r using each of the eight interference filters were made using the same neutral filter. The neutral filter was then removed leaving the two mirrored surfaces to reduce the intensity of the target field. Some difliculty was experienced in making the brightness matches when the sun threw a constantly-changing dappled pattern on the target, but after some experience this effect could be discounted, and it is not thought that it greatly affected the accuracy of the measurements. RESULTS
The results of two experiments to find out how C, decreases as r increases are shown in Fig. 5. And the values for a and logt&, calculated from these results are shown in Table 1. TABLE 1
Time
Position of target
Wavelength
Target
18.X111.67
1410-1430
Down sun
513 nm
25.X111.67
1155-1245
Overhead sun
489 nm
Black White Black White
Date
a 0.122 0122 O-108 0.117
woe
0.050 l-106 @057 0601
If the instrument is properly designed and calibrated and if the theoretical framework outlined above is correct, then these results should satisfy the following predictions. (a) A straight line should result when log C, is plotted against r (equation 3). Examination of Fig. 5 indicates that the curves are straight lines, within experimental error. (b) a should remain about constant for each experimental period irrespective of whether a black or white target was used (equation 3). This appears to be the case (Table 1). (c) For black targets log C,, (log C, when r = o) should be zero or slightly less (equations 2 and 3). But for white targets CO should vary with the position of the sun and it should be greater on 18th August when the target was down-sun than it was on 25th August
J. N.
1004
-4
LYTHGOE
-4
o
.4
.8
Leg,, CONTRAST
FIG. 5. The results of two experiments at Marfa Point, Malta, to show how the contrast between black and white targets and the water background is reduced as the horizontal range imreases. On August 25th the sun was overhead, on August 18th the target was slightly down-sun. The experiments were carried out during the following periods: August 18th, 14.10-14.30; August 25th, 11.55-12.20.
when the sun was overhead. These predictions are fulfilled except in one detail. The regression lines calculated for the black targets indicate a log C, slightly greater, rather than slightly Iess, than zero. This is an impossible result because it means that the black targets should be blacker than black. However, if the data do not exactly fall on a straight line, then the curve might very well be drawn so that log CO is zero or slightly less. it is clear that these results come near to fulfilling the theoretical predictions, but the fit is not exact. At this stage it is not certain whether the discrepancies reflect an error in the instrument and its calibration, the experimental procedure, or in the theory itself. However, these results fit the theory reasonably well, and the main object of the experiments, which is to find how the relative spectral contrast of the white target is reduced with distance, can proceed. In Fig. 6 are plotted the ranges at which the spectral contrast between the target and its water backwood falls to two known values, and from these C, can be calculated using equation 3. It would &arty have been better to have calculated. C,, by using r at several different values for F at each wavelength. Unfortunately this was not possible because in the much longer time required for the measurements the sun’s altitude would have changed too much and the diver would have run out of air. The values of eN and
Visual Pigments and Visual Range Underwater 8 Aug.67 2Q
15
15
5 g i L 15
15
5
888
8a
588
nl
WAVELEWGTH InmJ FJG. 6. The results of four experiments at Marfa Point, Malta, designed to show the horizontal range at which the spectral contrast between the white target and the water background fell
to some known level. The target was always erected so that it was down-sun from the observer in the early afternoon. The experiments were carried out during the following periods (local time): 8th August, 14.OG14.30; 12th August, 12.45-13.30; 14th August, 12.00-12.10; 25th August, 12.30-12.45.
of 500 wave numbers between 17,000 (588 nm) and 23,000 (435 nm) were calculated from the data using equations 3 and 5 (Fig. 7). From the experimental point of view the results obtained on 25th August were the most reliable and these have been used in the calculations on visual performance. These results in common with the others become unreliable at each end of the spectrum because the low luminance of the split-field made measurement difficult. a at intervals
The calculation of visual range The purpose of these calculations is to find out how the possession of visual pigments differing only in their X,, affect the range at which white, grey and black objects can be seen underwater. The relative amounts of light absorbed by the visual pigments from rN, and BN is first calculated, and from this the effective visual contrast (Vi,C,) is found. It is assumed that the level at which ViSC, becomes sub-liminal will be a measure of the visual range of the object.
1006
J. N. LYTHCOE
a
2
%I
0” 5; f a 0 mJ
t
*
.I*
I*
”
*
500
’
s
c
*
WAVELENGTH
0
600
500
600
(nm)
FIG. 7. Values for the beam attenuation
coefficient (a) the inherent spectral contrast for the white target calculated from the data obtained on 25th August (Fig. 4).
The calculations are based on equation should more properly be written: Vis
cr
s
18, but in these calculations
2?000 &*
vp.
P.
ah,
17000
-
\‘
23000
//,
I'?000
&.
Yp.
(CO)
this equation
P. Aih.
23000
BN. Vp. P. nh. c
(11)
17000
When oh is the mean value for each interval. of 500 wave numbers, P, is the spectral transmission of the pre-retinal media and Yp is the spectral absorption of the visual pigment. Only rhodopsins will be considered here because these afone have been extracted from the great majority of marine fishes. Rhodopsins are particularly suited for a study of this nature because when plotted on a frequency basis they have all the same shaped absorption curve (DARTNALL, 1952) and the same photosensitivity (DARTNALL, 1968), The proportion of light incident on the retina that is absorbed by the visual pigment depends chiefiy on the optical density of the visual pigment present. Also, as the optical density of the pigment increases, so its absorption spectrum becomes broader. In these calculations the reasonable figure of 0.4 fur the optical density of visual pigment in the fishes’ eye has been chosen
Visual Pigments and Visual Range Underwater
1007
(see DENTON and NICOL, 1964). The A,_ of rhodopsins extracted from marine fishes varies from 468 nm in a deep sea fish (DARTNALLand LYTHGOE,1965) to 528 nm, in some mackerels (MUNZ, 1964). The spectral absorption of the pre-retinal media varies widely from fish to fish and, in general, shallow water fishes have rather yellow corneas or lenses, whilst in those living in deep water they are very clear (DENTON, 1956). In fact there are no data for the absorption of the pre-retinal media in fishes suitable for a quantitative approach such as this and the exact values are not likely to be very significant. STILES'data for the human + , .
9
.
j,l(darker prey:
A,,
OF
i
VlsUAL
(liohl;r grw)
PIGMENT (nm)
FIG. 8. The horizontal range at which four grey targets of difforent re%ctances would be visible in shallow water when rhodopsins of di&rent hmox are used. These curves have been calculated for photopic conditions where contrasts of 0.02 (log 0.02 = -1.7) can be detected, and for scotopic conditions where a contrast of 02 (log 02 = -@ 7) might be detected. A rhodopsin of h,.x 520 nm would give the greatest sensitivity to the water background spacelight (see Fig. 10). These data were calculated from the values measured on 25th August, 1967.
J. N. LYTHGOE
1008
(STILES, 1967) has consequently been adopted because this absorption curve is similar to that found in some coastal water fishes (DENTON, 1956). The calculations of visC~ were made for Rhodopsins of Amax= 17500 wave numbers (571 nm), 18500 (541 MI), 19500 (513 nm), 20500 (488 run), 21500 (465 run), and when r = 1 m, 5 m, 10 m, 20 m and 40 m. The calculations were made for target reflectances varying from white through grey to black. The results of these calculations are shown in Figs. 8 and 9 and it is evident that the visual pigment h,,, does influence the range at which grey targets can be seen through the water. eye
.2
.4 TARGET
.6
.6
1.0
REFLECTANCE
FIG. 9. The horizontal range at which grey targeta of various reflectances can be seen in shallow water when rhodopsins of hmlx 541 run and 488 run are used. The limit of contrast perception threshold is here taken to be @2-a reasonable value for scotopic vision.
DISCUSSION The main intention in making the calculations outlined earlier was to demonstrate that the spectral absorption of the visual pigment contained in the eye can Sect the perceived contrast of a grey object against the water background and hence the range at which the object can just be seen through the water (Figs. 8 and 9). The calculations are sufficiently accurate to show quantitatively what advantages in visual range can be expected under some precisely defined conditions. The calculations are based on the way that the apparent spectral radiances of grey targets change as the visual range increases (Fig. 1). For close targets in shallow water the spectral distribution curve of the target light is considerably flatter than that for the water background spacelight. As the range of the target increases, its apparent spectral radiance approaches that of the water background spacelight, until finally the eye is unable to distinguish light from the two sources and the object becomes invisible. From Fig. 1 it is evident from the flatness of the curves for close targets that the amount of light from the target that would be absorbed by a visual pigment is virtually independent of the pigment h,,,. This is not true for the background spacelight where the visual pigment whose h,,, corresponds with the wavelength of maximum water background radiance will absorb more quanta than one whose AmoX is offset from that wavelength. When the target is somewhat brighter than the water background an “offset” visual pigment will have the effect of reducing the perceived brightness of the water background relative to that of the target which will then stand out in increased contrast against the water background. On the other hand when the target is darker than the water background a reduction in the perceived brightness of the water background relative to the target will reduce the
Visual Pigments and Visual Range Underwater
1009
contrast between the target and its background. Thus for close targets in shallow water the pigment that is most suitable for distinguishing targets brighter than the water back-
ground is precisely that least suitable for seeing dark objects. The situation is quite different for large targets whose high inherent contrast against the water background allows them to be seen at greater ranges. This is because the relative spectral radiance of the water background is at a maximum at approximately those wavelengths where the beam attenuation coefficient of light passing through the water is at a minimum. But the apparent spectral contrast between target and background falls most rapidly where the beam attenuation coefficient is high, and most slowly at about the wavelength of maximum spacelight radiance. The result is that, at the longer sighting ranges, the rate at which the spectral contrast falls becomes more important than the inherent spectral contrast. Thus for distant objects, be they dark or bright, low contrasts will be best perceived by eyes that contain a visual pigment with &,,,, corresponding to the wavelength of maximum background radiance. One very important factor that influences the eye’s ability to perceive low contrasts is the angle subtended at the eye by the target field. Once this angle falls below some critical value the contrast perception threshold increases, with the result that the visible range of small objects is less than for large ones of similar brightness. Because it is the range between the object and the eye that determines whether or not an offset visual pigment will improve visual range, practically all very small objects in shallow water will be best seen by an eye possessing an offset visual pigment. As the depth increases the effect of visual pigment &,_ on contrast perception gradually decreases until at abyssal depths no such advantage exists (LYTHGOE,1966). Furthermore, as the natural illumination falls in intensity-either because of increased depth or because of the onset of night-the ability of the eye to detect small increments in brightness falls. Anything that will tend to reduce the sensitivity of the eye (such as the possession of an offset visual pigment (Fig. 10)) will therefore tend to reduce its ability to detect contrasts and at very low intensities the need for maximum sensitivity might well be of overriding importance. Although the hypothesis that the possession of an offset visual pigment might improve the range of vision underwater was originally proposed to explain why the visual pigments extracted from fishes would not always confer the maximum sensitivity, it is still not
500 A max OF VISUAL
FIG. 10. The relative
550nm PIGMENT
number of quanta absorbed from the horizontal background spacelight when rhodopsins of different Amax,but all of optical density O-4, are used.
1010
J. N. LYTHGOE
possible to explain the distribution of visual pigments. Furthermore, there is almost total ignorance about the precise visual tasks the fish has to perform, and knowledge of these is necessary before any analysis of visual adaptation can be undertaken. There are as yet no data about the cone pigments in any marine fish and thus present analyses should properly be confmed to visual problems at night or in deep water. Even then, where two scotopic pigments are present, it is not known in fishes if they occur mixed or separate. On the other hand, certain visual tasks will be better performed with some visual pigments than with others and an understanding of these advantages may ultimately lead to a general understanding of the functional significance of visual pigments in ecology. At present visual pigments can be crudely divided into two categories. (1) Visual pigments whose absorption maximum corresponds with the transmission maximum of the water. These pigments will give greater sensitivity at depth (although an increase in optical density of pigment in the retina would serve as well, or better); and some improvement in sensitivity in shallow waters at night. In good light the range at which large objects, which present a high inherent contrast against the water background can be seen, will be increased. (2) Visual pigments whose absorption maximum is offset from the transmission maximum of the water will give an improved visual range for close objects, especially when the objects are small or are only slightly brighter than the water background. This improvement in visual range is reduced as the depth increases. The present work agrees with the earlier indications (LYTHGOE,1966) that for Mediterranean waters improved contrast perceptions results when pigments offset to longer wavelengths are used. The underwater measurements have not been made in other water types, but the earlier work indicated that in British Coastal and Estuaries waters it is the visual pigments offset to shorter wavelengths that will yield the improved perception of contrast for bright objects. Acknowledgements-No project of this kind could have been completed without the active help from many people. I particularly thank Mr. A. H. CHURCHand Mr. C. V. CARPERfor their help in constructing the instrument; and Dr. H. J. A. DARTNALL,Dr. C. C. HEMMINGS,Dr. J. D. MORELANDand Dr. PRWILLA SILVERfor their helpful discussion and advice throughout the project. In Malta Mr. J. J. BARBARAof the Dept. of Fisheries and Professor H. MICCALLEFof the Royal University of Malta provided many valuable facilities. The compressed air used in the diving was provided by Commander GRATTON and his team at the Mediterranean Fleet Diving Centre and I would like to thank them for this essential help. Finally GILLIAN LYTHG~Eskilfully and patiently undertook the job of diving tender and underwater assistant. Everyone who has tried to carry out experiments underwater will know how important this can be.
REFERENCES BAYLIS, L. E., LYTHGOE,R. J. and TANSLEY,K. (1936). Some new forms of visual purple found in sea fishes with a note of the visual cells of origin. Proc. R. Sot., B 816, 95-l 13. CLARKE,G. L. (1936). On the depth at which fishes can see. Ecology 17,452-456. DARTNALL,H. J. A. (1952). Visual pigment 467, a photosensitive pigment present in Tenth retinae. J. Physiol. 116, 257-289. DARTNALL,H. J. A. (1968). The photosensitivities of visual pigments in the presence of hydroxylamine. Vision Res. 8, 339-358. DARTNALL,H. J. A. and LYTHGOE,J. N. (1965). The spectral clustering of visual pigments. Vision Res. 5, 81-100. DENTON,E. J. (1956). Recherches sur I’absorption de la lumitre par le cristallin des Poissons. Bull. Inst. Oceanogr. Monaco No. 1071, pp. I-IO. DENTON,E. J. and NICOL, J. A. C. (1964). The choroidal tapeta of some cartilagenous fishes (Chondrichthyes). J. mar. bioi. Assoc. 44, 219-258.
Visual Pigments and Visual Range Underwater DENTON,E. J. and
WARREN, F.
1011
J. (1957). The photosensitive pifpnents in the retinae of deep sea fish.
J. mar. biol. Assoc. 36, 651-662.
DUNTLEY,S. Q. (1962). Underwater visibility. In 7&e Sea, Vol. I (edited by M. N. HILL). Interscience New York and London. LE Gm, Y. (1939). La penetration de la hnni&e dans la mer. Ann&es de I’Zmt. ~~o~u~~ 19, 393-436. LYTHGOE,J. N. (1966). Visual pigments and underwater vision. In Lighr OS an Ecological Factor, pp. 375-391 (edited by R. BmBmoa, G. C. EVANSand 0. RACKHAM).Blackwell, Oxford. MUNZ, F. W. (1957). Photosensitive pigments from retinas of deep-sea fishes. Science, N.Y. 125, 1142-l 143. MUNZ, F, W. (1958a). Photosensitive pigments from the retinae of certain deep sea fishes. J. Pbysioi. 140,220-225. MUMZ,F. W. (1958b). The photosensitive retinal pigments of fishes from relatively turbid coastal waters. J. gen. Physiol. 42,445-459. MUNZ, F. W. (1964). The visual pigments of epipelagic and rocky shore iishea. Vision Rex 4, 441654. TYLER,J. E. (1958). Natural water as a monochromater. Limnol. OceuBogr. 4, 102-10.5. Tne~, J. E. (1965). In situ spectroscopy in ocean and lake waters. J. opr. Sot. Anr. 55, 800-805.
WYSZECKI,G. and !&TLEs,W. S. (1967). Coior Scicncc, p. 216, John Wiley, New York, London, Sydney. Abstract-In shallow water the spectral radiance of a gmy object differs from that of the water background spacelight. The spectral absorbance of the visual pigments present in the eye will therefore affect the perceived contrast between an object and its water background, and hence the range at which the object can be seen underwater. A diver-operated instrument is described that allows the spectral contrast between a grey target and its water background to be measured. The data so obtained show that in Medi&rmnean waters those visual pigments with a hmsx corresponding to the wavelength of maximum light axon through the water are be& suited for detectin8 large very dark or very bright objects. Rut “offset” visual pigments are more suitable for dete&ing small grey objects in shallow water. R&ur&-En eau peu profonde, la radiance spectrale dun objet gris ditI&e de celle du fond huninenx de I’eau. L’absorption spectrale des pigments visuels de l’oeil affectera done le contra&e Peru entre un objet et b fond, et par co&quent la limite de visibilite sous l’eau. Ondecrituni ant manipult par tm plongeur et qui mesure le contra&e spectral entre cible grise et fond. Les r&hats obtenus en M&l&ran&e montrent que les pigments visuels de h,= correspondant a la longueu d’onde de transparence maximum de l’eau sent Its plus favorables pour d&e&r des tpamis objets t&s sombres ou t&s claim, mais que des pigments visuels &cart& de cette condition conviennent mieux pour d&c&r de petits objets gris en eau peu profonde. In Aachem Wasser unterscheidet sicfi die spektrale ~~~h~ eines grauen Objektes von der des ~~~~~~ des Wasaem. Die spektrale Absorption der Sehstoffc im Auge wird deshalb den wahrsenommenen Kontrast xwis&n einem Objekt und dessert Wasserhintergrud beeinflussen und somit die Entfermrng auf die das Objekt unter Wasser erkamn wird. Es wird ein taucherbetriebenes Instrument beachriehen, mit dem der spektraIe Kontrast zwischen einem grauen Gegemtand und seinem Wasserhintergnmd gemessen werden kann. Die damit erhahenen MeDwerte z&en, da8 in Mitts die Sebstoffe mit einem hmaX, das der We~e~~ m ~h~ion im Wasser entapricht, f& die Wahrnehmung sehr dnnkler oder sehr heller Objekte am be&en geeignet sind. Jedoch sind Sehstoffe mit einer L‘offset”-Absorption ti g&net urn kleine graue Objekte in flachem Wasser N erkennen. Pe3mMe -
CnexrpaJrbrfoe rr3nylrerrue ceporo o6=rcTa, rraxoxxmerocx B Bone ria MUIOTuHBaeTCx01 er0 Um~eHBx B TOMCJry¶ae, eCBB OH BaxOxriTCx B BOXC, rxe Z&TOrRy6oxO. Tarcrrhr 06pa3o~, crrexrpa.nb~oe ~or~o~~ 3pBTe&ubm IuirMeBToB BMerorrmxcx B masy 6yBeT BJIHBTBHa BOcrxpmrTrie KoBTpacTa hrmxxy &xTorb4 a Tesvi(PoBobf rra KOTO~OMOH ~axomrrcx B Bone, a ofcIoA8 R Ba npe,~eBBr B KOTOpbIX06l&xT MOXeT 6bmb B&UreaiIOB BOxOil. QlTBCblBaeTCxOuepaImOBBax amTapaTypa lTOABOLIBHrCa, CIIOMOIIIbK)xOTOpOieMOXCT 6blTb s3MCyCH CneRTpaJlbHb& KOHTpaCTMeSfCAy CepbIhi 06beETOM H +OHOMHa KOTOPOM ICOM Mecfe,
1012
J. N. LYTHGOE OH BEAeH B BOAe. ~OJly¶CHHbIe TalCEM O6pa3OM AaIiHbIe IlOKa3bIBaIOT,YTO B BOAaX Cpememoro ~oprTe3pmxb1s1emmembI 6ommenonxo~anao6Hapy~e~r 60~5n~m OPeHb TemibIx EJ'IEOgeIib qmfx O~MXTOB, EoTopbxe HhfemT ?.IIMX., COOT~e~cmymnym Amnie Mom hiBgCHM81IbHoro nponyma~~si cwra Irepe3 BOTH) qmy. cc~o6a~om1,w (CfOffsm) xc 3pETeJIbHbIe IInrMeETbI 6once rIpHCnOCO6neHbI AJIR O6HapyXeHSUl MWIblX CepbIX 06’bCXTOB B MWJXOfi BOAC
VISUAL
Pergamon Press 1968. Printed in Great Brimn.
PIGMENTS AND VISUAL UNDERWATER
RANGE
J. N. LYTHGOE M.R.C. VisionResearch Unit, institute of Ophthalmology, Judd Street, London, W.C.1 (Received 24 April 1968)
VISIONunderwater is severely limited by the optical properties of the water itself. Even in the clear waters of the Mediterranean it is rare for a diver to see any object at a range greater than 40 m and for British inshore waters a visual range of 5 m is considered good. Yet fishes appear to make good use of their surprisingly well developed eyes and it is possible that some of the special features of these eyes may be “adaptive” ones enabling the fish to see further through the water. The possibility that the visual pigments found in fishes might be adapted to render them most sensitive to the prevailing light conditions where they live was suggested by CLARKE (1936) and BAYLISSctal. (1936). The discovery, made almost simultaneously by DENTONand WARREN(1957) and by MUNZ (1957), that deep-sea fishes have visual pigments that are most sensitive to the pr~o~nantly blue light of abyssal depths strongly supported this suggestion. More recently MUNZ (1958, 1964) has shown that fishes living in the yellow-stained waters found close inshore tend to have visual pigments more sensitive to long wavelength light than do those living in the bluer waters of the open sea. Thus there is general support of the view that fishes possess visual pigments with maximum absorption at wavelengths (&,,3 more or less coincidental with the wavelength of maximum transmission of the water. However disparities between the properties of visual pigments actually extracted from the eye and those expected on this “Sensitivity hypothesis” are sufficiently frequent and consistent to suggest that this is not the whole story (LYTHGOE, 1966). These disparities may arise because the consideration of sensitivity alone is the wrong way to approach the problem. A fish needs to be able to see its prey, predators, companions and food from as far away as possible, and greater sensitivity to the incident daylight does not necessarily bring this about. The situation is similar to a man driving through fog at night. An increase in the brilliance of the headlights does not increase his visual range because there is also an increase in the light scattered back into the eye from the water droplets in the fog. But if the eye could be made more sensitive to the optical contrast between the distant objects on the road and their foggy background, these objects would become visible at a greater range. Usually underwater objects are seen because they appear to be either slightly brighter or slightly darker than the water background, but as the visual range between the object and the eye increases so the apparent contrast between it and its background decreases. 997
998
J.N. LYTHGOE
When the apparent contrast reaches a value too low for the eye to detect, the object becomes invisible. The possibility that some visual pigments may be more suitable than others to detect contrasts underwater springs from the fact that the further light travefs underwater the more monochromatic it becomes (TYLER, 1958, 1965). Thus daylight that has travelled the direct path from the surface to the object and from thence into the eye will have travelled a shorter path than light scattered into the eye from the water behind the object. The water background spacelight is therefore more monochromatic than that from the object unless, of course, the object is itself coloured. From Fig. 1 it becomes obvious that
WAVELENGTH
(nm)
FOG.I. The relative speetrai radiance of the water background (heavy line) just below the water surface, and the apparent spectral radiances of two matt grey targets, one slightly brighter (curves above heavy line) and the other slightly darker (curves below heavy line) than the background at various ranges (M = metres). Note that both families of curves approach the water background radiance as the distance increases. a visual pigment that has its maximum absorption offset from the wavelength of light that is best transmitted through the water will absorb less light from both the object and the background spacelight, but that relatively more light wiil be absorbed from the object than from the water background. The object will thus become brighter relative to the water background against which it is seen. The aim of this paper is to assess the advantages, in terms of visual range, to be expected from the use of various visual pigments in one type of coastal Mediterranean water. The investiga~on fell naturally into two parts: (1) The underwater measurement of the way in which the spectral contrast between a white object and its water background decreased as the visual range increased. (2) The use of these measurements in the computation of the visibility of white or grey objects (viewed horizontally in shallow water) as a function of visual pigment A,,,.
Visual Pigments and Visual Range Underwater
999
THEORY The image-forming light proceeding from an object to the eye underwater is reduced in intensity partly by absorption in the water mass and partly by loss through scattering. Simultaneously there is an increase in intensity due to light from other directions being scattered into the eye. In the simplest case where the path of sight is horizontal relative to the penetrating daylight the spectral radiance of the light JV, from the direction of the target changes with path length (r) through the water according to equation 1 (DUNTLEY, 1962). rN,. = rNoPr+ gN(l-e-Or) (1)
where the first term on the right represents the loss by absorption and scatter of imageforming light and the second term the gain of non-image forming light from scattering into the eye. a is the total spectral attenuation coefficient of a collimated beam of light passing through the water, rN,, is the spectral radiance of the target when r = o, gN is the spectral radiance of the water background and is independent of r. An object is visible only when the contrast between it and its background is large enough to detect. The apparent spectral contrast is defined by the equation:
cr=INrBLBN C, is a quantity depending on the two radiances rNr and eN and can be measured by physical means independent of the eye. By substituting the defining function for rNr (equation 1) for rN, in equation 2 it is apparent that for horizontal paths of sight C, is reduced as r increases, thus: C, = COe-m
(3)
(This equation has also been derived, but by another method, by LE GRANDE(1936)). Now if for a white target, i.e. when TN, > sN, rN, is reduced by a known factor, F, sothat:
.N,F= BN
(4)
then :
and similarly for a black target, where TN, < sN, the background a factor, F,sothat:
.NF=.N,
is similarly reduced by
(6)
and hence,
c, =
,,NF--,N gN
=-
F-l 1
(7)
From equation 3 it is evident that the inherent spectral contrast, CO(the contrast when I’ = o), can be calculated. CO is independent of depth because both gN and rN,, are reduced by the same factor as the depth increases. When the target is just beneath the surface the differential attenD
J. N.
1000
LYTHGOE
uation of daylight passing through the very thin water layer is insignificant, and ,N, is chiefly governed by the spectral reflectance of the target (if it has a matt surface) and the spectral irradiance of the daylight. In point of fact the spectral quality of daylight seems to have very little influence on the perception of underwater contrasts (LYTHGOE, 1966) and the daylight is here assumed to contain the same number of quanta at each frequency interval throughout the spectrum. Using equation 2 and assuming that TN, is approximately proportional to the diffuse spectral reflectance of the target at the very shallow depth under consideration here, the relative spectral energy distribution of ,N can be obtained. If C, is known for two or more values of r, a can be calculated from equation 3. Using these values of a and BN relative to *No it is possible to obtain rN, relative to ,N for any value of r. rN, and ,N are actual radiances, which can be measured at the plane of the eye with a photocell. However, the light reaching the front of the eye has then to pass into the eye and become absorbed by the visual pigment before it has any relevance to the visual capability of the animal. What is calculated here is the relative number of quanta that are absorbed by the visual pigment in the eye .N,. and BN and the visual contrast (,i,C,-) can be defined thus: .
.
J
rNr. Vp. P. dA -
viaCr
=
,N. Vp. P. dh
il
J
,N. Vp. P. dA
where Vp is the absorption curve of the visual pigment of known A,,,. and optical density, and P is the absorption of the pre-retinal media. METHODS The design of the instrument (Fig. 2) used to measure the apparent spectral contrast between the target. T,V~,and the water background spacelight, BN, is based on equations 4 and 6 for white and black targets respectively. A field derived from TN, is displayed against one derived from BN in a split-field fashion and this split field is viewed through one of a series of eight interference filters. One of a series of neutral density fikers is held by a magnet in the position indicated in Fig. 2. The transmission of this filter together with the refly factor of the two mirrors repizsents the factor, F. The neutral density iiiter is selected so that TN~F> ~$4 when r = o, and TN*F< fl when r is stightly leas than the visibk distance of the target or available measuring scale, whichever is the shorter. The instrument is then held to the eye so that the target fills the appropriate half of the split-field and the distance between the target and the diver is then varied until the two fields are of equal brightness. The distance between the neutral density filter and the target is then measured and recorded. The design of the instrument is governed by the important requirements that it should work immersed in water, and that it should be sufficiently robust to resist the inevitably rough treatment it receives in prolonged diving use. The neutral density filters were made by mounting Ilford gelatine filters between a microscope slide and a cover glass using the clear mounting cement “Depex.” The spectral transmission of the mounted filters was measured in an S.P. 600 Unican spectrophotometer and a calculated correction applied to allow for the decreased reflectance loss at the two glass surfaces when the filters are immersed in water. The spectral transmissions of the eight l-in. Balzer interference filters were measured in an S.P. 500 spectraphotometer. They had a ha-~ndwidth varying between 7 and 10 nm and a maximum transmission varying between O-37 and 0.59. They were protected by the manufacturer on both faces by coverglasses, and were mounted on a wheel so that they could be used in sequence. The split-field block was made of a 90” glass prism, half-silvered on one face, cemented to a glass rhomb whose outer long face was also silvered and protected from the sea water by a glass cover-slip cemented
Visual Pigments and Visual Range Underwater
FIG. 2. The diver-operated imtrumen t used to find the between a target and the water background spacelight of 8 interference filters allows these measurements to mode of operation is shown
1001
range at which the spectral contrast falls to aome known level. A series be made on a spectral basis. The in Fig. 3.
over it. The two long faces of the rhomb were not quite parallel so that the fields to be compared were separated by 5” 40’. It is essential that the eye should be able to focus on the plane of the @Meld and the collection angle of the instrument should allow the target to till the appropriate half of the 6eld compktely. For this reason a tube of machined perspex, 13 in. long, was used to separate the eye from the split-fkld. Perspex was used because it is colourless and because, having nearly the same refractive index as water, it is optically inert and scarcely interferes with the passage of light through it. When a uniformly illuminated field is viewed through the split-field block the ditference in brightness between the two fields due to reflection losses at the two aluminised surfaces on one side is very evident.
J. N. Lv,rsrc+ofi
1002
This light loss was estimated in two ways: (1) A uniformly ill~ted field was viewed through the instrument in the normal way using a 513 nm interference filter. Various combinations of finely graded neutral density filters were placed before the
brighter Geld until such a combination of l%ers was found that there was a visually exact match between the two fields. This indicated a reflectance factor of @617. (2) An S.E.I. spot photometer was used to obtain a series of measurements of each field. In this case the ilIuminated Seld was placed where the eye is usually positioned and the pempex tube and interference filter was removed. The measurements were made through the front of the instrument. Repeated measurements showed that the retleetance light loss was 0624 with a standard deviation of +0*021. The reflectance factor used in the calculations was O-621. The use of interferenoa Illtens means that the brightness of the two fields is greatly reduced relative to the surrounding daylight. Careful precautions have therefore to be taken to exclude all unwanted light. All surfaces were painted black and the perspex tube was shrouded in black plastic tape. The face plate was blacked out with felt except for a small aperture in front of one eye. A black rubber eyepiece attached to the end of the perspex tube was pressed against the face plate and thus an e%ctive light seal was made. &cause the two iields were viewed ~~~~y through the same interference filter, their spectral dlstrlbutlons were almost identical and the target range at which they appeared equally bright was the same irreape&ve of the adaptation state of the eye. However, because the contrast perception of the eye falls at low luminances the precision of the measurements was reduced at low intensities. Unakrwater sighting range The arrangement of apparatus to measure the decrease in contrast between a target and its water background is shown in Fig. 3. The measurements (off Marfa Quay on the North West Comer of Malta)
FIG. 3. The sighting range used to measure the spectral contrast between a target and its water background. The diver is holding the device shown in Fig. 2. The target and the measuring tape (which the diver is holding) are held up by inverted buckets filled with air. were made as near to noon as possible, but the target was down-sun from the observer in the afternoon.
The water background behind the target was unobscured by visible rocks or by obstructions of any kind. The target was made of a rigid square board of “perspex” with sides of I m. An adhesive sheet of white matt-surfaced plastic was applied to the visible face of the board and a sheet of black cotton velvet was applied to the back face. The diffuse spectral re&ctance of the white face is shown in Fig. 4. The target board was anchored to the bottom by cords attached to its two lower comers and held upright in the water by two cords tied to inverted air-Shed buckets. During all the experiments described the water was calm and there was no perceptible ground swell. To the base of the target was attached a wire-reinfomed surveyors’ tape, which was stretched out in a dire&on norm& to the plane of the target and held at a convenient height above the bottom by inverted air-filled buckets. The sighting range, being only 24 ft deep, was u~o~u~tely well within grappling range and indeed was entirely removed-preauma bly by fishermen-on one occasion. The whole set-up had therefore to be laid and taken up each day-a procees that took about 30 min. For the measurements described here the instrument was held to the eye as if it were a telescope with a diver steadying himself by grasping the measuring tape with his free hand. The instrument was then aligned on the target so that light from the target or from the background (whichever was the brighter) passed through the neutral density Iilter side of the instrument. Care was taken that the target completely filled the appropriate half of the split-field, and the iIIStNIl!Cnt was held so that the two fields from the same horizontal plane were compared. The diver then moved back and forth along the tape until the two fields were of equal brightness, whereupon the distance from the target (r) was read from the measuring tape and was recorded on a writing slate. The process was repeated using another neutral density filter until all available filters had
1003
Visual Pigments and Visual Range Underwater
WAVELENGTH
(nm)
FIG. 4. The diffuse reflectance (in air) of the white matt plastic target used in the measurements shown in Fig. 5. been tried. Both black and white targets were used, all the white target measurements being done first and the target was then reversed for the black target measurements. For the measurements of spectra1 contrast the white face of the target was used. Measurements of r using each of the eight interference filters were made using the same neutral filter. The neutral filter was then removed leaving the two mirrored surfaces to reduce the intensity of the target field. Some difliculty was experienced in making the brightness matches when the sun threw a constantly-changing dappled pattern on the target, but after some experience this effect could be discounted, and it is not thought that it greatly affected the accuracy of the measurements. RESULTS
The results of two experiments to find out how C, decreases as r increases are shown in Fig. 5. And the values for a and logt&, calculated from these results are shown in Table 1. TABLE 1
Time
Position of target
Wavelength
Target
18.X111.67
1410-1430
Down sun
513 nm
25.X111.67
1155-1245
Overhead sun
489 nm
Black White Black White
Date
a 0.122 0122 O-108 0.117
woe
0.050 l-106 @057 0601
If the instrument is properly designed and calibrated and if the theoretical framework outlined above is correct, then these results should satisfy the following predictions. (a) A straight line should result when log C, is plotted against r (equation 3). Examination of Fig. 5 indicates that the curves are straight lines, within experimental error. (b) a should remain about constant for each experimental period irrespective of whether a black or white target was used (equation 3). This appears to be the case (Table 1). (c) For black targets log C,, (log C, when r = o) should be zero or slightly less (equations 2 and 3). But for white targets CO should vary with the position of the sun and it should be greater on 18th August when the target was down-sun than it was on 25th August
J. N.
1004
-4
LYTHGOE
-4
o
.4
.8
Leg,, CONTRAST
FIG. 5. The results of two experiments at Marfa Point, Malta, to show how the contrast between black and white targets and the water background is reduced as the horizontal range imreases. On August 25th the sun was overhead, on August 18th the target was slightly down-sun. The experiments were carried out during the following periods: August 18th, 14.10-14.30; August 25th, 11.55-12.20.
when the sun was overhead. These predictions are fulfilled except in one detail. The regression lines calculated for the black targets indicate a log C, slightly greater, rather than slightly Iess, than zero. This is an impossible result because it means that the black targets should be blacker than black. However, if the data do not exactly fall on a straight line, then the curve might very well be drawn so that log CO is zero or slightly less. it is clear that these results come near to fulfilling the theoretical predictions, but the fit is not exact. At this stage it is not certain whether the discrepancies reflect an error in the instrument and its calibration, the experimental procedure, or in the theory itself. However, these results fit the theory reasonably well, and the main object of the experiments, which is to find how the relative spectral contrast of the white target is reduced with distance, can proceed. In Fig. 6 are plotted the ranges at which the spectral contrast between the target and its water backwood falls to two known values, and from these C, can be calculated using equation 3. It would &arty have been better to have calculated. C,, by using r at several different values for F at each wavelength. Unfortunately this was not possible because in the much longer time required for the measurements the sun’s altitude would have changed too much and the diver would have run out of air. The values of eN and
Visual Pigments and Visual Range Underwater 8 Aug.67 2Q
15
15
5 g i L 15
15
5
888
8a
588
nl
WAVELEWGTH InmJ FJG. 6. The results of four experiments at Marfa Point, Malta, designed to show the horizontal range at which the spectral contrast between the white target and the water background fell
to some known level. The target was always erected so that it was down-sun from the observer in the early afternoon. The experiments were carried out during the following periods (local time): 8th August, 14.OG14.30; 12th August, 12.45-13.30; 14th August, 12.00-12.10; 25th August, 12.30-12.45.
of 500 wave numbers between 17,000 (588 nm) and 23,000 (435 nm) were calculated from the data using equations 3 and 5 (Fig. 7). From the experimental point of view the results obtained on 25th August were the most reliable and these have been used in the calculations on visual performance. These results in common with the others become unreliable at each end of the spectrum because the low luminance of the split-field made measurement difficult. a at intervals
The calculation of visual range The purpose of these calculations is to find out how the possession of visual pigments differing only in their X,, affect the range at which white, grey and black objects can be seen underwater. The relative amounts of light absorbed by the visual pigments from rN, and BN is first calculated, and from this the effective visual contrast (Vi,C,) is found. It is assumed that the level at which ViSC, becomes sub-liminal will be a measure of the visual range of the object.
1006
J. N. LYTHCOE
a
2
%I
0” 5; f a 0 mJ
t
*
.I*
I*
”
*
500
’
s
c
*
WAVELENGTH
0
600
500
600
(nm)
FIG. 7. Values for the beam attenuation
coefficient (a) the inherent spectral contrast for the white target calculated from the data obtained on 25th August (Fig. 4).
The calculations are based on equation should more properly be written: Vis
cr
s
18, but in these calculations
2?000 &*
vp.
P.
ah,
17000
-
\‘
23000
//,
I'?000
&.
Yp.
(CO)
this equation
P. Aih.
23000
BN. Vp. P. nh. c
(11)
17000
When oh is the mean value for each interval. of 500 wave numbers, P, is the spectral transmission of the pre-retinal media and Yp is the spectral absorption of the visual pigment. Only rhodopsins will be considered here because these afone have been extracted from the great majority of marine fishes. Rhodopsins are particularly suited for a study of this nature because when plotted on a frequency basis they have all the same shaped absorption curve (DARTNALL, 1952) and the same photosensitivity (DARTNALL, 1968), The proportion of light incident on the retina that is absorbed by the visual pigment depends chiefiy on the optical density of the visual pigment present. Also, as the optical density of the pigment increases, so its absorption spectrum becomes broader. In these calculations the reasonable figure of 0.4 fur the optical density of visual pigment in the fishes’ eye has been chosen
Visual Pigments and Visual Range Underwater
1007
(see DENTON and NICOL, 1964). The A,_ of rhodopsins extracted from marine fishes varies from 468 nm in a deep sea fish (DARTNALLand LYTHGOE,1965) to 528 nm, in some mackerels (MUNZ, 1964). The spectral absorption of the pre-retinal media varies widely from fish to fish and, in general, shallow water fishes have rather yellow corneas or lenses, whilst in those living in deep water they are very clear (DENTON, 1956). In fact there are no data for the absorption of the pre-retinal media in fishes suitable for a quantitative approach such as this and the exact values are not likely to be very significant. STILES'data for the human + , .
9
.
j,l(darker prey:
A,,
OF
i
VlsUAL
(liohl;r grw)
PIGMENT (nm)
FIG. 8. The horizontal range at which four grey targets of difforent re%ctances would be visible in shallow water when rhodopsins of di&rent hmox are used. These curves have been calculated for photopic conditions where contrasts of 0.02 (log 0.02 = -1.7) can be detected, and for scotopic conditions where a contrast of 02 (log 02 = -@ 7) might be detected. A rhodopsin of h,.x 520 nm would give the greatest sensitivity to the water background spacelight (see Fig. 10). These data were calculated from the values measured on 25th August, 1967.
J. N. LYTHGOE
1008
(STILES, 1967) has consequently been adopted because this absorption curve is similar to that found in some coastal water fishes (DENTON, 1956). The calculations of visC~ were made for Rhodopsins of Amax= 17500 wave numbers (571 nm), 18500 (541 MI), 19500 (513 nm), 20500 (488 run), 21500 (465 run), and when r = 1 m, 5 m, 10 m, 20 m and 40 m. The calculations were made for target reflectances varying from white through grey to black. The results of these calculations are shown in Figs. 8 and 9 and it is evident that the visual pigment h,,, does influence the range at which grey targets can be seen through the water. eye
.2
.4 TARGET
.6
.6
1.0
REFLECTANCE
FIG. 9. The horizontal range at which grey targeta of various reflectances can be seen in shallow water when rhodopsins of hmlx 541 run and 488 run are used. The limit of contrast perception threshold is here taken to be @2-a reasonable value for scotopic vision.
DISCUSSION The main intention in making the calculations outlined earlier was to demonstrate that the spectral absorption of the visual pigment contained in the eye can Sect the perceived contrast of a grey object against the water background and hence the range at which the object can just be seen through the water (Figs. 8 and 9). The calculations are sufficiently accurate to show quantitatively what advantages in visual range can be expected under some precisely defined conditions. The calculations are based on the way that the apparent spectral radiances of grey targets change as the visual range increases (Fig. 1). For close targets in shallow water the spectral distribution curve of the target light is considerably flatter than that for the water background spacelight. As the range of the target increases, its apparent spectral radiance approaches that of the water background spacelight, until finally the eye is unable to distinguish light from the two sources and the object becomes invisible. From Fig. 1 it is evident from the flatness of the curves for close targets that the amount of light from the target that would be absorbed by a visual pigment is virtually independent of the pigment h,,,. This is not true for the background spacelight where the visual pigment whose h,,, corresponds with the wavelength of maximum water background radiance will absorb more quanta than one whose AmoX is offset from that wavelength. When the target is somewhat brighter than the water background an “offset” visual pigment will have the effect of reducing the perceived brightness of the water background relative to that of the target which will then stand out in increased contrast against the water background. On the other hand when the target is darker than the water background a reduction in the perceived brightness of the water background relative to the target will reduce the
Visual Pigments and Visual Range Underwater
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contrast between the target and its background. Thus for close targets in shallow water the pigment that is most suitable for distinguishing targets brighter than the water back-
ground is precisely that least suitable for seeing dark objects. The situation is quite different for large targets whose high inherent contrast against the water background allows them to be seen at greater ranges. This is because the relative spectral radiance of the water background is at a maximum at approximately those wavelengths where the beam attenuation coefficient of light passing through the water is at a minimum. But the apparent spectral contrast between target and background falls most rapidly where the beam attenuation coefficient is high, and most slowly at about the wavelength of maximum spacelight radiance. The result is that, at the longer sighting ranges, the rate at which the spectral contrast falls becomes more important than the inherent spectral contrast. Thus for distant objects, be they dark or bright, low contrasts will be best perceived by eyes that contain a visual pigment with &,,,, corresponding to the wavelength of maximum background radiance. One very important factor that influences the eye’s ability to perceive low contrasts is the angle subtended at the eye by the target field. Once this angle falls below some critical value the contrast perception threshold increases, with the result that the visible range of small objects is less than for large ones of similar brightness. Because it is the range between the object and the eye that determines whether or not an offset visual pigment will improve visual range, practically all very small objects in shallow water will be best seen by an eye possessing an offset visual pigment. As the depth increases the effect of visual pigment &,_ on contrast perception gradually decreases until at abyssal depths no such advantage exists (LYTHGOE,1966). Furthermore, as the natural illumination falls in intensity-either because of increased depth or because of the onset of night-the ability of the eye to detect small increments in brightness falls. Anything that will tend to reduce the sensitivity of the eye (such as the possession of an offset visual pigment (Fig. 10)) will therefore tend to reduce its ability to detect contrasts and at very low intensities the need for maximum sensitivity might well be of overriding importance. Although the hypothesis that the possession of an offset visual pigment might improve the range of vision underwater was originally proposed to explain why the visual pigments extracted from fishes would not always confer the maximum sensitivity, it is still not
500 A max OF VISUAL
FIG. 10. The relative
550nm PIGMENT
number of quanta absorbed from the horizontal background spacelight when rhodopsins of different Amax,but all of optical density O-4, are used.
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J. N. LYTHGOE
possible to explain the distribution of visual pigments. Furthermore, there is almost total ignorance about the precise visual tasks the fish has to perform, and knowledge of these is necessary before any analysis of visual adaptation can be undertaken. There are as yet no data about the cone pigments in any marine fish and thus present analyses should properly be confmed to visual problems at night or in deep water. Even then, where two scotopic pigments are present, it is not known in fishes if they occur mixed or separate. On the other hand, certain visual tasks will be better performed with some visual pigments than with others and an understanding of these advantages may ultimately lead to a general understanding of the functional significance of visual pigments in ecology. At present visual pigments can be crudely divided into two categories. (1) Visual pigments whose absorption maximum corresponds with the transmission maximum of the water. These pigments will give greater sensitivity at depth (although an increase in optical density of pigment in the retina would serve as well, or better); and some improvement in sensitivity in shallow waters at night. In good light the range at which large objects, which present a high inherent contrast against the water background can be seen, will be increased. (2) Visual pigments whose absorption maximum is offset from the transmission maximum of the water will give an improved visual range for close objects, especially when the objects are small or are only slightly brighter than the water background. This improvement in visual range is reduced as the depth increases. The present work agrees with the earlier indications (LYTHGOE,1966) that for Mediterranean waters improved contrast perceptions results when pigments offset to longer wavelengths are used. The underwater measurements have not been made in other water types, but the earlier work indicated that in British Coastal and Estuaries waters it is the visual pigments offset to shorter wavelengths that will yield the improved perception of contrast for bright objects. Acknowledgements-No project of this kind could have been completed without the active help from many people. I particularly thank Mr. A. H. CHURCHand Mr. C. V. CARPERfor their help in constructing the instrument; and Dr. H. J. A. DARTNALL,Dr. C. C. HEMMINGS,Dr. J. D. MORELANDand Dr. PRWILLA SILVERfor their helpful discussion and advice throughout the project. In Malta Mr. J. J. BARBARAof the Dept. of Fisheries and Professor H. MICCALLEFof the Royal University of Malta provided many valuable facilities. The compressed air used in the diving was provided by Commander GRATTON and his team at the Mediterranean Fleet Diving Centre and I would like to thank them for this essential help. Finally GILLIAN LYTHG~Eskilfully and patiently undertook the job of diving tender and underwater assistant. Everyone who has tried to carry out experiments underwater will know how important this can be.
REFERENCES BAYLIS, L. E., LYTHGOE,R. J. and TANSLEY,K. (1936). Some new forms of visual purple found in sea fishes with a note of the visual cells of origin. Proc. R. Sot., B 816, 95-l 13. CLARKE,G. L. (1936). On the depth at which fishes can see. Ecology 17,452-456. DARTNALL,H. J. A. (1952). Visual pigment 467, a photosensitive pigment present in Tenth retinae. J. Physiol. 116, 257-289. DARTNALL,H. J. A. (1968). The photosensitivities of visual pigments in the presence of hydroxylamine. Vision Res. 8, 339-358. DARTNALL,H. J. A. and LYTHGOE,J. N. (1965). The spectral clustering of visual pigments. Vision Res. 5, 81-100. DENTON,E. J. (1956). Recherches sur I’absorption de la lumitre par le cristallin des Poissons. Bull. Inst. Oceanogr. Monaco No. 1071, pp. I-IO. DENTON,E. J. and NICOL, J. A. C. (1964). The choroidal tapeta of some cartilagenous fishes (Chondrichthyes). J. mar. bioi. Assoc. 44, 219-258.
Visual Pigments and Visual Range Underwater DENTON,E. J. and
WARREN, F.
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J. (1957). The photosensitive pifpnents in the retinae of deep sea fish.
J. mar. biol. Assoc. 36, 651-662.
DUNTLEY,S. Q. (1962). Underwater visibility. In 7&e Sea, Vol. I (edited by M. N. HILL). Interscience New York and London. LE Gm, Y. (1939). La penetration de la hnni&e dans la mer. Ann&es de I’Zmt. ~~o~u~~ 19, 393-436. LYTHGOE,J. N. (1966). Visual pigments and underwater vision. In Lighr OS an Ecological Factor, pp. 375-391 (edited by R. BmBmoa, G. C. EVANSand 0. RACKHAM).Blackwell, Oxford. MUNZ, F. W. (1957). Photosensitive pigments from retinas of deep-sea fishes. Science, N.Y. 125, 1142-l 143. MUNZ, F, W. (1958a). Photosensitive pigments from the retinae of certain deep sea fishes. J. Pbysioi. 140,220-225. MUMZ,F. W. (1958b). The photosensitive retinal pigments of fishes from relatively turbid coastal waters. J. gen. Physiol. 42,445-459. MUNZ, F. W. (1964). The visual pigments of epipelagic and rocky shore iishea. Vision Rex 4, 441654. TYLER,J. E. (1958). Natural water as a monochromater. Limnol. OceuBogr. 4, 102-10.5. Tne~, J. E. (1965). In situ spectroscopy in ocean and lake waters. J. opr. Sot. Anr. 55, 800-805.
WYSZECKI,G. and !&TLEs,W. S. (1967). Coior Scicncc, p. 216, John Wiley, New York, London, Sydney. Abstract-In shallow water the spectral radiance of a gmy object differs from that of the water background spacelight. The spectral absorbance of the visual pigments present in the eye will therefore affect the perceived contrast between an object and its water background, and hence the range at which the object can be seen underwater. A diver-operated instrument is described that allows the spectral contrast between a grey target and its water background to be measured. The data so obtained show that in Medi&rmnean waters those visual pigments with a hmsx corresponding to the wavelength of maximum light axon through the water are be& suited for detectin8 large very dark or very bright objects. Rut “offset” visual pigments are more suitable for dete&ing small grey objects in shallow water. R&ur&-En eau peu profonde, la radiance spectrale dun objet gris ditI&e de celle du fond huninenx de I’eau. L’absorption spectrale des pigments visuels de l’oeil affectera done le contra&e Peru entre un objet et b fond, et par co&quent la limite de visibilite sous l’eau. Ondecrituni ant manipult par tm plongeur et qui mesure le contra&e spectral entre cible grise et fond. Les r&hats obtenus en M&l&ran&e montrent que les pigments visuels de h,= correspondant a la longueu d’onde de transparence maximum de l’eau sent Its plus favorables pour d&e&r des tpamis objets t&s sombres ou t&s claim, mais que des pigments visuels &cart& de cette condition conviennent mieux pour d&c&r de petits objets gris en eau peu profonde. In Aachem Wasser unterscheidet sicfi die spektrale ~~~h~ eines grauen Objektes von der des ~~~~~~ des Wasaem. Die spektrale Absorption der Sehstoffc im Auge wird deshalb den wahrsenommenen Kontrast xwis&n einem Objekt und dessert Wasserhintergrud beeinflussen und somit die Entfermrng auf die das Objekt unter Wasser erkamn wird. Es wird ein taucherbetriebenes Instrument beachriehen, mit dem der spektraIe Kontrast zwischen einem grauen Gegemtand und seinem Wasserhintergnmd gemessen werden kann. Die damit erhahenen MeDwerte z&en, da8 in Mitts die Sebstoffe mit einem hmaX, das der We~e~~ m ~h~ion im Wasser entapricht, f& die Wahrnehmung sehr dnnkler oder sehr heller Objekte am be&en geeignet sind. Jedoch sind Sehstoffe mit einer L‘offset”-Absorption ti g&net urn kleine graue Objekte in flachem Wasser N erkennen. Pe3mMe -
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