The pupillary response of cephalopods
1 Applied Vision Research Centre, The Henry Wellcome Laboratories for Vision
Sciences, Department of Optometry and Visual Science, City University,
Northampton Square, London EC1V 0HB, UK
2 School of Biological Sciences, University of Plymouth, Drake Circus,
Plymouth PL4 8AA, UK
3 Anatomisches Institut, Universität Tübingen,
Österbergstrasse 3, 72074 Tübingen, Germany
* Author for correspondence (e-mail: r.h.douglas{at}city.ac.uk)
Accepted 15 November 2004
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Summary |
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Key words: pupil, eye, cephalopod, squid, octopus, Eledone cirrhosa, cuttlefish, Sepia officinalis
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Introduction |
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Although it has been known for over 100 years that the pupils of most
cephalopods are able to change size on illumination
(Beer, 1897;
Bateson, 1890
;
Magnus, 1902
;
Weel and Thore, 1936
), the
detailed dynamics of the response are virtually undescribed. Perhaps
surprisingly, most is known about the pupil of the `primitive' pinhole eye of
Nautilus pompilius, whose area decreases on illumination from 4
mm2 to 0.2 mm2 over a period of 90 s
(Hurley et al., 1978
). The
only quantitative investigation of the pupil response in coleoid cephalopods
examined the response of Sepia officinalis and suggested pupil
constriction occurred in around 5 s and dilation in about 30 s
(Muntz, 1977
). Although faster
than Nautilus, this is still considerably slower than many other
animals, and the speed of the pupil response in coleoid cephalopods is
therefore generally quoted as being much less rapid than that of, for example,
mammals (e.g. Hurley et al.,
1978
; Messenger,
1981
). However, the temporal resolution of this earlier work was
poor as digital video technology was not available. Here we provide the first
detailed description of the timecourse of light-evoked pupillary constriction
for two species of coleoid cephalopod, Sepia officinalis (a
cuttlefish) and Eledone cirrhosa (an octopus), and show that the
response, especially in Sepia officinalis, is not only much faster
than hitherto reported but is in fact among the fastest in the animal
kingdom.
We also describe the dependence of the degree of pupillary constriction in both Sepia and Eledone on the level of irradiance, and show considerable individual variation in sensitivity. Pupil dilation following the cessation of a light stimulus is also shown to be very variable. Such variation may be the result of extensive light-independent changes in pupil diameter within an individual over short periods of time, which are especially apparent in lower levels of illumination.
Simple observation suggests that the two pupils of individual coleoid
cephalopods respond independently to light
(Magnus, 1902;
Weel and Thore, 1936
). This
lack of a consensual response in cephalopods is described quantitatively
here.
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Materials and methods |
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Direct pupil response to illumination
Five adult Sepia officinalis L. and three adult Eledone
cirrhosa Lamarck were removed from their home tanks during the light
phase of their light/dark cycle and placed in darkness in a jar with a
perforated lid within a shallow aquarium. Their pupils were filmed under
infrared illumination for 11-50 min using a camera positioned perpendicular to
the plane of the eye. Animals were subjected to a series of diffuse overhead
white light exposures from a Kodak slide projector and sufficient time was
allowed between exposures to allow redilation of the pupil. The light
intensity, which was adjusted by neutral density filters, was measured at the
end of each experiment where the animal's eye had been. As each animal was in
a slightly different position relative to the light source, the precise
intensities that each animal was exposed to varied. Pupil area was determined
by digitising individual video frames and analysing with Scion Image software.
To compensate for changes in image size due to refocusing of the camera
between light exposures, pupil area is expressed as a percentage of the
dark-adapted pupil area immediately prior to a given light stimulus.
Consensual pupil response
Both eyes of a single adult Sepia officinalis and an adult
Eledone cirrhosa were filmed separately in darkness under infrared
illumination and following a series of white light exposures (10 µW
cm-) from a 1500 fibre optic light source (Schott; Mainz, Germany),
to the right eye only. The pupil area of each eye was compared before and 2-5
s after stimulation of the right eye.
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Results |
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In Eledone, full constriction took just over 1 s, while the
response of Sepia was faster (Fig.
1). Since pupil closure was initially very rapid, before
approaching maximal constriction more slowly, a more accurate estimate of the
speed of contraction is given by the time taken to attain half the final pupil
area (t50; Douglas et
al., 1998). In Eledone this occurred on average after
0.65 s, while the equivalent time in Sepia was only 0.32 s. The
degree of constriction was related to the intensity of the light in both
species, although different animals varied greatly in their sensitivity
(Fig. 2).
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Although the pupil always responded to illumination, it also showed light-independent movements. This was especially apparent for Sepia in low levels of illumination, when pupil diameter varied extensively despite no change in the ambient illumination. Possibly as a consequence of this, the rate of pupil dilation following cessation of the light stimulus was also very variable. Usually it was immediate, the pupil opening within 1 s in Sepia, while at other times it was considerably delayed (Fig. 3).
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Absence of a consensual response
When the right eye alone was illuminated there was never any contraction of
the left pupil in either Eledone or Sepia
(Fig. 4). Thus, these coleoid
cephalopods do not possess a consensual pupil response.
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Discussion |
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Pupil dilation
Previous work (Muntz, 1977)
suggested the pupil of Sepia officinalis takes around 30 s to dilate
following a decrease in illumination. Here we show that full dilation can in
fact be achieved within 1 s (Fig.
3). However, this can vary significantly, most probably due to the
confounding effects of non-light-related factors on pupil size (see below),
possibly explaining the large difference between our work and that of Muntz
(1977
).
In most vertebrates pupil constriction is caused by a sphincter muscle
encircling the pupillary margin, while dilation is caused by radial fibres
forming a dilator muscle. Although it is probable that cephalopds also possess
both of these muscles (Magnus,
1902), the presence of a dilator has yet to be clearly
demonstrated anatomically (Froesch,
1973
). The fast rate of dilation noted here, however, is strongly
suggestive of the presence of such a muscle.
Lack of a consensual pupillary light response in coleoid cephalopods
In many animals illumination of one eye causes constriction in the other.
Mammals generally have such a consensual pupil response
(Lowenfeld, 1993), as do some
amphibia (von Campenhausen,
1963
), teleost fish (Douglas et
al., 1998
) and most rays (von
Studnitz, 1933
). However, in other teleosts
(Nilsson, 1980
) and amphibia
(Henning et al., 1991
), as
well as in most sharks (Kuchnow,
1971
), reptiles (Werner,
1972
) and birds (Schaeffel and
Wagner, 1992
), the pupils act independently. Among cephalopods the
situation appears equally varied. While the pin-hole eyes of Nautilus
display a consensual response (Hurley et
al., 1978
), here (Fig.
4) we confirm previous observations
(Beer, 1897
;
Magnus, 1902
;
Weel and Thore, 1936
;
Hanlon and Messenger, 1988
)
suggesting that the pupils of coleoid cephalopods respond independently to
light.
Cephalopods have laterally placed eyes and thus see much of their world
monocularly. Consequently, their two eyes will often see quite different
things. Interestingly, Octopus vulgaris often uses only one eye when
viewing objects (Muntz, 1963)
and, like many vertebrates, especially birds, display a degree of lateral
asymmetry in eye use (Byrne et al.,
2002
). If the pupil responds not only to the overall level of
illumination but also to other, more specific, stimuli, as will be suggested
below, it seems reasonable that the pupils of the two eyes should behave
independently.
The function of light-induced pupil constriction in cephalopods
The most obvious function of changes in pupil size is to regulate the light
flux incident on the retina. However, even a pupil constricted to 1% of its
dilated area, only decreases retinal illuminance by 2 log units, which is
significantly less than the total range of ambient illumination that a shallow
living cephalopod will experience throughout a day, indicating that, as in
other species, additional mechanisms of light adaptation are important.
Pupillary constriction will also enhance image quality. Light traversing
most lenses at different points is focussed at varying distances behind it,
resulting in a degraded image. Constricting the pupil will restrict the
passage of light to a smaller portion of the lens, thus decreasing the amount
of such longitudinal spherical aberration. In teleost fish, most of which have
a fixed pupil, spherical aberration is minimised by a refractive index
gradient within the lens (Sivak,
1990). If the lenses of cephalopods have significantly more
spherical aberration than those of fish, it may offer an explanation for why
the former have a variable pupil and the latter generally do not (Sivak,
1982
,
1991
). Although some studies
do suggest that the lenses of cephalopods may suffer from more spherical
aberration than those of fish (Sivak,
1982
,
1991
;
Sivak et al., 1994
), others
indicate this is not always the case
(Jagger and Sands, 1999
).
We have previously noted that among teleosts, pupil mobility is largely
restricted to species that attempt to blend in with the substrate (Douglas et
al., 1998,
2002
). In such animals a large
circular dark pupil would be very visible, and a contractile iris is most
likely part of the animal's camouflage mechanisms. Pupillary constriction in
cephalopods, many of whom have well developed camouflage strategies, may, at
least in part, serve a similar function
(Hanlon and Messenger,
1988
).
Light-independent pupillary movements
Although the degree of pupil constriction is related to the intensity of
the light in both Sepia and Eledone, different animals vary
greatly in their sensitivity (Fig.
2). Several previous studies
(Beer, 1897;
Magnus, 1902
;
Weel and Thore, 1936
) have
noted that different animals within the same tank, and therefore exposed to
very similar light levels, can have pupils constricted to varying degrees.
Thus, factors other than the overall illumination clearly influence pupil
size. Not surprisingly, therefore, we often observed extensive pupil
movements, especially in low light levels, despite the lack of any change in
light level.
In several species the pupil is known to reflect the `emotions' of an
individual (Lowenfield, 1993). In humans, for example, the pupil often dilates
when confronted by an attractive member of the opposite sex. Similarly,
chickens give a much larger response to the presentation of a red stimulus
(possibly indicating blood) than they do to a simple change in light level
(Barbur et al., 2002). The
pupil of cephalopods also dilates when they are `aroused' during fighting,
mating or viewing food (Beer,
1897
; Bateson,
1890
; Packard and Sanders,
1971
; Muntz, 1977
;
Wells, 1966
,
1978
;
Hurley et al., 1978
;
Messenger, 1981
).
A dilated pupil in relatively bright light may serve a number of functions.
It could, for example, be an intraspecific signal during courtship displays
(Wells, 1966;
Packard, 1972
). It might also
be one of a series of deimatic displays that help `create the illusion of
larger size' when facing a potential predator
(Wells, 1966
; Hanlon and
Messenger, 1988
,
1996
;
Messenger, 2001
). A dilated
pupil may also aid in the judgement of distances, something cephalopods are
able to do with accuracy (Wells,
1966
; Muntz and Gwyther,
1988
).
Many animals with laterally placed eyes use monocular cues, such as the
accommodative state of their eye, to determine their separation from an object
(Collett and Harkness, 1982).
However eyes with a single small aperture have a large depth of field,
minimising the need for accommodation. Consequently animals with constricted
pupils cannot use the refractive state of the eye as a cue to distance. Not
surprisingly therefore, cephalopods, like chameleons (a species known to use
accommodation as cue to distance;
Harkness, 1977
) but unlike
most animals, maintain a wide pupil when viewing close objects
(Wells, 1966
), making
accommodation a more useful cue to distance.
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Acknowledgments |
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References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Barbur, J. L., Prescott, N. B., Douglas, R. H., Jarvis, J. R. and Wathes, C. M. (2002). A comparative study of stimulus-specific pupil responses in the domestic fowl (Gallus gallus domesticus) and the human. Vision Res. 42,249 -255.[CrossRef][Medline]
Bateson, W. (1890). Contractility of the iris in fishes and cephalopods. J. Mar. Biol. Assn. UK 1, 215-216.
Beer, T. (1897). Die Accommodation des Cephalopodenauges. Pflug. Arch. Ges. Phys. 67,541 -586.
Byrne, R. A., Kuba, M. and Griebel, U. (2002). Lateral asymmetry of eye use in Octopus vulgaris. Anim. Behav. 64,461 -468.[CrossRef]
Collett, T. S. and Harkness, L. (1982). Distance vision in animals. In Advances in the Analysis of Visual Behaviour (ed. D. J. Ingle, M. Goodale and J. W. Mansfield), pp.111 -176. Cambridge: MIT Press.
Douglas, R. H., Harper, R. D. and Case, J. F. (1998). The pupil response of a teleost fish, Porichthys notatus: description and comparison to other species. Vision Res. 38,2697 -2710.[CrossRef][Medline]
Douglas, R. H., Collin, S. P. and Corrigan, J. (2002). The eyes of suckermouth catfish (Loricariidae, subfamily Hypostomus): pupil response, lenticular longitudinal spherical aberration and retinal topography. J. Exp. Biol. 205,3425 -3433.[Medline]
Froesch, D. (1973). On the fine structure of the Octopus iris. Z. Zellforsch. 145,119 -129.[CrossRef][Medline]
Gilbert, P. W., Sivak, J. G. and Pelham, R. E. (1981). Rapid pupil change in selachians. Can. J. Zool. 59,560 -564.
Hanlon, R. T. and Messenger, J. B. (1988). Adaptive colouration in young cuttlefish (Sepia officinalis L.): The morphology and development of body patterns and their relation to behaviour. Phil. Trans. R. Soc. B 320,437 -487.
Hanlon, R. T. and Messenger, J. B. (1996). Cephalopod Behaviour. Cambridge: Cambridge University Press.
Harkness, L. (1977). Chameleons use accommodation cues to judge distance. Nature 267,346 -349.[Medline]
Henning, J., Henning, P. A. and Himstedt, W. (1991). Peripheral and central contribution to the pupillary reflex control in amphibians: pupillographic and theoretical considerations. Biol. Cybern. 64,511 -518.
Hurley, A. C., Lange, G. D., and Hartline, P. H. (1978). The adjustable `pinhole' eye of Nautilus. J. Exp. Zool. 205,37 -44.
Jagger, W. S. and Sands, P. J. (1999). A wide-angle gradient index optical model of the crystalline lens and eye of the octopus. Vision Res. 39,2841 -2852.[CrossRef][Medline]
Kuchnow, K. P. (1971). The elasmobranch pupillary response. Vision Res. 11,1395 -1406.[CrossRef][Medline]
Land, M. F. (1981). Optics and vision in invertebrates. In Handbook of Sensory Physiology VII/6B (ed. H. Autrum), pp. 471-592. Berlin: Springer.
Land, M. F. and Nilsson, D.-E. (2002). Animal Eyes. Oxford: Oxford University Press.
Lowenfeld, I. E. (1993). The Pupil. Detroit: Wayne State University Press.
Magnus, R. (1902). Die Pupillarreaction der Octopoden. Plug. Arch. Ges. Phys. 92,623 -643.
Messenger, J. B. (1981). Comparative physiology of vision in molluscs. In Handbook of Sensory Physiology VII/6C (ed. H. Autrum), pp.93 -200. Berlin: Springer Verlag.
Messenger, J. B. (2001). Cephalopod chromatophores: neurobiology and natural history. Biol. Rev. 76,473 -528.[Medline]
Muntz, W. R. A. (1963). Intraocular transfer and the function of the optic lobes in octopus. Q. J. Exp. Psychol. 15,116 -124.
Muntz, W. R. A. (1977). Pupillary response of cephalopods. Symp. Zool. Soc. Lond. 38,277 -285.
Muntz, W. R. A. and Gwyther, J. (1988). Visual discrimination of distance by octopuses. J. Exp. Biol. 140,345 -353.
Nilsson, S. (1980). Symapathetic nervous control of the iris sphincter of the Atlantic cod, Gadus morhua. J. Comp. Physiol. 138A,149 -155.[CrossRef]
Packard, A. (1972). Cephalopods and fish: the limits of convergence. Biol. Rev. 47,241 -307.
Packard, A. and Sanders, G. D. (1971). Body patterns of Octopus vulgaris and the maturation of the response to disturbance. Anim. Behav. 19,780 -790.
Schaeffel, F. and Wagner, H. (1992). Barn owls have symmetrical accommodation in both eyes, but independent pupillary responses to light. Vision Res. 32,1149 -1155.[CrossRef][Medline]
Sivak, J. G. (1982). Optical properties of a cephalopod eye (the short finned squid, Illex illecebrosus). J. Comp. Physiol. 147A,323 -327.
Sivak, J. G. (1990). Optical variability of the fish lens. In The Visual System of Fish (ed. R. H. Douglas and M. B. A. Djamgoz), pp. 63-80. London: Chapman and Hall.
Sivak, J. G. (1991). Shape and focal properties of the cephalopod ocular lens. Rev. Can. Zool. 69,2501 -2506.
Sivak, J. G., West, J. A. and Campbell, M. C. (1994). Growth and optical development of the ocular lens of the squid (Sepioteuthis lessoniana). Vision Res. 34,2177 -2187.[CrossRef][Medline]
von Campenhausen, C. (1963). Quantitative Beziehungen zwischen Lichtreiz und Kontraktion des Musculus sphincter pupillae vom Scheibenzüngler (Discoglossus pictus). Kybernetik 1,249 -267.[Medline]
von Studnitz, G. (1933). Studien zur vergleichenden Physiologie der Iris III. Selachier. Z. Vergl. Physiol. 19,619 -631.[CrossRef]
Weel, P. B. V. and Thore, S. (1936). Über die Pupillarreaktion von Octopus vulgaris. Z. Vergl. Physiol. 23,26 -33.
Wells, M. J. (1966). Cephalopod sense organs. In Physiology of Mollusca (ed. K. M. Wilbur and C. M. Young), pp. 523-545. NewYork: Academic Press.
Wells, M. J. (1978). Octopus; Physiology and Behaviour of an Advanced Invertebrate. London: Chapman and Hall.
Werner, D. (1972). Beobachtungen an Ptyodactylus hasselquistii guttatus (Geckonidae). Verh. Naturfors. Ges. Basel 82,54 -87.