Anatomical and Behavioral studies on Vision in Nautilus and Octopus

6 Pages·1991·3.1 MB·English

by  W R A Muntz

Anatomical and behavioural studies on vision
in Nautilus and Octopus
W. R. A. Muntz
Department of Ecology and Evolutionary Biology, Monash University, Clayton, Victoria 3168, Australia
Abstract. Nautilus isacephalopodthat isprimitive in many respects, and isoftenconsidered to bea "living fossil". Theeye ofNautilus isapparently
aprimitivefeature, actingasapin-holecameraandlackingany lensorotherdioptricapparatus. Incontrast, inOctopusandmostothercoleoidcephalopods,
there is a well formed spherical lens. The basic structure ofthe retina is similar in the two animals, but there are alsoa number ofimportant differences:
the microvilli ofthe receptorsofNautilusdo not forma regularrectilineararray astheydo in Octopus; the microvilli from neighbouring receptorsoverlap,
which does notoccur in Octopus: the supporting cells have a different structure; the nuclei ofthe supporting cells and receptorcells are distributed either
sideofthebasementmembrane inOctopus, butnot inNautilus; ciliaarepresent inthe retinaofNautilusbut not Octopus; andthemyeloidbodiesaremuch
more developed in Nautilus.
Bothbehavioural experimentsandcalculation showthat, asexpected onanatomical grounds, visual acuity and sensitivity are muchbetter in Octopus
than Nautilus. Reasons for the limitations in the visual capabilities ofthe two animals are discussed.
Nautilus is the last surviving genus of a group that about2.5 timestheir radius (Matthiessen's ratio) and arewell
arose inthe Triassic, and hasapparently changed little since corrected for spherical aberration (Sivak, 1982; Sroczynski
Cretaceous times, at least as far as we can judge from the and Muntz, 1985). The overall size of the eyes of the two
shell. The animal shows many apparently primitive features, animals is, however, similar, and bothanimals have contrac-
such as the lack of an ink sac or chromatophores, the ex- tile pupils that are elongated in the horizontal direction
ternal shell, the funnel formedoftwooverlapping lobes, and (Muntz, 1977; Hurley etal., 1978). Figure 1 showsthe general
the simplepin-holecameraeye lackingany lensorotherdiop- appearance of the eyes ofNautiluspompilius Linnaeus and
tric apparatus (e.g. Morton, 1967). The ancestry ofthe genus Octopus vulgaris Lamarck.
hasbeendiscussedby, amongothers, TeichertandMatsumoto Descriptions ofthe retinal anatomy ofNautilus can be
(1987), who concluded that it can truly be called a "living found in Barber and Wright (1969), Muntz and Raj (1984),
fossil". and Muntz and Wentworth (1987); and ofOctopus in Young
The first octopods, on the other hand, are found in (1962a, 1971) and Yamamotoetal. (1965). These papers also
the Upper Cretaceous (Donovan, 1977), and the group must give referencestoearlierwork. Followingconvention, inthis
be counted among the most developed invertebrates in ex- paper the segments ofthe receptors facing the light, which
istence. Theoctopuseye, which resemblesthatofmostother contain the photopigment, will be referredtoas the distal or
coleoidcephalopods, has incontrast toNautilus avery well- outer segments, and the nuclear region as the proximal or
developed lens and superficially looks remarkably similar to inner segment.
theeyesofvertebrates. Thepresentpapercomparesthestruc- The basic elements ofthe retina in both Octopus and
ture and function of the eyes of these two very different Nautilus arethe receptorcells, withdistal segments consisting
cephalopods. ofa central core from which the microvilli (which contain
thevisualpigment) radiateoutwards, and the supporting cells
STRUCTURE OF THE EYE IN NAUTILUS with their processes lying between the receptor cell outer
AND OCTOPUS segments (Figs. 2, 3). The packing of the receptor cells is
roughly similar in the two species. Thus, there are about
The most obvious difference between the eyes of 20,000receptorcells mm-2 inN. pompilius, varying littleover
Nautilus and Octopus is the complete lack of any dioptric the retina (Muntz and Raj, 1984), and between 18,000 and
apparatus in the former genus. The pupil in Nautilus opens 55,000 mm-2 in O. vulgaris, depending on retinal position
directly tothe sea, andtheeye mustact as apin-holecamera. (Young, 1971). Althoughbasically similar, there are however
The eyes of octopuses in contrast have well developed also a number of important differences between the two
spherical lenses, which, as inmost fishes, have focal lengths species, which can be summarised as follows.
American Malacological Bulletin, Vol. 9(1) (1991):69-74
69
70 AMER. MALAC. BULL. 9(1) (1991)
(i) Transverse sections through the outer segments of above eachother (Muntz and Wentworth, 1987). In Octopus
the retinal receptors ofNautilus show that there are usually and the other coleoid cephalopods, the myeloid bodies are
five or six (occasionally fouror seven) bundles ofmicrovilli reduced to a few membranous strands.
running out from each receptor body to the bodies of It is interesting that some of the characteristics by
neighbouring receptors. The receptors thus form a roughly which theNautilus retinadiffers from thatofadultoctopuses
hexagonal array (Fig. 2a). The microvilli from neighbouring alsohavebeen foundduringthedevelopmentoftheembryos
receptors within a given bundle often interdigitate, although of coleoid cephalopods. Thus in the cuttlefish Sepiella
the extent ofthis interdigitation is not clear. The processes japonica Sasaki, embryos haveciliaonboth receptorandsup-
of the supporting cells run out in groups between these porting cells, the nuclei of both the receptor cells and the
bundles of microvilli. supporting cells lie distal to the basement membrane, and
In contrast in Octopus the receptor outer segments the supporting cells send long microvillous processes out
forma rectilineararray, withthe microvilli orientedvertically among the whole length of the receptor outer segments
or horizontally with respect to gravity (Fig. 3a). The (Yamamoto, 1985). Work in progress shows a similar situa-
microvilli of each receptor remain strictly segregated from tion in the embryos of the Australian octopuses Octopus
those ofthe neighbouring receptors, with no interdigitation. pallidus HoyleandO. australis Hoyle(WentworthandMuntz,
(ii) The structure ofthe supporting cells is quite dif- unpub. data).
ferent inthetwoanimals. InNautiluseachcell has a number
offine microvillous processes which project out betweenthe
receptorouter segments in groups, whereas in Octopuseach BEHAVIOURAL STUDIES
supporting cell has a single process, which is much larger
and contains screening pigment. Inthe formeranimalthecell Todate, nostudiesofvisionhavebeencarriedoutwith
nuclei ofboththe receptors andthe supportingcells liedistal Nautilus using any form of learnt behaviour, and it is not
to the basement membrane, whereas in Octopus the support- knownhow fartheanimalsarecapableoflearning. However,
ingcell nuclei liedistal andthe receptorcell nuclei proximal Nautilus shows two well developed forms of innate visual
to the basement membrane. behaviour, thepositivephototacticresponseandtheoptomotor
(iii) InNautilusthe supporting cells havecilia, as well response, which have been used to determine the animals'
as the microvillousprocessesthatextendbetween the recep- visual acuity, andalsotheirabsolute and spectral sensitivities
tors. It is not certain whetherthe receptorcells have cilia as (Muntz and Raj, 1984; Muntz, 1986, 1987).
well. Ciliary structures have not been reported in the retina As we shouldexpect forananimal withaneyehaving
of any other adult cephalopod, although the photosensitive the simple optics ofa pin-hole camera, visual performance
organs of many animals have receptors ofciliary origin, or in Nautilus is very poor compared to that of animals with
cilia, presumed not to be photosensitive, intermingled with lens bearing camera eyes. The minimum separable visual
the receptors (Vanfleteren, 1982). acuity, forexample, measuredusingtheoptomotorresponse,
(iv) The inner segments of Nautilus photoreceptors lies between 5.5° and 11.25°, which agrees well with values
have complex myeloid bodies, which often have the ap- calculated on the basis of the gross dimensions of the eye
pearance of a tubular structure, or a series of wavy plates and pupil, and with expectations based on photographing a
(Fig. 2). Ithasbeenarguedthatthisapparentlycomplexstruc- visual test chart using a scale model ofthe eye (Muntz and
ture consistsofa seriesofdimpledplates, stacked in register Raj, 1984). This can be compared with values of about 5'
MUNTZ: VISION IN NAUTILUS AND OCTOPUS 71
Fig.2.DiagramofthestructureoftheretinaofNautilus,asseenintangential Fig.3. Diagramofthestructureofthe retinaOctopus,asseen intangential
(above)andradialsection(below). Thediagramisnottoscale: inparticular (above) and radial section (below), from Young (1962a). Not to scale: in
the horizontal dimensions have been exaggerated compared to the vertical fact the distal segments vary between about 60 /tm and 180 fim in length
dimensionsforclarity. Themeanlengthofthedistalsegmentsisinfactabout depending on retinal position, while the proximal segments are about 90
360fim,andoftheproximalsegments 100^m, andthemeancentretocen- longandtheindividual rhabdomeresabout5 inwidth(Young, 1962a)
tredistancebetweenadjacentreceptors3.5nm: thereislittle variationover (rh., rhabdome; pig., pigment granuleat centreofrhabdome; ret., retinal
theretina(bas.m.,basementmembrane; dist., receptordistalsegmentwith cell;l.m.,limitingmembrane;dist.,distalsegmentofreceptor;bas.m..basal
microvilli radiating from acentral core; pr.s., receptorproximal segment; membrane; pr.s., proximal segmentsofretinal cells; col.f., finedendritic
sup., processes ofsupportingcells; m.. myeloid body: on., optic nerves; collateral ofretina cell; p.l., retinal nerve plexus; eff.. ending ofefferent
n.sup., nucleus of supporting cells; n.ret., nucleus of retinal cell). fibre in retina; ep.. epithelial cell; n.sup., nucleiofsupportingcells; sup.,
processes ofsupporting cells).
obtained with octopuses, various fishes andtwo aquatic mam- calculate the maximum depth at which surface light would
mals (Table 1): even withthemostfavourableestimateof5.5° be visible atall toNautilus. Reasonable estimates forthe first
theperformance levelofNautilus isover60times worsethan two factors are available, and the animals' spectral sensitiv-
for these other aquatic animals. ity was taken to be the same as the absorption spectrum of
By usingthepositivephototacticbehaviourofNautilus its visual pigment (see Muntz, 1987 for details). It appears
it has alsobeen possible todetermine its absolute sensitivity that some daylight should be visible to Nautilus down to
totungsten light (Muntz, 19S7). In itselfthis result isnotpar- 800 m, which is slightly deeper than the maximum depth at
ticularly useful, because the spectral output ofthe tungsten which the animal is found. This is, however, considerably
source used was very different from thatofthelighttowhich less than the maximum depth at which daylight should be
the animal will be exposed in its natural environment. visibletodeepseafishes, whichhasbeencalculatedby Clarke
However, given a knowledge ofthe spectral transmission of and Denton (1962) as over 1000 m. Calculations based on
the water in which the animals live, the spectral quality of the dimensionsoftheNautilus eye also indicate thatNautilus
thedaylight reachingthe surfaceofthe sea, andtheanimals' will be less sensitive, by about 2 log units, than a fish or
own spectral sensitivity, it is possible from these results to cephalopod that has a camera eye with a lens obeying
72 AMER. MALAC. BULL. 9(1) (1991)
Matthiessen's ratio (Muntz and Raj, 1984). ing a smoothbell-shaped spectral sensitivity curve maximal
mm
Finally, the positive phototactic behaviour has also at around 480 and compatible with a single visual pig-
been used to determine spectral sensitivity directly (Muntz, ment (White, 1924).
1986). The sensitivity curve obtained agreed well with the A few behavioural studies have been carried out on
absorption spectrum ofthe extractable visual pigment, which the visual acuity ofoctopuses. Thus Sutherland (1963), us-
was itself well fitted by Dartnall's (1953) visual pigment ing a training situation, obtained an estimate of 17' for
nomogram for an A,-based pigment with its maximum at Octopus vulgaris, andPackard (1969), usingthe same species
467 mm. and the optomotor response, found that in very small
In contrast to Nautilus, octopuses learn visual specimens (<3-22g) acuity improved with size. The most
discriminations very readily, andagreat deal ofinformation recent studies on acuity in octopuses (Muntz and Gwyther,
is now available on their visual capabilities (Wells, 1978; 1988a, 1989) used fully grown animals and a two choice
Messenger, 1981 for reviews). Most of this work has con- learning situation, and the stimuli were gratings ofequally
cerned higher visual functions, such as the ability to spaced black and white stripes oriented vertically, horizon-
discriminate shapes, the mechanisms by which such tally, or obliquely at 45°. The animals were trained to
discriminations are learnt, and the function of the various discriminate these gratings fromeachotherorfromauniform
partsofthecentral nervous system. Comparatively little work gray stimulus, and visual acuity was taken as the separation
hasbeendone onthe animals' more basic visual capabilities, betweenthebarsofthe gratings where performance reached
such as sensitivity or visual acuity, whichare probably more chance levels. The results showedthat the minimum separable
directly related to the optics ofthe eye and the structure and visual acuity ofO. australis and O. pallidus is about 5' (Fig.
functionofthe retina, and whichcanbecomparedtothedata 4). Withgratingsclosetothe animals' threshold, performance
that are available forNautilus. In the case ofsensitivity, for with the vertical gratings was best, and with the horizontal
example, there appear to have been no studies at all carried gratings worst, but the effect was not large.
outoncoleoidcephalopods usinglearning, andonlyone study The ability of Octopus pallidus and O. australis to
involving innate behaviour, in which the spectral sensitivity discriminate distances has alsobeen determinedbehavioural-
of Loligo pealei Lesueur larvae was measured using the ly, using the animals' tendency to attack the nearer of two
positive phototactic response in a manner rather similar to stimuli presented simultaneously (Muntz and Gwyther,
that used withNautilus. The results were also similar show- 1988b). Assuming that the animals are using accommoda-
Table 1. Minimumseparablevisualacuities, inminutesofarc,ofvariousaquaticanimalsmeasuredbehavioural-
ly using gratings. Learnt discriminations were used in all cases exceptNautilus where the optomotor response
was used.
Species Acuity Reference
MAMMALS
Harbour seal 8.3 Schusterman and Balliet, 1970
Phoca vitulina Linnaeus
Stellar Sea Lion 7.1 Schusterman and Balliet, 1970
Eumetopiasjubata (Schreber)
TELEOST FISHES
Convict fish 4.9 Yamanouchi, 1956
Microcanthus strigatus (Cuvier and
Valenciennes)
Minnow 10.8 Brunner, 1934
Phoxinus laevis Linnaeus
Skipjack tuna 5.5 Nakamura, 1968
Katsowomispelamis Linnaeus
Little tuna 7.4 Nakamura, 1968
Euthynnus affinis (Cantor)
Cichlid fish 5.8 Baerends et al., 1960
Aequidensportalegrensis (Hensel)
CEPHALOPODS
Nautilus 330-670 Muntz and Raj, 1984
Nautiluspompilius
Octopus 5.0 Muntz and Gwyther. 1988a
Octopuspallidus
O. australis
MUNTZ: VISION IN NAUTILUS AND OCTOPUS 73
tiontoestimatedistance, which varioustests indicated is the cephalopods. Even though Nautilus vision is poor, never-
most likely mechanism, the animals can detect blurring of theless its visual behavior is precise, inthat inthe optomotor
points on the retinal image comparable in size to a single response they follow the stripes accurately without visible
retinal receptor, and lens displacements of around 10 jiim. lag, and inthephototactic situation ifthedifferencebetween
Finally, trainingexperimentshave shownthat Octopus the stimuli is well above thresholdthe brighter light is chosen
vulgaris candiscriminatethe planeofpolarised light (Moody on every occasion. The eyes are also stabilised with respect
andParriss, 1961), andalsoithasbeenshownthattwospecies to gravity by means ofthe statocysts (Hartline et al., 1979).
ofdecapodlarvaeorientthemselvestothe planeofpolarised These facts suggest that vision is important to the animal.
light (Jander etal., 1968). It is not known whetherNautilus It is not, however, clear what use they make of such poor
has this ability. vision in their normal life. The habitat ofNautilus often has
strongcurrents, andtheoptomotorbehaviourcouldberelated
to holding station under these conditions. It could also be
DISCUSSION that the positive phototactic behaviour is related to
bioluminescence, which is a major source of light at depth
The evolution ofthe cameraeye has attracted interest inthe sea. Nautilus is often trapped in association with deep
ever since Darwin [1859 (reprinted 1958)] listed it as one of water bioluminescent shrimps, which also feed on decaying
the "organs of extreme perfection and complication", and animal material, and moving towardsbioluminescence could
wrotethattobelievethat suchorganscouldhave been formed help take the animals towards their food. Finally, Nautilus
by natural selection seems "absurd in the highest possible shows diurnal vertical migrations (Carlsonetal. 1984; Ward
,
degree". Darwin'ssolutiontotheproblem wastosuggestthat etal. 1984), and vision could be a factor in this behaviour.
,
theeyemusthavearisenthrough numerous inheritablegrada- Without further information on the normal behaviour ofthe
tions, eachofwhichwas useful to itspossessor, andthat while animals however, these remain speculations.
strictly we should look for such gradations among the InthecaseofOctopuswehavenobehavioural evidence
animal's lineal ancestors, we are usually forced to look at onitsvisual sensitivity, althoughpresumably it isconsiderably
living species ofthe same group to see what gradations are better than that ofNautilus. The minimum separable visual
possible. acuity of5' for Octopus is comparable to that of fishes and
The eye ofNautilus could be taken as such a grada- aquatic mammals (Table 1). Nevertheless, it is notclearwhy
tion on the route to the complex eyes of the more recent the acuity is not even better than this. The retinal mosaic is
rather finer than necessary for the acuity that is in fact
achieved (Muntz and Gwyther, 1988a), and the pupil size is
largeenoughthat diffraction will not be limiting. InEledone
cirrhosa (Lamarck), another octopod, spherical aberration
is far less than would be needed to limit acuity to this level
(Sroczyriski and Muntz, 1985). Furthermore, terrestrial
animals can achieve much better acuities; in the case of
humans, for example, the minimum separable lies between
0.5' and V (e.g. Senders, 1948), and intheAmericankestrel,
Falcosparx'ernius Linne, the acuity, measured behavioural-
ly using square wave gratings, is 0.19' (Fox et al., 1976).
Since, however, the minimum separable acuity, measured be-
haviourally, has been found to be about 5' for all aquatic
animals where it hasbeen measured, itcouldbetheenviron-
ment itself that is limiting. While not very many data are
available on the subject, it is clear that high spatial frequen-
cies are particularly heavily attenuated by the water body
itself, and itcouldbethattheabilityto resolvevery finedetail
is consequently irrelevant (see Muntz, 1990 for further
discussion).
Visualangle(minutes)
The ability ofoctopuses andothercoleoidcephalopods
Fig.4.VisualacuityofOctopus,measuredbehaviourallyforvariousstimulus to discriminate the plane of polarisation of light is usually
combinations. The animals weighed between 59 and 1134g. A. vertical
attributed to the regular rectilineararray ofthe microvilli of
gratingsagainstgrey; +,horizontalgratingsagainstgrey;X,obliquegratings
againstgrey; verticalgratingsagainsthorizontalgratings. DatafromMuntz theirreceptors (Moody and Parriss, 1961). Nautilus lacks such
and Gwyther (1988a, 1989). a rectilinear array. Nevertheless, the microvilli within any
74 AMER. MALAC. BULL. 9(1) (1991)
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Muntz, W. R. A. andJ. Gwyther. 1988b. Visualdiscriminationofdistance
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Muntz, W. R. A. and U. Raj. 1984. On the visual system of Nautilus
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