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Active marine predators: The

sensory world of cephalopods
Bernd U. Budelmann

The Marine Biomedical Institute, and Department of

Otolaryngology , University of Texas, Medical Branch ,
Galveston, Texas, 775551163, USA
Published online: 22 Jan 2009.

To cite this article: Bernd U. Budelmann (1996) Active marine predators: The sensory
world of cephalopods, Marine and Freshwater Behaviour and Physiology, 27:2-3, 59-75, DOI:
10.1080/10236249609378955
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Mar. Fresh. Behav. Physiol.,Vo\. 27 (2-3), pp 59-75

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ACTIVE MARINE PREDATORS:

THE SENSORY WORLD OF CEPHALOPODS

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BERND U. BUDELMANN*
The Marine Biomedical Institute, and Department of Otolaryngology,
University of Texas Medical Branch, Galveston, Texas 77555-1163, USA
(Received March 25, 1995; in final form May 28, 1995)
Most cephalopods are voracious and very mobile predators with highly developed sense organs that rival the
equivalent vertebrate sense organs in complexity. A brief description is given of cephalopod predation and the
sense organs that are directly, or indirectly, involved: (i) the vertebrate-like lens eyes with their complex
extraocular eye muscle system; (ii) the epidermal head and arm lines which are analogous to the lateral lines
of fishes and aquatic amphibians; (iii) the vestibular analogue statocysts with receptor systems for linear
(gravity) and angular accelerations; (iv) the proprioceptive neck receptor organ which controls head-to-body
positions; (v) the sucker and muscle mechanoreceptors; and (vi) the contact and distance chemoreceptors. In
addition, the possibility of hearing is discussed.
KEY WORDS: Eyes, statocysts, lateral line system, chemoreceptors, proprioceptors

INTRODUCTION
Throughout their life, from a few days after hatching to reproduction and breeding,
octopuses, cuttlefishes and squids are voracious, very mobile and often fast-moving
predators. They inhabit every part of the ocean, down to a depth of more than 7000 m
(Nesis, 1987; Roper and Ross, 1982; Aldred et al, 1983); they are absent, however, from
fresh-water habitats. Most cephalopods start as tiny hatchlings in the millimeter size
range and then, in about a year, grow to adults that range from approximately 1.5 cm
(Jdiosepius) to 18 m irchioteuthis). Accordingly, they feed on a variety of prey that ranges
in size from plankton to forms that may even be larger than themselves. Most
cephalopods are generalist feeders and take both small and large prey; others are quite
prey selective, or at least prefer certain prey species above others. Several cephalopods
show a time preference for feeding at dawn, during the day, at dusk, or at night. For
details and references on feeding, see Hanlon and Messenger (1996).
In their natural habitat, all cephalopods feed on live prey, except Nautilus which is a
scavenger. The majority of the prey are fishes (except elasmobranchs), crustaceans and
molluscs (including cephalopods and even members of their own species), but other
invertebrates, such as polycheates and echinoderms, are taken as well (for references,
see Nixon and Budelmann, 1984). Because of their small seize, most cephalopod
* This paper is dedicated to Professor Theodore H. Bullock on the occasion of his 80th birthday.
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hatchlings and juvenile stages feed on plankton; only a few species (e.g., Neoteuthis and
Mastigoteuthis which have minute suckers, and Argonautd) continue to feed exclusively
on plankton throughout their life. To some extent, the form of the suckers and associated
hooks allows prediction of the type of prey taken (Nixon and Dilly, 1977).
The mode by which cephalopods hunt varies within and between the species; it ranges
from ambushing and luring to stalking, pursuing and hunting in disguise (for details, see
Hanlon and Messenger, 1996). Such a predatory lifestyle necessarily requires
sophisticated and highly effective sense organs and an elaborate nervous system. It is
not surprising, then, that during the course of evolution cephalopods - though
confined to their molluscan design - developed sense organs and nervous systems that
are the most sophisticated of all the invertebrates; some rival the equivalent vertebrate
systems in sophistication (Packard, 1972; Young, 1977,1989a; Budelmann, 1994,1995). In
fact, cuttlefishes and squids are the only invertebrate predators (perhaps with the
exception of the swimming crab Macropipus (Schfer, 1954) and a few. insects that
regularly chase and feed on adult vertebrates (fishes).
Most of our knowledge, especially about the function, of cephalopod sense organs is
based on semi-adult or adult specimen of only a few of the approximately 700 species.
The fact, however, that some cephalopods hatch as miniature replicas of the adults
may indicate that their sense organs and prdation behaviour does not differ much
from the adults. On the other hand, there are also species that at early life stages have a
distinct larval form (Sweeney et al, 1992) and, consequently, use different feeding
strategies. For example, the paralarvae of Octopus dofleini seem to feed on neuston, as
presumably do young Octopus vulgaris (Marliave, 1981; von Boletzky, 1987), and the
snouted hatchlings of ommastrephid squids quite likely are suspension feeders (O'Dor
etal, 1985). Furthermore, in Sepia hatchlings the equilibrium receptor organs are not yet
fully developed and have only 20% of their receptor cells (von Blow and Fioroni, 1989;
Forkel and Budelmann, unpublished), and the nervous system of an Octopus hatchling
has only half a million nerve cells, as compared to half a billion nerve cells of an adult
(Young, 1963b; Packard, 1972). It would be surprising if the much lower numbers of
receptor cells and nerve cells of the early life stages did not limit, or at least influence,
the capacity of the sense organs and the processing of sensory information.
On the other hand, even at very early life stages most cephalopods are extremely
successful predators and grow at an enormous rate. Octopus and Sepia, for example,
can double their weight within three weeks, and the squid Sepioteuthis can double its
weight already within 8 days (which is a daily weight increase of 13%; Mangold and von
Boletzky, 1973; Hanlon etal, 1991). Clearly, the capacities of the sense organs of the early
life stages of cephalopods must be excellent to allow such a successful predatory life style.
The following review briefly describes the various cephalopod sense organs, all of
which are directly, or indirectly, involved in prdation. Part of this review has recently
been published elsewhere in a more extensive form (Budelmann, 1994).

EYES AND VISION

Cephalopods are famous for their well developed eyes and complex visual behaviour. In
most species the eyes are the most important sense organs with regard to prdation. For
recent reviews on eyes and vision, see Land (1981, 1984), Messenger (1981, 1991) and
Hartline and Lange (1984).

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Eye gross morphology. In only a few cephalopod species the eyes are simple cups
(Cirrothauma) or lensless "pinhole camera" eyes (Nautilus) (Young, 1965; Aldred et al.,
1983); in most species they reach a design that is strikingly similar in overall anatomy
to the vertebrate lens eye (Figure 1A). The cephalopod eyes are mostly spherical, but
sometimes oval, telescopic (4mphitretus) or stalked (e.g., Bathothauma, and several
larval forms; Sweeney et al., 1992), and may even differ in form and size between the left
and right side (Histioteuthis); in deep-sea forms they reach a diameter of 35-40 cm
(Land, 1981 ; Wentworth and Muntz, 1989; Young, 1970,1991a). Most eyes have a cornea;
the pupil is circular, horizontal or of irregular shape, and in response to different
intensities of light it changes its size (Muntz, 1977). The rigid lens consists of an anterior
and a posterior part; it is suspended by ciliary muscles which allow for some
accommodation for near vision. The biological significance for accommodation,
however, is less clear since the long receptor cells and the lens' extremely short focal
length of 2.5 times the lens radius already provide a depth of focus from infinity to a few
centimeters (Messenger, 1981,1991; Hartline and Lange, 1984).
Retina. The structure of the retina is much simpler than in the vertebrate eye; it has
only two neural components, the receptor cells and efferent fibres, and there is no
separation into rods and cones (Figure IB; Yamamoto et al., 1965; Lund, 1966; Young,
1971; Cohen, 1973a, b). The outer segments of the receptor cells - different from the
vertebrate retina - face the lens. They carry arrays of microvilli which form
rhabdomeres (similar as in an insect eye). The outer segments contain the main
photopigment which is rhodopsin (Amax = 470-500 nm); a second pigment,
retinochrome (Amax = 490-552 nm), occurs mainly in the inner segments (see
Messenger, 1991). The axons of the receptor cells give off collaterals which, together
with efferent fibres, form a plexus beneath the cell bodies. The efferent innervation
influences the size of the receptive field (Tasaki et al., 1982) and is involved in the
control of the screening-pigment migration (Gleadall etal, 1993). The receptor cell can
be as long as 700 /xm; their density varies, species-specifically, between 20,000 and
100,000 cells per mm 2 . In some cephalopods (e.g., Octopus and Sepia) there is a strip
of longer and thinner receptor cells along the equator of the eye; this strip most
probably serves as a fovea (Young, 1963a). In the retina of deep-sea cephalopods, the
cell density may reach 250,000 cells per mm 2 and the retina may show complex
subdivisions. In Octopus, the angular receptor separation is 1.3 min, which is similar to
that of man (Young, 1962,1971; Packard, 1972; Land, 1981 ; Messenger, 1981,1991). Behind
the retina is a choroid, a sciera, an external argentea, and a plexus of intrinsic eye
muscles (Alexandrowicz, 1927).
The cephalopod eye produces a perfectly focused image on the retina because of the
layered construction of the spherical lens and the anatomy of the whole eye (Land, 1984).
As in vertebrates, the visual acuity is in the range of 5-10 minutes of arc (Muntz and
Gwynther, 1988), and the fusion frequency to flashes of light is, intensity-dependent,
between 20 and 60 Hz (Hamasaki, 1968; Bullock and Budelmann, 1991).
Colour vision. Most data indicate that cephalopods cannot see colours (Messenger,
1981,1991); however, it is still not quite clear whether all cephalopods are completely
colour-blind, since all the negative behavioural findings are not unequivocal (see
Budelmann, 1994). Furthermore, three different visual pigments (rhodopsin, Amax
484 nm; 3-dehydroretinal-opsin, Amax 500 nm; 4-hydroxyretinal-opsin, Amax 471 nm)
were recently found in different parts of the retina of the deep-sea squids Watasenia and
Bathyteuthis and two different pigments in the mesopelagic squids Pyroteuthis and
Pterigioteuthis and the deep sea octopus Japetella (Matsui etal, 1988; Seidu etal., 1990;

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EF

ON

Figure I The vertebrate-like lens eye of octopus, cuttlefish and squid. A: Section of the eye of Octopus; note
that the lens is composed of two parts. AL, anterior part of eye lens; CM, ciliary muscle; IR, iris; LI, eyelid; PL,
posterior part of eye lens; RET, retina; WB, white body. Borax Carmine stain. Scale bar is 1 mm. B: Blockdiagram of the retina of Octopus vulgaris. Arrow indicates the direction of light; note that the outer segments of the
visual cells face the lens, i.e., are oriented towards the light. BM, basal membrane; CL, collaterals of visual cells;
DVC, distal part of visual cell with lateral microvilli that form rhabdomeres; EC, epithelial cell; EF, efferent
fibres; MI, microvilli (orthogonally arranged in neighbouring visual cells); ON, optic nerve; PVC, proximal
part of visual cell; S, sciera. (A, courtesy of J. Z.%ung; B, from Wells, 1978). Reproduced from Octopus. Physiology and Behaviour of an Advanced Invertebrate, 1978, Chapman and Hall, London, by copyright permission of
Chapman and Hall.

Kito et al, 1992); these findings, however, seem to be exceptions since in all other
cephalopods investigated only a single pigment occurs with a Amax that varies with the
depth in which the animal lives (Muntz and Johnson, 1978).
Polarized light vision. Cephalopods see the plane of the polarized light, due to the
orthogonal arrangement of the microvilli of the retina receptor cells (Figure IB;
Moody and Parris, 1961 ; Moody, 1962; Saidel et al., 1983). The most attractive biological
reasons for this ability are the contrast enhancement of underwater targets and the fact
that light becomes polarized when reflected from a fish scale; this means that for
cephalopods a fish becomes more visible, and thus an easy prey, because in ordinary
light its shiny surface camouflages the fish against the background (Denton, 1970;
Land, 1984; Hawryshyn, 1992).
Visual processing. The visual information from the retina runs to large optic lobes.
In Octopus, they contain 60-90 million nerve cells each and together have a volume
1.6 times that of the rest of the brain (Young, 1963b). This relation, however, varies
considerably from species to species but, in general, correlates well with the size and
the complexity of the eyes (Maddock and Young, 1987; Young, 1988). The optic lobes are
smaller in most octopods than in cuttlefishes and squids; this may indicate that in
octopods vision is not quite as important. The anatomy of the optic lobes is highly

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/
m.rect.
ant. ma j.

Figure 2 The extraocular eye muscles of octopus, cuttlefish and squid. A: Arrangement of the eye muscles of
the left eye of Octopus vulgaris (left) and Sepia officinalis (right), seen laterally as flattened preparations.
m.ant.I,II,III, anterior muscle 1,11,111; m.ant.conj.1,11, anterior conjunctive muscle 1,11; m.inf.1,11, inferior
muscle 1,11; m.obl.inf.ant., anterior inferior oblique muscle; rn.obl.mf.post, posterior inferior oblique muscle;
m.obi.sup.ant., anterior superior oblique muscle; m.obl.sup.post, posterior superior oblique muscle; m.
post.1,11, posterior muscle 1,11; m.rect.ant.maj., major anterior rectus muscle; m.rect.ant.min., minor anterior
rectus muscle; m.rectpost., posterior rectus muscle; m.rect.sup., superior rectus muscle; m.sup.I,II,III,
superior muscle I,II,III; m.sup.conj., superior conjunctive muscle; m.tr.I,II,III, trochlear muscle I, II, III.
B: Directions of presumed linear and rotatory movements (arrows) of the left eye of the octopod Octopus (left)
and the decapods Loligo, Sepioteuthis and Sepia (right). The different lengths of the "rotatory" arrows indicate
the degree of rotation the muscles can produce. Note that m.ant.II and m.sup.conj. (open arrows) are absent in
Sepia Abbreviations as in A. (From Budelmann and Young, 1984,1993). Reproduced from the Philosophical
Transactions of the Royal Society of London, Series B, 1984, Volume 306:159-189, and 1993, Volume 340:93-125,
by copyright permission of The Royal Society..

complex, with outer cortical layers and a central medulla (Young, 1971, 1974). The
cortical layers resemble the organization of the vertebrate retina. The visual image is

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projected rather precisely onto the outer plexiform layer; from there almost certainly a
successive abstraction of the image occurs. The axons of the second-order visual cells
form a system of columns and may serve as feature detectors, similar to those in
the mammalian visual cortex (Messenger, 1991; Young, 1991a,b). At least some
cephalopods have remarkable visual abilities. Octopus can be trained to distinguish
between shapes that differ in form, size, brightness, or orientation (see Wells, 1978;
Messenger, 1981).
Eye movements. Besides voluntary eye movements, cephalopods show pronounced
compensatory eye reflexes, such as counter-rolling, vertical displacement and
nystagmus, to stabilize the visual image on the retina (e.g., Budelmann, 1970, 1990;
Collewijn, 1970; Messenger, 1970). All these eye movements are produced by four
(Nautilus), seven (octopods), or 13-14 (cuttlefishes and squids) extraocular eye muscles
(Figure 2; Budelmann and Young, 1984, 1993; Neumeister and Budelmann,
unpublished). This increase in the number of eye muscles matches the increase in
complexity of the eye movements in these groups. The additional six to seven eye
muscles in cuttlefishes and squids (as compared to octopods) are partly anterior and
partly dorsal; they are all involved in convergent eye movements for binocular vision
which is absent in octopods.
Dorsal light reflex, extraocular photoreceptors and countershading. In cephalopods,
the eyes are not only involved in vision but also in a "dorsal light reflex" that, as in many
fishes and crustaceans, stabilizes their swimming behaviours (Preuss and Budelmann,
1995a) and, via the chromatophore system, in a countershading reflex (Ferguson et al.,
1994). In addition to the eyes, cephalopods have extraocular photoreceptors in the brain
and mantle ganglion (e.g., Herring, 1988). Although they contain rhodopsin and
retinochrome (Nishioka et al, 1966; Hara and Hara, 1980; Ozaki et al, 1983) and
respond to light (Mauro and Baumann, 1968; Mauro and Sten-Knudsen, 1972), their
function is not visual but to detect the downwelling light in midwater to regulate
counterillumination (e. g., Young etal, 1979).

THE "LATERAL LINE" SYSTEM

Cephalopods, like fishes and aquatic amphibians, have a mechanoreceptive system
that is highly sensitive to local water movements. In cuttlefishes and squids, and at least
in octopod hatchlings, this lateral line analogue system consists of 4-5 lines of
epidermal hair cells located on the head and arms (Figure 3; Sundermann, 1983;
Budelmann and Bleckmann, 1988). It responds to water movements as low as 0.06 /xm,
which is equivalent to the threshold of the hair cells of the fish lateral lines (Bleckmann
et al. ,1991). Biologically, this sensitivity means that, for example, a cuttlefish that is partly
buried in the sand is able to detect a moving fish of 1 meter in body length from a distance
of about 30 m; however, in a free-swimming cuttlefish or squid the system is less effective
since the animals to some extent move ("vibrate") in synchrony with the water column
(which, in turn, reduces the amount of ciliary deflection of the hair cells). In which
behavioural context the lateral line analogue system is used, is less clear. Behavioural
data indicate that it is involved in prey detection (Budelmann et al, 1991); but it seems
quite likely that it is additionally involved in predator avoidance and perhaps in
schooling behaviour. Whether the system is more developed in species that live in the
deep-sea or in an environment where vision is restricted, or whether it is tuned to

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0.1

:
o

100
Frequency (Hz)

Figure 3 The lateral line analogue system in cuttlefish and squid. A: Epidermal lines on the head of a 14-days
old Sepia officinalis (oblique lateral view). Four lines (L1-L4) are seen that run in anterior/posterior direction;
three lines (L1-L3) continue onto an arm (A). E, eye; M, anterior edge of mantle. Scale bar is 0.5 mm. B:Thresholds of the dorsal head lines ofSepia officinalis to local water movements. The peak-to-peak water displacement
(closed circles, solid line, left Ordinate) and velocity (open circles, dashed line, right Ordinate) are shown as a
function of stimulus frequency (abscissa). (A, Budelmann and Fertl, unpublished; B, from Budelmann and
Bleckmann, 1988). Reproduced from the Journal of Comparative Physiology A, 1991, Volume 168:141-150, by
copyright permission of Springer-Verlag.

certain frequencies for a selective detection of predators, prey or conspecifics, remains

to be seen.
EQUILIBRIUM RECEPTOR SYSTEMS
Cephalopods have a highly developed equilibrium receptor system (statocysts) that
serves to stabilize and regulate all motor activities in the three dimensions of space.
Except in Nautilus, it reaches a level of complexity that is equivalent to that of the
vertebrate vestibular system (Budelmann, 1990).
Gross morphology. Cephalopod statocysts are of three basic designs. The Nautilustype of statocyst is a simple oval-shaped cavity that is completely lined with hair cells
(Figure 4A). It serves, first of all, as a gravity receptor system, but new morphological
data indicate that the detection of angular acceleration is possible as well (Neumeister
and Budelmann, unpublished). The sac-like octopod-type of statocyst and the
irregularly-shaped decapod-type of statocyst are far more differentiated (Figures 4B
and 4Q; they are the most complex of all the invertebrate equilibrium receptor systems
(Young, 1960; Stephens and Young, 1982; Budelmann, 1988, 1990). The octopod- and
decapod-type of statocysts have a gravity receptor system (macula/statolith [statoconia]
system; one in octopods, and three in decapods resembling the situation in fishes) and,
in addition, an angular acceleration receptor system (crista/cupula system) which is
divided into segments arranged in the three dimensions of space.
Receptor epithelia. The structural organization of the statocyst sensory epithelia
is one of the most sophisticated of any mechanoreceptive epithelium. The maculae

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Figure 4 The equilibrium receptor organs (statocysts) of cephalopods. A: Cut-open statocyst of Nautilus; the
statoconia are removed. K, opening of Klliker's canal. Scale bar is 0.3 mm. B: The octopod-type of statocyst
of Octopus vulgaris. Lateral view of the left statocyst sac with its single macula/statolith system and a crista/
cupula system divided into nine segments. S, statolith, attached to the macula; 1-9, crista segments 1-9 (the
cupulae are not seen). Scale bar is 0.5 mm. C: The decapod-type of statocyst of Sepia officinalis. The two statocyst cavities are cut open by a transverse vertical cut To the left: Anterior view, showing the three macula/statolith (statoconia) systems in each cavity and two of the four crista segments. To the right: Posterior view,
showing the remaining two crista segments. In the cavity on the right, some of the cartilaginous anticrista lobes
have been removed to show the course of thecrista segments. 1, crista transversalis anterior; 2, crista longitudinalis; 3, crista transversalis posterior; 4, crista verticalis; I, statoconial layer of macula neglecta inferior; P,
statolith of macula statica princeps; S, statoconial layer of macula neglecta superior. Scale bar is 1 mm.
(A, from Budelmann, 1994; B, from Budelmann et al, 1987; C, from Budelmann, 1976). Reproduced from
Marine and Freshwater Behaviour and Physiology, 1994, Volume 25:13-33, by copyright permission of Gordon
and Breach. Reproduced from the Philosophical Transactions of the Royal Society of London, Series B, 1987,
Volume 315:305-343, by copyright permission of The Royal Society. Reproduced from Structure and Function
of Proprioceptors in the Invertebrates (Mill, P. J., ed.), 1976, pp. 529-566, by copyright permission of Chapman
and Hall.

are composed of secondary sensory cells (without an axon) that are in afferent synaptic
contact with two types of first-order afferent neurons (Figure 5A; Colmers, 1981);
in addition, each crista segment contains primary sensory cells (with an axon)
(Figure 5B; Budelmann et al, 1987). The hair cells are stimulated by the movement of
the statolith (or statoconia) and cupulae, which are attached to them. The activity of the
hair cells.and first-order afferent neurons is influenced at various levels by a strong,

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Figure 5 The cellular, neuronal and synaptic organization of the sensory epithelia (macula, crista) of the statocyst of Octopus vulgaris. A: Diagram (cross section) of the macula. The secondary sensory hair cells (he) are in
afferent synaptic contact with two types of first-order afferent neurons (in, intramacular afferent neurons; pn,
perimacular afferent neurons). Hair cells and neurons receive many efferent endings (e). st, proximal part of the
statolith/statoconial layer. Arrows in the distal ends of the hair cells indicate the direction of the hair cells' polarization. B: Diagram (cross section) of the crista. The crista is composed of three different types of receptor
cells: primary sensory hair cells (dhc), large secondary sensory hair cells (flhc, Ihc), which are in afferent synaptic contact with large first-order afferent neurons (In), and small secondary sensory hair cells (vhc), which are in
afferent synaptic contact with small first-order afferent neurons (sn). All these elements receive multiple efferent endings (e). Arrows in the distal ends of the hair cells indicate the direction of the hair cells' polarization.
The insets at the left show diagrams of the small and large cupulae attached to the crista segments, cup II, base
of large cupula. (A, from Budelmann, 1988; B, from Budelmann et aL, 1987). Reproduced from Sensory Biology
of Aquatic Animals (Atema, I , Fay, R. R., Popper, A. N. and Tavolga.W N., eds), 1988, pp. 757-782, by copyright
permission of Springer-Verlag. Reproduced from the Philosophical Transactions of the Royal Society of London,
Series B, 1987, Volume 315:305-343, by copyright permission of The Royal Society.

mostly inhibitory efferent innervation that comes from the brain (Williamson, 1985). In
both receptor epithelia, L-glutamate is the putative excitatory transmitter, and

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acetylcholine, dopamine, noradrenaline, and GABA have mostly inhibitory functions

(Tu and Budelmann, 1994, also for references).
In octopods, the angular acceleration receptor system is divided into two receptor
sub-systems, one with large and one with small cupulae attached to it (Figure 5B).The
system with the large cupula is about 10 times more sensitive to angular accelerations
than the system with the small cupula. The biological significance for the presence of
two differently sensitive sub-systems could be the two types of movement of an Octopus:
slow crawling and fast swimming by jet propulsion (Williamson and Budelman, 1985;
Budelmann et al. ,1987).
In cuttlefishes and squids, there is a remarkable variability in the size and form of the
statocysts, specifically in the form and dimension of the angular acceleration receptor
systems. This reflects differences in, and can even predict, the animals' movement
behaviour, since the dimension of a statocyst (i.e., the volume of the endolymph fluid
and the size of the statolith/statoconia) affects the sensitivity of the systems: as in
vertebrate vestibular systems, large statocysts, in general, are more sensitive to gravity
and angular accelerations and, thus, occur in slowly moving animals, whereas smaller
statocysts are less sensitive and occur in fast-moving animals (Maddock and Young,
1984; Young, 1984,1989b).

Figure 6 The proprioceptive neck receptor organ of squid which controls head-to-body position. The scanning electron micrograph shows the dorsal neck region (nuchal cartilage complex) with the neck receptor
organ of Lolliguncula brevis (the mantle is removed). The anterior (AHQ and posterior (PHQ hair cell groups
of the organ are situated on either side of the nuchal crest (NCR); they are covered by the nuchal cartilage (NQ.
(Note that the anterior edge of the nuchal cartilage is bent upwards due to fixation). Scale bar is 100 /jm. (From
Preuss and Budelmann, 1995b). Reproduced from the Philosophical Transactions of the Royal Society of London,
Series B, 1995, in press, by copyright permission of The Royal Society.

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69

The information from the statocysts is used in equilibrium control. Such control is of
particular importance for animals that move in the three dimensions of space. Part of
that control system are compensatory eye adjustments, similar to those of the
vertebrate vestibulo-oculomotor reflex (VOR). In cephalopods, the organization of
the central nervous pathways involved in oculomotor control shows striking parallels
to the vertebrate VOR system and some brain regions have even been compared with
the vertebrate cerebellum (Messenger, 1967; Young, 1976; Budelmann and Young, 1984).

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THE NECK RECEPTOR ORGAN

In squids, epidermal sensory hair cells have recently been found on the dorsal side of the
neck that form a proprioceptive neck receptor organ. The cells form an anterior and
posterior group on either side of the nuchal crest, right underneath the lower nuchal
cartilage (Figure 6). In each group, the hair cells are polarized parallel to the animal' s
GL

CBR

CRN

Figure 7 Sucker mechanoreceptors. Diagram of a section through a tentacular sucker and peduncle oiLolliguncula brevis. In addition to the neurons of the sucker ganglion five different peripheral neurons occur in the
infiindibulum, acetabulum and peduncle. A, acetabular branch or radial nerves; AE, acetabular epithelium;
AM, acetabulo-cutaneous muscle; AS, acetabular sphinter muscle; CBR, ciliated bipolar receptor neuron;
CRN, cuticular ring neuron; EIE, external infundibular epithelium; EU, extracuplair branch of radial nerves;
GL, gland cells; HM, helicoidal peduncle muscles; I, infundibular branch of radial nerve; HE, inner infundibular epithelium; LM, longitudinal peduncle muscles; MAR, multipolar acetabular receptor neuron; MM,
meridian muscle; MMR, multipolar muscle receptor neuron; PN, peduncle nerve; PS, principal sphincter
muscle; RAM, radial acetabular muscle; RIM, radial infundibular muscle; RN, radial nerve; S, somata of neurons of the sucker ganglion; SG, sucker ganglion; TCE, toothed cuticular epithelium; TCR, toothed cuticular
receptor neuron. Courtesy of P. A. Santi.

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BERND U. BUDELMANN

transverse or longitudinal body axis and are involved in the control of pitch and roll
head-to-body positions (Preuss and Budelmann, 1995b).

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SUCKER AND MUSCLE MECHANORECEPTORS

Avariety of putative mechanoreceptors have been described in the suckers of octopuses,
cuttlefishes and squids (Figure 7; Graziadei, 1962,1964a,b, 1965a; Santi, 1975; Santi and
Graziadei, 1975; Graziadei and Gagne, 1976a,b). No physiological and behavioural
experiments, however, have yet been performed with any of these receptors, but almost
certainly they are involved in touch discrimination and touch learning (cf. Wells, 1978)
and play an important role in prey capture. Comparatively little is known about muscle
proprioceptors. They have been described in the musculature of the arms, sucker' s
peduncle, mantle, fins, lips, intestines, hearts, and in the substellar organ (Sereni and
Young, 1932; Alexandrowicz, 1927, 1928, 1960a,b; Gray, 1960; Graziadei, 1960, 1965b;
Boyle, 1976; Kier et al., 1985). Since the cephalopod muscles lack a skeletal "reference",
the structure and location of the muscle receptors indicate that they most likely serve as
proprioceptors for muscle tension and movement, rather than for position (Boyle,
1986b).

CHEMORECEPTION
All cephalopods are sensitive to chemical stimuli, but chemoreception seems not to be a
highly developed sense. An exception is Nautilus who, being a slowly-moving scavenger
with presumably poor vision, needs a well developed sense of chemoreception.
Depending on their location rather than structure, the chemoreceptors are involved
either in distance or in contact chemoreception.
Distance chemoreception. The organs involved in distance chemoreception are the
rhinophores of Nautilus and the olfactory organs (olfactory pits) of octopuses,
cuttlefishes and squids. The rhinophore lies right below the eye. It is an elongated saclike structure lined with two types of ciliated receptor cells (Young, 1965; Barber and
Wright, 1969); to date, no data are available on its physiology. The olfactory organ also
lies close to the eye (Figure 8A); it contains at least five types of ciliated receptor cells
(Watkinson, 1909; Woodhams and Messenger, 1974; Emery, 1975c, 1976; Wildenburg
and Fioroni, 1989; Lucero et al, 1992). In behavioural experiments, octopods and
squids are able to sense avariety of different chemicals, some at concentrations as low
as 10~5 molar (Boyle, 1986a; Chase and Wells, 1986; Gilly and Lucero, 1992; Lee, 1992).
Contact chemoreception. The receptors involved in contact chemoreception occur in
the distal region of the long digital tentacles of Nautilus (Bidder, 1962; Fukuda, 1980,
1987) and in the lips and suckers of octopuses, cuttlefishes and squids (Figure 8B;
Graziadei, 1962,1964a,b, 1965a; Wells etal, 1965; Emery, 1975a,b; Santi, 1975; Graziadei
and Gagne, 1976b). There are about 10,000 chemoreceptor cells in a sucker of an octopod
(a total of 16 million cells per animal), but only about 100 such cells are present in a sucker
of a cuttlefish (Graziadei, 1964a,b). This difference can be explained by the fact that
octopods, different from cuttlefishes and squids, often explore out-of-sight habitats with
their arms and suckers in the search for food.

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71

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Figure 8 The two locations of chemoreceptors in Octopus. A: Olfactory organ ("olfactory pit") below and
posterior to the eye with distance chemoreceptors. The olfactory organs of cuttlefishes and squids are in similar
locations. B: Rim (R) of a sucker (of a juvenile Octopus joubini) with contact chemoreceptors. Scale bar is
50 m. (A, from Emery, 1976; B, courtesy of M.Villoch). Reproduced from Tissue & Cell, 1976, Volume 8:
33-46, by copyright permission of Churchill Livingstone.

HEARING
Cephalopods can sense vibrational stimuli with the statocysts and the lateral line
analogue system (Williamson, 1988; Budelmann, 1992). Whether cephalopods can
actually "hear", is basically a semantic problem and the answer lies with the definition
of underwater sound and underwater hearing (see Budelmann, 1992). At least,
cephalopods have no specialized sense organ associated with gas-filled cavities that
can be compressed by the pressure wave of underwater sound. The fact that octopus,
cuttlefish and squid are able to sense low frequency "infra sound" is not due to sound
pressure but rather to particle motion detection, presumably via statocyst sensory cells
(Packard et al, 1990).
Acknowledgements

The author's work mentioned in the text was supported in part by grants of the Deutsche
Forschungsgemeinschaft (Bu 404/1-3 and SFB 4/A2) and the National Institutes of
Health (ROI EY 08312). The author's participation at the conference was supported by
the Marine Medicine Budget of The Marine Biomdical Institute of The University of
Texas Medical Branch at Galveston.
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