RESPONSE OF NAUTILUS TO VARIATION IN AMBIENT PRESSURE
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h. exp. Biol. 137, 175-189 (1988) 175
Printed in Great Britain © The Company of Biologists Limited 1988
RESPONSE OF NAUTILUS TO VARIATION IN AMBIENT
PRESSURE
BY MICHAEL JORDAN
Institute of Marine Biomedical Research, University of North Carolina at
Wilmington, Wilmington, NC 28403, USA
JOHN A. CHAMBERLAIN, JR
Department of Geology, Brooklyn College of the City University of New York,
Brooklyn, NY 11210, USA and Osborn Laboratories of Marine Sciences, New
York Aquarium, New York Zoological Society, Brooklyn, NY 11224, USA
AND REBECCA B. CHAMBERLAIN
Metuchen, NJ 08840, USA
Accepted 12 January 1988
Summary
Juvenile Nautilus, tested in a high-pressure animal maintenance apparatus, are
sensitive to increases in ambient hydrostatic pressure as small as lxlO 5 Nm~ 2
(= 1 atm = 100kPa). They respond to such pressure increases in a characteristic
'depth alarm' behaviour pattern, which consists primarily of rapid upward
swimming. These activity bursts may serve to restore them to their original depth.
The animals apparently continue this behaviour until fatigued. Pressure decrease
elicits no obvious response. The pressure-sensing mechanism may be located
within the statocyst, or possibly in the posterior mantle or siphuncle. The
operation of. the latter two mechanisms involves tensional strain induced by the
hydrostatic load in the outermost septum and wall of the siphuncular tube.
Introduction
An obvious analogy can be drawn between the shell of Nautilus and a
submarine. Both shell and ship are constructed on the plan of a hollow, tube-
shaped hull supported by bulkheads; both use a fluid ballast system to regulate
buoyancy; both maintain low internal gas pressure relative to ambient hydrostatic
pressure; and both depend on the mechanical strength of their superstructure to
resist the adverse pressure head thus created. Moreover, both must possess a
sensory system capable of providing information that will enable them to avoid
depths at which ambient pressure exceeds strength. Violating these principles
Produces dire consequences for both submarine and cephalopod, as witnessed by
Key words: Nautilus, pressure sensitivity, depth alarm behaviour.176 M. JORDAN, J. A. CHAMBERLAIN AND R. B. CHAMBERLAIN
the unfortunate USS Thresher incident of 1963, and by the fragmented Nautilus
remains illustrated by Ward & Martin (1980).
Knowledge of the behaviour patterns and responses of Nautilus to external
stimuli has increased in the last two decades. This recent work involves
observation on feeding behaviour and food preferences (Wells, 1966; Haven,
1972; Ward & Wicksten, 1980), reproductive behaviour (Haven, 1977; Mikami &
Okutani, 1977), locomotory and respiratory behaviour (Bidder, 1962; Packard,
Bone & Hignette, 1980; Chamberlain, 1981, 1987; Wells, 1987), activity cycles
(Saunders, 1984, 1985; Zann, 1984) and diurnal vertical migration (Carlson,
McKibben & Degruy, 1984; Ward, Carlson, Weekly & Blumbaugh, 1984). Kanie
et al. (1980) and Kanie & Hattori (1983) imploded live Nautilus in a hyperbaric
chamber. They observed a fluctuating, but generally elevated, funnel pulse rate as
they increased ambient pressure. In terms of funnel pulsing, no obvious awareness
of the animal to its impending implosion could be seen.
However, none of these reports provide much help in determining whether
Nautilus can detect pressure change. We cannot say whether these cephalopods
use pressure, or some other depth-dependent environmental parameter (e.g.
temperature, light intensity) as an index for selecting habitats, for avoiding
implosion, or for monitoring position during diurnal migration. In this paper, we
document behavioural responses of live Nautilus to measured variation in ambient
hydrostatic pressure.
Materials and methods
The analysis we present here is based on observation of 17 juvenile specimens of
Nautilus pompilius (43-143 g in mass). They were captured in the Tanon Straight
area of the Philippine Islands, and were maintained at the New York Aquarium for
2-4 months prior to testing. All specimens were vigorous, healthy animals in full
command of their buoyancy apparatus.
Pressure testing was done using a high-pressure animal maintenance system
designed and built by M. Jordan (see Fig. 1). This device consists of six main
components: (1) an 8-1 stainless-steel pressure chamber; (2) a pressure regulator
for controlling pressure in the system; (3) a piston pump for pressurizing and
circulating water through the system; (4) a variable speed d.c. motor and gear train
for delivering power to the pump; (5) a pulse dampener for minimizing minor
pressure fluctuations resulting from movement of pistons in the pump; and (6) a
pressure gauge for monitoring pressure inside the test chamber. The apparatus
was connected to a satellite tank system at atmospheric pressure which served as a
reservoir for filtered, temperature-controlled, oxygenated water (Fig. 1). Cham-
berlain, Jordan & Cheung (1987) give a more complete description of this system.
Our procedure was to expose specimens to a series of step-wise pressure
increments as illustrated in Fig. 2A for specimen 05-969-6. Each stepped rise ua
pressure was initiated by resetting the pressure regulator. Chamber p r e s s u S
levelled off as the actual pressure in the system approached the new setting of theNautilus pressure behaviour 111
0
£%
Fig. 1. High-pressure animal maintenance system. A, Pressure chamber; B, pressure
regulator; C, pressure pump; D, variable-speed d.c. motor; E, pulse dampener;
F, pressure gauge; G, reservoir tank; H, chiller and filter. Flow in high-pressure loop is
from G through C, A, B, H and back to G.
regulator. An individual test run consisted of 5-10 such pressure increments.
Maximum pressure achieved in the course of these experiments was about
2xlO 6 Nm~ 2 . We terminated a test by quickly releasing the pressure as seen on the
right in Fig. 2A. Twenty such tests were made.
Water flux through the pressure chamber remained constant as pressure
changed. We used through-chamber flow rates of about 48 lh" 1 . This was
sufficient to flush the test chamber completely once every lOmin. Periodic
measurement of oxygen concentration, made by drawing water samples from the
test chamber during a test run, did not reveal significant reduction in oxygen
availability as a consequence of these flow conditions.
We observed the animals through an acrylic window in one end of the pressure
chamber. In attempting to quantify observed behaviour, we recognized, for the
purposes of our analysis, four different activity states: (1) inactive, attached to
chamber wall with tentacles; (2) unattached, but no locomotory movement, gentle
rocking and pulsing of funnel; (3) active swimming, tentacles at least partly
:tended; (4) strong, upward swimming, tentacles fully extended. The general
K tensity level of these behaviours increases with the numerical value of the
activity state.178 M. JORDAN, J. A. CHAMBERLAIN AND R. B. CHAMBERLAIN
100 200 400
3
I
J
100 200 300 400
Time (min)
Fig. 2. Response of specimen 05-969-6 to pressure change. (A) Variation in pressure
as a function of time for the 05-969-6 test. Circled inflection points indicate points
where pressure was increased by adjusting pressure regulator. Equivalent depth is the
depth below sea surface required to produce pressure shown at left. (B) Activity state
of specimen during testing. Units on activity axis refer to the following types of
behaviour: (1) inactive, attached with tentacles to chamber wall; (2) unattached, but
no locomotory movement, gentle rocking and pulsing of funnel; (3) active swimming,
tentacles at least partly extended; (4) strong, upward swimming, tentacles fully
extended. Circles on time axis correspond to the circled inflection points on the
pressure/time curve.
Results
Activity peaks
During each test we recorded pressure and activity state, as defined above, at
regular 30-s intervals. This procedure allowed us to produce a time/activity graph
for each animal (see Fig. 2B). Changes in behaviour are expressed as upward or
downward deflections of the time/activity curve. The behaviour illustrated in
Fig. 2B can be conveniently described as consisting of a series of short-lived
periods of intense activity, which we refer to here as activity peaks, separated by
longer intervals of little or no activity.
Tentacle extension, noted above as accompanying the most intense levels of
behaviour comprising these activity peaks, is qualitatively different from tentacle
extension associated with other forms of behaviour. During feeding, for example,
both Bidder (1962) and Ward & Wicksten (1980) describe the formation of a 'con^
of search' configuration in which the lateral digital tentacles are directed radialrjl
outwards, presumably to enhance chemoreception. In this posture, extendedNautilus pressure behaviour 179
tentacles are held rigidly in position, although the tips may bend, conforming to
the flow around them. During 'escape', as described by Bidder (1962) and others,
tentacles are usually held in a loose, tapering mass behind the body. When
deployed in this manner, tentacle flaccidity is so pronounced that tentacles often
flutter passively in the flow of water around the moving animal. During the activity
peaks, the extended tentacles flexed rapidly and repeatedly, but with no apparent
rhythm or focus to their movement.
Activity/pressure correlation
The clear correlation between incremental pressure increases and activity peaks
seen in Fig. 2 strongly suggests that there is a causal relationship between stepped
ambient pressure increase and bursts of swimming activity for specimen 05-969-6.
To determine whether the results seen in Fig. 2 have a more general applicability,
we tabulated times of occurrence for the total number of pressure increases and
activity peaks observed during the course of our work (17 animals; 20 tests; three
animals tested twice; 138 pressure increments; 152 activity peaks). We considered
that a pressure increment was correlated with an activity peak if behaviour was
modified within 15 s of the inception of a pressure jump.
We found that the overwhelming majority (91 %) of all pressure increments
were correlated with activity peaks as defined by our 15-s rule. Only 9 % of the
pressure increments produced no change in activity, and in no case (0 %) did a
pressure increment elicit a decrease in activity. In addition, the overwhelming
majority (90 %) of activity peaks occurred in conjunction with pressure incre-
ments. Only 10 % of the observed activity peaks were unrelated to increase in
pressure using our definition above. Thus, the apparent correlation between
pressure increase and activity is not likely to be the product of activity peaks
occurring so frequently (e.g. every 15 s) that some of them fortuitously coincide
with pressure increments. Instead, our animals, with few exceptions, became
active only when pressure was suddenly raised.
We tested the hypothesis that there is an equal probability that an activity peak
will be either synchronous or asynchronous with respect to a pressure increment
under the 15-s requirement. We obtained X2 = 93-6; P< 0-001, which indicates
that the hypothesis of equal probabilities may be rejected. Since the value of X2
will depend on the number of extraneous activity peaks, this result implies that our
sample was drawn from a population of specimens that responded only when
pressure was increased.
We determined how the number of pressure increments not correlated with
activity peaks (i.e. missed increments) is distributed among the total sample of test
runs. We found that in 10 runs the specimens tested made no errors; they
responded in the form of an activity peak each time pressure was raised. In seven
tests, animals missed one pressure increment, and in three tests, they missed two
increments. Similar results are obtained when these figures are converted to
frequencies. Ten animals missed 10 % or fewer of the total number of pressure
increments to which they were exposed. Six animals missed 10-20% of the180 M . J O R D A N , J. A . CHAMBERLAIN AND R. B . CHAMBERLAIN
pressure increments and one missed 20-30 %. Thus, there appear to be only minor
differences in the nature of the response to pressure increase from animal to
animal. All consistently reacted to increases in ambient pressure.
We also determined how activity peaks not correlated with pressure increments
(extraneous activity peaks) are distributed among the test sample. In 10 tests,
specimens showed total correlation, that is, they responded only when pressure
was increased, and therefore exhibited no extraneous activity peaks. In seven
tests, specimens had one extraneous peak, and in the three remaining tests,
animals showed two or three extraneous peaks. Comparable results are obtained
when these figures are converted to frequencies. Extraneous activity peaks
comprised 10 % or less of the peaks in nine animals, 10-20 % in six animals, and
> 2 0 % in the remaining two specimens. For no specimen do extraneous peaks
form a majority of the peaks elicited and, in most, extraneous peaks comprise a
small fraction of the total.
Extraneous and pressure-induced activity peaks differ not only in frequency of
occurrence but also in magnitude. To show this, we calculated mean peak activity
state in two ways: (1) in terms of peak activity state (absolute magnitude), and (2)
in terms of change in activity state (relative magnitude). Absolute magnitude
refers to the highest activity state achieved in an activity peak. Relative magnitude
refers to the highest activity state achieved minus the activity state prior to the
onset of activity increase. For extraneous peaks (N= 14), we obtained means of
2-36 ±0-75 (S.D.) and 1-75 ±0-91 for absolute and relative magnitude, respect-
ively. For pressure-induced peaks (N= 124), we found means of 3-70 ± 0-54 and
2-39 ± 0-72, respectively. Calculating Student's r-statistic for each case gives
t = 8-419, P < 0-001 and t = 3-207, P < 0-002, respectively. Thus, in both cases it is
possible to reject the hypothesis of equal means. We infer from this result that
pressure-induced peaks are generally more intense. They produce higher activity
states than peaks not associated with pressure increase.
Peak intensity and pressure
Our testing procedure involved augmenting ambient pressure in successive
steps. Consequently, each pressure increment within a given test series is initiated
at increasingly elevated ambient pressures (Fig. 2A). Do the response patterns
identified above show any variation with respect to ambient pressure? We
evaluated this question by tabulating missed pressure increments and peak
intensity as a function of pressure. It is evident from Table 1 that missed
increments occur only at low pressures. In the upper portion of the pressure
regime studied, our test animals made no mistakes at all; every increment in
pressure elicited a corresponding response in the form of an activity peak.
Peak intensity data contained in Table 2 do not show pressure-related variation
similar to that seen in Table 1. Instead, mean activity peak intensities for the four
pressure categories do not differ appreciably (ANOVA: F= 1-971; P> 0-2; 3 and
120 d.f. Kruskal-Wallis test: X2 = 1-777; P>0-5). Thus, we cannot reject the null
hypothesis of equal pressure category means, and we conclude that our specimens,Nautilus pressure behaviour 181
Table 1. Numerical abundance of missed pressure peaks as a function of ambient
hydrostatic pressure
Pressure Total Missed Relative
(xlO 6 NrrT 2 ) increments increments frequency
0-1 27 8 0-30
1-2 67 6 0-09
2-3 36 0 0
>3 8 0 0
Total increments, total number of pressure increments for all test specimens falling within
pressure range indicated in first column.
Missed increments, pressure increments not associated with activity peaks.
Relative frequency, missed peaks/total peaks.
Table 2. Absolute peak intensity as a function of ambient hydrostatic pressure
Absolute
Pressure Total peak intensity Mean
(xl0 6 Nm~ 2 ) increments 4 3 2 intensity S.D.
0-1 22 16 3 3 3-59 0-717
1-2 57 44 12 1 3-75 0-469
2-3 37 24 13 0 3-65 0-477
>3 8 5 3 0 3-63 0-484
Absolute intensity and intensity categories as defined in text.
although they were more likely to miss increments at low ambient pressures, when
they did respond, they did so equally strongly at all pressures. In the context of
peak intensity levels, we observe no significant variation of this parameter as a
function of pressure.
The data reported in Table 3 suggest that although peak intensity may not vary
with pressure, the change in intensity associated with activity peaks decreases in
the higher pressure ranges. Both ANOVA (F= 3-980; P182 M. JORDAN, J. A. CHAMBERLAIN AND R. B. CHAMBERLAIN
(intensity change) differs significantly among the pressure categories. At higher
pressures, incrementing pressure produced a smaller change in activity than at
lower pressure. The reason for this is seen in Fig. 2B. At higher experimental
pressures, between-peak activity levels were higher than at low pressures. Thus,
change in intensity at high pressure tends to be less than for lower pressures. It
would appear that at higher ambient pressures, our animals did not settle down as
fully after an increment in pressure as they did when pressure was lower. In this
sense, one can say that our animals do show a kind of increased activity at higher
pressure.
Peak length and pressure
We also examined whether the character of activity peaks varied during the
course of our experiments. We were primarily interested in the duration of activity
peaks (peak length), and whether peak length depends in some way on pressure.
In the treatment below, we define peak length as the time during which an animal
maintains highest peak activity. The mean length of the 124 pressure-induced
activity peaks identified above was 5-01 ± 4-68min.
Fig. 2A shows that step-wise pressure increments vary in magnitude during a
test run, although not in any systematic way. We found that the 124 pressure
increments correlated with an activity peak ranged in magnitude from 6-89x 104 to
5-5xlO 5 Nm~ 2 . The mean pressure increment was 2-29X105 ±3-91xlO 4 Nm~ 2 .
These figures are equivalent to the increase in hydrostatic pressure resulting from
depth increases of 7m (minimum increase) to 57m (maximum increase), with a
mean of 20 m.
Regressing peak length against the magnitude of the pressure increments did
not yield strong correlations. The linear correlation coefficient for this association,
for example, was 0-044. Various non-linear correlation coefficients were similarly
insignificant. We infer from this that peak lengths are not related to the size of the
pressure increments that produced the peaks. We also studied peak length as a
function of ambient hydrostatic pressure at the beginning of the corresponding
pressure increment (circled points in Fig. 2A), and showed that the pressure at
which increments occurred had no effect on peak length (r = 0-038, and non-linear
correlation coefficients were correspondingly insignificant). Thus, we conclude
that the pressure in the test chamber at the start of a pressure increment does not
influence activity peak length. Peak length would appear to be controlled by other
phenomena not related to pressure.
Pressure decrease and activity
Although our experimental procedure was not designed specifically for evaluat-
ing the effect on behaviour of a decrease in pressure, the large pressure drop
terminating a test run (Fig. 2A) provides some information about this. Comparing
Figs 2A and 2B shows that during the entire terminal pressure decrease, beginning
at 316min and ending when pressure goes to atmospheric at 334 min, specimenNautilus pressure behaviour 183
-3 - 2 - 1 0 1
Change in activity state
Fig. 3. Change in activity state occurring during release of pressure at conclusion of
test run. Change in activity state: —3, decrease of three activity levels; —2, decrease of
two levels; —1, decrease of one level; 0, no change in activity; 1, increase of one level.
05-969-6 remained inactive. Activity did not increase during any part of this
2xlO 6 Nm~ 2 pressure decrement.
To determine if the behaviour of specimen 05-969-6 is a common feature of the
response patterns of the other test animals, we tabulated activity state at the start
and conclusion of the terminal pressure decrease. We found that in our 18 tests
(two animals were killed by implosion before terminal pressure decrease), one
showed an increase in activity state, four (including 06-969-6) showed no change
and 13 showed a decrease in activity state (Fig. 3). The mean change in activity
level for these 18 tests is —1-11 ± 1-048. Thus, terminal pressure decrements on
average actually elicit a reduction in activity state.
The response of our animals to pressure decrease seems clearly different from
their response to pressure increase. This inference is strengthened by two-sample
Mesting of the pressure increment and decrement data sets. The null hypothesis
for this test is that the mean change in activity associated with pressure increments
and the mean change associated with terminal pressure decrease are equal. Our
computation allows us to reject the null hypothesis of equal means (/ = 18-12;
P< 0-001).
Discussion
Depth alarm behaviour
Our analysis of activity patterns reveals a strong, statistically significant
Correlation between pressure increase and increase in activity level (Tables 2, 3;
Fig. 2). This pressure-related activity differs from other activity patterns in two184 M. JORDAN, J. A. CHAMBERLAIN AND R. B. CHAMBERLAIN major ways: it contains strong tendencies for upward directed swimming and for seemingly uncoordinated streaming of tentacles. In addition, our data suggest that these activity bursts are relatively short-lived, usually of about 5 min duration, and that a pressure decrease, even when large, does not elicit significant changes in behaviour (Figs 2, 3). These results indicate that within the constraints of our experimental pro- cedures, i.e. under rapid pressure increase, Nautilus senses increasing pressure and responds to this stimulus with a unique behaviour pattern of intense activity characterized by fast upward swimming. Presumably, protracted increases in pressure would produce the same response. It appears also that this behaviour may be functional, and not merely the product of uncontrolled movement with no specific focus, as tentacle streaming might suggest. The basis of our argument involves cameral gas pressure, pumping efficiency and depth. Nautilus does not concentrate gas to offset hydrostatic pressure as do many physoclist fish. This has two important effects: (1) the hydrostatic load acting on the shell can cause catastrophic failure, as noted above; and (2) the osmotic pump, driving evacuation of cameral water, operates with diminishing effective- ness as hydrostatic pressure increases (Ward & Martin, 1978; Greenwald, Ward & Greenwald, 1980; Chamberlain & Moore, 1982). Thus, depth increase leads to potentially serious consequences. If Nautilus interprets rapid pressure increase as a rapid downward drift in depth, it is obviously adaptive that such change triggers rapid upward swimming. Such a 'depth alarm' response may also be initiated by a slow depth increase (i.e. by slowly increasing ambient pressure), presumably the more usual situation. Depth alarm activity does not appear modifiable. In particular, there is no evidence in our data to indicate that individuals intensify their responses as pressure increases towards dangerous levels. In this regard, it is especially noteworthy that in the two cases of catastrophic shell implosion noted above, the animals' behaviour did not change before the disaster. In fact, one animal was not fully active at the time of its implosion or for the previous several minutes. In general, depth alarm behaviour appears to be an all-or-nothing response, rather than one whose intensity is geared to the magnitude of the stimulus. Why this should be the case is not obvious. Perhaps the cause lies in the comparatively primitive neural anatomy of Nautilus noted by Young (1965); that is, Nautilus may not be wired to evoke differential behavioural responses to this kind of stimulus. The longevity of depth alarm bursts is also of interest. The 5-min average duration of these bursts, when combined with Nautilus's observed swimming speeds of about 20cms" 1 (Chamberlain & Westermann, 1976; Ward, Stone, Westermann & Martin, 1977; Chamberlain, 1987), results in distances (about 60 m) which are sufficient to offset the apparent depth increase (about 20 m on average - see above) due to our pressure increment procedure. However, the implication that the duration of these bursts is governed by attempts to restor< depth is not supported by our observation that there is no statistical correlatio 1 between burst duration and the magnitude of pressure increments. Moreover, in
Nautilus pressure behaviour 185
our experiment there is no pressure decrease associated with upward swimming
activity, and thus perhaps no real means for the animal to evaluate its apparent
ascent.
Although our data are not sufficiently incisive to rule out depth restoration as
the prime control of depth alarm duration, a more reasonable alternative presents
itself. Wells (1987) points out that Nautilus cannot operate at peak capacity
without eventually incurring a significant oxygen debt. Thus, like other aerobes,
Nautilus should experience fatigue when its oxygen resources are exhausted. Little
is known about the resistance of Nautilus to fatigue, but it is perhaps significant
that several workers. (Packard etal. 1980; Zann, 1984; Chamberlain, 1987) have
noted that periods of continuous peak activity generally do not exceed 5-10 min.
This is essentially the same result that we have obtained here. Taken together,
these observations indicate a time-tp-fatigue of up to about 10 min. Thus, we
surmise that fatigue may be the factor limiting the duration of depth alarm
behaviour. In our view, increments in pressure set off depth alarm activity, and the
animals simply remain active until fatigue forces them to slow down and pay off
their oxygen debt.
Our tests also give an indication of the sensitivity of Nautilus to pressure change.
Although the minimum pressure increase to which Nautilus reacts was not
systematically tested as part of our experimental procedure, it is quite clear that
this minimum must be less than the pressure increments we used (2-3xKPNm~ 2
on average; equivalent to a depth increase of about 20m). The actual sensitivity
limit may be much less than this because we observed that animals often initiated
depth alarm behaviour well before the top of a pressure increment was attained.
Our feeling is that Nautilus can detect and respond to pressure changes as small as
lxlO 5 Nm~ 2 , or that produced by a depth increase of only about 10 m.
Pressure detection mechanism
The Nautilus in our tests were placed inside a stainless-steel cylinder in which
temperature and illumination were held constant. In such alien surroundings,
there can be little doubt that the animals received no other depth-related
environmental cues than the pressure modifications we purposely induced. This
suggests that hydrostatic pressure may be a means by which Nautilus monitors
depth. However, further work is required to determine if Nautilus relies
exclusively on pressure for this purpose.
At least one other cephalopod species, Loligo forbesi, appears to react to
pressure in a manner not unlike that we describe here for Nautilus (Knight-Jones
& Morgan, 1966), and many cephalopods (e.g. Spirula, vampyroteuthids,
cirroteuthids) have deep-water lifestyles that would appear to require a depth-
monitoring system. Pressure-sensing organs have not, however, been positively
identified in these animals, although statocysts have long been regarded as the
Rhief candidates for this function. Their role in balance and attitude control in
Octopus is well known (see Wells, 1978), and their structure is not incompatible186 M. JORDAN, J. A . CHAMBERLAIN AND R. B . CHAMBERLAIN with a pressure-sensing function. Statocysts contain hard, relatively incom- pressible masses (statoliths), ensconced within fluid-filled cavities which can presumably distort under pressure. Such differential compressibility forms the operational basis for pressure receptors in many animals (see Knight-Jones & Morgan, 1966). Young (1977) points out that many deep-water cephalopods have statocysts noted for their enlarged, separated inner and outer sacs, reduced anticristae and elaborate networks of hair cells and nerve fibres. He hypothesizes that a likely function of these organs, which differ markedly from statocysts of shallow-water forms, may be one of sensing pressure change. Nautilus also has statocysts with these general features (Young, 1965), although Nautilus statocysts differ in some ways from those of its coleoid relatives, particularly in their simpler plan and in the fact that they communicate to the external environment by means of a narrow passage (Kolliker's canal). Thus, Nautilus, may perhaps rely on its statocysts for information on depth, as is inferred to be the case for some coleoids. Gas-filled organs (such as the teleost swim bladder) constitute an important pressure-sensing mechanism in many marine organisms (Knight-Jones & Morgan, 1966). Like most teleosts, but unlike most of its contemporary relatives, Nautilus also contains large internal gas spaces (the camerae) which, in principle, could supply the differential compressibility needed for a baroreceptor mechanism. A cameral pressure-sensing mechanism could operate through compressibility differ- ences between: (1) shell and camerae or (2) siphuncle and camerae. Since cameral gas pressure remains constant at slightly less than lxlO 5 Nm~ 2 (1 atm), change in depth will elicit a corresponding change in the hydrostatic load acting on the shell and outermost septum. Mollusc shell carbonate is a linear elastic material (Currey & Taylor, 1974). That linear elastic compliance occurs in the shell of Nautilus is seen in the strain gauge data of Saunders & Wehman (1977; fig. 4) and Kanie & Hattori (1983; fig. 3). Using these authors' stress/strain plots for the outermost septum and shell wall gives the results shown in Table 4 for the strain produced by a stress equivalent to that which Nautilus seems capable of detecting (lxlO 5 N irT 2 ). The evident disparity between the figures for specimen 1 compared with specimens 2 and 3 probably reflects differences in the freshness of the shells used. In either case, but especially in the strains calculated from Kanie & Hattori's data, it is obvious that the movement of these components, particularly of the outermost septum, would be more than ample to be detected by receptor cells lining the adapertural septal surface. The siphuncular tube also resists the hydrostatic load, but unlike the carbonate shell and septa, its main structural member, the so-called 'horny tube', consists of pliant conchiolin sheets stretched between adjacent septa. Chamberlain & Moore (1982) measured the ultimate failing strength of Nautilus siphuncular tube but provided no quantitative figures for strain. Nevertheless, we did observe that as we increased pressure inside the tube, the tube wall bulged outwards into th camerae. For a tube segment within a single chamber, the total displacement 1 involved in this movement may have been as much as lmm over the pressure
Nautilus pressure behaviour 187
Table 4. Compliance (strain) in carbonate load-bearing components of Nautilus
shell produced by stress equal to probable minimum pressure change detectable by
the live animal (ixlO5Nm~2)
Strain due to
Shell Stress unit stress
Specimen component mode (urn) Reference
1 Outermost septum T 1 Saunders & Wehman, 1977
Shell wall C 01
2 Outermost septum T 17 Kanie & Hattori, 1983
Shell wall C 12
3 Outermost septum T 19 Kanie & Hattori, 1983
Shell wall C 13
T, tension; C, compression; unit stress, minimum detectable stress.
range studied ( l x l 0 5 - 8 x l 0 7 N m 2 ). The scale of this movement would also
undoubtedly be sufficient to stimulate receptor cells located within the siphuncular
tissue. Pressure change could perhaps also be sensed by the siphuncular epi-
thelium in terms of the osmotic potential needed to balance hydrostatic pressure.
The rapidity with which Nautilus detects pressure change, however, weighs against
an osmotic mechanism.
Of these two models of Nautilus baroreception, the siphuncular hypothesis
appears to us to be the more reasonable. This is because of the septal formation
process. In preparing to construct a new septum, the body pulls away from the old
septum and moves forward in the body chamber. During this time, baroreceptor
cells aligned along the posterior body surface would not be in contact with a load-
bearing septum, and could not function properly. Thus, a septal mechanism would
operate only intermittently; it would not provide the kind of continuity in depth
monitoring that Nautilus probably requires. A siphuncle-based system would not
suffer this deficiency, and on this ground appears to be the more plausible of our
two proposals.
To our knowledge, possible baroreceptor cells have not been observed in either
the posterior mantle or in the siphuncle of Nautilus, nor for that matter in the
statocyst. However, no-one seems to have looked for them.
We are grateful to the Griffis Foundation, N. Griffis, Director, for supporting
the development of our high-pressure apparatus. We thank M. J. Wells (Univer-
sity of Cambridge) for his advice on cephalopod sensory organs and behaviour,
nd for helping us clarify some of the ideas presented here. We are grateful to
D. Ruggieri, Director of the New York Aquarium, for providing testing
facilities and for his long-standing interest in this project. Other Aquarium188 M. JORDAN, J. A. CHAMBERLAIN AND R. B. CHAMBERLAIN
personnel, particularly Kate McClave and Shelagh Palma, aided in the day-to-day
maintenance of our equipment. Fran Hackett typed the manuscript and Paul
Heyer prepared the figures.
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