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Response of Nautilus to Variation in Ambient Pressure

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Response of Nautilus to Variation in Ambient Pressure 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 lxlO5Nm~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 pressuS levelled off as the actual pressure in the system approached the new setting of the Nautilus 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 2xlO6Nm~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 Ktensity 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 I 3 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, extended Nautilus 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
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