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Telemetered Cephalopod Energetics: Swimming, Soaring, and Blimping1
1 Census of Marine Life, CORE, 1755 Massachusetts Ave., Washington, D.C. 20036
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Cephalopods are uniquely suited to field energetic studies. Their hollow mantles that pump water for respiration and jetting also can accommodate differential transducer-transmitters. These transmitters indicate pressure-flow power output, which can be calibrated against oxygen consumption by swim-tunnel respirometry. Radio-acoustic positioning telemetry (RAPT) records pressure-flow power and animal movements with meter accuracy in nature. Despite inherent inefficiencies, jetting is the primary mode of locomotion for both primitive nautilus and powerful, migratory oceanic squids. In between, large-finned squid and cuttlefish mix jetting with fin undulation in complex gaits that increase locomotor efficiency. Our studies show that the complex nervous systems cephalopods evolved to control mixed gaits are also sensitive to flow and density fields in nature and that they use these to further reduce locomotion costs. Buoyed up by evacuated shells, nautilus and cuttlefish live in boundary layers and navigate cheaply through them like balloonists. Large-finned, negatively buoyant squid soar like eagles in rising currents, but lose control in currents above one body length per second. Many muscular squids have life histories linked to current systems. Neutrally buoyant ammoniacal cephalopods in the mesopelagic are a limiting case in need of study. The small density differential between seawater and isotonic ammonium chloride trebles their volume, making them blimp-like with very low power densities. Some species live entirely in this restricted habitat, but most become ammoniacal late in ontogeny, as they approach semelparous reproduction. Ammonium retained for buoyancy as carbon is terminally mobilized from muscle protein for gametes and energy, compensates for lost muscle power.
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INTRODUCTION |
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The primitive, externally shelled cephalopods, of which Nautilus is the only living example, were essentially defined by their jet propulsion. As in other mollusks, muscles attached to the shell retracted the head, but in cephalopods control systems evolved to turn the displaced water into a powerful jet (Wells and O'Dor, 1991
). The funnel, which directs the water, is a sheet of highly deformable muscular hydrostat composed of helically striated fibers in a three-dimensional array like the fins (Kier, 1989). The divergence and success of modern coleoid cephalopods in a wide array of marine habitats can be viewed as an exploration of how many ways a sheet of muscular hydrostat can move water and how fast and sophisticated the movements of such a sheet can become.
The most obvious example is the mantle, a spherical bag of hydrostat in an octopus and a cylinder closed at one end in a squid. The cephalopods we think of as ‘typical’ are the ones we eat; usually strong jet swimmers with thick, dense muscular mantle pumps that are sliced into squid rings. The early work on cephalopod locomotion focused on jet swimming (Trueman and Packard, 1968; O'Dor, 1982), but later research coupling telemetered measurements of jet pressures with respirometry in swim-tunnels and synchronized video in mesocosms (Webber and O'Dor, 1986; Pörtner et al., 1993) made it clear that cephalopod success was as much about finesse as brute force. Although there is still discussion about how best to calculate the efficiency of cephalopod jet propulsion (Anderson and DeMont, 2000), it is lower than that of fish undulations at comparable sizes and speeds (O'Dor and Webber, 1991). Most cephalopods also have hydrostat sheets organized as fins in a wide range of configurations (Kier, 1989; Hoar et al., 1994). Some can smoothly mix undulating-sheet locomotion with jetting over an amazing spectrum of activities, but others seem more specialized.
A critical specialization in the locomotor spectrum for aquatic animals is buoyancy. Flesh is denser than seawater, and it takes energy for animals to move off bottom. One option is to compensate for dense tissues such as muscle with reservoirs of buoyant material, but energy is required to create these reservoirs. Such floats also increase volume and must be pushed through the high-drag aquatic medium. Neither cephalopods nor fishes that migrate extensively or swim fast can afford the energy costs. Negatively buoyant pelagic animals either create dynamic lift, a relatively energetically inexpensive byproduct of rapid forward swimming (similar to flying) or they soar. Soaring is energetically advantageous whether it is active, as in climb-and-glide swimming that uses a slow, low-drag climb to store potential energy for a long glide (Weihs, 1973; O'Dor, 1988), or passive in currents. There are many ocean habitats where animals can ride upwelling currents just as birds do in air (O'Dor et al., 1994).
Buoyancy in fishes typically comes from gases stored in swim bladders or lipids in livers, but cephalopods rarely use either. The exclusively marine cephalopods began as specialists at evacuating rigid shells osmotically by pumping sodium ions or retaining low-density iso-osmotic ammonium chloride solutions. Neutral buoyancy from a gas bladder increases volume by 6%; a cuttlebone, 9%; lipid or a nautilus shell, 30%; ammonium, 300%. Many cephalopods have vertic ecologies, making extensive use of vertical migrations, both on a daily basis (O'Dor et al., 1993; Webber et al., 2000) and on an ontogenetic one (Vecchione, 1987a; Jackson, 1997). Because of expansion of gas with reduction of pressure, only lipids and ammonium allow extensive, rapid vertical movement. However, while a fighter plane that increased its volume by 30% would still be an airplane, one that increased by 300% would effectively be transformed into a blimp. While pelagic cephalopods may have a spectrum of life styles by mixing jetting and finning, once the transition to a neutrally buoyant blimp is made, it is likely to be irreversible. Thus, the resultant planktonic cephalopods are probably trapped, either evolutionarily or ontogenetically.
The development of radio-acoustic positioning telemetry (RAPT) makes it possible to monitor where marine animals go in nature, by triangulation with a resolution of less than a meter, and what propels them, by telemetering jet pressure. This technique supports earlier evidence that cephalopod lives in nature are much more complex than captive observations suggest (Hanlon and Messenger, 1996). We can now estimate the proportion of an animal's life that it spends at various points on its activity spectrum (O'Dor et al., 1993) and evaluate the importance of various types of locomotion quantitatively in relation to energy consumption. In the past, comparative physiology has often equated what animals can do to what they do, with little justification, particularly in marine systems where observation was limited. In these systems, directly linking performance to practice is a powerful new tool for integrating physiology, ecology and evolutionary change.
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The original version of Figure 1 was published a decade ago in an effort to predict natural behavior of cephalopods from laboratory studies (O'Dor and Webber, 1991
). Jet pressures were recorded in swim-tunnel respirometers at speeds up to the maximum observed for a species and correlated with oxygen consumptions up to the critical (or maximum aerobic) speed (filled circles). Converting the fitted relationships to gross costs of transport (COT) predicted optimum speeds (open circles) to maximize distance traveled for energy consumed or maximum range. The present figure adds typical cruising speeds (stars) for similar species selected from subsequent tracking studies in nature listed in Table 1. These directly confirm steady swimming for periods of several hours. Although maximizing range appears to have overestimated the cruising speeds of cephalopods, it did set reasonable upper limits and helped demonstrate that many cephalopods have life histories based on virtually continuous migrations and produce multiple micro-cohorts each year (Boyle and Boletzky, 1996).
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The original question was, "Why is locomotion so much more costly for cephalopods than fishes?" The more refined question now is, "Why are the estimates higher than the reality (Bartol et al., 2001a,
b)?" Nautilus is the exception in both cases; it actually swims more cheaply than fishes at very low speeds, and it maintains speeds close to the predicted optima. However, its speeds are very low. In fact, neutrally buoyant Nautilus use tentacles to stick themselves to surfaces the way astronauts in microgravity use Velcro to prevent themselves from drifting around in their sleep. Nautilus do sleep, or at least go torporous, and, if their tentacles release, they move around tanks at speeds almost as high as the optimum—just from breathing. At low speeds and low pressures their jets can be quite efficient, and Nautilus are pure jetters, with no fins to confuse the results. This is an important consideration because mixed fin and jet locomotion seems to have set gaits that work efficiently and are chosen by cephalopods in nature (Hoar et al., 1994; Bartol et al., 2001a, b). Unlike salmon that seem basically to have evolved to swim in tunnels at variable speeds, many cephalopods seem awkward in swim-tunnels and, in nature, they seek out microhabitats where current velocities are matched to their most efficient gaits (O'Dor et al., 2002). Figure 1 also illustrates a tradeoff between decreasing fin length, increasing speed and increasing energy cost. In open water, short-finned ommastrephid squids like Illex manage about 50% of the optimum and loliginids with long, thick fins like Loligo and Sepioteuthis, about 40%, but cuttlefish with thin fringing fins are below 20%. Thus, the field data reinforce the laboratory conclusion that fins lower swimming costs, but reduce swimming speeds. We have made mechanistic speculations that the low speeds at which cephalopod fins cease to function effectively relate to limiting muscle contraction speeds and the absence of rigid bone to amplify speed, but let us look at reality.
Cuttlefish
Figure 2A shows a track of a mature female giant cuttlefish Sepia apama on the breeding grounds at Whyalla, South Australia (Hall and Hanlon, 2002), as the direct readout on the computer screen in the field from a VEMCO Ltd. (www.vemco.com) RAPT system using VRAP 4.08 software (O'Dor et al., 1998). Radio buoys at the positions and distances indicated by letters, continuously triangulated positions as the animal moved steadily away from the array, never to return (O'Dor et al., 2001). The buoys also collected jet pressure records in 60 sec blocks as shown in Figure 2B. The speeds calculated between the numbered points were 0.041 m sec–1 for 161 m between points 1 and 2, in the first 66 min and 0.035 m sec–1 for 125 m between 2 and 3, in 59 min, giving a relatively steady average of 0.038 m sec–1 over 2 hr. Figure 2B, from midway between points 1 and 2, is typical of jet pressure records for cruising at about 0.05 m sec–1, with an average pressure of 0.07 kPa. This pressure is only slightly above the average pressure during quiet resting, suggesting that the situation for this neutrally buoyant cuttlefish is like that for Nautilus. With no requirement for dynamic lift, respiration produces locomotion, and, in this case, is synergistic with the undulating fins.
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Although this speed is far below optimal in purely locomotor terms, it may be beneficial for crypsis, seeking mates, predator avoidance and/or hunting. The concept of an optimal speed is not realistic unless travel and fuel economy are the only considerations. Refueling can dramatically alter the assumptions. In this case, cuttlefish appear to travel to Whyalla from all over Spencer Gulf for a terminal spawning event at an age of about 18 months. At 0.05 m sec–1, a typical 250 km migration would take about 2 months of continuous swimming, not unreasonable for a one-way trip that is built into a life history strategy.
Reef squid
The RAPT studies of Australian cephalopods also included Sepioteuthis australis, a loliginid reef squid with fins running the full length of its mantle, but wider and more muscular than those of cuttlefish. Tracks of a 0.7 kg squid from the Lincoln Marine Science Centre in Port Lincoln, South Australia, showed it covering almost 1.5 km in 3 hr averaging, equivalent to 0.15 m sec–1 (O'Dor et al., 2002). However, in the detailed analysis in Figure 3, we estimated that this speed was the complex result of a swimming speed of 0.17 m sec–1 based on jet pressure, a northward current of 0.075 m sec–1 and a trajectory that crisscrossed the current. Although the ocean is far from being a simple tank of static water, this speed is similar to the long-term averages (0.14–0.18 m sec–1) for Loligo vulgaris reynaudii monitored as they circled egg beds in South Africa (Sauer et al., 1997).
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In fact, the behavior of the large Sepioteuthis australis above was exceptional. Most of the smaller squids tracked moved very little over periods of up to 19 days, but remained associated with the rocky House Reef. This behavior is similar to that seen on a larger scale in Loligo forbesi in the Azores (O'Dor et al., 1994
) and supports the concept of large-finned squids as soarers. The precision of the RAPT system revealed that squid holding position on House Reef moved consistently with the tidal cycle, presumably positioning themselves to hang in currents being pushed up over the reef. This behavior would allow negatively buoyant squid to stay up in the water column with minimal effort and observe prey being swept toward them, like birds of prey near cliffs.
Ammoniacal squid
Observations on the neutrally buoyant ammoniacal cephalopods of the mesopelagic zone are rare and based on submarine or ROV observations that are typically brief (Roper and Vecchione, 1997; Veccione et al., 2001). There are probably still many species that have never been sampled, let alone observed, and almost none with well-characterized behaviors. A few have been observed in captivity (Seibel et al., 1998), some that have had their metabolic rates measured and more have had their metabolism characterized biochemically (Seibel et al., 1997). All that have been studied have lower metabolic rates and biochemical capacity than the surface dwellers that have been studied in nature. Based on the locomotor limitations of blimping volumes up by 300% (Webber et al., 2000), it seems likely that these animals are either concentrating in areas where currents are minimal or are drifting in currents (Vecchione, 1987b). Even the relatively powerful surface forms appear to be overwhelmed by currents on the order of one mantle length per second (O'Dor et al., 2002).
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Telemetric approaches for examining the in situ behavior and energetics of shallow water cephalopods are now well developed, although still expensive and technically demanding. A major limitation is the size of the present generation of differential pressure tags, which can only be used in animals weighing over 400 g. Smaller tags are technically feasible that would lower this to 40 g, but it would take a significant increase in demand to justify developing these. This would increase the number of species available for study at least ten-fold and allow studies of earlier life stages when growth and feeding rates are higher. It takes coordinated efforts by scientists to drive technology development, so make a plan to track your favorite species!
Understanding the long-term behavior of the ammoniacal mesopelagic cephalopods is important ecologically because they transfer energy from lower trophic levels, as it passively sinks, to higher ones that actively move the energy and nutrients back to the surface. Estimates of the global biomass of such cephalopods required to sustain sperm whale populations (Clarke, 1996) indicate that cephalopod production must have exceeded fish production historically, and recent catch records suggest that over-fishing globally (Pauly et al., 1998) may have shifted the balance even further towards cephalopods (Caddy and Rodhouse, 1998). As our understanding of large marine predators increases, the critical role of concentrations of mesopelagic cephalopods in the lives of such species as elephant seals (Costa, 1993; Boehlert et al., 2001), billfishes (Carey and Robison, 1981) and tuna (Block et al., 2001) is becoming clear.
The Census of Marine Life (CoML; www.coml.org) project, Tracking of Pacific Pelagics (TOPP), uses a range of sophisticated new electronic tags to examine this type of interaction for multi-species, multi-trophic level systems in the open ocean. Although most of the project focuses on top predators that are large enough to carry satellite telemetry devices, squid have been included as the lowest trophic level that can be studied with existing technology. A feasibility study in the Sea of Cortez with the "jumbo squid," Dosidicus gigas, has shown that these large "killer" squid can carry both traditional acoustic telemetry transmitters and pop-up satellite archival tags (PSAT). This species is a major prey item for sperm whales in the Sea of Cortez, but whales displace their feeding to other species when jumbo squid abundance declines (Jaquet and Gendron, 2002). Jumbo squid are a negatively buoyant muscular type that makes extensive vertical migrations (Yatsu et al., 1999) and are taken in commercial fisheries, but, at present, we know almost nothing about the activities of the squids that are the likely alternate prey. In fact, Vecchione et al. (2001) indicate that we have not even identified many of the inhabitants of these depths, much less characterized their behaviors. As indicated earlier, a few minutes of video may give us an idea of what animals can do, but it takes days or weeks of continuous observation to understand what they do do—how they budget their time.
Not all of the technologies that work to understand the natural behaviors of cephalopods near the surface are applicable to those in the deep, and not all of those used to study fishes in the deep will work for cephalopods. One unique approach to studying deep-sea fishes lowers a platform with a video camera, a rotating acoustic transmitter-receiver and transponder tags hidden in bait (Collins et al., 1998). The fish are videotaped as they swallow the bait and then tracked in polar coordinates by recording the direction the transmitter is pointing and the time for the tag to reply to each signal. This provides a continuous record of each fish's position to the range limit of the tags for long periods, similar to that provided by RAPT. This technology would work equally well for cephalopods, except for the fact that, unlike fishes that are able to swallow prey whole, cephalopod esophaguses pass through the middle of their brains. Only a giant squid could swallow a finger-sized transponder tag without chopping it up! However, as their buoyancy systems discussed earlier do not involve swimbladders, cephalopods can be brought to the surface without exploding (Seibel et al., 1997), and it is possible to tag them at the surface and release them again at depth (O'Dor et al., 1993). Approached this way, a bottom-resident transponder system would work equally well for cephalopods.
High spatial resolution tracking in mid-ocean/mid-water is, however, still a challenge. Resolution of fixed triangulating systems from either the surface or the bottom would be limited by the long baselines required to calculate positions thousands of meters from surface or bottom. Resolution of rotating systems at mid-water depths would be limited by the accuracy with which the transmitter/receiver could be positioned. A combination of acoustic telemetry and new acoustic imaging technology may allow us to study the behaviors of blimping cephalopods in situ, at the same time we view and track their large vertebrate predators.
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ACKNOWLEDGMENTS |
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Thanks to the Australian Research Council for the grant to George Jackson, University of Tasmania, that supported the efforts of Jill Aitken, Yanko Andrade and Julian Finn, who collected and analyzed much of the data reviewed here, as well as the Natural Sciences and Engineering Research Council of Canada for ongoing support of RAPT development.
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1 From the Symposium Dynamics and Energetics of Animal Swimming and Flying presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 2–6 January 2002, at Anaheim, California.
2 E-mail: rodor{at}coreocean.org
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