Aerobic respiratory costs of swimming in the negatively buoyant brief squid Lolliguncula brevis
1 Department of Organismic Biology, Ecology, and Evolution, 621 Charles E. Young Drive South, University of California, Los Angeles, CA 90095-1606, USA and
2 School of Marine Science, Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA 23062-1346, USA
*e-mail: ikbartol{at}lifesci.ucla.edu
Accepted August 6, 2001
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Summary |
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Key words: squid, respiration, power, negative buoyancy, swimming, Lolliguncula brevis, locomotion.
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Introduction |
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The assumption that all squid, the most mobile of the cephalopods, are not competitive with fishes because of the inefficiency of jet propulsion may be too simplistic. Squid, like fishes, are diverse and have evolved many behavioral and physiological mechanisms that allow them to compete in a variety of environments. One species, the brief squid Lolliguncula brevis, is particularly distinctive from the squid Loligo opalescens and Illex illecebrosus considered in previous studies. Brief squid have small rounded bodies, large rounded fins, heavily keeled third (III) arms, and may live in shallow, complex, temporally variable environments (Hixon, 1980; Bartol et al., 2001a). Conversely, Loligo opalescens and Illex illecebrosus are larger, more elongate and pelagic (Hixon, 1980; Hixon, 1983; ODor, 1983; Hanlon and Messenger, 1996). Brief squid swim at low speeds, at which the costs of jet propulsion are reduced, and they use significant fin movement, avoiding the volume limitations of jet propulsion. Thus, the inherent inefficiencies of jet propulsion may not be as pronounced for L. brevis. Loligo opalescens and Illex illecebrosus swim at moderate to high speeds and use their fins primarily for steering and maneuvering (ODor, 1988a; Hoar et al., 1994). L. brevis is also the only cephalopod to invade the inshore, euryhaline waters of the Chesapeake Bay, where it is abundant [ranking in the upper 10 % of annual nektonic trawl catches (Bartol et al., 2001a)] and competes as a predator with bay fauna that number in the hundreds of species.
Aside from jet propulsion, squid are distinct from many pelagic nekton because they are often negatively buoyant. Birds, which are negatively buoyant in air, expend considerable energy staying aloft at low speeds, when lift forces are minimal, and overcoming drag forces at high speeds (drag increases exponentially with speed). Oxygen consumption/power is low at intermediate speeds when lift forces are greater than at low speeds because of increased flow over the body and wings and when drag forces are less important than at high speeds. The resulting O2 consumption/power versus speed curve is U-shaped [see Tucker (Tucker, 1968; Tucker, 1973) and Pennycuick (Pennycuick, 1968; Pennycuick, 1989)]. A similar relationship may exist in negatively buoyant squid because they also presumably have high lift generation costs at low speeds and substantial drag costs at high speeds. Parabolic power versus speed relationships have been detected in the negatively buoyant mandarin fish Synchiropus picturatus (Blake, 1979a). No such relationship has been observed previously in squid, but low speeds (110 cm s1), speeds frequently used by brief squid and when lift generation costs are highest, have not yet been examined.
L. brevis is morphologically, ecologically and physiologically unlike many cephalopods, especially those considered in previous comparisons between squid and fishes, and may swim differently. The reliance of brief squid on fin motion and their preference for low-speed swimming may minimize the inefficiencies of jet propulsion and therefore reduce the costs of swimming. Moreover, negative buoyancy and the costs associated with maintaining vertical position in the water column may influence the relationship between O2 consumption/power and speed, such that costs are lower at intermediate speeds than at high or low speeds. Brief squid that swim at these intermediate speeds may be more competitive with fish than is presently thought. Therefore, O2 consumption rates and power estimates for L. brevis of various sizes swimming over a continuum of speeds were measured (i) to characterize the O2 consumption/power versus speed relationship and (ii) to compare their energetics with those of other ecologically comparable nekton.
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Materials and methods |
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O2 consumption measurements
Two separate swim tunnel respirometers, one with a capacity of 15.6 l and the other with a capacity of 3.8 l, were used. Within each swim tunnel respirometer, flow velocity was controlled using two propellers attached to a stainless-steel shaft in a rotor-stator configuration driven by a 187 W (0.25 horse power) variable-speed motor with a belt and pulleys. To keep the water temperature as constant as possible within the respirometer and to facilitate the removal of air bubbles, each of the tunnels was completely submerged in a 378 l aquarium filled with aerated sea water. During the experiments, water from within the respirometers was pumped to a submerged microcell using a peristaltic pump, and dissolved O2 levels were measured using a Strathkelvin 1302 O2 electrode and Strathkelvin 78 L O2 meter. Electrode output was expressed as percentage O2 saturation and recorded continuously over the speed trials using a Kipp and Zonen BD 41 strip chart recorder.
Lolliguncula brevis shorter than 4 cm in DML were examined in the 3.8 l respirometer, and L. brevis 4 cm or more in DML were tested in the 15.6 l respirometer. Each squid was placed in the respirometer and allowed to acclimate for 40 min. Flow was set at 3 cm s1 during the initial 10 min and final 20 min of the acclimation period. During an interim 10 min period, flow speeds were gradually elevated to 1821 cm s1 to allow the squid to acclimate to higher flow speeds. The 40 min acclimation/training period was selected on the basis of recovery times from exercise and stress, which are extremely short in squid (Pörtner et al., 1993), and acclimation periods used for L. brevis in other studies (Finke et al., 1996; Zielinski et al., 2000). After the 40 min adjustment period, the respirometer lid was closed, O2 levels were recorded for 15 min while the squid swam at 3 cm s1, and the respirometer was then opened, allowing water from the surrounding waterbath to enter the respirometer. This flushing procedure was carried out for 10 min to ensure that fresh, oxygenated water was present in the system for the next trial. This procedure was repeated for speeds of 6, 9, 12, 15, 18, 21, 24, 27 and 30 cm s1 or until the squid could no longer keep pace with flow velocity. Because of high behavioral variation and high O2 consumption rates at the lowest speed tested, repeat measurements at 3 cm s1 were periodically performed following an intermediate speed (912 cm s1) flushing period. When low-speed O2 consumption rates measured at the beginning and at an intermediate stage in the trial differed significantly, the trial was terminated.
During each trial, swimming behavior was recorded using a Sony Hi-8 video camera. After the final trial, each squid was measured (DML) (±0.1 cm) and weighed (±0.01 g), and blanks were run to correct for bacterial O2 consumption, electrode drift and/or the endogenous O2 consumption of the electrode. Rates of O2 consumption were determined from the slope of percentage O2 saturation versus time curves (corrected for background components and/or electrode drift) recorded over the final 10 min period of each speed range. Mean water temperature and salinity for this study were 24.5±2.0°C and 29.2±5.6 (means ± S.E.M.), respectively.
Video analysis
Portions of the video footage were analyzed on a Peak Motus v.3.0 motion measurement system (Peak Performance Technologies, Englewood, CO, USA) to account for some of the variability in swimming behavior. For all squid tested, two representative minutes of footage at each speed were examined. Mantle angle (±1°), arm angle (±1°) and the distance from the eye to the respirometer floor (±0.1 cm) were recorded every second within the 2 min video sequence. Changes in position along the axis parallel to flow and the number of fin beats per second were also recorded. For all squid, the mean overall body angle of attack (which was simply the mean of the mantle and arm angles), the mean distance from the bottom of the respirometer, the mean number of fin beats per second and the mean horizontal change in position during each 2 min video sequence were computed. Using an acoustic Doppler velocimeter (Son-Tek, Inc., San Diego, CA, USA), bottom flow profiles were recorded in each swim tunnel for the range of speeds considered in this study. These measurements were used in conjunction with mean height above the bottom and mean horizontal change in position to calculate actual swimming velocities. A few squid exceeded 10 % of the cross-sectional area of the tunnel; speed adjustments were made for these squid to account for blocking effects (Webb, 1975).
Statistical procedures
Polynomial regression analysis was performed both on data pooled by size class (size classes: 2.93.9, 4.04.9, 5.05.9, 6.06.9, 7.07.9 and 8.08.9 cm DML) and on data collected for individual squid. Regression analysis involved fitting the data initially to a linear regression and subsequently to higher-degree polynomial regressions when additional terms significantly improved the accuracy of the prediction of dependent values (Zar, 1984; Sokal and Rohlf, 1981). Unfortunately, regression analyses performed on pooled data did little to characterize the nature of patterns apparent in scatter plots for individual squid. This was because high variability among individuals masked underlying relationships. Furthermore, when the data were analyzed separately for each squid, the limited number of data points precluded the consistent detection of significant linear or curvilinear relationships.
Because of this high variation among individual squid, an additional procedure was employed to determine whether a significant parabolic relationship existed between O2 consumption rates and speed, i.e. were O2 consumption rates at intermediate speeds lower than those at low and high speeds? For each squid tested, the data were divided into three speed ranges: <0.5 DML s1, 0.51.5 DML s1 and >1.5 DML s1. A speed of 0.5 DML s1 was a logical low-end cut-off because the squid demonstrated greater lateral variation about a given point at speeds below 0.5 DML s1 (mean lateral deviation 4.16±4.53 cm, mean ± S.D., N=19) compared with speeds of 0.5 DML s1 or above (mean lateral deviation 1.78±1.67 cm, mean ± S.D., N=19). A speed of 1.5 DML s1 was a reasonable high-end cut-off because anaerobic end products may begin to accumulate in L. brevis at speeds above 1.5 DML s1 (Finke et al., 1996). Mean O2 consumption rates were calculated for each speed range for each squid tested, and a randomized-block analysis of variance (ANOVA), treating each squid as a block, was used to determine whether there was an overall significant difference in O2 consumption rate for the three speed ranges. A randomized-block ANOVA (also called an ANOVA with repeated measures) was used because repeated measurements (O2 consumption rates) were collected from the same squid over time and blocking subjects helped account for variation among squid. Level differences were determined using NewmanKeuls multiple-comparison tests for randomized-block ANOVAs (Zar, 1984).
Mean wet masses and mean mass-specific O2 consumption rates for the three speed ranges were calculated for the six size classes. To characterize the metabolic scaling relationship in brief squid, a power-law regression of mean mass-specific O2 consumption rates pooled across the three speed ranges versus mean wet masses for the six size classes was performed. (Data from the three speed ranges were pooled because there was little difference in power-law relationships among the speed ranges.) The power-law function was defined as:
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where R is mass-specific rate of O2 consumption, a is the mass coefficient, M is wet mass and b is the mass exponent.
Power and efficiency calculations
Power curves for two Lolligunucla brevis, one measuring 4.4 cm in DML and the other measuring 7.6 cm in DML, were generated to determine the nature of the hydrodynamic power/speed relationship. The power curves were based on kinematic and force data presented in the companion manuscript published in this volume (Bartol et al., 2001b), to which we refer the reader for detailed descriptions of the forces discussed below. Five power terms were calculated: (i) induced power, the power required by the fins to generate lift to keep the squid up in the water column; (ii) vertical jet power, the power needed by the jet to generate lift to keep the squid up in the water column; (iii) parasite/profile power, the power required to overcome pressure and friction drag on the fins, body and arms; (iv) refilling power, the power required to overcome mantle refilling forces; and (v) total power, the sum of the above power terms. Induced power (W) was computed by multiplying predicted vertical fin thrust (N) by induced velocity (m s1), the only term in this section not described in Bartol et al. (Bartol et al., 2001b). Induced velocity, which is the velocity of fluid passing through an area swept out by the fins (Pennycuick, 1972; Blake, 1979b; Norberg, 1990), was determined by high-speed (250 frames s1) videotaping of the two squid swimming in a flume seeded with brine shrimp eggs (see Bartol et al., 2001b) and measuring fin flapping speeds and particle trajectories underneath the fins during downstrokes. At low speeds, the vertical components of fin flapping speed and particle speed were reasonably consistent, but at higher speeds the vertical speed component of particle trajectories was much lower than that of the fins because translational flow had a large effect on induced velocity. Consequently, only particle trajectories were used to determine induced velocity at speeds above 6 cm s1. More precise methods of measuring induced power, which are based on vortex theory and circulation measurements [see Rayner (Rayner, 1979), Spedding (Spedding, 1987) and Norberg (Norberg, 1990)], were beyond the scope of this project. Moreover, induced power estimates using RankineFroude axial momentum jet theory are known significantly to underestimate induced power at low speeds because non-steady effects are not considered (Norberg, 1990). Vertical jet power (W) was the product of vertical jet thrust (N) and the vertical component of jet speed (m s1), parasite/profile power (W) was the product of total drag (N) on the body, fins and arms and swimming speed (m s1), and refilling power (W) was the product of refilling force (N) and swimming speed (m s1).
Using power estimates from a 4.4 and 7.6 cm DML squid and O2 consumption rates from a 4.5 and 7.5 cm DML squid, respectively, aerobic efficiencies (Na) were calculated for a range of speeds. Aerobic efficiency was defined as the ratio of the power required to move the squid through the water [i.e. power output, which is simply total power (W) calculated as above divided by wet mass (kg)] to the aerobically supplied power (i.e. power input, which is based on active metabolic rate). Active metabolic rate (ml O2 kg1 h1) was converted to power input using the common assumption that 1 ml of O2 yields 20 J and multiplying by 1/3600 s to arrive at J s1 kg1 (W kg1). For aerobic efficiency comparisons with other cephalopods, it was necessary to generate gross cost of transport (COT) curves and to determine Umr (the speed of maximum range), which is the minimum of the COT curve. For hydrodynamic estimates of COT (J kg1 m1), power output (W kg1) calculated as above was divided by speed (m s1). For aerobic estimates of COT, power input (W kg1) calculated as above was divided by speed (m s1).
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Results |
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For all size classes, there was a clear decline in mean angle of attack and number of fin beats per second with increased swimming velocity (Fig. 1, Fig. 2). Most squid tested were capable of detecting areas of lower flow within the tunnel respirometer and consistently swam at speeds lower than the target velocity. Moreover, several behaviors were employed by some to aid swimming and presumably to reduce swimming costs. A number of squid remained on the tunnel floor either in a horizontal orientation, with the body and appendages aligned parallel to flow, or in an inverted V-posture, with the tips of the mantle and arms touching the tunnel floor and the head projected upwards. Since these squid were in contact with the bottom, they were not actually swimming. Other squid frequently pushed off the bottom and/or downstream collimator with their arms during trials to assist locomotion. Some squid even swam with their body and fin pressed against the respirometer side wall to exploit low flows near the wall and to help maintain horizontal and vertical position. These behaviors were most prevalent during low- and high-speed trials when squid had the most difficulty matching free-stream flow.
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Rates of O2 consumption
Partial (J-shaped) or full (U-shaped) parabolic patterns of O2 consumption rate as a function of speed were observed for many squid with measurements from all three speed ranges (<0.5 DML s1, 0.51.5 DML s1, >1.5 DML s1) (Fig. 3). Mean O2 consumption rates for the three speed ranges (a, b and c, respectively) for each of the cooperative squid tested are included in Fig. 3. A randomized-block ANOVA performed on these mean data indicated that there was a significant difference among the three speed ranges (Table 1). Subsequent NewmanKeuls multiple-comparison tests revealed that O2 consumption rates were lowest at intermediate speeds (0.51.5 DML s1, b) and highest at the highest speeds (>1.5 DML s1, c).
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Discussion |
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Lift generation and stability control at low speeds
The high rates of O2 consumption of L. brevis at low speeds are largely because of induced power and vertical jet power demands. During hovering and at low speeds, little momentum is directed downwards as a result of the forward motion of the squid, and lift forces, which scale with the square of velocity, are low. Consequently, to generate the necessary downward momentum to counteract negative buoyancy (negative buoyancy is approximately 3.44.0 % in brief squid), L. brevis flaps its fins progressively faster and at higher amplitudes as speed decreases (Bartol et al., 2001b), a phenomenon also observed in birds and fish (Norberg, 1990; Blake, 1979b; Webb, 1974). The downwash of water produced by the fins (of finite length) alters the pressure distribution so that the lift vector increases, but the resultant vector also tilts backwards. The power required to overcome this rearward component of the resultant force vector (induced drag) is costly at low speeds when large downward deflections are necessary (Vogel, 1994; Dickinson, 1996). In L. brevis, some of the downward momentum at low speeds is also generated by the jet, which is directed more vertically at such speeds (Bartol et al., 2001b). Directing the jet vertically is energetically costly because water has to be expelled at high velocity both to keep the squid aloft and for it to swim horizontally. The power drains of the fins (induced power) and jet (vertical jet power) were clearly apparent in the power curves. The observed increase in vertical jet power at high speeds was an interesting artifact of a greater dependence on the jet for vertical thrust as fin activity decreased and higher jet velocities at higher speeds.
Profile, parasite and inertial power demands made up a smaller component of the observed low-speed rate of O2 consumption. To generate greater lift, the fins and third (III) arms with heavy keels, which resemble traditional human-made lift-generating airfoils, as well as the mantle, head and remaining arms were positioned at high angles of attack. Both the fins and third (III) arms were extended laterally at low speeds, while the body of the squid was positioned at high angles of attack, forcing water to move faster over their upper surfaces, increasing the pressure differential above and below the biofoils and, consequently, increasing lift. Similarly, negatively buoyant elasmobranchs, tuna and mackerel increase pectoral fin area and/or angle of attack at low speeds to increase lift (Magnuson, 1978; Bone and Marshall, 1982; He and Wardle, 1986). Although the mantle, head and remaining arms (i.e. the body) do not resemble traditional airfoils/biofoils, they too generate lift when positioned at high angles of attack (Bartol et al., 2001b). Body lift plays a critical role in lift generation in ski jumpers (Ward-Smith and Clements, 1982), honeybees (Nachtigall and Hanauer-Thieser, 1992), birds (Tobalske and Dial, 1996) and negatively buoyant fish (He and Wardle, 1986; Heine, 1992). Positioning various body appendages at high angles of attack increases pressure drag, which results from flow separation from the surface of the animal, and friction drag, which results from viscous shearing stresses in the boundary layer, on the fins and body.
Even with added drag forces from high angles of attack, parasite power, the work required to overcome pressure and friction drag on the body, is small at speeds below 0.5 DML s1 because forward swimming speed is so low. Profile power, the work required to overcome pressure and friction drag on the fins, is affected by high fin flapping speed and induced velocity at low speeds and, consequently, contributes more to energetic costs at such speeds. However, relative to induced and vertical jet power, profile power demands are low, as in birds (Pennycuick, 1972). Inertial power, the rate of work needed to accelerate the fins at each stroke, may also add some cost to swimming at low speeds, when stroke amplitudes, stroke twisting and unsteady effects are high (Norberg, 1990). Inertial power was not considered in this study, but was probably considerably lower than induced and vertical jet power at low speeds given that Norberg (Norberg, 1976) found inertial power to be approximately 2 % of total aerodynamic power at low speeds in bats.
In addition to high power costs, high fin activity and amplitude and high angles of attack at low speeds, further evidence that lift generation is a critical and energetically costly component of low-speed O2 consumption may be found in the respiratory costs of uncooperative squid. Squid that remained on the bottom or that consistently pushed off the bottom generally did not have high costs at low speeds like free-swimming squid. These organisms had linear rather than parabolic O2 consumption curves.
Positioning the body and appendages at high angles of attack and actively moving the fins are critical not only for lift generation at low speeds but also for stability control. High angles of attack increase drag, requiring the propulsors (i.e. the fins) to beat more rapidly to provide greater thrust. This increased thrust is better matched to body inertia, a force that can provide significant resistance to the return of aquatic organisms to desired paths at low speeds and, thus, provides greater stability control (Webb, 1993; Webb, 2000). High body/arm angles of attack coupled with active fins at low speeds for purposes of stability control have also been observed in neutrally buoyant fishes, such as trout and bluegill (Webb, 1993).
Drag costs at high speeds
Drag forces scale approximately with the square of velocity just like lift, which explains the observed exponential increase in profile and parasite power as speed increased. In squid, the power required to refill the mantle also increases exponentially with speed, as it becomes necessary to accelerate greater volumes of water at higher speeds to fill the mantle. Therefore, exponential increases in rates of O2 consumption with speed were expected, as have been widely reported in fish (Brett, 1965; Webb, 1973; Blake, 1983; Dewar and Graham, 1994) and squid (ODor, 1982; Webber and ODor, 1986). In the present study, exponential increases in rates of O2 consumption were not always apparent, even at speeds above 0.5 DML s1. Anaerobic metabolism, which may begin as early as 1.52.0 DML s1 and account for 14.4 and 21.9 % of the energy required for swimming at 2.5 and 3.5 DML s1, respectively (Finke et al., 1996), may be responsible for the lack of exponential relationships. Even with anaerobic recruitment, sizable lift generation costs at low speeds and considerable drag costs at high speeds allowed for the development of O2 consumption minima at speeds between 0.5 and 1.5 DML s1.
O2 consumption minima and behaviors that reduce costs of locomotion
A minimum O2 consumption speed range (Umin) of 0.51.5 DML s1 and a minimum power speed range (Ump) of 1.21.7 DML s1 are strong evidence that squid can swim the longest on a given amount of fuel at intermediate speeds. The slight discrepancy in values is not surprising given that O2 consumption rates did not incorporate anaerobic costs and power estimates did not account for unsteady lift and propulsive mechanisms (Bartol et al., 2001b). Oxygen and power minima at intermediate speeds are reasonable given the lift, stability and drag demands described above. At intermediate speeds, less of a downward deflection of fluid is required to balance the buoyant weight because the fins, body and arms come in contact with more water per unit time, and thrust forces are better matched to body inertia than at low speeds. Therefore, the fins and jet can be used more for forward propulsion and less for lift generation and stability control, thus reducing swimming costs. Furthermore, because swimming speed and concomitant drag are not high at intermediate speeds, profile/parasite drag costs are not expensive compared with high speeds.
Given that swimming costs are lowest at intermediate speeds, negatively buoyant squid such as L. brevis should spend more time swimming at intermediate speeds than hovering. Observations of negatively buoyant Loligo forbesi in nature reveal that it seeks out current speeds close to the optimal speeds detected in this study and holds position against the current while swimming (ODor et al., 2001). In flow-through tanks in the laboratory, many brief squid tended to congregate near tank intakes in areas of low/moderate flow or swam continuously, which is also consistent with the prediction above. However, squid were also frequently observed away from intakes hovering arms-first with their arms oriented in front of the body at low angles of attack (often in a conical arrangement), while their mantles were positioned near the tank floor at high angles of attack. In this posture, fin flapping was often employed. This behavior is of interest because several squid that did not demonstrate parabolic O2 consumption curves swam near the bottom in a similar manner at low speeds. Blake (Blake, 1979a) determined that negatively buoyant fish reduce induced power costs from 30 to 60 % by positioning themselves near the bottom and exploiting ground effects. Thus, brief squid positioned near the bottom in this arms-first posture may have been taking advantage of similar effects to lower overall low-speed metabolic costs. In nature, negatively buoyant Loligo forbesi and Sepioteuthis australis appear to use climb and glide behaviors and upwelling regions to reduce the large metabolic costs associated with counteracting negative buoyancy (ODor et al., 1994; Webber et al., 2000).
Metabolic allometry
The relationship between organism mass (M) and metabolic rate (R) is frequently described by a power-law function R=aMb, where a is the mass coefficient and b is the mass exponent (Schmidt-Nielsen, 1997). This relationship is not well understood in most cephalopods, and the scaling data that are available are quite variable. The mass-specific exponent (i.e. b when metabolic rates are expressed per unit mass) for L. brevis in this study was 0.24, which is within the range of that measured in other aquatic invertebrates and algae [mass-specific b ranges from 0.53 to +0.28 (Patterson, 1992)]. This mass-specific exponent is also consistent with that reported by ODor and Webber (ODor and Webber, 1986) for Illex illecebrosus (b=0.25 to 0.27) and by Seibel et al. (Seibel et al., 1997) for Vampyroteuthis infernalis (b=0.30), Japatella diaphana (b=0.27) and Histioteuthis heteropsis (b=0.20). However, less concordance has been found in other metabolic studies on cephalopods. Manginnis and Wells (Manginnis and Wells, 1969) determined that mass-specific b was 0.17 for Octopus cyanea; Johansen et al. (Johansen et al., 1982) reported a mass-specific b between 0.23 and 0.01 for Sepia officinalis; Macy (Macy, 1980) found b to be between 0.56 and +0.28 for Loligo pealei; and Segawa and Hanlon (Segawa and Hanlon, 1988) determined a mass-specific b of 0.10 for Octopus maya, 0.09 for Lolliguncula brevis and 0.15 for Loligo forbesi. The wide range of mass-specific exponents among the various cephalopods is probably a product of inter- and intra-species behavioral variation during experimentation, which was frequently reported.
The O2 consumption rates recorded in this study are in reasonable agreement with those reported previously for L. brevis. Segawa and Hanlon (Segawa and Hanlon, 1988) placed L. brevis in 24 l bottles for 0.31.3 h, and determined that O2 consumption rates of brief squid hovering in the middle or near/on the bottom of bottles ranged from 24.4 µmol h1 g1 for a 39.98 g squid to 28.4 µmol h1 g1 for a 2.00 g squid. Wells et al. (Wells et al., 1988) measured O2 uptake of L. brevis hovering in 2 l jars over a wide range of temperatures, and reported that mean O2 consumption rates of brief squid (mean mass 9.2110.78 g) varied from 24.3 µmol h1 g1 at 20°C to 34.1 µmol h1 g1 at 2730°C (Q10=1.47).
Wells et al. (Wells et al., 1988) and Finke et al. (Finke et al., 1996) provided limited data on O2 consumption rates of L. brevis during swimming. Wells et al. (Wells et al., 1988) measured O2 extraction by five L. brevis at two swimming speeds, 9.5 and 16 cm s1. Unfortunately, only extraction percentages were presented and, without knowledge of the tunnel dimensions and trial duration, swimming O2 consumption rates could not be calculated in µmol O2 h1 g1 for comparative purposes. Finke et al. (Finke et al., 1996) measured O2 consumption rates of four L. brevis (11.915.1 g) during swimming that increased from 21 µmol O2 h1 g1 at 0.5 DML s1 to 36 µmol O2 h1 g1 at 2.9 DML s1. These values, which were measured at 2022°C, are similar to those recorded in the present study for squid of similar size at 24°C (see Table 2). No parabolic relationship was detected by Finke et al. (Finke et al., 1996), but no speeds lower than 0.5 DML s1, speeds at which lift generation is especially costly, were considered. Interestingly, Finke et al. (Finke et al., 1996) discovered that the pressure of mantle contractions actually falls in some brief squid between speeds of 0.5 and 1.1 DML s1 and attributed this to a reduction in lift requirements.
Anaerobic metabolism
In the present study, L. brevis was capable of sustained speeds as high as 27 cm s1 for 15 min, which is slightly higher than the upper aerobic limit (22.3 cm s1) measured by Finke et al. (Finke et al., 1996) for L. brevis (11.915.1 g), but anaerobic metabolism may be used at much lower speeds. Finke et al. (Finke et al., 1996) determined that anaerobic metabolism contributes to energy production in L. brevis beginning at speeds of 1.52.0 DML s1 by measuring -glycerophosphate, succinate and octopine accumulation in the mantle tissue. This finding, coupled with the small factorial scope of aerobic metabolism recorded in this study (1.201.64), suggests that brief squid are adapted for low-speed swimming. Consequently, it is possible that anaerobic metabolism during the 10 min training period, when speeds briefly approached 1821 cm s1, may have produced an O2 debt that elevated O2 consumption rates during low-speed trials. This is unlikely, however. L. brevis does not accumulate large O2 debts, recovers quickly from anaerobic metabolism and returns to pretrial respiratory rates even after extreme exhaustion within 20 min, the length of the recovery period after training in the present study (ODor, 1982; ODor and Webber, 1986; Pörtner et al., 1993). Moreover, squid that had significantly higher low-speed O2 consumption rates at the beginning compared with the middle of the trials (during checks) were not considered in this experiment. Therefore, O2 consumption rates measured above 1.52 DML s1 in the present study may not reflect the total metabolic costs for swimming, but O2 consumption rates at speeds of 0.51.5 DML s1, when costs are lowest, and at speeds below 0.5 DML s1, when costs are high, are probably qualitatively representative.
Aerobic efficiency
As mentioned above, there is some inherent error in aerobic-based power estimates (i.e. anaerobic contributions are not considered) and hydrodynamic-based power estimates (i.e. unsteady mechanisms are not considered). Consequently, it is not surprising that aerobic estimates of the speed of maximum range (Umr) were 1.01.5 DML s1 higher than hydrodynamic estimates. Although hydrodynamic-based estimates of Umr are not available for other cephalopods, aerobic-based estimates for at least one squid are similar to aerobic-based estimates for L. brevis of similar size. On the basis of O2 consumption data at 17.5°C (ODor, 1982), a 41 g Loligo opalescens has a Umr of approximately 3 DML s1 (40 cm s1) and a Ucrit of approximately 3.4 DML s1 (45 cm s1). In this study, aerobic-based estimates of Umr and Ucrit for a 32 g L. brevis tested at 24°C were 2.5 DML s1 (19 cm s1) and 3.5 DML s1 (26 cm s1), respectively.
The aerobic efficiencies for L. brevis reported in the present study appear to be low relative to efficiencies reported for other cephalopods, but there are some key differences in how efficiencies were calculated in the different studies. ODor and Webber (ODor and Webber, 1991) reported aerobic efficiencies of 6.1 % for Nautilis pompilius, 2.8 % for Sepia officinalis, 5.9 % for Loligo pealei and 13 % for Illex illecebrosus at Umr. With the exception of Sepia officinalis, all these cephalopods have higher efficiencies than the 4.4/4.5 cm DML and 7.5/7.6 cm DML L. brevis in this study, which had aerobic efficiencies of 1.22.7 % and 1.85.0 %, respectively, at Umr. ODor and Webber (ODor and Webber, 1991) reported aerobic efficiencies of 8 % for Nautilis pompilius, 7 % for Sepia officinalis, 15 % for Loligo pealei and 18 % for Illex illecebrosus at Ucrit. On the basis of these estimates, Loligo pealei and Illex illecebrosus have higher efficiencies than the 4.4/4.5 and 7.5/7.6 cm DML L. brevis in this study, which had efficiencies of 3.3 % and 8.8 %, respectively, at Ucrit. However, direct comparisons between efficiencies are misleading because ODor and Webbers (ODor and Webber, 1991) estimates were based on cephalopods 600 g in mass, while efficiency estimates in this study were based on squid weighing less than 35 g. Because of lower mass-specific O2 consumption rates, larger cephalopods will have higher aerobic efficiencies. This was observed in the present study and can be seen when a 500 g Illex illecebrosus, which has aerobic efficiencies of 8.4 % and 14 % at Umr and Ucrit, respectively (ODor, 1988b), is compared with efficiencies for the 600 g Illex illecebrosus described above. Efficiencies for a 600 g L. brevis were not computed for comparison because a 600 g L. brevis has little physiological relevance [L. brevis does not reach sizes above 60 g (Hixon, 1980)], and there is insufficient data for scaling power output to such sizes.
Although power input was calculated in a similar manner for both studies, power output was calculated from jet pressures and funnel area by ODor and Webber (ODor and Webber, 1991), while power output was calculated from kinematic data and force measurements in the present study. These differences also may lead to disparate estimates of efficiency. Aerobic efficiencies for Loligo opalescens that are more directly comparable with efficiencies in this study may be calculated using power output estimates from hydrodynamic/kinematic data from ODor (ODor, 1988a) and power input estimates from metabolic data given by ODor (ODor, 1982). On the basis of these data, aerobic efficiency at 2.5 DML s1 for a 3040 g Loligo opalescens is 3.2 %, which is lower than an aerobic efficiency of 5 % for a 32 g L. brevis in the present study.
Energetic comparisons with cephalopods
L. brevis rarely swam faster than 24 cm s1 for sustained periods, whereas Loligo opalescens and Illex illecebrosus swim up to 45 and 100 cm s1, respectively, for sustained periods (ODor, 1982; Webber and ODor, 1986) (Fig. 6A). When velocities are converted to DML s1, however, L. brevis is more competitive, reaching speeds of approximately 3.5 DML s1, which is similar to those achieved by Loligo opalescens (Fig. 6B). Oxygen consumption rates during swimming for a typical L. brevis (31 g, 24°C) recorded in this study are lower than those of Illex illecebrosus [30 g (adjusted), 200 g (unadjusted), 15°C] recorded by Webber and ODor (Webber and ODor, 1986) and Loligo opalescens (41 g, 18°C) measured by ODor (ODor, 1982). Loligo opalescens and Illex illecebrosus are negatively buoyant, yet parabolic metabolic relationships have not been reported. This is surprising given that ODor (ODor, 1988a) determined that 6692 % of the total force required for Illex illecebrosus to swim at 10 cm s1 is associated with maintenance of vertical position and counteracting negative buoyancy. The absence of parabolic oxygen consumption patterns may be because speeds below 10 cm s1 (0.75 DML s1) and below 28 cm s1 (1.2 DML s1) were not considered in respiratory trials of Loligo opalescens or Illex illecebrosus, respectively. As observed in the present study, high lift generation costs occur at speeds below 0.5 DML s1.
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Concluding remarks
There are surprisingly few reports on parabolic O2 consumption rate/power curves as a function of swimming speed among negatively buoyant fishes and squid. This is presumably because low speeds are often omitted from energetic/hydrodynamic studies because the organism demonstrates inconsistent behavior at such speeds. In this study, some variation in low-speed swimming behavior was also observed, but this variation was interpreted to be integrally linked to costs associated with keeping position in the water column. This is not an unrealistic assumption given that power predictions based on hydrodynamic data also indicate high costs at low speeds and that recent research (Webber et al., 2000; ODor et al., 2001) suggests that cephalopods expend considerable energy counteracting negative buoyancy in nature. The absence of low-speed energetic/hydrodynamic data for many nekton has left a void in our understanding of the costs of low-speed swimming, which may be high even among neutrally buoyant fish because of power requirements for stability (Webb, 1993; Webb, 2000). With the development of digital particle image velocimetry (DPIV) and three-dimensional defocusing digital particle image velocimetry (DDPIV) (Pereira et al., 2000), which provide quantitative data on momentum transfer over short time scales, it is now possible to assess swimming costs effectively at low speed when movements are highly unsteady. Future particle image velocimetry studies should provide valuable insight into the dynamics and mechanics of low-speed swimming.
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