post-dive blood lactate concentrations in emperor penguins ...

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Catheters and TDRs were removed under anesthesia at the end ... 4. Blood [lactate] (mmoll. −1. ) 0. 2. 4. 6. 8. 10. 12. 14. Diving duration (min). Fig. 2. Two-phase ...
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The Journal of Experimental Biology 200, 1623–1626 (1997) Printed in Great Britain © The Company of Biologists Limited 1997 JEB0736

POST-DIVE BLOOD LACTATE CONCENTRATIONS IN EMPEROR PENGUINS, APTENODYTES FORSTERI P. J. PONGANIS*, G. L. KOOYMAN, L. N. STARKE, C. A. KOOYMAN AND T. G. KOOYMAN Accepted 17 March 1997

Scholander Hall, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093-0204, USA Summary In order to determine an aerobic diving limit (ADL) in versus diving duration relationship. All dives longer than emperor penguins (Aptenodytes forsteri), post-dive blood 7 min were associated with lactate concentrations greater lactate concentrations were measured in penguins foraging than 5 mmol l−1. We conclude that the ADL in emperor at an isolated sea ice hole. Resting lactate concentrations penguins ranges between 5 and 7 min. These are the first were 1.2–2.7 mmol l−1. Serial samples revealed that lactate determinations of post-dive lactate concentrations in any level usually peaked within 5 min after dives and that free-diving bird and are currently the only physiological 7–12 min was required for lactate concentrations to assessment of an ADL in an avian species. decrease from 5–8 mmol l−1 to less than 2.5 mmol l−1. Postdive lactate level was not elevated above 3 mmol l−1 for Key words: aerobic diving limit, Antarctica, catheter, time/depth recorder, sub-ice observation chamber, Weddell seal, emperor dives shorter than 5 min. Two-phase regression analysis penguin, Aptenodytes forsteri. revealed a transition at 5.6 min in the post-dive lactate level

Introduction Emperor penguins Aptenodytes forsteri can dive as deep as 534 m (Kooyman and Kooyman, 1995) and for as long as 22 min (Robertson, 1995). Frequency analysis of diving durations during foraging trips at sea has revealed that 21 % of all dives are longer than 5 min in duration, and that 3 % exceed 8 min in duration (Kooyman and Kooyman, 1995). The proportional contributions of aerobic and anaerobic metabolism to the energy requirements of diving are unknown, but they may be significant in determining the durations of dives, surface intervals and diving bouts. An aerobic dive limit (ADL), the diving duration beyond which the post-dive lactate concentration increases above resting levels (Kooyman, 1985), has been used in other species to evaluate which dives are defined as aerobic, i.e. those dives in which there is no net lactate production. Although an ADL has been measured only in the Weddell seal Leptonychotes weddellii (Kooyman et al. 1980, 1983), estimates of ADLs, based either on O2 store/metabolic rate calculations or on analyses of diving duration frequencies, have been applied to many species (Gentry and Kooyman, 1986; Kooyman, 1989; Kooyman et al. 1992a; Le Boeuf et al. 1988; Lydersen et al., 1992). This limit for the emperor penguin has been calculated as 5 min on the basis of O2 stores and an estimated diving metabolic rate (Kooyman and Ponganis, 1990). More recent analysis of emperor penguin diving duration versus surface interval relationships has inferred a behavioral ADL of 8 min *e-mail: [email protected]

(Kooyman and Kooyman, 1995). Because of the differences in these ADL estimations as well as the potential effects of metabolism on diving behavior, we attempted to determine an ADL in emperor penguins by measuring post-dive lactate concentrations in free-diving birds.

Materials and methods In McMurdo Sound, Antarctica, an experimental diving hole, penguin corral and camp (Kooyman et al. 1992b) were set up on sea ice over a water depth of 600 m. Seventeen adult emperor penguins Aptenodytes forsteri (G. R. Gray) of 21–25 kg body mass (mb) were collected locally and held in the corral for 30–40 days. They were allowed daily access to the diving hole. While diving, they fed on fish, probably Pagothenis borchgrevinki. The penguins typically left the water after dives and stood on the ice prior to the next dive. This behavior was the basis of the blood sampling protocol. Birds selected for catheterization were those most approachable and calm while in the close presence of researchers. Penguins were anesthetized using isoflurane and catheterized percutaneously as described previously (Kooyman and Ponganis, 1994). The catheter, placed either in a foot vein or in a wing vein, was secured using Coban (3M) wrap and Loctite epoxy glue. A 15 cm extension tube and

AND OTHERS

Results Control blood lactate concentrations ranged from 1.2 to 2.7 mmol l−1; the mean value was 1.7±0.71 mmol l−1 (mean ± S.D., N=3). On four occasions, serial samples after dives showed that the blood lactate concentration peaked within 5 min after a dive. In one animal, lactate level peaked at 12 min post-dive. This animal had made three consecutive 6–6.5 min dives before leaving the water and shivered continuously for 31 min after surfacing. In three cases where multiple samples were obtained after the peak lactate value, 7–12 min was required for blood lactate concentration to decrease from 5– 8 mmol l−1 to below 2.5 mmol l−1 (Fig. 1). Mean time (± S.D.) between the end of a dive and the first sample was 3.6±1.78 min (N=22). Blood lactate determinations were made after 22 dives in four birds. Two-phase regression analysis (Yeager and Ultsch, 1989) of the post-dive blood lactate concentration and diving duration data (Fig. 2) yielded a transition at 5.6 min between the two regression equations with a minimum residual sum of squares (RSS) of 81. Continuous linear and exponential

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stopcock extended from the catheter either to the posterior aspect of the foot or to the back near the axilla. The dead space in the catheter tubing was filled with 33 % ethanol/normal saline (0.9 %) solution prior to returning the animal to the corral. Tessa tape secured the distal end of the tubing to the feathers. Before recovery from anesthesia, a Mark 4.5 time–depth recorder (TDR, Wildlife Computers) was glued with Loctite onto the lower back. Four hours after recovery from anesthesia, the birds were allowed free access to the diving hole. Diving durations and surface intervals were recorded using a stopwatch and verified using the TDR records. Blood sampling occurred over a few hours to 2 days following implantation of the catheter. The duration of the sampling period was dependent on the functioning of the catheter. Catheters and TDRs were removed under anesthesia at the end of the sampling period. Observations of diving behavior were made from a sub-ice observation chamber and during SCUBA diving. Blood collection was accomplished using a slow, calm approach to the bird so as to minimize disturbance and stress. Stopcock manipulation and blood collection were achieved from behind the upright bird once it had been surrounded by two or three kneeling persons. Most samples were collected within 5 min after a dive. Usually, only one post-dive sample was obtained. On five occasions, multiple post-dive blood samples were drawn over periods of 7–60 min. Control samples were drawn during rest periods in the corral. Blood samples (1 ml) were drawn into heparinized syringes and were immediately analyzed for hematocrit by microcentrifugation and for blood lactate concentration using a YSI sport lactate analyzer (model 1500, sensitivity 0.01 mmol l−1). Graphic analysis of the data was conducted using Table Curve (Jandel).

EP9 EP15 EP10 WS1 WS2

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20 30 40 50 Time after peak lactate level (min)

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Fig. 1. Decline in blood lactate concentration after the peak post-dive value in three emperor penguins (EP9, EP10, EP15), an adult Weddell seal (WS1) and a juvenile Weddell seal (WS2). The peak value occurred within 5 min post-dive in the seals EP10 and EP15. Although elevated above 5 mmol l−1 at 5 and 7 min post-dive, the lactate concentration peaked at 12 min post-dive in EP9. Values were recorded after dive durations of 6.5, 8.1 and 7.7 min of EP9, EP10 and EP15, respectively, after a 43 min dive of WS1 (Kooyman et al. 1980) and after a 25 min dive of WS2 (Castellini et al. 1988). During these sampling periods, WS1 rested at the surface, WS2 made short dives and the emperor penguins stood on the sea ice. The abscissa represents sample collection time with reference to the time (0 min) at which the peak lactate sample was collected.

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8 10 6 Diving duration (min)

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Fig. 2. Two-phase regression analysis of post-dive blood lactate levels and diving duration in four emperor penguins demonstrating a transition at 5.6 min. For dives shorter than 5.6 min (filled symbols), y=1.48+0.27x, r2=0.55, P