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Oil pollution of Antarctic penguins: Effects on energy metabolism and physiology
Marine Pollution Bulletin H~ikanson, L. (19911b). Environmental hazard analysis--contamination of nutrients, mercury and cesium-137 in natural waters. Limnologica
20,339-346. Krom. M. D. (1986). An evaluation of the concept of assimilative capacity as applied to marine waters. A m b i o 15,208-214. Krom, M. D., Hornung, H. & Cohen, Y. (1990). Determination of the environmental capacity of Haifa Bay with respect to the input of mercury. Mar. Pollut. Bull. 21,349-354. Landner, L. (ed.) (1989). ('hemicals in the Aquatic Environment. A d v a n c e d Hazard Assessment. Springer Verlag, Berlin. Mackey, D. & Paterson, S. (1982). Fugacity revisited. Environ. A~4. Technol. 16,654 6611. Nixon, S. W. (19911). Marine eutrophication: a growing international problem. Arnbio 3, 101. O'Connor, D. J. (1981). Modeling of eutrophication in estuaries. In Estuaries and Nutrients (B. J. Neilson & L. E. Cronin, eds), pp. 183223. Humana Press, Clifton, New Jersey. OECD (1982). Eutrophication of waters. Monitoring, assessment and control. OECD. Paris.
Marine l'ollution Bulletin. Volume22, No. 8. pp. 388 391, 1991.
Printedin Great Britain.
Pilesj6, P., Persson, J. & Hfikanson, L. ( 1991 ). Digital bathymetric inl~rmation for calculations of morphometrical parameters and surface water retention time for coastal areas. National Swedish Environmental Protection Agency (SNV) Report, Solna (in press) (in Swedish). Schindler, D. W., Fee, E. J. & Ruszczynski, T. (1978). Phosphorus input and its consequences for phytoplankton standing crop and production in the experimental lakes area and in similar lakes. J. kish. Res. Board Can. 35, 190-196. Wallin, M., Hfikanson, L. & Persson, J. ( 1991 ). Nutrient loading models for coastal waters, especially for the assessment of environmental effects of marine fish farms. National Swedish Environmental Protection Agency (SNV) Report no. 3915, Solna (in Swedish). Vollenweider, R. A. (1976). Advances in defining critical loading levels for phosphorus in lake eutrophication. Mere. lsl. itaL htrobiol. 33, 53-83.
I)025 326X/91 $3.00+0.00 © 1991PergamonPresspie
Oil Pollution of Antarctic Penguins: Effects on Energy Metabolism and Physiology BORIS M. CULIK*, RORY P. WILSON*, ANTHONY T. WOAKESt and FRANCISCO W. SANUDO~
*Abt. Meereszoologie, lnstitut fiir Meereskunde, Diisternbrooker Weg 20, 2300 Kiel L Germany +School of Biological Sciences, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK +~Ave.Quintana 280, 3ro "A", Buenos Aires, Argentina
In the vicinity of Antarctic stations, the environment and associated wildlife are threatened by pollution. We propose that penguins are particularly susceptible and present behaviourai and physiological data on oiled Ad61ie penguins (Pygoscelis adeliae) in air and in water compared to non-oiled birds. In air, oiled penguins had reduced heart rate (90 vs. 98 bpm), body temperature (38.6 vs. 39.2°C) and energy expenditure (4.7 vs. 5.2 W • kg -I) compared to controls, respectively. In a swim tank, oiled penguins tried to leave the water and showed erratic swimming behaviour. Their swimming speed was lower than that of controls (1.6 as opposed to 1.8 m • s -~) and they had an increased heart rate at the surface (321 vs. 252 bpm). Metabolic rate while swimming was 50% higher in oiled birds than in controls (18.8 vs. 12.7 W . kg-l), and cost of transport was 73% higher (12.1 vs. 7 J - kg -! m-I).
In Antarctica, ice-free areas near the coast that are suitable for penguin colonies are rather rare. These areas are also often used as sites for research bases, which leads to local, but circumpolar, conflict with wildlife 388
(Culik et al., 1990a). Antarctic stations pollute the environment with PCBs, raw sewage, fuel, and air emissions from burning wastes (Mar. Pollut. Bull. 19, 652) and only recently have funds been made available for cleanup in some areas (Mar. Pollut. Bull. 21, 269). The most spectacular case of oil pollution, the wreckage of the Bahia Paraiso (Barinaga & Lindley, 1989; Eppley & Rubega, 1989) near Palmer station affected, among other birds breeding Addlie penguins (Pygoscelis adeliae). It was preceded by the wreckage of the Nella Dan (Lyons, 1988) at Macquarie Island, which has breeding colonies of Gentoo (P. papua), King (Aptenodytes patagonicus), Royal (Eudyptes schlegeli) and Rockhopper (E. crestatus) penguins, and followed by the running aground of the Peruvian research vessel Humboldt (Mar. Pollut. Bull. 20, 206). Both incidents were accompanied by oil leakage. Chronic oil pollution in penguins has also been reported from the Falklands and South Georgia, resulting from disintegrating oil tanks from old whaling stations and harbour activities (Bourne, 1985a). Penguins are more vulnerable to oil spills than flying birds, since they must swim through oil that occurs between their breeding colonies and feeding grounds
Volume 22 ~Numbcr g/August 1991
(Kerley & Erasmus, 1986). Oil and other surface active agents such as detergents and faecal matter destroy the water-proofing quality of the feathers and cause loss of buoyancy and insulation (Clark & Gregory, 1971; Ambrose, 1990). Seabirds cannot avoid polluted areas and "appear to take little notice of oil until they swim into it" (Bourne, 1985b). The degree of pollution cannot be easily quantified, as dead penguins found on the beaches represent only a small,proportion of those dying (Randall et al. 1980). Most oiled penguins presumably die in the water. Contrary to the opinion of Laws (1985), local environmental impacts may very well be important on a broader scale, especially for penguins. In this paper we present new data on behavioural and physiological parameters of oiled Addlie penguins. We recorded activity, heart rate (HR) body temperature (h0 and metabolic rate (MR) of birds in air and while swimming in a 21 m long canal, and compare those data to previously published results from non-oiled Addlie penguins (Culik & Wilson, 1991a).
Material and Methods Ad61ie penguins living at Esperanza Bay (56°59'W, 63°24'S), Antarctic Peninsula, were studied during December 1989 and January 1990. Telemetric HR/t, transmitters were implanted (for methods see Culik et aL 1990b) in two adult Ad61ie penguins (4.3 and 4.5 kg) incubating eggs in a nearby colony (controls). The eggs of the birds were kept warm for the duration of the operation (approx. 30 min). After 1 h recovery in the laboratory, the birds and their eggs were replaced on the nest. The penguins immediately resumed incubation. After termination of the experiments, the transmitters were removed in a second operation. Four adult Ad61ie penguins (3.3-4.6 kg) not attending nests were captured in a nearby colony. These birds were also implanted with transmitters and subsequently kept in an outdoor enclosure (oiled birds). The birds were fed once daily with 400 g food consisting of deboned cod, duck food pellets and vegetable oil (16:3:1) in gelatine. Oiling of these birds occurred accidentally by preening after being fed, thus spreading food remains and oil over the feathers. Within 2 days, the feathers of these birds lost their waterproofing qualities and the penguins were thoroughly wet when it rained. These birds were autopsied after termination of the experiments. Metabolic rate on land was measured in a 100 1. respiration chamber (flow rate 1500 l • h-l). In order to measure metabolism in the water (for details see Culik & Wilson, 1991 b), individual penguins were introduced into a plywood tank, 21 m long, 0.9 m wide and 0.7 m deep filled with sea-water (2-6°C) for a single experiment lasting 90 to 120 min after a 10 min acclimation period. The tank was sealed (I.1 m below the water surface by transparent PVC sheets (0.9 X 3 m) and had one respiration chamber at each end. Air was sucked into each chamber by a pump at a mean flow rate of 750 l . h -~, and pumped to the laboratory, to be analysed using an OXYGOR 6N paramagnetic oxygen
analyser and an UNOR 6N infrared gas analyser (Maihak, Hamburg). From a ladder placed over the middle of the tank, the birds were observed to be either in chamber A or B where they were classified as resting, being active ('unrest'), preening, swimming or jumping out of the water. Between chambers A and B swimming behaviour of the bird and position were monitored. All observations as well as real time were recorded orally onto magnetic tape (Sony Walkman Professional, quartz-locked speed) and later transcribed in the laboratory using a handheld computer (Husky Hunter, Coventry, UK). We determined the duration of the five classes of activity, distance swum and mean speed, and matched these with the dataset from the respirometry recordings. We regressed the duration of each behaviour and the mass of the bird against oxygen consumption (ml. 5 min-t), and considered only those behavioural variables which were significant (i.e. p < 0.05). Power input (Pi) and cost of transport (COT, i.e. the amount of energy required to move 1 kg body mass over 1 m) at the observed speed were calculated after eliminating all observations from the datasets where time swum or speed were zero (c.f. Schmidt-Nielsen, 1972) and correcting the remaining data using the regression to remove energy expenditure due to other activies (c.f. Culik & Wilson, 1991b). Differences between oiled birds and controls were tested by ANOVA at p=0.5. 'SE' refers to standard error. 'rf refers to the number of measurements made rather than to the number of individual penguins.
Results HR, tt, and MR while resting in air were significantly lower in oiled penguins (90 bpm, SE 2.5; 38.6°C, SE 0.3; 4.7 W . kg-~, SE 0.1; n = 3 4 ) than in controls (98 bpm, SE 1.1; 39.2°C, SE 0.1; 5.2 W - k g -~, SE 0.05; n=55). Activity in the water (per 5 min) was similar in both groups (n=94), with on average 108 s rest (SE 4.9), 154 s swimming (SE 5.9), 13.2 s unrest (SE 2.6) and <1 s preening. Jumping, i.e. escape behaviour, was recorded significantly more in oiled birds (n=58) occurring for 33.9 s (SE 4.6) as opposed to 6.2 s (SE 3.4) in controls (n = 37). The distance swum per 5 min was significantly lower in oiled birds (133 m, SE 12.3) than in controls (222 m, SE 21.7), and the same was found for speed (1.6 m . s-j, SE 0.05 compared to 1.8 m. s-I, SE 0.07). Speed distribution, however, showed a maximum at 1.2-1.8 m- s-~ in both groups (62% of all observations). Preceding a dive, HR in oiled penguins was on average 321 bpm (SE 5.1, n = 4 7 ) significantly higher than that of controls (252 bpm, SE 6.3, n = 4 7 , t-test, p < 0.05). Immediately after a dive, HR in controls and oiled penguins reached 297 bpm (SE 5.2, n = 20) and 315 bpm (SE 4.5, n=30), respectively, and this difference is also significant. ECG was not received in oiled birds while submerged and t b of the penguins could not be measured in the water. 389
Marine Pollution Bulletin Cost of T r a n s p o r t (J.kg".n~') 20
14 15~
10:
5 b
Control 0
i
i
1.1
1.3
1.5
i
i
i
i
i
~
17
1.9
2.1
2.3
2.5
~2.6
Speed (m/s) Fig. 1 Cost o f transport (J • kg -1 • m -~, i.e. power/speed) with respect to swimming speed (m • s-I) in Ad61ie penguins implanted with heart rate/body temperature transmitters when non-oiled (Control) and lightly oiled with vegetable oil (Oiled). Vertical bars show standard error (pooled) and 'n' is given for each speed range.
While swimming in the tank, oiled birds had on average a Pi of 18.8 W . kg -1 (SE 0.8, n = 5 8 ) which is significantly higher than the 12.7 W . kg -1 (SE 0.9, n = 3 7 ) measured in controls. COT (Fig. 1) is power divided by speed and averaged 12.1 J . kg - j - m -l (SE 0.7) in oiled birds compared to the 7.0 J " kg-] • m -1 (SE 0.4) of controls. Discussion
All physiological variables measured in oiled Addlie penguins resting in air showed reduced values as opposed to controls. The thermoneutral zone (TNZ) for this species ranges from - 1 0 to 20°C (Chappell & Souza, 1988) and we assume that the lightly oiled birds were within their TNZ during the experiments (+5°C). Hughes et al. (1989) report a decreased t b in oiled gulls, concomitant with a reduced food intake at +17°C. A reduction in t b has also been reported for oiled African penguins (Spheniscus demersus) in air at +18 to 25°C and in water at 20°C (Erasmus et al. 1981). Oiling results in a dose-dependent increase in thermal conductance and an upward shift in the lower critical temperature (LCT) (Hartung, 1967). We propose, that within their TNZ, MR and thereby t b may be reduced in oiled penguins in order to limit heat loss. At temperatures below LCT, heat loss is countered by an increase in metabolism, which then is significantly higher at this temperature than in controls, although t b may not reach the same levels (McEwan & Koelink, 1972). Oiled African penguins immersed in water at 20°C attempted to leave the pool within 4 rain of entering, whereas the control birds stayed voluntarily in the water (Erasmus et al., 1981). Oiled Addlie penguins (this study) had a strong tendency to leave the water as shown by the high incidence of jumping. Swimming was erratic as shown by the short distance travelled in each 5 min interval, although the duration of swimming activity was the same as in controls. The oiled birds were repeatedly observed to shiver on the surface between activity bouts and their feathers were completely wet at the end of each experiment, having lost all 390
insulative properties. From these observations alone, we conclude that, despite being lightly oiled, these penguins were suffering from heat loss in water. Water repellency of the feathers is a function of both their structural and surface properties (Hartung, 1967; Rijke, 1970). Rijke (1970) suggests that a certain extent of water penetration is likely to occur in penguins, probably to reduce buoyancy, but that the rich growth of barbules resists excessive water penetration. On the water surface, HR of oiled birds was significantly higher than in controls, concomitant with the high metabolic rate of the birds. From the erratic swimming behaviour we propose that, due to high heat loss, these birds were probably not able to reduce MR and HR while swimming under-water. Oiled penguins may not be able to physiologically adjust for diving. MR while swimming was on average 50% higher in oiled Ad61ie penguins than in controls, which coincides well with data from oiled African penguins (Erasmus & Wessels, 1985) and oiled ducks (A. platyrhynchos and Somateria molissima, Jenssen & Ekker, 1989). We recorded a mean Pi of 18.8 W • kg -~ which corresponds to 5x RMR in Ad61ie penguins (c.f. Culik and Wilson, 1991b) and is the highest MR measured in this species. COT was 73% higher in oiled penguins than in controls, which is presumably not only due to heat loss but also to increased body drag. Bannasch (pers. comm.) found that even small changes in the surface properties of cast penguin models, such as attachment of wool threads to study flow dynamics, had a significant effect on the drag coefficient (cw) and resulted in a 25% increase in measured drag. Addlie penguins live in an extreme environment, and even when on land rarely find conditions within their thermoneutral zone (Culik et al., 1989). Low thermal conductance of their feathers is essential for survival, and destruction of these properties by surface-active agents causes excessive heat loss, especially in seawater at c. 0°C. Ultimately, this prevents the birds from foraging, which in breeding birds results in reproductive failure and death of the young. On land, increased heat loss below LCT results is increased MR and high rates of fat consumption. Addlie penguins fast during reproduction and moult (Pr6vost & Sapin-Jaloustre, 1965) and abnormally high MR due to oiling may lead to mass losses which cannot be recuperated. Oiled penguins require on average 60 days for recovery (Randall et aL, 1980), and oil is easily transferred from premoult to postmoult feathers (Kerley el al., 1985). When this happens, even freshly moulted birds eventually die in the water when dehydration and hunger forces them to return to the sea (Randall et al., 1980). This work was funded by the Deutsche Forschungsgemeinschafl grant Nr. AD 24/11-4. We would like to thank the Instituto Antarctico Argentino and the Alfred-Wegener Institute for logistic support, and especially T. Reins, A. Hillner, N. R. Coria and H. J. Spairani for their help.
Ambrose, R (1990). Rapeseed oil kills waterbirds. Mar. Pollut. Bull. 2 i, 371. Barinaga, M. & Lindley, D. (1989). Wrecked ship causes damage to Antarctic ecosystem. Nature 337,495.
Volume 22/Number 8/August 1991 Bourne, W. R. P. (1985a). South Atlantic snapshots. Mar. Pollut. Bull, 16, 5-6. Bourne, W. R. P. (1985b). Oil and seabirds. Mar. Pollut. Bull. 16, 8586. Butler, P. ,1. & Woakes, A. J. (1984). Heart rate and aerobic metabolism in Humboldt penguins (Spheniscus humboldtii) during voluntary dives. J. Exp. Biol, 108,419 428. ChappelL M. A. & Souza, S. L. (1988). Thermoregulation, gas exchange and ventilation in Ad61ie penguins (Pygoscelis adeliae). J. ('omp. Phvsiol B 157,783-790. Clark, R. B. & Gregory. K. G. (1971). Feather-wetting in cleaned birds. Mar. Polhtt. Bull. 2, 78-79. Culik, B., Adelung, D., Heisc, M., Wilson, R. P., Coria, N. R. & Spairani, H. J. (1989). In situ heart rate and activity of incubating Ad61ie penguins ( f'ygoscelis adeliae ). Polar Biol. 9,365-37(I. Culik, B., Adelung, D. & Woakes, A. J. (1990a). The effect of disturbance on the heart rate and behaviour of Ad61ie penguins (Pygoscelis adeliae) during the breeding season. In Antatr'tic Ecosystems (K. R. Kerry & G. Hempel, eds), pp. 177-182. Springer-Verlag, Berlin. Culik, B., Woakes, A. J., Adclung, D.. Wilson, R. P., Coria, N. R. & Spairani, H. J. (1990b). Energy requirements of Ad61ie penguin ( Pygoscelis adeliae ) chicks. J. Comp. t'hysioL B 160, 61 70. Culik, B. & Wilson, R. P. (1991a). Swimming energetics and performance of instrumented Addlie penguins (Pygoscelis adeliae)..1. Exp. Biol. (in press). Culik, B. & Wilson, R. P. ( 1991 b). Energetics of under-water swimming in Adelie penguins (l[vgoscelis adeliae). J. Comp. Phy~iol B (in press). Eppley, Z. A. & Rubega, M. A. (1989). Indirect effects of an oil spill. Nature 340, 513. Erasmus, T., Randall, R. M. & Randall, B. M. (1981). Oil pollution, insulation and body temperatures in the jackass penguin (Spheniscus demersus). Comp. Biochem. Physiol. 69A, 169-171.
Erasmus, T. & Wessels, E. D. (1985). Heat production studies on normal and oil-covered jackass penguins (Spheniscus demersus) in air and water. S. Afr. J. Zool. 20,209-212. Hartung, R. (1967). Energy metabolism in oil-covered ducks. J. WiMl, Manage. 31,798-804. Hughes, M. R., Kassera, C. & Thomas, B. (1989). Effect of externally applied bunker fuel on body mass and temperature, plasma concentration and water flux of Glaucous-winged gulls, Larus glaucescens. Can. J. Zool, 68, 716-721. Jenssen, B. M. & Ekker, M. (1989). Rehabilitation of oiled birds: a physiological evaluation of four cleaning agents. Mar. Pollut. Bull. 20,509-512. Kerley, G. I. H., Erasmus, T. & Mason, R. P. (1985). Effect of moult on crude oil load in a jackass penguin Spheniscus denlersus. Mar. Pollut. Bull. 16,474-476. Kerley, G. 1. H. & Erasmus, T. (1986). Oil pollution of cape gannets: to clean or not to clean? Mar. Polha. Bull. 17,498 5(10. Laws, R. M. (19851. International stewardship of the Antarctic: problems, successes and future options. Mar. Pollut. Bull. 16, 49-55. Lyons, D. (1988). The last voyage of the Nella Dan. ANARE News 53, 3. Antarctic division, Kingston, Australia. McEwan, E. H. & Koelink, A. F. C. (1972). The heat production of oiled mallards and scaup. Can. J. Zool. 51, 27 31. Pr6vost, J. & Sapin-Jaloustre, J. (1965). Ecologie des manchots Antarctiques. In Biogeography and Ecology in Antarctica (J. van Mieghem, P. van Oye & J. Schell, eds), pp. 551-648. Monographiae Biologicae, Junk, The Hague. Randall, R. M., Randall, B. M. & Bevan, J. (1980). Oil Pollution and penguins--is cleaning justified? Mar. Polha. Bull. 11,234-237. Rijke, A. M. (19701. Wettability and phylogenetic development of feather structures in water birds. J. Exp. Biol. 52,469-479. Schmidt-Nielsen, K. (1972). Locomotion: Energy cost of swimming, flying and running. Science 177,222-228.
391
20,339-346. Krom. M. D. (1986). An evaluation of the concept of assimilative capacity as applied to marine waters. A m b i o 15,208-214. Krom, M. D., Hornung, H. & Cohen, Y. (1990). Determination of the environmental capacity of Haifa Bay with respect to the input of mercury. Mar. Pollut. Bull. 21,349-354. Landner, L. (ed.) (1989). ('hemicals in the Aquatic Environment. A d v a n c e d Hazard Assessment. Springer Verlag, Berlin. Mackey, D. & Paterson, S. (1982). Fugacity revisited. Environ. A~4. Technol. 16,654 6611. Nixon, S. W. (19911). Marine eutrophication: a growing international problem. Arnbio 3, 101. O'Connor, D. J. (1981). Modeling of eutrophication in estuaries. In Estuaries and Nutrients (B. J. Neilson & L. E. Cronin, eds), pp. 183223. Humana Press, Clifton, New Jersey. OECD (1982). Eutrophication of waters. Monitoring, assessment and control. OECD. Paris.
Marine l'ollution Bulletin. Volume22, No. 8. pp. 388 391, 1991.
Printedin Great Britain.
Pilesj6, P., Persson, J. & Hfikanson, L. ( 1991 ). Digital bathymetric inl~rmation for calculations of morphometrical parameters and surface water retention time for coastal areas. National Swedish Environmental Protection Agency (SNV) Report, Solna (in press) (in Swedish). Schindler, D. W., Fee, E. J. & Ruszczynski, T. (1978). Phosphorus input and its consequences for phytoplankton standing crop and production in the experimental lakes area and in similar lakes. J. kish. Res. Board Can. 35, 190-196. Wallin, M., Hfikanson, L. & Persson, J. ( 1991 ). Nutrient loading models for coastal waters, especially for the assessment of environmental effects of marine fish farms. National Swedish Environmental Protection Agency (SNV) Report no. 3915, Solna (in Swedish). Vollenweider, R. A. (1976). Advances in defining critical loading levels for phosphorus in lake eutrophication. Mere. lsl. itaL htrobiol. 33, 53-83.
I)025 326X/91 $3.00+0.00 © 1991PergamonPresspie
Oil Pollution of Antarctic Penguins: Effects on Energy Metabolism and Physiology BORIS M. CULIK*, RORY P. WILSON*, ANTHONY T. WOAKESt and FRANCISCO W. SANUDO~
*Abt. Meereszoologie, lnstitut fiir Meereskunde, Diisternbrooker Weg 20, 2300 Kiel L Germany +School of Biological Sciences, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK +~Ave.Quintana 280, 3ro "A", Buenos Aires, Argentina
In the vicinity of Antarctic stations, the environment and associated wildlife are threatened by pollution. We propose that penguins are particularly susceptible and present behaviourai and physiological data on oiled Ad61ie penguins (Pygoscelis adeliae) in air and in water compared to non-oiled birds. In air, oiled penguins had reduced heart rate (90 vs. 98 bpm), body temperature (38.6 vs. 39.2°C) and energy expenditure (4.7 vs. 5.2 W • kg -I) compared to controls, respectively. In a swim tank, oiled penguins tried to leave the water and showed erratic swimming behaviour. Their swimming speed was lower than that of controls (1.6 as opposed to 1.8 m • s -~) and they had an increased heart rate at the surface (321 vs. 252 bpm). Metabolic rate while swimming was 50% higher in oiled birds than in controls (18.8 vs. 12.7 W . kg-l), and cost of transport was 73% higher (12.1 vs. 7 J - kg -! m-I).
In Antarctica, ice-free areas near the coast that are suitable for penguin colonies are rather rare. These areas are also often used as sites for research bases, which leads to local, but circumpolar, conflict with wildlife 388
(Culik et al., 1990a). Antarctic stations pollute the environment with PCBs, raw sewage, fuel, and air emissions from burning wastes (Mar. Pollut. Bull. 19, 652) and only recently have funds been made available for cleanup in some areas (Mar. Pollut. Bull. 21, 269). The most spectacular case of oil pollution, the wreckage of the Bahia Paraiso (Barinaga & Lindley, 1989; Eppley & Rubega, 1989) near Palmer station affected, among other birds breeding Addlie penguins (Pygoscelis adeliae). It was preceded by the wreckage of the Nella Dan (Lyons, 1988) at Macquarie Island, which has breeding colonies of Gentoo (P. papua), King (Aptenodytes patagonicus), Royal (Eudyptes schlegeli) and Rockhopper (E. crestatus) penguins, and followed by the running aground of the Peruvian research vessel Humboldt (Mar. Pollut. Bull. 20, 206). Both incidents were accompanied by oil leakage. Chronic oil pollution in penguins has also been reported from the Falklands and South Georgia, resulting from disintegrating oil tanks from old whaling stations and harbour activities (Bourne, 1985a). Penguins are more vulnerable to oil spills than flying birds, since they must swim through oil that occurs between their breeding colonies and feeding grounds
Volume 22 ~Numbcr g/August 1991
(Kerley & Erasmus, 1986). Oil and other surface active agents such as detergents and faecal matter destroy the water-proofing quality of the feathers and cause loss of buoyancy and insulation (Clark & Gregory, 1971; Ambrose, 1990). Seabirds cannot avoid polluted areas and "appear to take little notice of oil until they swim into it" (Bourne, 1985b). The degree of pollution cannot be easily quantified, as dead penguins found on the beaches represent only a small,proportion of those dying (Randall et al. 1980). Most oiled penguins presumably die in the water. Contrary to the opinion of Laws (1985), local environmental impacts may very well be important on a broader scale, especially for penguins. In this paper we present new data on behavioural and physiological parameters of oiled Addlie penguins. We recorded activity, heart rate (HR) body temperature (h0 and metabolic rate (MR) of birds in air and while swimming in a 21 m long canal, and compare those data to previously published results from non-oiled Addlie penguins (Culik & Wilson, 1991a).
Material and Methods Ad61ie penguins living at Esperanza Bay (56°59'W, 63°24'S), Antarctic Peninsula, were studied during December 1989 and January 1990. Telemetric HR/t, transmitters were implanted (for methods see Culik et aL 1990b) in two adult Ad61ie penguins (4.3 and 4.5 kg) incubating eggs in a nearby colony (controls). The eggs of the birds were kept warm for the duration of the operation (approx. 30 min). After 1 h recovery in the laboratory, the birds and their eggs were replaced on the nest. The penguins immediately resumed incubation. After termination of the experiments, the transmitters were removed in a second operation. Four adult Ad61ie penguins (3.3-4.6 kg) not attending nests were captured in a nearby colony. These birds were also implanted with transmitters and subsequently kept in an outdoor enclosure (oiled birds). The birds were fed once daily with 400 g food consisting of deboned cod, duck food pellets and vegetable oil (16:3:1) in gelatine. Oiling of these birds occurred accidentally by preening after being fed, thus spreading food remains and oil over the feathers. Within 2 days, the feathers of these birds lost their waterproofing qualities and the penguins were thoroughly wet when it rained. These birds were autopsied after termination of the experiments. Metabolic rate on land was measured in a 100 1. respiration chamber (flow rate 1500 l • h-l). In order to measure metabolism in the water (for details see Culik & Wilson, 1991 b), individual penguins were introduced into a plywood tank, 21 m long, 0.9 m wide and 0.7 m deep filled with sea-water (2-6°C) for a single experiment lasting 90 to 120 min after a 10 min acclimation period. The tank was sealed (I.1 m below the water surface by transparent PVC sheets (0.9 X 3 m) and had one respiration chamber at each end. Air was sucked into each chamber by a pump at a mean flow rate of 750 l . h -~, and pumped to the laboratory, to be analysed using an OXYGOR 6N paramagnetic oxygen
analyser and an UNOR 6N infrared gas analyser (Maihak, Hamburg). From a ladder placed over the middle of the tank, the birds were observed to be either in chamber A or B where they were classified as resting, being active ('unrest'), preening, swimming or jumping out of the water. Between chambers A and B swimming behaviour of the bird and position were monitored. All observations as well as real time were recorded orally onto magnetic tape (Sony Walkman Professional, quartz-locked speed) and later transcribed in the laboratory using a handheld computer (Husky Hunter, Coventry, UK). We determined the duration of the five classes of activity, distance swum and mean speed, and matched these with the dataset from the respirometry recordings. We regressed the duration of each behaviour and the mass of the bird against oxygen consumption (ml. 5 min-t), and considered only those behavioural variables which were significant (i.e. p < 0.05). Power input (Pi) and cost of transport (COT, i.e. the amount of energy required to move 1 kg body mass over 1 m) at the observed speed were calculated after eliminating all observations from the datasets where time swum or speed were zero (c.f. Schmidt-Nielsen, 1972) and correcting the remaining data using the regression to remove energy expenditure due to other activies (c.f. Culik & Wilson, 1991b). Differences between oiled birds and controls were tested by ANOVA at p=0.5. 'SE' refers to standard error. 'rf refers to the number of measurements made rather than to the number of individual penguins.
Results HR, tt, and MR while resting in air were significantly lower in oiled penguins (90 bpm, SE 2.5; 38.6°C, SE 0.3; 4.7 W . kg-~, SE 0.1; n = 3 4 ) than in controls (98 bpm, SE 1.1; 39.2°C, SE 0.1; 5.2 W - k g -~, SE 0.05; n=55). Activity in the water (per 5 min) was similar in both groups (n=94), with on average 108 s rest (SE 4.9), 154 s swimming (SE 5.9), 13.2 s unrest (SE 2.6) and <1 s preening. Jumping, i.e. escape behaviour, was recorded significantly more in oiled birds (n=58) occurring for 33.9 s (SE 4.6) as opposed to 6.2 s (SE 3.4) in controls (n = 37). The distance swum per 5 min was significantly lower in oiled birds (133 m, SE 12.3) than in controls (222 m, SE 21.7), and the same was found for speed (1.6 m . s-j, SE 0.05 compared to 1.8 m. s-I, SE 0.07). Speed distribution, however, showed a maximum at 1.2-1.8 m- s-~ in both groups (62% of all observations). Preceding a dive, HR in oiled penguins was on average 321 bpm (SE 5.1, n = 4 7 ) significantly higher than that of controls (252 bpm, SE 6.3, n = 4 7 , t-test, p < 0.05). Immediately after a dive, HR in controls and oiled penguins reached 297 bpm (SE 5.2, n = 20) and 315 bpm (SE 4.5, n=30), respectively, and this difference is also significant. ECG was not received in oiled birds while submerged and t b of the penguins could not be measured in the water. 389
Marine Pollution Bulletin Cost of T r a n s p o r t (J.kg".n~') 20
14 15~
10:
5 b
Control 0
i
i
1.1
1.3
1.5
i
i
i
i
i
~
17
1.9
2.1
2.3
2.5
~2.6
Speed (m/s) Fig. 1 Cost o f transport (J • kg -1 • m -~, i.e. power/speed) with respect to swimming speed (m • s-I) in Ad61ie penguins implanted with heart rate/body temperature transmitters when non-oiled (Control) and lightly oiled with vegetable oil (Oiled). Vertical bars show standard error (pooled) and 'n' is given for each speed range.
While swimming in the tank, oiled birds had on average a Pi of 18.8 W . kg -1 (SE 0.8, n = 5 8 ) which is significantly higher than the 12.7 W . kg -1 (SE 0.9, n = 3 7 ) measured in controls. COT (Fig. 1) is power divided by speed and averaged 12.1 J . kg - j - m -l (SE 0.7) in oiled birds compared to the 7.0 J " kg-] • m -1 (SE 0.4) of controls. Discussion
All physiological variables measured in oiled Addlie penguins resting in air showed reduced values as opposed to controls. The thermoneutral zone (TNZ) for this species ranges from - 1 0 to 20°C (Chappell & Souza, 1988) and we assume that the lightly oiled birds were within their TNZ during the experiments (+5°C). Hughes et al. (1989) report a decreased t b in oiled gulls, concomitant with a reduced food intake at +17°C. A reduction in t b has also been reported for oiled African penguins (Spheniscus demersus) in air at +18 to 25°C and in water at 20°C (Erasmus et al. 1981). Oiling results in a dose-dependent increase in thermal conductance and an upward shift in the lower critical temperature (LCT) (Hartung, 1967). We propose, that within their TNZ, MR and thereby t b may be reduced in oiled penguins in order to limit heat loss. At temperatures below LCT, heat loss is countered by an increase in metabolism, which then is significantly higher at this temperature than in controls, although t b may not reach the same levels (McEwan & Koelink, 1972). Oiled African penguins immersed in water at 20°C attempted to leave the pool within 4 rain of entering, whereas the control birds stayed voluntarily in the water (Erasmus et al., 1981). Oiled Addlie penguins (this study) had a strong tendency to leave the water as shown by the high incidence of jumping. Swimming was erratic as shown by the short distance travelled in each 5 min interval, although the duration of swimming activity was the same as in controls. The oiled birds were repeatedly observed to shiver on the surface between activity bouts and their feathers were completely wet at the end of each experiment, having lost all 390
insulative properties. From these observations alone, we conclude that, despite being lightly oiled, these penguins were suffering from heat loss in water. Water repellency of the feathers is a function of both their structural and surface properties (Hartung, 1967; Rijke, 1970). Rijke (1970) suggests that a certain extent of water penetration is likely to occur in penguins, probably to reduce buoyancy, but that the rich growth of barbules resists excessive water penetration. On the water surface, HR of oiled birds was significantly higher than in controls, concomitant with the high metabolic rate of the birds. From the erratic swimming behaviour we propose that, due to high heat loss, these birds were probably not able to reduce MR and HR while swimming under-water. Oiled penguins may not be able to physiologically adjust for diving. MR while swimming was on average 50% higher in oiled Ad61ie penguins than in controls, which coincides well with data from oiled African penguins (Erasmus & Wessels, 1985) and oiled ducks (A. platyrhynchos and Somateria molissima, Jenssen & Ekker, 1989). We recorded a mean Pi of 18.8 W • kg -~ which corresponds to 5x RMR in Ad61ie penguins (c.f. Culik and Wilson, 1991b) and is the highest MR measured in this species. COT was 73% higher in oiled penguins than in controls, which is presumably not only due to heat loss but also to increased body drag. Bannasch (pers. comm.) found that even small changes in the surface properties of cast penguin models, such as attachment of wool threads to study flow dynamics, had a significant effect on the drag coefficient (cw) and resulted in a 25% increase in measured drag. Addlie penguins live in an extreme environment, and even when on land rarely find conditions within their thermoneutral zone (Culik et al., 1989). Low thermal conductance of their feathers is essential for survival, and destruction of these properties by surface-active agents causes excessive heat loss, especially in seawater at c. 0°C. Ultimately, this prevents the birds from foraging, which in breeding birds results in reproductive failure and death of the young. On land, increased heat loss below LCT results is increased MR and high rates of fat consumption. Addlie penguins fast during reproduction and moult (Pr6vost & Sapin-Jaloustre, 1965) and abnormally high MR due to oiling may lead to mass losses which cannot be recuperated. Oiled penguins require on average 60 days for recovery (Randall et aL, 1980), and oil is easily transferred from premoult to postmoult feathers (Kerley el al., 1985). When this happens, even freshly moulted birds eventually die in the water when dehydration and hunger forces them to return to the sea (Randall et al., 1980). This work was funded by the Deutsche Forschungsgemeinschafl grant Nr. AD 24/11-4. We would like to thank the Instituto Antarctico Argentino and the Alfred-Wegener Institute for logistic support, and especially T. Reins, A. Hillner, N. R. Coria and H. J. Spairani for their help.
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