Finding food in the open ocean: foraging strategies in Humboldt penguins.

Penguins are excellent "model" organisms allowing us to study the behaviour of marine homeotherms at sea. Penguins regularly return to their breeding colonies, enabling biologists to equip them with remote sensing devices such as physiological or behavioural data-loggers, radio- or satellite transmitters. Foraging trips at sea can last from days to weeks and after return of the birds to their breeding sites, the devices can easily be removed for analysis of on-board stored data, yielding a wealth of information. Investigation of penguin behaviour at sea becomes particularly revealing when other sources of information can be matched to the data set, such as satellite data on wind, temperature, ice cover, and chlorophyll-a concentrations. Penguins and other marine homeotherms are true inhabitants of the high seas. Depending on the season, the marine behaviour varies: during reproduction, penguins are central-place foragers, and must return regularly to their nest to feed their chicks. During the remainder of the year, there are no constraints and the birds travel large distances at sea. Breeding Humboldt penguins react to climatic change by varying their daily foraging range and dive duration. Similar to other representatives of the family Spheniscidae, Humboldt penguins avoid food shortages by migrating into more productive marine areas. Navigational clues such as daylength, sea surface temperature, local wind direction and olfaction might provide important aids in finding patchily distributed prey in the open ocean. DMS, a chemical compound produced by decaying algae, seems to be a further clue that indirectly points the way to feeding areas.

Humboldt penguins outmanoeuvring El Niño.

We satellite-tracked five Humboldt penguins during the strong 1997/98 El Niño Southern Oscillation (ENSO) from their breeding island Pan de Azúcar (26 degrees 09'S, 70 degrees 40'W) in Northern Chile and related their activities at sea to satellite-derived information on sea surface temperature (SST), sea surface temperature anomaly (SSTA), wind direction and speed, chlorophyll a concentrations and statistical data on fishery landings. We found that Humboldt penguins migrated by up to 895 km as marine productivity decreased. The total daily dive duration was highly correlated with SSTA, ranging from 3.1 to 12.5 h when the water was at its warmest (+4 degrees C). Birds travelled between 2 and 116 km every day, travelling further when SSTA was highest. Diving depths (maximum 54 m), however, were not increased with respect to previous years. Two penguins migrated south and, independently of each other, located an area of high chlorophyll a concentration 150 km off the coast. Humboldt penguins seem to use day length, temperature gradients, wind direction and olfaction to adapt to changing environmental conditions and to find suitable feeding grounds. This makes Humboldt penguins biological in situ detectors of highly productive marine areas, with a potential use in the verification of trends detected by remote sensors on board satellites.

Asian small-clawed otters (Amblonyx cinerea): resting and swimming metabolic rates.

Open-flow oxygen and carbon dioxide respirometry was used in Neumünster Zoo (Germany) to examine the energy requirements of six Asian small-clawed otters (Amblonyx cinerea) at rest and swimming voluntarily under water. Our aim was to compare their energy requirements with those of other warm-blooded species to elucidate scale effects and to test whether the least aquatic of the three otter species differs markedly from these and its larger relatives. While at rest on land (16 degrees C, n = 26), otters (n = 6, mean body mass 3.1 +/- 0.4 kg) had a respiratory quotient of 0.77 and a resting metabolic rate of 5.0 +/- 0.8 Wkg-1(SD). This increased to 9.1 +/- 0.8 Wkg-1 during rest in water (11-15 degrees C, n = 4) and to 17.6 +/- 1.4 Wkg-1 during foraging and feeding activities in a channel (12 degrees C, n = 5). While swimming under water (n = 620 measurements) in an 11-m long channel, otters preferred a speed range between 0.7 ms-1 and 1.2 ms-1. Transport costs were minimal at 1 ms-1 and amounted to 1.47 +/- 0.24 JN-1 m-1 (n = 213). Metabolic rates of small-clawed otters in air were similar to those of larger otter species, and about double those of terrestrial mammals of comparable size. In water, metabolic rates during rest and swimming were larger than those extrapolated from larger otter species and submerged swimming homeotherms. This is attributed to high thermoregulatory costs, and high body drag at low Reynolds numbers.

Energy metabolism of underwater swimming in river-otters (Lutra lutra L.).

We used a still-water swim channel in conjunction with open-flow oxygen and carbon dioxide respirometry to examine the energy requirements of river-otters (Lutra lutra L.) swimming voluntarily underwater in Neumünster Zoo (Germany). While at rest on land (5 degrees C), river-otters had a respiratory quotient of 0.77 and a resting metabolic rate of 4.1 W kg-1. This increased to an estimated 6.4 W kg-1 during rest in water (11-15 degrees C) and to 12.3 W kg-1 when the animals were feeding in the channel. River-otters swimming under water preferred a mean speed of 0.89 m s-1, and their energy requirements attained 11.6 W kg-1. Cost of transport, however, was minimal at 1.3 m s-1 and amounted to 0.95 J N-1 m-1.

Energy requirements of beavers (Castor canadensis) swimming underwater.

Energy requirements of beavers (Castor canadensis) swimming voluntarily underwater were investigated in Neumünster Zoo (Germany) in a covered, still-water swim channel with oxygen and carbon dioxide respirometry. During the experiments, all activities of the beavers were monitored and recorded. While at rest within their thermoneutral zone on land (17 degrees C), beavers had a respiratory quotient of 0.95 and a resting metabolic rate of 1.58 W kg-1. When resting in water, energy requirements rose to 2.31 W kg-1. When swimming underwater in the channel, beavers preferred a mean speed of 0.64 m s-1, and their energy requirements rose to 2.64 W kg-1. Cost of transport, however, was minimal at 0.9 m s-1 and amounted to 0.36 J N-1 m-1. Although beavers must compromise form and function to operate on water and on land, their energy requirements while diving amount to only 1.65 times the resting metabolic rate and compare well with those of accomplished swimmers such as aquatic mammals and birds.

Diving energetics in king penguins (Aptenodytes patagonicus).

Dive duration in wild king penguins and the energetic cost of swimming in a 30m long swim channel were determined at Ile de la Possession, Crozet Archipelago, using external data loggers and respirometry, respectively. Calibrated electronic data loggers equipped with a pressure sensor were used to determine dive durations: 95% of dives were less than 6 min long and 66% of dives were less than 4 min long. Dive patterns show that king penguins may intersperse long dive durations (4-6.3 min) with short ones (1.5-3 min) and make surface pauses of variable duration between them (0.5-3.5 min), or dive regularly (for up to 5 h) with long dive durations (5 min) and constant interdive surface intervals (1.5 min). The latter indicates that the aerobic dive limits (ADL) of this species could be higher and oxygen consumption lower than previously reported. Assuming that king penguins dive within their aerobic limit, different approaches to the analysis of the data obtained in the swim channel are discussed to derive the ADL. Swimming speeds observed in the channel ranged from 0.9 to 3.4 m s-1. Transport costs were lowest between 1.8 and 2.2 m s-1. Although at 2.2 m s-1 king penguins used only 10.3 Wkg-1 over a dive+surface cycle (minimal transport costs of 4.7 J kg-1 m-1), we speculate that tisse oxygen consumption during submergence may be as low as 0.23 ml O2 kg-1 s-1 (2.1 times standard metabolic rate, SMR) or perhaps lower (which gives an ADL of 4.2 min). During surface phases, oxygen uptake would be increased to at least 1 ml O2kg-1 s-1 (9.3 times SMR). This implies that at least 70% of all dives are aerobic. Potential physiological mechanisms allowing king penguins to partition O2 consumption between submergence and surface periods remain, however, unclear.

Reliability of stomach temperature changes in determining feeding characteristics of seabirds

We examined the accuracy of stomach temperature archival units (STAUs), which are typically used to determine feeding activity in marine endotherms, with regard to determination of the time of prey ingestion as well as the number of prey items ingested and their masses. Units were deployed in nine species of free-living seabirds, where feeding conditions were uncontrolled, eight species of captive seabirds, where feeding conditions could be partially controlled, and in laboratory stomach simulations, where variables could be strictly controlled. The quality of data obtained on the timing of feeding, the mass ingested and the number of prey items ingested was subject to two main sources of error (i) those induced by changes in animal activity and (ii) those resulting from the physical form of the STAUs themselves. Animal activity factors considered important included the following: variability in (a) body temperature, (b) stomach blood perfusion, (c) consistency of stomach contents and (d) stomach churning and changes in body orientation. The physical form (size and buoyancy) of the STAU affected the location of the unit within the stomach, and thus the likelihood that ingested prey comes into contact with the sensor. The timing of prey ingestion can generally be determined accurately; however, considerable errors in mass estimates can occur if data acquired using STAUs are not critically assessed. An understanding of these sources of errors will allow researchers to construct STAUs appropriate to the species being studied and to analyze data critically so that errors are reduced.

UNDERWATER SWIMMING AT LOW ENERGETIC COST BY PYGOSCELID PENGUINS

Energetic requirements of under-water swimming in pygoscelid penguins were studied in Antarctica, using respirometry together with a 21 m long swim canal and externally attached devices recording the swimming speed and dive duration of unrestrained animals. Field measurements were compared with measurements of the hydrodynamic properties of an Adelie penguin model in a circulating water tank. Minimium transport costs during underwater swimming in Adelie (Pygoscelis adeliae), chinstrap (P. antarctica) and gentoo (P. papua) penguins averaged 4.9, 3.7 and 7.6 J kg-1 m-1, respectively, at their preferred swimming speeds of 2.2, 2.4 and 1.8 m s-1, allowing the birds to dive aerobically for 110, 130 and 93 s, respectively. From the swim canal measurements, we calculated a drag coefficient (CD) of 0.0368 for a typical Adelie penguin at 2.2 m s-1. This value is significantly lower than the CD of 0.04 of an ideal spindle and the CD of 0.0496 measured on the model in the laboratory. The reasons for this difference are discussed.

HYDRODYNAMIC ASPECTS OF DESIGN AND ATTACHMENT OF A BACK-MOUNTED DEVICE IN PENGUINS

Wind tunnel and water tank experiments were carried out on a penguin model in order to optimise the shape and attachment of a back-mounted datalogger. Device-induced turbulence was minimised when the unit was placed in the most caudal position. Drag was further reduced by shaping the device to match the body contour. The hydrodynamic resistance of the package could be reduced by 65 % compared with an earlier unit. These results are discussed together with results from new studies on kinematics and energetics of underwater swimming of live instrumented penguins.

The cost of a hot meal: facultative specific dynamic action may ensure temperature homeostasis in post-ingestive endotherms.

1. Resting metabolic rate was determined in Adelie penguins (Pygoscelis adeliae) that had been fed warm and cold ingesta. 2. Post-ingestion metabolic rate was found to be related to food temperature rather than to specific dynamic action. 3. Calorimetric calculations indicate that up to 13% of Adelie penguin daily energy expenditure may be used heating ingested food to body temperature. 4. Heating food costs are predicted to be higher in endotherms living in cold regions and in species with low assimilation efficiencies, but may be minimized by appropriate foraging behaviour.

Energy requirements of Adélie penguin (Pygoscelis adeliae) chicks.

The energy requirements of Adélie penguin (Pygoscelis adeliae) chicks were analysed with respect to body mass (W, 0.145-3.35 kg, n = 36) and various forms of activity (lying, standing, minor activity, locomotion, walking on a treadmill). Direct respirometry was used to measure O2 consumption (VO2, l.h-1) and CO2 production. Heart rate (HR, bpm) was recorded from the ECG obtained by both externally attached electrodes and implantable HR-transmitters. The parameters measured were not affected by hand-rearing of the chicks or by implanting transmitters. HR measured in the laboratory and in the field were comparable. Oxygen uptake ranged from VO2 = 1.50.W0.921 in lying chicks to VO2 = 2.25.W1.024 at maximal activity, RQ = 0.76. Metabolic rate in small wild chicks (0.14-0.38 kg) was not affected by time of day, nor was their feeding frequency in the colony (Dec 20-21). Regressions of HR on VO2 were highly significant (p less than 0.0001) in transmitter implanted chicks (n = 4), and two relationships are proposed for the pooled data, one for minor activities (VO2 = -7.23 + 1.82.W + 0.03 HR), and one for walking (VO2 = -11.89 + 1.117.W + 0.058.HR). Oxygen consumption, mass of the chick (2-3 kg), and duration of walking (T, s) were related as VO2 = -0.746 + 1.87.W + 0.076.T, whereas mass-specific O2 consumption was related to walking speed (S, m.s-1) as VO2.W-1 = 1.60 + 7.39.S.