sign in sign up
<<
Home , Aptenodytes, Emperor penguin, Ice diving, Penguin

DIVING BEHAVIOR OF THE EMPEROR , APTENOD YTES FORSTERI

G. L. KOOYMAN,C. M. DRABEK,R. ELSNER,AND W. B. CAMPBELL

ONE of the most unexpecteddiscoveries in the avian world was the breedingof Emperor Penguinsduring the winter night (Wilson, 1905: 488). The large sizeof the chick at fledgingand the time required for this developmentforces the EmperorPenguin to lay its singleegg in late May and June (Stonehouse,1953; Prdvost,1961) and incubate it throughthe antarcticnight. The rookeriesare establishedon fast seaice, no formalnest is built, and the adult male incubatesthe eggin his brood pouchsupported on his feet. The newly hatchedchick is similarlymain- tained. Fledgingdoes not occuruntil late December,and from March throughApril, dependingon the , the are again returning to the rookeriesto form pairs and breed. Becauseof thesereproductive commitmentsno other or mammalspecies is so obligatedto remain in closeproximity to the antarctic continent and the fast sea that bordersits shores.This meansthat EmperorPenguins not only dive and feedduring winter darkness, as otherantarctic do, but at times must do so in heavy pack ice and possiblyhave to do so even under fast ice, conditionsthat other penguinsseldom, if ever, encounter.These featuresplus the fact that this speciesis the largestof divingbirds make informationabout such diving capacities as submersiondurations, depth, and swimmingspeed of especialinterest.

MATERIALS AND METHODS We were able to study and measuredives of birds in both natural and experi- mental conditions.Observations on natural dive patterns and group diving behavior were obtained at Cape Royds in 1967, in the icebreaker channel between Cape Royds and Cape Armitage in 1967, and near the rookery at in 1968 and 1969 (Figures 1 and 2). The usual method was to watch the birds' surface behavior from the edge of the ice and to time their dives. On three different occasionsit was possible1) to study their underwater behavior by lying at the ice edge and watch- ing them dive below us, 2) to observethem while diving with scuba, and 3) in 1969 at Cape Crozier to suture small (4.5 g) capillary Teflon depth-recorderssuper- ficially to the back of the necksof birds groupedat the edgeof the ice. Thesebirds later enteredthe water for what appearedto be feedingdives; 2 to 3 hours after attaching the depth tubes the birds were recapturedand the recordersremoved. The depth-recordersfunction on the same principle as those developedby Lord Kelvin in 1878 exceptthe capillarytube is made of Teflon rather than glass(Fryer, 1958). Essentiallyit is a 61-cm coil of tubing, sealedat one end and coated on the insidewith a water solubledye that leavesa ring at maximum compression. Experimentaldives were conductedseveral miles offshoreand northwest of Cape Armitage at a station that consistedof a heated hut over a man-made hole in annual . These experimentswere conductedduring three different austral summers,

775 The , 88: 775-795. October 1971 776 KOOY•V[AN•DRABEK• ELSNER•AND CA•V[PBELL [Auk, Vol. 88

t 80 ø

NEW ZEALAND 270o- 90o • AMERICA AFRICA 0 o

• CAPEBIRD DUNLOP ,SLAND

I ...... CROZIER

Figure 1. Locality map of the field studies. In November of 1963 and 1967 annual sea ice extended north of the Ross Ice Shelf to Cape Royds, and in 1968 and 1969 it was as far north as Cape Bird. Birds were studied diving under natural conditionsat Cape Royds and Cape Crozier. Experimentaldives were conducteda few miles offshorefrom Cape Armitage and the birds for thesestudies were collected at Cape Roydsin 1967and Cape Bird in 1968.

1963, 1967,and 1968,and sea ice thicknessvaried from 1.5-3.9 m. Techniquesand instrumentsemployed were the same as those for the , Leptonychotes weddelli(Kooyman, 1965, 1968). In brief, the birds were releasedat a hole so iso- lated that they had to return to it after eachdive. A sub-iceobservation chamber was used to watch the birds during most of the experiments. Diving depth and October 1971] Diving Behavior 777

- / •'•;• B

Figure 2. Aerial photo o• Cape Crozier, Ross Island, •tarctica in •ovember 1969. The black c•ffs arc about IS0 m h•h. The dark area, A, is an Emperor Pen•in rooke• o• about $00 chic• and adult. B h the •a ice •oot where the deep •ng measuremen• were obtained. C is tbe East and West Crozier Ad•lie Pen•in rooked. depth changerates were obtained with depth-time recordersand glass capillary depth tubes. The glasscapillary tubes were much the same as the Teflon capillary tubes mentioned above. In this experimental situation the tubes were tied to the foot and removed usually after each dive while the bird was resting in the water. The depth-time recorder used was a clock and pressuregauge arranged to record continuously against time on a smoked glass disk. The entire unit was housedin a water-tight aluminum cylinder. The total out-of-water was 700 g. A 1.9-cm wide cotton webbing halter was placed on the pcngnin to which the depth- time recorder was attached by means of qnick-rcleasesnaps. Swimming speedswere obtained by training the birds to swim between two holes 27 m apart. The bird was released into the station hole where it dived until it found the other hole, which was not covered by a hut. After finding the outdoor hole the bird swamto it immediately whenever releasedin the station hole. During these experimentsan observer always watched from the sub-ice observation chamber, which was placed between the two holes, to determine whether the birds swam directly to the other hole and to plot visually the profile of the dive and record the wingbeat rate. The observerwas aided in preparing his profile plots by a line with markings at 3-m intervals hanging from the entrance. All snow was removed from the ice for a 30-m radius from the hut and water transparency was such that the observer could easily see both the entrance hole, 6 m away, and the exit hole, 21 m away. 778 KOOYStAq_'q',DRABEK, ELS•ER, AB?DCA3.•I•BELL [Auk, Vol. 88

,.o 80

c• w

2O

0-1 I-3 3-6 6-9 9-12 12-1515-18 18+ DURATIONOF DIVE (MIN)

Figure 3. Histogram analysis of 238 dive durations obtained from 10 adult birds.

All birds for the experimentaldives were collectedfrom groups gathering at the ice edge, which was located at Cape Royds in 1967 and Cape Bird in 1968. Only two birds at a time were captured and flown to the dive station, 25 to 50 km south of open water. Experiments were not begun until the following day, and the hold- ing pen was a 1.2 X 3.7-m plywood box with a snow-covered floor. rates and other respiratory patterns were obtained by direct observations of birds at the station hole. The birds weighed from 21.3-29.5 kg with a mean weight of 24.5 kg. Sex differenceswere not determined. October 1971] Emperor Penguin Diving Behavior 779

RESULTS

DIvI•o CAPACITmS

Duration.--Dive durations of birds in natural conditions are difficult to time precisely becausethey dive in groups and individual birds are impossibleto singleout. If the whole groupis treated as a singleunit, the result is approximatelythe averagesubmergence of all birds. When we timed birds this way and were reasonablyconfident that only one group was being measured,we obtained durations ranging from 2.5 to nearly 9 minutes. All were instancesduring which the birds appeared to be feeding. A total of 238 dive timeswere measured during the experimentalstudies at the dive station. Most of the diveswere less than 1 minute (Figure 3), and many of theseshort dives represented the penguin'sattempts to get out of the ice holeby divingto about3 m, ascendingrapidly, and leaping clearof the water. The majorityof divesfrom 1-6 minutesrepresented exploratoryforays by the birdsin the vicinity of the hole. During these dives they would investigatethe sub-icechamber, attempt to pierce throughthe thinner,but impenetrableice wherethe chambertube passed throughthe ice, and perusebright areasin the ice. They wouldalso go to depthson thesedives often beyondthe range of the viewer. Dive durationsin excessof 6 minuteswere also exploratory in nature,but in thesecases they wereprobably out of visualcontact with the stationhole and chamberfor portionsof the dive,and their lengthis possiblyrelated to the degreeof disorientationand difficulty in relocatingthe hole. The longestdive recordedwas one wherethe bird neverreturned, although it was seen swimmingnear the chamberafter 18 minutes submersion. Depth.---Almost all depth measurementswere obtained with small capillarydepth tubes, weighing only a few gramsand offeringlittle resist- anceto swimming,and it is unlikelythat they had muchof an inhibiting effect during the dives. Becausethe birds at the experimentalstation werediving alone,under thick ice, and in strangesurroundings, they were probably more interestedin obtaining information about the under-ice configurationthan diving deeply.As a result,the maximumdive measured of 38 m is much lessthan the depth estimateof 265 m we obtainedfor birdsdiving under more normal conditions (Tables 1 and 2). Descent and ascent rates.--These rates were measured in two ways: with a depth-timerecorder that givesa continuousrecord of depth against time for the entire dive; and by calculatingthe averagedepth-time change rate for the entire dive when the submersiontime and maximum depth are known. The latter method is necessarilyconservative because any time-consumingdeviations by the bird are part of the calculation. The 780 KOO¾•rAZq,DKaBEK, ELS•ER, AND CAkViPBELL [Auk, Vol. 88

TABLE 1 DEPTI:[ •IEASUREMEIqTS O•' INDIVIDUALS DIVING SINGLY AT Ti::IE EXPERIkViEIqTALDIVE STATION1

Depth in meters Penguin 0-10 10-20 20-30 30-40 B 6 13 22 38 4 15 22 30 7 15 24 7 15 24 8 15 2O 8 10 22 18 D 6 15 23 32 11 24 10

F 5 12 26 3 11 9 G 3o M 15 Total 9 14 9 4

1 Depths expressedin xneters for convenienceof conversion to pressure, 10 xn of depth equals approximately 1 atmosphere of pressure. maximumcalculated depth changerate was 72 m/rain and the maximum measuredrate was approximately120 m/rain (Table 3). It should be noted that when the depth changeof 120 m/rain (about 4.5 mph) was determinedthe penguin was encumberedby a harnessand depth-time recorderweighing 700 g. That the depth-timerecorder exerted a signifi- cant drag on the penguinswas confirmedby the chamberobservers who noted an obviousincrease in swimmingeffort when the unit was attached. When the instrumentpacks were on the birds, they seemedmuch more active and excited than birds not instrumented,consequently we were probably measuringescape or avoidancevelocities of the birds. The exceptionallyhigh ratesof changewere ascents from shallowdepths where

TABLE 2 DEPTYI MEASUREMENTSOF PENGUINS DIVING IN GROUPSAT CAPE CROZIER1' '*

Penguins Depth in meters

7 75 lO 265 14 240 15 130 18 45

Six of the 24 birds with recorderswere recovered,all within 3 hours. Maximum depth of 265 m equals 870 feet. October 1971] Emperor Penguin Diving Behavior 781

TABLE 3 DESCENT AND ASCENT RATES•

Descent Ascent

Depth Time Rate Depth Time Rate Penguin (sec) (m/min) (sec) (m/min) D 15 47 19 10 9 67 (Measured) 11 30 25 7 11 38 5 11 27

F 12 8 90 12 8 9O (Measured) 11 8 85 6 3 120 9 7 80 5 3 100 5 5 60 B 14 32 53 (Calculated) 17 37 55 17 55 37 18 30 72

:t Measured rate determined directly froin segmentsof dive profiles. Calculated average rate for dive estimatedby dividing maximumdepth by dive duration. the bird's bouyancy was assisting. The descentrates in both birds observedwere slower than ascent,and chamberobservers were also impressedwith the greatereffort to swimdown than up. Swimmingspeeds.--These estimates were obta/nedby timing penguins as they swam betweenholes a known distanceapart. Speedswere deter- minedonly after the birdshad learnedwhere the other hole was and had begunto swimdirectly to it after enteringthe water at the dive station. The fastestspeed recorded was 9.6 km/hr (5.2 mph) at whichtime the bird was averagingabout 4.9 m/wingbeat(Table 4). Distancecovered

TABLE 4 SWIMMING VELOCITIES AND WINGBEAT FREQUENCY

Speed Penguin ( km/hr ) B eat/min Meters/ beat H 7.4 7.6 5.7 9.4 9.4 49 2.8 5.4 40 1.9 6.3 30 3.0 7.8 41 2.7 8.3 8.5 9.6 29 4.8 6.3 24 3.9 7.6 33 2.7 5.4 31 2.5 782 KOOYMAl•I,DRABEK, ELSIgER,AND CAMPBELL [Auk, Vol. 88

DISTANCE(METERS) 5 I0 15 20 25 30 I I I I.• I

Figure 4. Dive profiles of a penguin swimming between two ice holes spaced 27 m apart. The ice thickness was about 1.5 m. Profile depths represent distance below the under-ice surface.

per wingbeat varied considerablydepending on whether measurement started while the bird was still acceleratingor after it had reached a constantspeed. During the trip from onehole to the other the bird usually swam at a shallowdepth, saving time and effort (Figure 4). The lower profile of Figure 4 representsone of the fastestspeeds the penguinsmade.

RESPIRATION The respiratorypattern seemsto indicate that recoveryfrom dives is rapid (Table 5 and Figure 5). The respirationrate increasesonly slightly after dives of less than 1 minute, but the rates increase markedly immediately after dives of more than 1 minute. When a bird returns from a dive it hyperventilatesvigorously. At this time inhalation is. through the open mouth and exhalationis with the mouth closed. When resting in the water, the bird's is very arrhythmic and the mouth re- mains closed. The pattern consistsof a deep inspiration, followed by apneusisfor a number of seconds.Expiration is a long sigh ended by anotherrapid, deepinspiration. Diving is usuallypreceded by a few rapid breathsand starts after what appearsto be a deep inspiration. The birds were never seen to exhale under water.

SHIVERING The Emperor Penguin'shabit of breedingduring the antarctic winter exposesit to extremelylow .Stonehouse (1953) recorded October 1971] Emperor Penguin Diving Behavior 783

TABLE 5 DIVE P•ECOVER¾P•ESPIRATIOBI P•TES

Dive duration Minutes after Surfacing (minutes) 1 2 3 4 5 < 1 N 5 3 3 3 3 X 7.2 5.7 6.3 5.3 4.3 ]R 5-10 4-7 4-10 3-7 3-6

14 N 19 14 7 4 4 • 13.6 8.3 5.4 5.2 3.7 R 7-22 5-17 2-9 4-7 3-5

4-8 N 17 6 4 4 4 • 16.0 9.3 5.5 6.0 4.5 R 12-25 7-18 5-6 5-7 3-5

•8 N 8 6 2 3 3 • 14.7 13.7 7.0 5.7 5.0 ]R 10-18 6-23 5-6 4-6

a low of -35øC at Dion Islets rookery, Pr•vost (1961) one of -30øC at the Pointe Geologierookery, and we noted a -45øC at Cape Crozier in September1968, which is certainly not the lowestwinter temperaturethat occursthere. Consequently,it was somewhatsurprising that a bird con- sideredto be so well-adaptedto cold would show any signsof discomfort after relatively short periodsof time in sea water of -1.9øC (Table 6). Four out of six birds appearedto shiversometime during the experiments. That this shiveringwas a responseto cold rather than trembling from fright or nervousreaction to the experimentalconditions is indicatedby the fact that its onsetdid not occuras soonas they were placed in the water, with the one importantexception of a moltingbird whosefeather coat was in poor conditionand who began shiveringimmediately after enteringthe water. Normally EmperorPenguins do no swimmingduring the molt. It is also interestingto note that when much active diving was involved,the onsetof shiveringoccurred later than when birds just restedin the water. Also, groupsof birds observeddiving in ice holes at CapeCrozier appeared to get out of the water at intervalsand preen, suggestingthat wheneverpossible the birdsprefer not to stayin the water for long, continuousperiods.

ORIENTATION Vision.--We soon found that we had to exercisecaution in conducting these experimentsbecause the birds on occasionappeared to become disoriented under the ice. Dives of more than 9 minutes reflected this con- fusionand probablysome of the shorterdives did also. Under-icediving is not a uniqueexperience for the birds, they not only dive under large floes 784 KOOYMAIg, DInaBEX, ELS•V•R, AND CAZVIPBEI,I, [Auk, Vol. 88

16 DIVE DURATION o = <1 MIN 14 ,•: I-4 MIN 0 = 4-8 MIN '• =>8 MIN

2

o I I I I I I 2 3 4 5 POST DIVE TIME (MIN)

Figure 5. Post dive respiration rates. The first 2 to 3 minutes after the dive breathing is regular and deep. If the surface time goes much beyond 3 minutes respirationbecomes arrhythmic with a sustainedinspiratory phase. October 1971] Emperor Penguin Diving Behavior 785

Figure 6. An isolated penguin hole about 1.5 km distant from the Ross Ice Shelf. The ice thickness at the hole was between 15-30 cm. in the pack ice, but we also saw them diving under a thin (ca. 30 cm thick) but extensivesea ice sheet at Cape Crozier. In this instancethe birds were swimmingbetween several isolated holes spacedfrom 240 to over 365 m apart (Figure 6). Some of the floes they dive under are no doubtseveral feet thick and probablyin somesituations they dive under thick fast ice throughscattered open leads. During our experimentswe saw birds make such errors as swimmingforcefully first, into the bottom of thick ice. Often this was in placesthat lacked the platelet ice coat sothe undersurfaceappeared brighter and apparentlydeceptively thin. One of our penguinswas so determinedto drive throughthe 2-m- thick ice that it selectedplaces where there was a 1-m-thicklayer of platelet ice collectedon the undersurfaceas well. In this instance the bird actuallydisappeared out of sight as it penetratedthrough the soft platelet layer to the firm sea ice above it. Once we recognizedthis orientationproblem we took a number of precautions.Still it wasremarkable to note that even thoughthe sub-ice chamber,which was a prominentunderwater reference point, was only 5-10 m fromthe stationhole, birds that cameto investigatethe chamber were sometimesconfused as to where the breathinghole was. In one casethe bird was near the chamber,started to swim towardsthe hole, turned around, appeareduncertain, and slowly returned towards the chamber. A strong light was then directed into the water from the breathinghole and the bird immediatelyregained its bearings. Acoustics.--Underwaterrecordings were made in two experiments 786 KOOYMA•q, DRABE,K,ELS•qER, ANr• CA•VmgLL [Auk, Vol. 88

TABLE 6 O•qSET O1*Sl•lVERIIq'G AlVTERWATER ENTRY

Penguin Shivering onsettime Time in Number of (min) water dives Shivering individuals B 60 7 dives B 34 No dives B 12 No dives C 100 20 dives D 65 27 dives D 60 33 dives M • Immediate

Nonshiveringindividuals F 46 5 dives G 62 10 dives

Molting bird.

during the penguins'first diving experienceat the station hole. Our equipment,Atlantic ResearchCorporation hydrophone and Martel tape- recorder,had an estimated frequency responseof 0.5-8 Khz. We noted no unusualsounds that might be attributed to the penguins,nor during our underwaterobservations did we see any indicationsof throat or body movementsthat suggestedvocalizations.

G•gNlgaaL SwmnxNo OBSEaVaTXONS Group behavior.--Emperor Penguinsare most often seen swimmingas a group that in our experienceseems to act as a fairly tight unit. The most extreme exampleof this unity was seen near the Cape Crozier rookery. The birds were diving at widely separatedholes in very thin sea ice (ca. 15-30 cm thick). A group of birds would suddenlyappear in the hole, almost in unison. Sometimesas many as 30 birds surfaced in a 3-m diameterhole (Figure 7). Then, as if on command,they all dived. Our open water observationsboth at Cape Royds and Cape Crozier were similar. Our only underwaterobservation of birds swim- ming togetherwas made near Cape Royds. The water depth was about 20 m and the birds swam as a group here also (Figure 8). In this case they often dived to the bottom and appearedto be searchingunder the scattered boulders. Posture.--Whenswimming submerged penguins pull the head in close to the body (Figure 8). The excursionduring the beat is great, the wing tips nearly touchon the upstrokeand then comefully down to the sides. Between strokes, when the bird is gliding, the are extendedlaterally. The birds have remarkablemaneuverability and can literally pivot on their wingsas they flip over and reversedirections. October 1971] Emperor Penguin Diving Behavior 787

Figure 7. Emperor Penguins surfacing in breathing hole 3 m in diameter. Ap- proximately 20 birds are shown, but as many as 30 birds at one time were counted in this hole.

Next to the wings the feet seem to be the most important guidance accessory.As the birds dive they kick their feet vigorously in unison, with the bottom of the foot facing dorsally. While cruisingthe feet may be held with the solesfacing each other, or they may be turned with the solesup. When comingto the surfacethe feet are turned down into the normal standing posture and act as a brake. The seemsto play a passiverole as a fixed rudder. The eyesare directeddownward and apparentlytheir best visual field is in this direction. There appearsto be someoverlap in the visual field in the frontal direction and even more so in the direction ventral to the beak that makes binocularvision possible.When birds approacheach other closelyor when a human approachesthem they often raise the beak and look at the intruder from the lower portionof the head. When swimmingunder the ice they must tilt their headsto one side in to see above. They were never noted to swim on their backs to make upward scanning easier. Com]ort movements.•ne behavior pattern of uncertain function is what appears to be in-water conditioning. Such patterns have been describedextensively in the by McKinney (1965), and a comprehensivereport of these movementsin Ad61ie Penguins is in preparation(Ainley, pers. comm.). While surfacedthe birds frequently roll onto one side, raise the uppermostflipper, and rake that side with the ipsilateralfoot. This maneuvermay servethe purposeof fluffing and combingwater out of the feathersto maintain their insulativeeffective- ness. The behavior has been noted in Emperor and Ad61iePenguins, both at the experimentaldive hole and in open water; it has also been 788 KOOYMAN, DRABEK, ELSNrR, ^X•O CANIPBELL [Auk, Vol. 88

Figure 8. Three Emperor Penguins swimming underwater. Note the tucked in position of the head, attitude of the feet with soles directed upward, and nearness of birds to each other. seen in Ad•lie Penguinsin our laboratory pools at Scripps Institution of Oceanographywhere the water temperatureis no lower than 56øC.

Discussion SUBMERSION ENDURANCE The physiologicaladjustments to prolonged submersionin birds has been studied in a few speciesof birds, mainly the domesticduck. The major features of these adjustments have been reviewed recently (Andersen, 1966) and the similarities between birds and are noted. Some of the more salient characteristicsof those diving birds studied are: blood volume as a function of per cent body weight is greater than in terrestrial birds (Andersen, 1966); upon submergencea rapid and profoundbradycardia develops (Bert, 1870; Scholander,1940; Eliassen, 1960); stroke volume seemsto remain the same (Johansenand Aakhus, 1963); cardiac output decreasesand blood flow to the muscles is reduced (Johansen,1964); and there is a depressionof metabolicrate October 1971] •Emperor Penguin Diving Behavior 789

(Scholander,1940; Pickwell, 1968). These parametersreflect a general circulatory redistributionthat enhancesasphyxial tolerancebecause those organscapable of extensive,anaerobic are isolatedfrom the circulatingblood , which is then conservedfor suchorgans as the brain and heart that have a relatively low resistanceto . Probably becauseof its availability the domesticduck has receiveda preponderanceof attention,but rather interestingis the fact that although it is a shallowwater feeder,it appearsable to stay submergedlonger than many of the true divers such as guillemots, , and some penguins. The longestexperimental dive that a bird has recoveredfrom was the forced submersion of a for 17 minutes where it had been trained not to exhaleduring the dive (Richet, 1899). By clampingthe trachea this sameinvestigator found that survival time in one duck was as long as 25 minutes. Forced submersionsof the , Eudypteschrysolophus for 5 minutesand the GentooPenguin, papua, for 7 minutes have been reported by Scholander(1940). The impressionwas that they were near their limit. Measured submersion durationsof unrestraineddivers are marked by their brevity. Dewar (1924) summarizesa number of speciesand no dives exceed2 minutes. No physiologicalexperiments have been performedon diving Emperor Penguins,but a comparisonof their submersionperformance to those of other aquatic birds indicates that such studies would be of interest. A duration of 18 minutesis especiallynoteworthy considering that the bird was swimmingactively during the dive. Emperor Penguin dive durationseven compare favorably with thoseof someof the muchlarger marinemammals, such as northernfur seals(Callorhinus ursinus) and California sea lions (Zalophus californianus) (see Irving, 1964; Harrison and Kooyman, 1968 for summariesof submergenceendurance). Conso- nant with this submersioncapacity are the data on ,the concentrationof which is about 17 g/100 ml of blood (Lenfant et al., 1969). This is high compared with that of most birds and in fact is greater than in many diving mammals(Lenfant, 1969).

PRESSURE EFFECTS The deepestdive we measuredof about 265 m is considerablygreater than the 60-m depth reported for the conxnonloon, Gavia iraruer, and the Old-squaw, Clangula byemalls (Schorger, 1947), which are the deepestreported for other speciesto our knowledge. We have noted what we believe to be feedingdives under circumstancessimilar to our depth- recordingexperiments at Cape Crozier when we measuredthe deep dives. In these supposedfeeding forays the birds were diving as a group, usually returning to the surfacenear where they originally submerged. 790 Koo•^•, DRABEl<,ELSNER, Ai'qD CAI•{PBEL• [Auk, Vol. 88

Upon surfacingthey often made head and neck motionssuggestive of swallowing.Breathing is exceptionallyheavy between dives of this kind. The diet of birds in the Cape Crozierarea wheremost of theseobserva- tions were obtainedappears to be ,based on the stomachcontents of chicksfound dead (LeResche,pers. comm.). Such a diet is significant becausewe believesquid in this area are primarily a deep-dwellinggroup. The rapid rates of depth changeand the diving depthswe recordedin this study are of interestbecause of both the internal pressureequalization problemsand gas absorption.So long as no obstructionsbetween various gas cavitiesoccur and somemeans exist of compensatingfor the internal changein gas volume,no equalizationproblem should develop. Volume- compensatingmechanisms in the penguin have not been investigated. The lack of pneumaticbones in penguinsis advantageousin a number of ways, one of which would be the eliminationof the need for pressure equilibration.Unlike seals,which dive with little air, penguinsseem to dive on inspirationand consequentlyhave a large volumeof air. This is of particularinterest in light of Richet's(1899) experimentsin which volumeof air in a duck'slungs and air sacsduring the dive seemeddirectly relatedto submergencecapability. Andersen (1959) and Pickwell (1968) haveshown that duringsubmergence birds utilize the oxygenin the air sacs. Thereforeone would expectgas absorptionto increasewith depth, which would seemto createa problemof blood oxygenregulation at depth and gas excretionupon rapid ascent. If so, a of both anoxia and gas embolismexists. No experimentaldata exist relevant to pressureeffects in birds. The little information available for diving mammalshas been reviewed recently (Scholander, 1964; Kooyman and Andersen, 1969) and the existingevidence supports the hypothesisthat in these probably little gas exchangeoccurs in the lungs during deep dives. On compressionthe structurallyweak lung alveoliare thoughtto becomemuch reducedif not atelectaticat depths as shallow as 30 m becauseof the high dead spaceto lung volumeratio and the rigidity of the bronchioles into which most of the alveolar gas is compressed.Because diving birds possessair sacs,they have a potentially much larger relative gas volume, and Emperor Penguinsalso dive on inspiration. Both of theseproperties would seem to be disadvantagesto deep divers unlessthey have some responsesto pressuredifferent from those of diving mammals. Experi- mentson greensea turtles, Cheloniamydas, have shownthat lung collapse and gas absorptionoccur (Berkson,1967). In this study it was found that under certain conditionsgas emboli did develop during . The problemsof anoxia during ascent from deep dives have been reviewed (Mithoefer, 1965; Schaefer, 1965), and the possibility that Emperor Penguinsmay utilize lung oxygen on deep dives raises the October 1971] Emperor Penguin Diving Behavior 791 questionof why they might not be susceptibleto this condition. Increased pressureresults in higher oxygen tensionswithin the lungs and blood. In man this enableshim to extend his diving time while at depth; but as he ascendsthe oxygen tension may drop to an anoxic level resulting in unconsciousness.This risk is especiallygreat if the swimmer hyper- ventilatesbefore the dive, thus reducingCO2 tensionand further lessening the urge to breatheat critical oxygentensions.

TEMPERATURE REGULATION Maintenance of body must require some exceptional in this ,not only for heat conservation,but for unloadingexcess heat during or after vigorousexercise. These problems have beenreviewed recently by Stonehouse(1970) who summarizeswhat little is known about the thermal characteristicsof Emperor Penguin .The subdermalfat thicknessis about 2 cm on the abdomen and back at the start of breeding,feather length is about 4 cm, plumage thickness1.0-1.5 cm, and heat flux acrossa dried and salted skin is slightly less than for other penguins,a pattern consistentwith the other valuesof plumageand fat thicknessthat are somewhatgreater than for other penguins. Circulatoryanatomy of the extremitieshas not beenstudied, but they very likely have some kind of heat conservingcirculatory adaptations such as counter- blood flow similar to that described for the (Scholander and Schevill, 1955). Of interest here is the fact that oneof our birds(D) cut its wingtip just beforethe divingexperi- mentsand bloodwas seenflowing freely from the woundfor nearly 2 minutesof the first dive. Continuedblood flow in suchsuperficial vessels during diving could result in considerableheat lossunless there was some kind of heat conservingmechanism such as the abovementioned counter- currentflow. This bleedingis also of particularinterest with regard to blood oxygen conservation.In Scholander's(1940) experimentswith forced-divedpenguins, blood flow to peripheral areas nearly ceased, indicatingmajor peripheralvasoconstriction and vascularshunting of blood. The short durationof the dive (2 minutes15 seconds)when we observedbleeding may indicatesome elective ability in bloodshunting during an anticipated short dive. Variation in respirationpatterns may also have a significant effect on the thermal balanceof theseanimals. The long drawn-out breathswhile restingin the water may result in considerablyless heat lost per amount of oxygenconsumed than the deep, open-mouthed,rapid breathingafter extendeddives. In addition, the short breath-holdsbetween inspiration and expirationpermit the resting bird to continuescanning underwater. 792 KOOY3/ZAN,DP•BE•:, ELSNER, AND CA•rPBELL [Auk, Vol. 88

ORIENTATION Little information is available on swimmingspeeds in aquatic birds and mammals. One Addlie Penguin (Pygoscelisadeliae) that learned to swim betweentwo breathing holes 120 m apart was timed at a rate of 7.2 kin/hr. Weddell seals have been observed to swim between holes 1.9 km apart at an averagespeed as high as 10.4 km/hr (Kooyman, 1968), and a trained porpoise(Stenella attenuata) was clockedat a top speedof 45 km/hr for a few seconds(Lang and Pryor, 1966). The maximumswimming speed that we measuredof 9.6 km/hr (15.3 mph), if assumedto be a sustainablerate, meansthat the birds could swim a total distanceof possibly3 km during an 18-minutedive. Even while diving in heavy pack ice or under most other conditionsthat the birds may find themselves,this shouldbe more than adequatefor swimming betweenspaces in ice floesor betweenholes in thin ice. If they dive betweenfar and widely separatedholes in thick ice, the risks become much greater with the increasingproblem of under-iceorientation. Unlike the Weddell seal, which seemsto have very exact under-ice orientationabilities and consistentpatterns of diving and exploratory behavior(Kooyman, 1968), the EmperorPenguin appeared to have no suchcharacteristics. In fact someof the erraticswimming behavior such as attemptingto pierceforcefully through 2-m thick ice gavequite the oppositeimpression. Yet as mentionedearlier, these birds must at times dive underice and undervery rigorousconditions, such as the antarctic night. Perhapsone important differencein our studiesand the natural conditionsis the advantage,as yet unstudied,of groupdiving. We found no evidenceof acousticorientation, and visual cues seemed to be of utmost importanceto our birds. Even when only a few feet from the hole,but in a positionthat resultedin the hole being visually obscured,the birds frequentlyseemed confused. During the swimming speedexperiments one bird made 11 dives before finding anotherhole only 27 m from the originalhole, and then only after a piece of 30-cm-ø foil was lowered into it. When the second bird was released the aluminum foil was already in place and the bird found the hole on the first dive. At Cape Crozier we watched groups of birds diving between scattered holesthat werevisually isolated from one another,which seems to suggest they need somethingmore than vision for safe navigation. However these holes were so numerousthat even during randomly deep diving belowthem the probabilityof comingto the surfacenear oneseems great. Also the network of refrozen cracks and other discontinuities in the ice shouldhave made good visual landmarks. October 1971] Emperor Penguin Diving Behavior 793

ACKNOWLEDGi•EIffTS This study was supported by the National Science Foundation (NSF GA 4038 and GA 13713 to G. L. Kooyman and GA 1215 to R. Eisner) through the Office of Polar Programs and by NIH Career Development Award KE HE 7469 to R. Elsner. The grants were administeredby the University of California, San Diego. Specialthanks are due to It. K. Lee and W. Boggs for assistancein scuba; R. Allison for making available and helping us with the Ad•lie Penguins; and J. J. Wright, M. Saltveit, and D. Foster for help at Cape Crozier. U.S. Navy Air De- velopment Squadron (VX-6) helicopter crews gave us outstanding support in the field, especiallyLcdr. J. Brandau, who sustaineda very painful injury while assisting us at Cape Crozier during the deep diving experiments.

SUMMARY The diving behavior of the Emperor Penguin was studied by several means: 1) direct observationfrom the ice edge, 2) an observationcham- ber, 3) scuba,and 4) direct measurementof dive depthsusing two kinds of depth-recorders.Dive durations were determined for 238 dives and the maximum submergencewas over 18 minutes. Of 40 depth measure- mentsobtained, the maximumwas 265 m. The most rapid depth change rate was a short ascentof 120 m/min; during such maneuversthe birds' bouyancyseems to assistthem greatly. Averageswimming speed for birds betweentwo holes27 m apart rangedfrom 5.4 to 9.6 km/hr. Respirationpatterns and shiveringvaried considerablydepending on the birds' activity. Respirationwas deep and rapid after prolonged dives,whereas after short divesor while restingin the water it became slowwith a very extendedexpiratory phase. The onsetof shiveringwas much delayedin birds diving actively when comparedto those just resting in the water. During experimentaldives singlebirds were often noticeablyconfused and uncertainof the location of the breathing hole. The birds seemed to rely on vision for under-iceorientation. Tape recordingswere made during some dives, and the birds made no obvious vocalizations. In addition to the orientationobservations, general swimming behavior of birds, such as group activity, posture, and maneuverabilitywere noted.

L•T•RATtm• C•T•D

A•DERS•, H. T. 1959. A note on the composition of alveolar air in tbe . Acta Physiol. Scand., 46: 240-243. A•D•RSE•, H. T. 1966. Physiological in diving . Physiol. Rev., 46: 212-243. B•Rxso•, H. 1967. Physiological adjustments to deep diving in the Pacific green turtle (Chelonia mydas agassizii). Comp. Biochem. Physiol., 21: 507-524. B•T, P. 1870. Leqonssur la physiolo•e compar•e de la respiration. Paris, Bail- libre. D•wA•, J.M. 1924. The bird as a diver. London, Witherby. 794 KOOYlVIAN,DRABEK, ELSNZa, ^Nn C^•VBELL [Auk, Vol. 88

ELIASSEN,E. 1960. Cardiovascularresponses to submersionasphyxia in avian div- ers. Arbok Univ. Bergen,Mat.-Nat., Ser. No. 2. FRYER,D. H. 1958. Cartographyand aidsto navigation.Pp. 438-465in A history of technology,vol. 5 (C. Singer,C. J. Holmyard,A. R. Hall, and T. I. Williams, Eds.). London, Oxford Univ. Press. I-I^RmSON,R. J., aND G. L. Koo¾•r^•. 1968. General physiologyof the pinnipeda. Pp. 211-296 in The behavior and of (R. J. Harrison, R. C. Hubbard, R. S. Peterson,C. E. Rice, and R. J. Schusterman,Eds.). New York, Appleton-Century-Crofts. IRVXNC,L. 1964. Comparative and physiologyof gas transport mecha- nisms.Pp. 177-212 in Handbook of physiology,section 3: Respiration,vol. 1 (W. O. Fenn and H. Rahn, Eds.). Washington,D.C., Amer. Physiol. Soc. Jo*t^•s•N, K. 1964. Regional distribution of circulating blood during submersion asphyxiain the duck. Acta Physiol. Scand.,62: 1-9. Jo*t^•sE•, K., ^•i• T. A^xrt•Js. 1963. Central cardiovascularresponses to sub- mersion in the duck. Amer. J. Physiol., 205: 1167-1171. Koo¾•^N, G.L. 1965. Techniquesused in measuringdiving capacitiesof Weddell seals. Polar Rec., 12: 391-394. Koo¾•vr^N,G. L. 1968. An analysisof somebehavioral and physiologicalcharac- teristicsrelated to divingin the Weddellseal. Antarctic Res. Ser., 11: 227-261. Koo¾•vr^N,G. L., ANnH. T. ANnERSVP.1969. Deep Diving. Pp. 65-94 in The biologyof marinemammals (H. T. Andersen,Ed.). New York, AcademicPress. L^NC,T. G., aND K. PRYOR.1966. Hydrodynamicperformance of porpoises (Stenellaattenuata). Science, 152: 531-533. L•NE^NT,C. 1969. Physiologicalproperties of bloodof marinemammals. Pp. 95- 110 in The biologyof marinemammals (H. T. Andersen,Ed.). New York, Academic Press. L•N•^•T, C., G. L. Koo¾•vr^N,R. E•;S•ER,^X• C. M. DR^Brae.1969. Respiratory functionof the bloodof the Ad•lie penguin,Pygoscelis adeliae. Amer. J. Physiol., 216: 1598-1600. McK•N•¾, F. 1965. The comfortmovements of Anatidae.Behaviour, 25: 120-220. M•T*tOEV•R,J. C. 1965. Breathholding.Pp. 1011-1026in Handbookof physiology section3: Respiration,vol. 2 (W. O. Fenn and H. Rahn, Eds.). Washington, D.C., Amer. Physiol. Soc. PmXWErr,G.V. 1968. Energymetabolism in ducksduring submergence asphyxia: assessmentby a directmethod. Comp. Biochem.Physiol., 27: 455-485. PR•.VOSI,J. 1961. Ecologiedu manchotempereur. Paris, Hermann. RXCaE•,C. 1899. De la r6sistancedes canards& l'asphyxie.J. Physiol. Pathol. Gert., 1: 641-650. SC**^•R, K. E. 1965. Circulatory adaptation to the requirementsof life under more than one atmosphereof pressure.Pp. 1843-1874in Handbook of physiol- ogy, section2: Circulation,vol. 3 (W. F. Hamilton and P. Down, Eds.). Wash- ington, D.C., Amer. Physiol. Soc. SC**O•^•nER,P. F. 1940. Experimental investigationson the respiratory function of diving mammals and birds. Hv&lradets Skrifter; Norske ¾ikenskapsAkad. Oslo, 22: 1-131. SC•rOL^NnER,P. F. 1964. Animals in aquatic environments: diving mammals and birds. Pp. 729-739 in Handbook of physiology, section 4: Adaptation to the environment. (D. B. Dill, Ed.). Washington, D.C., Amer. Physiol. Soc. October 1971] Emperor Penguin Diving Behavior 795

SCt{OI,AI•DER, P. F., AND W. E. SCiqEVILL. 1955. Counter-current vascular heat ex- changein the of whales. J. Appl. Physiol., 8: 279-282. SC•{ORGER,A. ¾V. 1947. The deep diving of the and the Old-squaw and its mechanism.;Vilson Bull., 59: 151-159. S•O•E•OUSE, B. 1953. The Emperor Penguin /orsterl. 1. Breeding behaviour and development. Falkland Islands DependenciesSurv., Sci. Rept. No. 6: 1-33. STOI•EI-IOLISE,B. 1970. Adaptation in polar and subpolar penguins (Spheniscidae). Pp. 526-541 in Antarctic ecology, vol. 1 (M. W. Holdgate, Ed.). London, Aca- demic Press. W•LSO•, E. A. 1905. On the whales, seals, and birds of and South Victoria Land. Pp. 469-492 in The voyage of the discovery (by R. F. Scott) vol. 2, appendix 2. London, Smith, Elder and Co. Physiological Research Laboratory, Scripps Institution of - ography,University of California, San Diego, La Jolla, California 92037. Present ad&ess of secondauthor: Department of Biological Sciences, University of Arizona, Tucson, Arizona 85721. Accepted 9 June 1970.