Ecology and Physiology of Fasting in King Penguin Chicks

ECOLOGY AND PHYSIOLOGY OF FASTING IN KING PENGUIN CHICKS

YVES CHEREL,l JEAN-CLAUDESTAHL, 2'3 AND YVON LE MAHO l •Laboratoired'Etude des R•gulations Physiologiques, associf d l'Universit•Louis Pasteur, CentreNational de la RechercheScientifique, 23 rue Becquerel,67087 Strasbourg, France, and 2Institutdes Sciences de l'Evolution,Universitf des Sciences et Techniquesdu Languedoc, PlaceEugene Bataillon, 34060 Montpellier, France

ABSTRACT.--CaptiveKing Penguin (Aptenodytespatagonica) chicks can fast for 5 months during the subantarcticwinter with a 70%decrease in bodymass. To investigatethe adaptive value of this remarkableresistance to starvation,we comparedcaptive chicks with free- ranging chicksin their colony at PossessionIsland, Crozet Archipelago.The chicksin the colony,from mid-April to beginningof September(i.e. all winter) were fed only every 39 daysby their parents;some were not fed at all. In spring(October-December) the surviving chickswere fed every 6 days,and their growth was completed.Overall chick mortalityin the colonyduring the winter and subsequentspring was about 50%. Mortality was highest in October,6 monthsafter the beginningof the winter, and may be attributedmainly to starvation.The decreasein body massin the free-rangingchicks was remarkably similar to that for captivebirds. In both groups,three periodswere characterizedaccording to the observedchanges in the daily decreasein body massper unit bodymass (dm/mdt): dm/mdt droppedduring the first period(I) of 5-6 days,was minimumand steadyduring periodII, which lastedabout 4 months,and increasedin period III. Bloodanalysis of the captivechicks indicated the three periods correspondto modificationsin protein breakdown. An initial decreasein uricacidemiaindicates period I is a short period of transition, marked by a decreasein protein breakdown. In period II a minimum and constanturicacidemia, in parallel with a progressiveincrease in ketonemia,indicates efficient protein sparingwhile most of the energy is derived from lipids. Period III is critical because,from a rise in uricacidemia concomitantwith a decreasingketonemia, proteins are no longer spared.The extremeresis- tanceof King Penguinchicks to starvationin winter may be explainedpartly by the ability to spareproteins for severalmonths (period II). It occursat a growth stagewhen the parents' feedingvisits are rare. Other laboratoryand field investigationsof birds suggestthat the meansby which a wide variety of domesticand wild speciesadapt to fastingalso may be interpreted in terms of three periodscorresponding to changesin protein breakdown.Re- ceived6 June 1986, accepted30 October1986.

RECENTphysiological data show that King lasts about 11 months. This prolonged down Penguin (Aptenodytespatagonica) chicks resist stage may be divided into three parts (Stone- starvation in winter remarkably well. At 3-4 house 1960, Barrat 1976). First, from hatching months of age they may tolerate a fast of 4-6 in mid-January,the chicks are fed regularly; months and a 70% decrease in body mass they grow rapidly and reach a body mass of (Cherel and Le Maho 1985). King Penguin 10-12 kg in 3-4 months. Then, from May to chicks are fed infrequently during winter and August during the austral winter, the chicks have a very high mortality due to starvation are left alone for long intervals and not fed. (Stonehouse 1960). No quantitative informa- Their body mass falls to about two-thirds or tion seems to be available on the duration of one-half of the autumn maximum. When the the fast or the rate of decreasein body mass. parents resume feeding (October-December), The adaptive significanceof the extreme resis- growth is completed, and the chicks molt be- tance to starvation observed in experimental fore going to sea. chicks therefore remains poorly understood. A wide variety of birds fast and exhibit a The fiedging period of King Penguin chicks decreasein body massduring certain stagesof their annual life cycle. Birds fast when food is scarce(Trautman et al. 1939), but also when it 3 Present address: National Museum of New Zea- is plentiful if they are engaged in other im- land, Private Bag,Wellington, New Zealand. portant activities that compete with feeding,

254 The Auk 104:254-262. April 1987 April 1987] Fastingin KingPenguin Chicks 255 such as incubation, molting, and migration TABLE1. Feedingfrequency in King Penguinchicks (Mrosovskyand Sherry 1980). Although there during winter and spring. has been recent interest in the energetics of Feeding birds fastingduring breeding (Croxall 1982,Le frequency Maho 1984), to our knowledge there are no No. of No. of (no. days/ comparisonsof physiologicaldata on fastingin mealsa daysb no. meals) captive birds with similar data on free-ranging Winter animals. May 5 227 45.4 We report here the changes in body mass, June 4 353 88.3 ratesof feeding, and mortality in free-ranging July 10 296 29.6 King Penguin chicksduring winter and spring, August 12 330 27.5 i.e. during seasonsof food shortageand growth, Spring respectively. We measured also fast duration October 14 103 7.4 November 23 106 4.6 and changesin body massand plasmaconcen- December 10 82 8.2 tration of uric acid and •-hydroxybutyrate (•- aIn winter determinedby visual observationsof 20 chicks;in spr•ng OHB) in captive chicks. Uric acid is the major determined by daily weighings of 5 chicks. nitrogen excretory product in birds (Poulson • Total number of days of weighingsor visual observationsfor all and MacNabb 1970) and is an index of protein chicks. breakdown in penguins (Robin et al. 1983). On the other hand, an increase in plasma concen- 5 nonmolting chicks in mid-October (spring group) tration of •-OHB, the main ketone body in were kept in captivity at the station. BecauseKing birds, characterizesthe part of a fast during Penguin chicksare at thermoneutrality under natu- which most energy is derived from lipids (Le ral ambient conditions, both in winter and summer Maho et al. 1981). (BarrS1984), there was no complicationof tempera- ture regimebetween the colonyand the station.Wind velocity was usually higher in the stationthan at the MATERIALS AND METHODS colony,however, so we protectedthe captivechicks from the wind. Water was provided ad libitum.The Field and experimentalstudies were performedat animalswere weighed daily with a platform balance Possession Island, Crozet Archipelago (46ø25'S, (accuracy_+20 g). A 5-ml blood sample was taken 51ø45'E),between April and December, during the from a flipper vein by heparinizedsyringes every 2 subantarcticwinter and following spring.Two groups daysduring the first 10 days of fasting and every 3 of King Penguin chickswere used:free-ranging birds days thereafter. The hematocrit of King Penguin in the breeding coloniesof Baiedu Marin and chicks chickswas maintained at 42-45% (Cherel and Le Maho caught in these coloniesand kept in the nearby sta- 1985). Blood was collectedimmediately in polyeth- tion. ylene microtubesat 5øCand centrifuged. Plasmawas Free-rangingchicks.--Fifty-five King Penguin chicks deproteinized in 7% perchloric acid and the super- were banded in the breeding colony. Twenty-five natant solution neutralized with 10% KOH for the were usedto determine the beginning of winter star- enzymatic determination of/•-OHB (Williamson and vation, from the time they were no longer fed by Mellanby 1974).Uric acidwas assayed on whole plas- their parents.Changes in body massand rate of feed- ma using the uricase method (Scheibe et al. 1974). ing were followed in 10 other chicks.Five birds were Student'st-tests were used for statisticalcompari- studied during the austral winter, from June to mid- sons.Values given in the text are means _+SE. September,and the other 5 during spring, from mid- Octoberto November. These 10 chickswere weighed RESULTS daily with a pesola-typebalance (accuracy+100 g). The remaining 20 banded chicks were observedvi- FREE-RANGING CHICKS sually, and every feeding visit of the adults during winter was noted. The parents were banded also to Winter starvation.--The 25 King Penguin monitor their presencein the colony. chicks on the colony started winter starvation The mortality rate of chicks during winter and on 15 April + 2.3 days. For 20 banded chicks springwas estimatedby countingthose birds appar- ently dying as a result of weaknessbecause of star- watchedfrom the beginning of May to the end vation in a predetermined area of the colony con- of August,the mean interval betweentwo suc- taining 186 chicks at the beginning of April. cessiveparental feeding visitswas 39 days (Ta- Experimentalchicks.--Seven King Penguin chicks ble 1). It is unlikely that this interval was over- caughtin the secondhalf of May (winter group) and estimatedbecause of undetectedadult feeding 256 CHEIL, STAHL,,AND LE MAHO [Auk, Vol. 104

8 30 •'•....=..Bird A ' 6 n- 20

>- o • •o 3 BirdB•"*•--v• o

25 50 75 100 o A M J J A S O N D TIME, days of fasting MONTH I JUNE I JULY I AUGUST'•-- Fig. 2. Mortality during the fledging period in Fig. 1. Rate of decreasein body massin 2 free- King Penguin chicks,expressed as a percentageof ranging King Penguin chicksfasting during winter. the total number of birds that died from starvation The birds began fasting before time 0. Bird B died during April through Decemberin a defined colony from starvation;bird A was still fasting at day 100. area. Seetext for explanationof open symbols.

However, it increasedto 33.3 and 37.0 g.kg -•' visits becausethe parents stayed ashore with 24 h -• in the two chicks that died. their offspring for as long as 1.9 + 0.5 days From the area of the colony demarcatedat (range 1-11 days, n = 20). Thus, during the the beginningof April, only 94 of the 186chicks winter period of May through August, these left for the sea in December. We estimated the King Penguin chicks received on the average overall mortality during winter and spring to only 3 meals. be 49%. The mortality rate was biphasic(Fig. None of the 5 other chicks (which were 2). A first peak occurredin April-May, and ac- weighed daily) were fed from 1 June to mid- counted for one-third of the overall mortality. September,a period of 100 days. Overall, they Mortality was relatively low until October, presumablyfasted for about 150 days,because, when it increased greatly; one-fourth of the as indicated above, the chicks in the colony overall mortality occurred during this month. started to fast in mid-April. Thus, they had al- Mortality droppedthereafter until the end of ready been starved for 40-50 days on 1 June. the fledging period in December. In June these 5 chicks had a mean body mass In a colonyof King Penguins,it is difficult of 6.6 + 0.3 kg (range 6.1-7.4 kg); it was 3.4 + to find chicks that have died from starvation, 0.4 kg (range2.6-3.7 kg) in mid-September.This becausedying chicksare rapidly consumedby representsa 49 + 3% lossin massduring the Hall's (Macronecteshalli) and Antarctic (M. gi- 100 days of the study. The decreasein body ganteus)giant-petrels. The mean body massof mass of these chicks was curvilinear (a linear 11 undamagedcorpses collected in September regressionthrough a semi-log plot gave a bet- was 2.9 + 0.1 kg, similar to the body massesat ter fit than a linear regressionthrough the un- death of the 2 birds out of 5 that were weighed transformeddata), excepta terminal sharp drop daily (seeabove). for two birds (e.g. open symbolsfor bird B in Spring growth.--As previously described Fig. 1) that starved to death at body massesof (Stonehouse1960), the King Penguin chicksre- 2.6 and 2.8 kg. ceived considerablefood from their parents in If an animal losesa constantmass dm per 24 spring and began to fatten. From October to h throughout the starvation period, dm repre- December the mean interval between two meals sents an increasing proportion of instanta- was 6.2 days(Table 1), and until the beginning neousbody massm; therefore,the specificdai- of molt, the body massesof the 5 free-ranging ly changein bodymass dm/mdt better expresses birds increased41% from 7.9 + 0.4 kg (range the rate of changein mass(Le Maho et al. 1981, 6.4-8.6 kg) to 11.1 _+ 0.4 kg (range 10.5-12.2 Cherel and Le Maho 1985). In each of the five kg). King Penguin chicks,dm/mdt was maintained The patternin the changesin body massof at a steady value, and ranged from 5.5 to 7.8 each of the 5 free-ranging chicks was a se- g.kg-•-24 h -• (• = 6.4 + 0.4 g'kg-•'24 h-l). quenceof sharprises in body massafter every April1987] Fastingin KingPenguin Chicks 257

10 20 30 40 50 60

TIME, days

JOCTOBER I NOVEMBER I DECEMBER- Fig. 3. Changein body massin a free-ranging

King Penguinchick during spring growth and molt. o@

3 / •-o meal (1.8 _+ 0.1 kg, range 0.5-3.6 kg, n = 47) followed by a decreaseuntil the next feed (Fig. ,, ...... I x 3). During the first 24 h of fasting, the mean 0 25 .5o 75 •00 125 150 dm/mdt was 71.6 _+2.8 g.kg-t.24 h • (n = 47); TIME, days of fasting it decreasedto 33.2 _+ 3.2 g.kg-t.24 h -• (n = 33) the third day and stabilized at 14.0 _+ 0.4 g.kg -•.24 h -• (n = 7) the sixth day after feed- Fig.4. (A) Rateof bodymass decrease during fasting. ing in winter in a captive King Penguin chick. (B) Specificdaily changein body mass(drn/rndt) during EXPERIMENTAL CHICKS fasting.(C) Plasma/•-hydroxybutyrate (/•-OHB) and uric acid concentrationsduring fasting. See text for Winter group.--Seven King Penguin chicks definition of periods I, II, and III. were capturedat the end of their first growth phase,i.e. at their maximal body massbefore winter starvation.The initial body massof the g. kg-•. 24 h •, dependingon the bird. Thiswide chicksaveraged 12.08 kg; after 166days of fast- range suggeststhe chicks had begun to fast at ing the averagewas 3.35 kg, a lossof 72%in 5- different timesbefore being caught.During pe- 6 months (Table 2). The decreasein body mass riod II (133 _+5 days), dm/mdt was maintained of the 7 birds was characterizedby three pe- at a meanvalue of 6.3 _+0.2 g. kg-•. 24 h • (range riods (Fig. 4A). During period I, which lasted 5.7-7.7 g.kg-*.24 h •). In contrast, period III 6-9 days, there was a rapid decrease in body (24 + 2 days) was characterizedby a sharp in- mass and a decreasein dm/mdt. During the creasein dm/mdt that was 21.2 _+1.5 g.kg -•. first day of captivity, dm/mdt was 11.5-61.1 24 h ' on the last day of fasting (Fig. 4B).

TABLE2. Changein body massof experimentalfasting King Penguin chicksduring winter and spring. Values are means_+ SE, with rangesin parentheses.

Duration of fasting Initial body mass Final body massa Decreasein Season (days) (kg) (kg) body mass(%) Winter 166 + 5 12.08 + 0.12 3.35 + 0.07 72 + 1 (n = 7) (152-184) (11.56-12.50) (3.00-3.58) (70-76) Spring 10 10.98 + 0.21 8.25 _+0.21 25 + 1 (n = 5) (10.58-11.63) (7.78-9.03) (22-28) Final refersto the end of the experiment,i.e. winter birdsfasting until periodIII o[ fasting,spring birds until the beginningof periodII. 258 CHEREL,STAHL, AND LE MAHO [Auk,Vol. 104

sampleswere lactescent.For two birds, lactes- cencewas still presentin the bloodsampled on • PeriodI PeriodII the third day. This indicatesactive digestion • 50 very soonafter the last meal before capture. In period I, plasma uric acid concentration decreasedby 77%from the firstto the fifth day • 25 •«•o-•-.•.__.__.of fasting. It then stabilized in period II at 0.25 + 0.02 mmol/1 (Fig. 5B). By contrast,the fi-OHB level increasedby 60% during the 10 " 1.0 days of starvation.

DISCUSSION

ø-' i King Penguin chicks tolerate a 72% decrease in body massduring a winter fast. This is com- a i *' parableto a 63-66%body mass loss in Common 2 4 6 8 10 Swift chicks (Apus apus;Koskimies 1950). We found remarkablesimilarity in the way body TIME, days of fasting mass decreasedin free-ranging and captive Fig.& (A) Specificdaily change in bodymass (din / chicksduring long-termfasting. The rateof de- mdt), and (B) plasma uric acid concentration,in 5 creasein body massof captive birds has been captiveKing Penguinchicks during a 10-dayfast in found previouslyto reflectprotein breakdown; October(spring). See text for definitionof periodsI therefore,physiological data obtainedon cap- and II. Mean values ß SEM (not drawn when 2 SEM tive King Penguinchicks probably provides re- were lessthan the heightof the symbols)are shown. liable informationon how free-rangingchicks adapt to starvation. The changesin plasma uric acid concentra- The growth curve of free-rangingKing Pen- tion paralleledthose in dm/mdt (Fig. 4C). In guin chicksin spring was marked by a succes- period I the decreasein plasma uric acid con- sion of sharp increasesin body massalternat- centration was highly variable in the chicks, ing with more gradual decreases(Fig. 3). The presumablybecause they had startedto fast at short decreases were similar to those that char- differenttimes before being caught. During pe- acterizedperiod I in captive birds. The longer riod II plasma uric acid concentrationdid not drops(Fig. 3) were similar to period I plus the vary significantly,and remained at a low value beginning of period II in the captivebirds. Be- (0.17 + 0.01 mmol/1). During period III it in- causeboth groupsof winter birdsprobably had creasedto 0.97 + 0.08 mmol/1. By contrast, fastedfor differentperiods before the studybe- plasmaconcentration of fi-OHB increasedpro- gan, the early responsesto starvation cannot gressively during period II (from 1.90 + 0.22 be compared.During prolongedfasting in the to 4.51 + 0.31 retool/l) and decreasedrapidly winter birds, however, the pattern of the in period III (to 0.50 + 0.11 mmol/1). changein bodymass in free-rangingchicks (Fig. Springgroup.--The mean initial body massof 1) was similar to that defined as periodsII and the 5 King Penguin chickswas 10.98 kg, and III in the experimentalbirds (Fig. 4). Thus, the after 10 daysof fastingtheir meanbody mass specificdaily change in body mass,dm/mdt, was 8.25 kg. They lost about 25% of their initial was similar over the three periods. Nearly bodymass (Table 2). PeriodI lasted6 + i days. identical values were then observed in each dm/mdt was 75.0 + 7.7 g.kg-*-24 h-• during group in spring and winter (Table 3). the first 24 h of fasting,but declinedsharply The highest rate of decreasein body mass afterward (Fig. 5A). It reached 34.7 + 3.8 wasduring the first daysof fasting(beginning g-kg •.24 h -• the third day and stabilized at of period I) in both groupsof birds in spring 13.6+ 0.5 g.kg-•.24 h-• betweendays 6 and (Table 3). This confirmsprevious data from ex- 10 of starvation,i.e. at the beginningof period perimental King Penguin chicks and adults (Le II (Fig. 5A). Maho and Despin 1976, Bart6 1984). Much of After the initial 24 h of captivity,all plasma this initial decreasein body masswas presum- April 1987] Fastingin KingPenguin Chicks 259

T^BLE3. Specificdaily changein body mass(g.kg-•.24 h-•) during the three periods of fasting in King Penguin chicks.Values are means + SE.

Period of fasting Beginningof End of Season Status period I Period II period III Spring Free-ranging 71.6 + 2.8 14.0 + 0.4 (n=47) (n=7) Experimental 75.0 + 7.7 13.6 + 0.5 (n = 5) (n = 5) Winter Free-ranging 6.4 + 0.4a 35.2 + 1.9 (. = 5) (n = 2) Experimental 6.3 + 0.2a 21.2 + 1.5 b (n = 7) (n = 7)

0.001 comparedwith spring birds. 0.005 comparedwith free-rangingchicks. ably related to the productionof urine and feces Emperor Penguins (Aptenodytesforsteri; Robin (Koskimies 1950, Ricketts and Prince 1984). The et al. 1986). early reduction of the plasma concentrationof The period III decrease in the plasma con- uric acid (Fig. 5), suggeststhat the observed centrationof O-OHB of experimentalbirds, as drop in dm/mdt also was due in part to a de- uricacidemia increased abruptly (Fig. 4), ac- creasein protein utilization. cords with earlier data (Cherel and Le Maho Digestion in King Penguinsoccurs over less 1985) indicating that this period is marked by than 2 days (Copestake et al. 1983), but there an increase in protein catabolism.There is a was still a 3-4-fold decrease in dm/mdt in the characteristic increase in dm/mdt. The final, following days, until the end of period I. This rapid decreasein body mass in chicks that additional decrease may be attributed princi- starved to death (Fig. 1) indicates they died pally to reduced protein catabolism,as there while in this period of increasedprotein utili- was a parallel decreasein plasmauric acid con- zation. These chicks presumably would have centration (Fig. 5). Thus, in their colony King survived if their parents had returned earlier, Penguin chicks reduce protein utilization as period III is reversiblein Emperor Penguins within only a few days of fasting. (Le Maho 1984). In spring and winter the minimum, steady The values of dm/mdt reached near death in values of dm/mdt characterizing period II in the free-living chickswere higher than those the captive chickswere similar to thosefor the at the end of the fast in the experimental birds free-ranging chicks (Table 3). The progressive (Table 3). In captive birds the fast was always increase in ketonemia in captive birds, while interrupted before it endangeredthe life of the uricacidemia remained minimum and constant, animal. is consistent with earlier experimental data Adaptivesignificance of winter fastingin King (Cherel and Le Maho 1985) indicating that pe- Penguinchicks.--King Penguin chicks are fed riod II is a long phase of protein sparing and infrequently during the australwinter because lipid mobilization. In spring, however, the of the uncertain and erratic availability of food chicks lost massat twice the rate of period II in the sea (Stonehouse 1960). The high adap- in the winter fast (Table 3). If body massat the tive value of the ability of chicksto resiststar- end of period II is similar for both spring and vation is clearly related to the low feeding rate winter birds,period II probablylasts only about in winter. We estimatedonly one meal every 62 days in spring vs. 133 days in winter. This 5-6 weeks. A 2-4-week interval had been in- difference might be due to more efficient pro- dicatedpreviously, but it was an underestimate tein sparing in the winter, becauseplasma uric becausenone of 10 King Penguin chickskept acid concentrationduring period II was lower during the winter in a pen accessibleto the in winter than in spring (Figs.4C and 5B). Such parentswas fed during a 12-day period. Two seasonal differences were observed in adult other chicks,observed daily for one month in 260 CHEREL,STAHL, AND LE MAHO [Auk,Vol. 104 their colony, fasted continuously (Stonehouse chicks(Fig. 3). There are large changesin body 1960). A large proportion of King Penguin massfrom day to day, dependingon the amount chicksprobably fast all winter (Fig. 1). This fail- of food received and the duration of each bout ure to feed did not seem to result from the of fasting (Tickell 1968).Chicks of Gray-headed disturbancecaused by weighings: the 5 free- (D. chrysostoma)and Black-browed (D. mela- rangingchicks that were weigheddaily in spring nophris)albatrosses also respond to fasting by were fed normally, and grew and molted like an initial drop in body mass followed by a other chicks in the colony. steadycurvilinear decline, like the adults dur- The ability of King Penguin chicksto fast all ing incubationshifts (Prince et al. 1981, Rick- winter in their colony is consistentwith the etts and Prince 1984). All of these observations previousobservation (Stonehouse 1960) that the are consistentwith periods I and II. largestpeak in mortalityoccurs in October,about Incubatingfemale ducksand geeseeat little 6 months after the beginning of winter. Stone- or nothing, and generally lose about 40% of house(1960) indicated that only birds weighing their prebreedingbody mass.Carcass analyses at least 6 kg at the beginning of winter can fast indicate significantamounts of pectoralmuscle the entire period. The smallerpeak in mortality and gizzard protein are used regularly during observedat the beginning of winter (Fig. 2) may this spontaneousfast, but most of the energy be attributed to the smallest chicks, which are is derived from fat, and lipid storesare essen- either inadequatelyfed or too young, and there- tially exhaustedby the time of hatching(Milne fore unable to starve for a long time. 1976, Korschgen1977, Ankney and Macinnes Threeperiods of fastingin birds.--The three pe- 1978,Raveling 1979).In late incubation,how- riods that characterizethe changesin protein ever, some females leave their nests to feed utilization during fasting in captive King Pen- while others starve to death (Korschgen1977, guin chicks(Cherel and Le Maho 1985),captive Ankney and Macinnes1978). Failed nesters still adult EmperorPenguins (Le Maho et al. 1976, have a relatively high muscle protein content, Groscolas and Clement 1976), and domestic but dead birds have depletedboth fat and pro- geese(Le Maho et al. 1981)also occur naturally tein stores(Ankney and Macinnes 1978). This in King Penguin chicksin their colony. suggeststhe femalesare usually at the end of Early reports indicated that pheasantsand period II at hatching,whereas those that leave domesticfowl and geeseadapt to experimental their nest before chicks hatch may have en- fasting by initially decreasingtheir rates of tered period III. Some birds die on the nest body massloss and nitrogen excretion.These while in prolongedperiod III. The protein de- rates are maintained at a reduced level for sev- pletion describedin seabirdsafter long storms eral days and then increase(Schimanski 1879, (Duron et al. 1984) and in waterfowl during Phillips et al. 1932,Benedict and Lee 1937,Er- prolongedcold weather (Trautman et al. 1939) rington 1939).These early datademonstrate the may correspondto period III. three periods of fasting more recently de- The high rate of energy expenditureof mi- scribed in captive birds (Le Maho et al. 1976, grating birds due to the costof flying contrasts 1981; Cherel and Le Maho 1985). Period I, a with the fasting birds achieving the lowest short period of transition,is marked by a con- possibleenergy expenditure.It has been sug- siderable decreasein the relative rate of body gestedthat it is beneficialfor a migratingbird massloss and by high fat mobilization. Period to lose protein mass(pectoral muscles).The II, a long phaseof economy,exhibits a low rel- suppositionis that flight muscleswork at a ative rate of decreasein body mass;most of the power output near maximum efficiencyearly energy expenditurederives from lipids, and in the flight and, becauseof the decreasein proteinsare spared.Period III, the critical pe- transportedmass, well below maximum effi- riod, is characterizedby an increasein the rel- ciency toward the end of the flight. By con- ative rate of body massloss and coincideswith stantly using surplusmuscle as a fuel reserve, a risein proteinutilization while there still are the working conditionsfor the remaining mus- availablelipid stores. cle would be maintained nearer to those for Field data on the Wandering Albatross (Di- maximumefficiency (Pennycuick 1975). It is then omedeaexulans) have shown that the chicks' remarkablethat during migrationbody massin growth curvesresemble those of King Penguin passerinesis lost throughlosses of dry lipids, April 1987] Fastingin KingPenguin Chicks 261 and the nonfat 'body mass remains constant DURON, M., M. J. LECESTRE,& P; DURON. 1984. Mor- (Odum et al. 1964, Odum 1965). This may cor- talit• de la Mouette Tridactyle sur le littoral de respondto an extreme situation of period II in la Vend•e au PaysBasque. Courrier de la Nature which proteins are totally spared. However, 90: 12-16. protein depletion has been described in birds ERRINGTON,P. L. 1939. The comparativeability of that have encountered unfavorable winds the Bobwhite and the Ring-necked Pheasant to withstand cold and hunger. Wilson Bull. 51: 22- (Odum et al. 1964,Odum 1965),suggesting they 37. are in period III. GROSCOLAS,R., & C. CLEMENT. 1976. Utilisation des Our findings on King Penguin chicksaccord r•serves •nerg•tiques au cours du je•ne de la with data available for a wide variety of birds reproduction chez le Manchot Empereur, Apte- either starving under natural conditionsor ex- nodytesforsteri. C. R. Acad.Sci. Paris S•r. D 282: perimentally fasted.Such data may provide an 297-300. understanding of the strategy of wild species KORSCHGEN,C. E. 1977. Breeding stressof female for survivingiong-termfasting. Eiders in Maine. J. Wildl. Mgmt. 41: 360-373. KOSKIMIES,J. 1950. The life of the Swift, Micropus apus(L.), in relation to the weather. Ann. Acad. Sci. Fennicae Ser. A IV 15: 1-151. . ACKNOWLEDGMENTS LE MAHO, Y. 1984. Adaptations m•taboliques au We are indebted to Dr. S. Dejours for help in ed- jefineprolong• chez l'oiseau. J. Physiol.Paris 79: iting. We thank Mrs. O. Frain and Mr. S. Liess for 113-119. their technicalcontribution. This studywas support- , P. DELCLITTE,& J. CHATONNET. 1976. Ther- ed by grants from Terres Australeset Antarctiques moregulation in fasting Emperor Penguins un- Fran9aisesand from CNRS (Action Th6matiquePro- der naturalconditions. Amer. J. Physiol.231: 913- gramm6e'No. 4584,"R6ponses physiologiques et bio- 922. chimiquest• des situationsvitales critiques,"and Re- ß& B. DESPIN.1976. R•duction de la d•pense cherche,'Coop6rativesur Programme No. 764, •nerg•tique au coursdu jefine chez le Manchot "Ecosyst•mesterrestres subantarctiques et antarc- Royal (Aptenodytespatagonicus). C. R. Acad. Sci. tiques"); Paris S•r. D 283: 979-982. --, H. Vu VAN KHA, H. KOUBI,G. DEWASMES,J. GIRARD,P. FERRE,& M. CAGNARD.1981. Body LITERATURE CITED composition, energy expenditureß and plasma ANKNE•,C.D., & C.D. MACINNES. 1978. Nutrient metabolitesin long-term fasting geese.Amer. J. Physiol. 241: E342-E354. re•rvesand reproductive performance of fe~ mile Lesser Snow Geese. Auk 95: 459-471. MILNE, H. 1976. Body weights and carcasscompo- sition of the Common Eider. 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