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Ecology and Physiology of Fasting in King Penguin Chicks

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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 body mass(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 par- allel 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' feeding visits 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.
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