The resting metabolic rates of Laysan albatross and Bonin petrel
chicks of known age were measured on Midway Atoll in the North Pacific
Ocean. The mass-specific metabolism peaked at hatching and then declined to
adult levels in Laysan albatross nestlings. The mass specific metabolism of
hatchling Bonin petrels was similar to that of adults, but it tripled shortly after
hatching. Fasting and feeding episodes affected day-to-day changes in petrel
chick metabolism

Grant, Gilbert S.

Whittow, G Causey

Pacific Science

ScholarSpace at University of Hawai'i at Manoa

Pacific Science (1984), vol. 38, no. 2© 1984 by the University of Hawaii Press. All rights reservedMetabolic Rate of Laysan Albatross and Bonin Petrel Chickson Midway Atoll!GILBERT S. GRANT2 ,3 AND G. CAUSEY WHiTTOW2ABSTRACT: The resting metabolic rates of Laysan albatross and Bonin petrelchicks of known age were measured on Midway Atoll in the North PacificOcean. The mass-specific metabolism peaked at hatching and then declined toadult levels in Laysan albatross nestlings . The mass specific metabolism ofhatchling Bonin petrels was similar to that of adults, but it tripled shortly afterhatching. Fasting and feeding episodes affected day-to-day changes in petrelchick metabolism.METHODSThe metabolic rates of Laysan albatrosschicks of known age on Sand Island, MidwayAtoll (28°13' N, 177°23' W) were measured ina building immediately adjacent to the nestingsites. The chicks were placed in a small plexi-glas chamber or in an air-tight wooden box(0.7 m on all sides), depending on the size ofthe chick. In the latter instance, a plexiglascover allowed observation during a series ofmeasurements. Ambient air was drawnthrough the metabolic chamber by means ofavacuum pump. The flow rate (1-5liters ' min - 1) was adjusted to obtain a de-crease of approximately 1 percent in the O 2concentration from the air inlet to the outlet.The birds were weighed, to the nearest gram,on a Terraillon balance, immediately after thefinal metabolic measurements. All albatrossmetabolic measurements were made between1000-1800 hr , 21 January-14 Ma y 1981.Chamber temperatures ranged from 19.3to 26.0°C during these measurements.Mea surements could be made only until the107th day of nestling life, when we had toleave Midway; the birds fledge at 165 days.Metabolic measurements on Bonin petrelchicks of known age were made in a smallplexiglas chamber (kept in the building ad-jacent to the nesting site) at chamber tempera-tures of 21.3 to 29.0°C. All measurementswere between 1000-1900hr, 2 March to 19May 1981. The flow rate (ca. 200-500 cm": min -1) was also adjusted to achieve170THE RESTING METABOLIC RATES of chicks rep-resent the major part of their energy expen-diture, as they do not fly and their level ofactivity .is generally low (Blem 1978). Themetabolic rate increases as the chick growsbut the relationship between metabolic rateand body mass var ies during growth, the par-ticular pattern of variation depending on anumber of factors (Ricklefs 1974). In theProcellariiformes, which have relatively longnestling periods, the metabolic rate of grow-ing chicks is known only for Leach's storm-petrel , Oceanodroma leucorhoa (Ricklefs,White, and Cullen 1980a). The present notestems from the opportunity to study the re-lationship between metabolism and growth intwo other procellariiform species that differedgreatly in body size, and for which the meta-bolic rates of the developing embryos areknown (Pettit et aI. 1982a, 1982b). The twospecies studied (Laysan albatross, Diomedeaimmutabilis; Bonin petrel , Pterodroma hypo-leuca) share the same nesting sites in theNorthwestern Ha waiian Islands.1 Supported by National Science Found ation GrantNo. PCM 76-12351-AOIadministered by G. C. Whitlow.This study was supported also by the Sea Grant CollegeProgram (NIjR-14). Manu script accepted 14 December1983.2 University of Hawaii, John A. Burns School ofMedicine, Department of Physiology, and the PBRCKewalo Marine Laboratory, Honolulu , Hawaii 96822.3Present Address: North Caro lina State Museum ofNatural History, P.O. Box 27647, Raleigh, N.C. 27611.iiLUUaotJiCUl!iJIlLia::mtillUuiii, j·P 6 . 3 ' i i i , t :::tlrt:,W_ .l..IIWUlDPetrel Chick Metabolic Rate-GRANT AND WHITTOW 171a decrease of approximately I percent in theO 2 concentration between the inlet and out-flow from the chamber. Petrels were weighedon a torsion balance (OWL 5) to the nearest0.01 g, immediately after the metabolicmeasurements. Measurements were madeuntil a few days prior to fledging (mean ageof fledging = 82 days; Pettit, Grant, andWhittow 1982).Chicks of both species settled down withina few minutes and remained calm in the meta-bolic chambers during a series of measure-ments that typically lasted 3-5 hours.Metabolic values obtained for each individualon a particular day were similar and wereaveraged.Gas samples were collected in glass sy-ringes, the barrels of which were coated withmineral oil, and analyzed with a Scholandermicro-gas analyzer. All gas values are con-verted to standard temperature and pressurefor the dry gas (STPO). Two methods wereused in the field to ascertain the accuracy ofthe gas analyzer: (I) the composition of freshair , measured by the gas analyzer, averaged20.90 percent O 2 and 0.04 percent CO 2 (theexpected values), and (2) analysis of exhaustgases from the combustion of ethanol in thechamber. The respiratory quotient (RQ) ofcombusted ethanol should be 0.67. Wemeasured an ethanol RQ of 0.66 with theScholander micro-gas analyzer, providingconfirmation of its accuracy. The restingmetabolism was calculated from the mea-sured oxygen consumption (\'02) and RQ.Chamber temperatures were measured with acalibrated Kane-May Limited Depen-datherm instrument.RESULTSThe resting metabolism and mass of alba-tross chicks from hatching to 107 days ofage are presented in Figure I. Hatchling(age < I day) albatross metabolism wasmeasured by the open flow system and com-pared to values obtained with the closed man-ometric system used by Pettit et al. (I982a).The \'02 for a hatchling measured via the opensystem average 190cm3 0 2 ·hr- 1 , comparedwith a mean value of 159cm3 0 2·hr - 1measured by Pettit et al. (1982a). TheRQ of albatross chicks averaged 0.78(Figure I). The mass-specific metabolism(V02 -;- mass) peaked near hatching(0.77 cm ' °2 ' g -l . hr - 1) and declinedsteadily, reaching adult levels at approxi-mately 75 days (Figure I).The resting metabolism and mass of petrelchicks from hatching to 76 days ofage (withina week of fledging) are shown in Figure 2. TheRQ of petrel chicks averaged 0.76. Mass-specific metabolism tripled between hatchingand 2 days of age and declined to adult levelsat 20 days of age (Figure 2).DISCUSSIONThe mass-specific oxygen uptake ofthe Laysan albatross hatchling was0.77 em" °2 , g -l . hr - I-45 percent higherthan the adult rate of oxygen consumption ofthe Laysanalbatross (0.53 cm' °2 ' g-l . hr - 1;Grant and Whittow 1983) and also greaterthan that of the adult wandering albatross(Diomedea exulans; 0.5 em 3 O 2 • g - 1 • hr - 1;Brown and Adams 1984). The hatchling\'0 2 of Bonin petrels (1.1 cm ' °2 ' g-l . hr - 1;Pettit et al. 1982b) was similar to that ofadults(1.1 em:'°2 , g -l . hr - 1; Grant and Whittow1983). Mass-specific metabolism peaked tolevels nearly three times hatchling and adultvalues during the first few days of nestling lifein petrels but not in albatrosses. This funda-mental difference between the albatross andpetrel may be related to differences in the re-lative incubation periods and embryonicgrowth in the two Procellariiformes (Pettit etal. 1982a, 1982b). According to Ricklefs(1974), the maximal mass-specific metabolicrate occurs earlier in the precocial than in thealtricial chick. By this criterion, the Laysanalbatross is more precocial than is the Boninpetrel. However, by other criteria (e.g. , yolkcontent of the egg) petrels are considered to besemiprecocial (Nice 1962, Carey, Rahn, andParisi 1980, Ricklefs, White, and Cullen1980b) while albatross are semialtricial (Nice1962). Clearly, additional information isneeded on the metabolism during growth ofother species.172 PACIFIC SCIEN CE, Volume 38, April 1984Hatchling • Fledgling3600• •+••U) •U) 2400 •ca~12000Embryo Nestli ng Ad utt•• •• • •._-+· . -- - - --• •N 1000CI.>.8 ~ •\ I , • +•I ~ • • • •C¥ • •~ .7 •.6u-u.6+eu N •CI. CI •U) .=- • •I •U).3U)ca~0-4 0 25 75 125 165Age (days)F IGURE I. Mass (g), metabolism (Yo,; ern"°2 ' hr " "), RQ, and mass-specific metabolism (Vo,; em?°2 , g - I . hr - I)of Laysan albatros s embryos, nestlings, and adults in relation to age. Adult values (from Gr ant and Whittow 1983) arepresented as mean (horizontal bar) ± two standa rd deviat ions (vertical bar). Embryo and hatchling values are fromPettit et al. (1982a). Curves are fitted by eye. The bro ken line indicates extrapolated values (see text).,j, ! . I A AA • iii i . , I;;;; lA- .. M i., p i I .i ;.tti :; ,ga ;. #1 'kt:.oPetrel Chick Metabolic Rate- G RANT AND WHITTOW 173-6 0 12 24 36 48 60 72Hatchling Fledgling300•• • • ••• •U') 200U') +fa •::E1 0 00Em btyo Nestling Adult• •• •• •• tN 200 .--c •.>.8•••• •• • ho- •• • +• • • •• • • • • •C¥ • • •CI:: .7 •. 6....... . . ..-3o••12 24• • •36 48•••60I72• +Age (days)FIGURE 2. Mass (g), metabolism (Yo, ; cm3 . °2 ' hr - ' ), RQ, and mass-specific metabolism (Yo, ;ern" .°2 , g-I .hr- ') of Bonin petrel embryos, nestlings, and adults. Adult values (from Grant and Whittow 1983)are .presented as mean (horizontal bar) ± two standard deviations (vertical bar) . Embryo and hatching values are fromPettit et al. (1982b). Cur ves are fitted by eye. The broken line indicates extrapol ated values (see text).174 PACIFIC SCIENCE, Volume 38, Apri11984T ABLE IO XYGEN COST OF D EVELOPMENT IN THR EE P ROCELLARII FOR M C HICKSSPECIESTOTAL O 2COST OF CHICKDEVELOPMENT(lite rs)FLEDGLINGMASS-HATCHLI NGMASS(g)OXYGEN COSTPER GRAM OFCHICK*(liters-g - 1)Oceanodroma leucorhoaPterodroma hypoleucaDiomedea immutabilis• Total O2 cost/fledgling mass- hatchling mass.tFrom Ricklefs, White, and Cullen 1980a.IFrom Palmer, 1962.§From Pettit et al. 1982b.IFrom Pettit, Grant, and Whittow 1982.*From Pettit et al. 1982a.• • From Fisher 1967.209.3 t393.44,43 9T ABLE 240.51I77§,1I1,792 * '**5.172.222.48O XYGEN COS T OF EM BRYONIC AND C HICK D EVELOPMENTO 2 COSTOF EMBRYONICDEVELOPMENT %OF(liters) TOTALO 2 COSTPER GRAM OFYOLK- FREEHATCHLING(liters-g - 1)O 2 COSTOF CHICKDEVELOPMENT %OF(liter s) TOTALTOTAL O 2COST OFDEVELOPMENT(chick + em bryo)(liters)Pterodroma hypoleucaDiomedea immutabilis• Pettit et al. 1982b.tp ett it et al. I98211.5.6*29.7 t1.40.70.2180.178393443998.699 .3398.64468 .7The total amount of oxygen consumedthroughout the nestling period can be esti-mated by measuring the area under the VO2curve (Figures I and 2). Bonin Petrel chicksconsumed approximately 373 liters of oxygenduring the first 78 days of nestling life. Theaverage fledging time for this species was 82days (Pettit, Grant, and Whittow 1982); ex-trapolation of the V0 2 curves in Figure 2 to 82days yielded an estimate of 393.4 liters for thetotal oxygen cost ofchick development (TableI). The estimate for the Laysan albatross re-quired a greater degree of extrapolation andthe resulting figure of 4439 liters is corre-spondingly lessexact. Table I also includes anestimate for Leach's storm-petrel, which issmaller than the Bonin petrel. When the totalamount of oxygen consumed is divided by themass of body tissue synthesized (fledglingmass minus hatchling mass), it is clear that theoxygen cost per gram of tissue is higher inLeach's petrel than in the Bonin petrel orLaysan albatross. It is possible that the meta-bolic rate of Leach 's petrel was elevated at theair temperature at which the measurementswere made so that its higher oxygen cost ofdevelopment might be construed to imply ahigher energy allocation to thermoregulation.The figure for the oxygen cost per gram oftissue is even higher (6.11 liter ' g - 1) in thedark-rumped petrel (Pterodroma phaeopygia),a species that breeds at high altitude in theHawaiian Islands (Simons and Whittow, pers.comm.).Using data published previously (Pettit etal. 1982a, 1982b) it is possible to compare thecost of embryonic development with that ofdevelopment of the chick, and also to com-pute the total oxygen cost of embryonic andchick growth (Table 2). As expected, the costof growth of the chick greatly exceeds the costof embryonic growth. The cost of embryonic1 2 ·2 if t,! ' ; O· f ' ttltj : @,;;ttO, J iJ...JUIPetrel Chick Metabolic Ra te- GRANT AND WHITTOW250r-- - .....,- - - -r- - - "'T""- - - ,......- - .....,.- - - ""T"- - - "'T""- - --, 250175II ::~I II '" II .~ .... I225 / I 225/"{ / / <j I/ Mass II / /- 2 4 24 I II II , ~ Ma ss I I en'"/ / I I en= 200 % I~,' I 200 '".:> / ,F' I I , ~/ , I I..J• _ _ _ I F/ /-~V0 2,,-'//1 75 I , 75.//I/< ::150 1 50t::7.~=:=====: ~ . t::7= =: . 7. 737 38 3 9 4 0 41 4 2 4 3 4 4 45Age (days)FIGURE 3. Simultaneous mass (g), O2 consumption (Vo, ern" °2 , hr - t ) , and RQ values for a Bonin petre l chickduring 8 days, involving four feeding (F) episode s and several fasting episodes (up to 4 days long in one instance ). Theinset shows the relat ionship between the increases in Va, and mass associated with feeding and decreases during fastingintervals. The regression line for this relationship is as follows: Ll Va, = I.2lLlmass + 0.543; (r 2 = 0.980, n = 7).growth in the Bonin petrel, which has therelatively longer incubation per iod, is aslightly grea ter percentage of total costs tha nin the Laysan albatross. Comparison ofTab les 1 and 2 reveals also that the oxygencost of a unit mass of chick is considerablygreater tha n that of an embryo.Much of the day-to-day variation in Va(F igure 2) in the petrel chick can be attributedto feeding history. In Figure 3 we have plottedVa 2' mass , and RQ of a petrel chick over 8days involving four feeding episodes andseveral days of fasti ng. The insert shows theconcurrent changes in Va with cha nges inmass . V0 2 and mass incre~sed with feedingand decreased during prolonged fasts.The relative ly low RQ values for both theLaysan albatross and Bonin pet rel suggestthat they were largely metabolizing fa tsduring the fasting periods an d also after beingfed. This would be in accord with the highproportion of stomach oils in the diet s of Pro-cellariiform chicks (Fisher 1972, Im ber 1976).The rest ing metabolism of a growing chickrepresents the energy expended in the syn-thesis of new tissue , thermoregulation, andphysio logica l activity (maintenance). Thepresent data do not permit an ana lysis of theresting metabolism into these components.However, the similar values for mass-specificmetabolic rates ofhatchlings and adults in theBonin petrel, and the post-hatching increasein mass-specific metabolism, were phenom-ena not observed in the Laysan albatross.They seem to be worthy of further study interms of the allocation of energy to variousfunctions in the chicks of small and largespecies.In summary, the mass-specific metabolismpeaked at hatching, and declined to adultlevels during the first third or half of nestlinglife in the Laysan albatross. In the Bonin176petrel, the mass-specific metabolism was si-milar in the hatchling and adult but increasedconsiderably shortly after hatching. The RQremained essentially con stant throughout thenestling period in both species and most of theday- to-day changes in metabolism in theBonin petrel were due to episodes of fastingand feeding .ACKNOWLEDGMENTSWe are grateful to J . C. Barnes, command-ing officer, for assistance during our stay atthe U.S. Naval Air Facility, Midway Atoll,and to the U.S. Fish and Wildlife Service forgra nting permits for this work.LITERA TURE CITEDBLEM, C. R. 1978. The energetics of youngJapanese quai l, Coturnix coturnix japonica.Compo Biochem. Ph ysiol. 59A: 219-223 .BROWN, C. R., and N. J. ADAMS. 1984:Basal metabolic rate and energy expend!"ture during incubation in the wanderingalbatross (Diomedea ex ulans). Condor 86 :182-186.CAREY, c., H . RAHN, and P. PARISI. 1980,Calories, water, lipid and yolk in avianeggs. Condor 82: 335-343.FISHER, H. 1972. The nutrition of birds. Pages431-469 in D. S. Farner and J . R. King, eds.Avian biology, vol. 2. Academic Press, NewYork.FISHER, H. I. 1967. Body weights in LaysanPACIFIC SCIENCE, Volume 38, April 1984albatrosses Diomedea immutabilis. Ibis109: 373-382.GRANT, G. S., and G . C. WHITTOW. 1983.Metabolic cost of incubation in the Laysanalbatross and Bonin petrel. CompoBiochem. Physiol. 74A :77-82.IMBER, M . J . 1976. The origin of petrelstomach oils-a review. Condor 78: 366-369.NICE, M . M . 1962. Development of behaviorin precocial birds. Trans. Linnean Soc .N .Y. 8: 1- 211.PALMER, R. S., ed. 1962. H andbook of NorthAmerican birds. Vol. 1. Yale UniversityPress, New Haven. 567 pp .PETTIT, T . N., G . S. GRANT, and G . C.WHITTOW. 1982. Body temperatures andgrowth of Bonin petrel chicks. Wilson Bull.94:358-36 1.PETTIT, T . N., G. S. GRANT, G . C. WHITTOW,H. RAHN, and C. V. PAGANELLI. 1982a.Embryo nic oxygen consumption andgro wth in the Laysan and black-footedalbatross . Amer. J. Physiol. 242:R I2 1-R 128. .- - -. 1982b. Respirat or y gas exchange andgrowth of Bonin petrel embryos. Ph ysiol.Zoo l. 55 : 162- 170.RICKLEFS, R. E. 1974. Energetics of repro-duction in birds. Pages 152- 292 in R. A.Paynter, ed . Avian energetics. Publ. NuttallOrnithol. Club, No. 15. Cambridge,Massachusetts.RICKLEFS, R. E. , S. C. WHITE, and J . CULLEN.1980a. Energetics of postnatal gro wth inLeach 's storm-petrel. Auk 97: 566-575 .--- . 1980b. Postnatal deve lopment ofLeach's storm-petrel. Auk 97 :768-781.,,, ::2£ #(1 .. § fIL l C ' { w .. p,e: ',-, . iii.4iW#'5tlWift:e:5 m#

Metabolic Rate of Laysan Albatross and Bonin Petrel Chicks on Midway Atoll

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Metabolic Rate of Laysan Albatross and Bonin Petrel Chicks on Midway Atoll

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