Pacific Science (1984), vol. 38, no. 2 © 1984 by the University of Hawaii Press. All rights reserved

Metabolic Rate of Albatross and Bonin Petrel Chicks on !

2 2 GILBERT S. GRANT ,3 AND G. CAUSEY WHiTTOW

ABSTRACT: The resting metabolic rates ofLaysan 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.

THE RESTING METABOLIC RATES of chicks rep­ METHODS resent the major part of their energy expen­ diture, as they do not fly and their level of The metabolic rates of Laysan albatross activity .is generally low (Blem 1978). The chicks ofknown age on Sand Island, Midway metabolic rate increases as the chick grows Atoll (28°13' N, 177°23' W) were measured in but the relationship between metabolic rate a building immediately adjacent to the nesting and body mass var ies during growth, the par­ sites. The chicks were placed in a small plexi­ ticular pattern of variation depending on a glas chamber or in an air-tight wooden box number of factors (Ricklefs 1974). In the (0.7 m on all sides), depending on the size of , which have relatively long the chick. In the latter instance, a plexiglas nestling periods, the metabolic rate of grow­ cover allowed observation during a series of ing chicks is known only for Leach's storm­ measurements. Ambient air was drawn petrel, Oceanodroma leucorhoa (Ricklefs, through the metabolic chamber by means ofa White, and Cullen 1980a). The present note vacuum pump. The flow rate (1-5 stems from the opportunity to study the re­ liters ' min - 1) was adjusted to obtain a de­

lationship between metabolism and growth in crease of approximately 1 percent in the O 2 two other procellariiform species that differed concentration from the air inlet to the outlet. greatly in body size, and for which the meta­ The were weighed, to the nearest gram, bolic rates of the developing embryos are on a Terraillon balance, immediately after the known (Pettit et aI. 1982a, 1982b). The two final metabolic measurements. All albatross species studied (Laysan albatross, Diomedea metabolic measurements were made between immutabilis; Bonin petrel, Pterodroma hypo­ 1000-1800 hr, 21 January-14 Ma y 1981. leuca) share the same nesting sites in the Chamber temperatures ranged from 19.3 Northwestern Ha waiian Islands. to 26.0°C during these measurements. Mea surements could be made only until the 107th day of nestling life, when we had to leave Midway; the birds fledge at 165 days. 1 Supported by National Science Found ation Grant Metabolic measurements on Bonin petrel No.PCM 76-12351-AOIadministered by G. C. Whitlow. This study was supported also by the Sea Grant College chicks of known age were made in a small Program (NIjR-14). Manu script accepted 14 December plexiglas chamber (kept in the building ad­ 1983. jacent to the nesting site) at chamber tempera­ 2 University of Hawaii, John A. Burns School of tures of 21.3 to 29.0°C. All measurements Medicine, Department of Physiology, and the PBRC Kewalo Marine Laboratory, Honolulu , Hawaii 96822. were between 1000-1900hr, 2 March to 19 3Present Address: North Caro lina State Museum of May 1981. The flow rate (ca. 200­ Natural History, P.O. Box 27647, Raleigh, N.C. 27611. 500 cm": min -1) was also adjusted to achieve 170

iiLUUaotJiCUl!iJIlLia::mtillUuiii, j·P 6 . 3 ' i i i , t :::tlrt:,W_ .l..IIWUlD Petrel Chick Metabolic Rate-GRANT AND WHITTOW 171 a decrease of approximately I percent in the measured by Pettit et al. (1982a). The

O 2 concentration between the inlet and out­ RQ of albatross chicks averaged 0.78 flow from the chamber. Petrels were weighed (Figure I). The mass-specific metabolism on a torsion balance (OWL 5) to the nearest (V02 -;- mass) peaked near hatching 1 0.01 g, immediately after the metabolic (0.77 cm ' °2 ' g -l . hr - ) and declined measurements. Measurements were made steadily, reaching adult levels at approxi­ until a few days prior to fledging (mean age mately 75 days (Figure I). of fledging = 82 days; Pettit, Grant, and The resting metabolism and mass of petrel Whittow 1982). chicks from hatching to 76 days ofage (within Chicks of both species settled down within a week offledging) are shown in Figure 2. The a few minutes and remained calm in the meta­ RQ of petrel chicks averaged 0.76. Mass­ bolic chambers during a series of measure­ specific metabolism tripled between hatching ments that typically lasted 3-5 hours. and 2 days of age and declined to adult levels Metabolic values obtained for each individual at 20 days of age (Figure 2). on a particular day were similar and were averaged. Gas samples were collected in glass sy­ DISCUSSION ringes, the barrels of which were coated with mineral oil, and analyzed with a Scholander The mass-specific oxygen uptake of micro-gas analyzer. All gas values are con­ the Laysan albatross hatchling was I-45 verted to standard temperature and pressure 0.77 em" °2 , g -l . hr - percent higher for the dry gas (STPO). Two methods were than the adult rate ofoxygen consumption of 1 used in the field to ascertain the accuracy of the Laysanalbatross (0.53 cm' °2 ' g-l . hr - ; the gas analyzer: (I) the composition of fresh Grant and Whittow 1983) and also greater air, measured by the gas analyzer, averaged than that of the adult wandering albatross 3 20.90 percent O 2 and 0.04 percent CO 2 (the (Diomedea exulans; 0.5 em O 2 • g - 1 • hr - 1; expected values), and (2) analysis of exhaust Brown and Adams 1984). The hatchling 1 gases from the combustion of ethanol in the of Bonin petrels (1.1 cm ' ' g -l . hr - ; \'0 2 °2 chamber. The respiratory quotient (RQ) of Pettit et al. 1982b) was similar to that ofadults 1 combusted ethanol should be 0.67. We (1.1 em:' °2 , g -l . hr - ; Grant and Whittow measured an ethanol RQ of 0.66 with the 1983). Mass-specific metabolism peaked to Scholander micro-gas analyzer, providing levels nearly three times hatchling and adult confirmation of its accuracy. The resting values during the first few days of nestling life metabolism was calculated from the mea­ in petrels but not in albatrosses. This funda­ ) sured oxygen consumption (\'02 and RQ. mental difference between the albatross and Chamber temperatures were measured with a petrel may be related to differences in the re­ calibrated Kane-May Limited Depen­ lative incubation periods and embryonic datherm instrument. growth in the two Procellariiformes (Pettit et al. 1982a, 1982b). According to Ricklefs (1974), the maximal mass-specific metabolic RESULTS rate occurs earlier in the precocial than in the The resting metabolism and mass of alba­ altricial chick. By this criterion, the Laysan tross chicks from hatching to 107 days of albatross is more precocial than is the Bonin age are presented in Figure I. Hatchling petrel. However, by other criteria (e.g., yolk (age < I day) albatross metabolism was content ofthe egg) petrels are considered to be measured by the open flow system and com­ semiprecocial (Nice 1962, Carey, Rahn, and pared to values obtained with the closed man­ Parisi 1980, Ricklefs, White, and Cullen ometric system used by Pettit et al. (I982a). 1980b) while albatross are semialtricial (Nice

The \'0 2 for a hatchling measured via the open 1962). Clearly, additional information is 3 1 system average 190cm 0 2 ·hr- , compared needed on the metabolism during growth of 3 1 with a mean value of 159cm 0 2·hr- other species. 172 PACIFIC SCIEN CE, Volume 38, April 1984

Hatchling Fledgling 3600 • • •

U) •• U) • ca 2400 • ~ + 1200

0 Embryo Ad utt Nestli ng • • • • • • - -- · . -- - • • ._-+ N 1000 CI .>

.8 ~ \ , • • I• I ~ • • • • C¥ • • + ~ .7 •

.6

u

-u .6 eu N CI. CI • • U) .=- • I • • U) .3 + U) ca ~ 0 -4 0 25 75 125 165

Age (days) I F IGURE I. Mass (g), metabolism (Yo,; ern" °2 ' hr" "), RQ, and mass-specific metabolism (Vo,; em? °2 , g-I . hr - ) of Laysan albatros s embryos, nestlings, and adults in relation to age. Adult values (from Grant and Whittow 1983) are presented as mean (horizontal bar) ± two standa rd deviat ions (vertical bar). Embryo and hatchling values are from Pettit 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:. Petrel Chick Metabolic Rate- G RANT AND WHITTOW 173

-6 0 12 24 36 48 60 72

Hatchling Fledgling 300 • • • • • • • • U') 200 U') fa • + ::E 1 0 0

0 Em btyo Nestling Adult • • • • • • • N 200 .-- c • .> t

o

.8 • • ••• •• • • • • ho-•• • •• • • • C¥ • • •• .7 + CI:: •

. 6

• - 3 •

• •• ...... ••• I • +

o 12 24 36 48 60 72

Age (days)

3 FIGURE 2. Mass (g), metabolism (Yo, ; cm . °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 from Pettit et al. (1982b). Cur ves are fitted by eye. The broken line indicates extrapol ated values (see text). 174 PACIFIC SCIENCE, Volume 38, Apri11984

T ABLE I

O XYGEN COST OF D EVELOPMENT IN THREE P ROCELLARII FOR M C HICKS

TOTAL O 2 FLEDGLING OXYGEN COST COST OF CHICK MASS-HATCHLI NG PER GRAM OF DEVELOPMENT MASS CHICK* SPECIES (liters) (g) (liters-g - 1)

Oceanodroma leucorhoa 209.3 t 40.51 5.17 Pterodroma hypoleuca 393.4 I77§,1I 2.22 Diomedea immutabilis 4,43 9 1,792 * '** 2.48

• 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.

T ABLE 2

O XYGEN COS T OF EM BRYONIC AND C HICK D EVELOPMENT

O 2 COST TOTAL O 2 O 2 COST PER GRAM OF O 2 COST COST OF OF EMBRYONIC YOLK- FREE OF CHICK DEVELOPMENT DEVELOPMENT %OF HATCHLING DEVELOPMENT %OF (chick + em bryo) (liters) TOTAL (liters-g- 1) (liters) TOTAL (liters)

Pterodroma hypoleuca 5.6* 1.4 0.218 393 98.6 398.6 Diomedea immutabilis 29.7t 0.7 0.178 4439 99.3 4468 .7

• Pettit et al. 1982b. tp ettit et al. I98211 .

The total amount of oxygen consumed Leach's petrel than in the Bonin petrel or throughout the nestling period can be esti­ Laysan albatross. It is possible that the meta­ mated by measuring the area under the VO2 bolic rate ofLeach's petrel was elevated at the curve (Figures I and 2). Bonin Petrel chicks air temperature at which the measurements consumed approximately 373 liters ofoxygen were made so that its higher oxygen cost of during the first 78 days of nestling life. The development might be construed to imply a average fledging time for this species was 82 higher energy allocation to thermoregulation. days (Pettit, Grant, and Whittow 1982); ex­ The figure for the oxygen cost per gram of trapolation ofthe V0 2 curves in Figure 2 to 82 tissue is even higher (6.11 liter ' g- 1) in the days yielded an estimate of393.4 liters for the dark-rumped petrel (Pterodroma phaeopygia), total oxygen cost ofchick development (Table a species that breeds at high altitude in the I). The estimate for the Laysan albatross re­ Hawaiian Islands (Simons and Whittow, pers. quired a greater degree of extrapolation and comm.). the resulting figure of 4439 liters is corre­ Using data published previously (Pettit et spondingly lessexact. Table I also includes an al. 1982a, 1982b) it is possible to compare the estimate for Leach's storm-petrel, which is cost of embryonic development with that of smaller than the Bonin petrel. When the total development of the chick, and also to com­ amount of oxygen consumed is divided by the pute the total oxygen cost of embryonic and mass of body tissue synthesized (fledgling chick growth (Table 2). As expected, the cost mass minus hatchling mass), it is clear that the of growth of the chick greatly exceeds the cost oxygen cost per gram of tissue is higher in of embryonic growth. The cost of embryonic

1 2 ·2 if t,!' ; O· f ' ttltj : @,;;ttO, J iJ...JUI Petrel Chick Metabolic Rate- GRANT AND WHITTOW 175

250r--- .....,--- -r--- "'T""--- ,...... -- .....,.--- ""T"--- "'T""-- --, 250 I I I I I I I . ~'" I 225 .... 225 / = / , I~,' I I I , ~'" F' , I I / •_ __I ..J / ~ F/ , ,-' / - V / 1 75 0 2 I , 75 /. / I / < :: 150 1 50

t::7 ~ ~ t::7 = . . =

. 7 : .7 37 38= 3 9 4:=====:0 41 4 2 4 3 4 4 45 Age (days)

t FIGURE 3. Simultaneous mass (g), O 2 consumption (Vo, ern" °2 , hr - ), and RQ values for a Bonin petre l chick during 8 days, involving four feeding (F) episode s and several fasting episodes (up to 4 days long in one instance). The inset shows the relat ionship between the increases in Va, and mass associated with feeding and decreases during fasting intervals. 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 the proportion ofstomach oils in the diets ofPro­ relatively longer incubation period, is a cellariiform chicks (Fisher 1972, Im ber 1976). slightly grea ter percentage of total costs tha n The resting metabolism of a growing chick in the Laysan albatross. Comparison of represents the energy expended in the syn­ Tables 1 and 2 reveals also that the oxygen thesis of new tissue, thermoregulation, and cost of a unit mass of chick is considerably physio logica l activity (maintenance). The greater tha n that of an embryo. present data do not permit an analysis of the Much of the day-to-day variation in Va resting metabolism into these components. (F igure 2) in the petrel chick can be attributed However, the similar values for mass-specific to feeding history. In Figure 3 we have plotted metabolic rates ofhatchlings and adults in the Va 2' mass, and RQ of a petrel chick over 8 Bonin petrel, and the post-hatching increase days involving four feeding episodes and in mass-specific metabolism, were phenom­ several days of fasti ng. The insert shows the ena not observed in the Laysan albatross. concurrent changes in Va with cha nges in They seem to be worthy of further study in incre~sed mass . V0 2 and mass with feeding terms of the allocation of energy to various and decreased during prolonged fasts. functions in the chicks of small and large The relatively low RQ values for both the species. Laysan albatross and Bonin petrel suggest In summary, the mass-specific metabolism that they were largely metabolizing fats peaked at hatching, and declined to adult during the fasting periods and also after being levels during the first third or half of nestling fed. This would be in accord with the high life in the Laysan albatross. In the Bonin 176 PACIFIC SCIENCE, Volume 38, April 1984 petrel, the mass-specific metabolism was si­ albatrosses Diomedea immutabilis. Ibis milar in the hatchling and adult but increased 109: 373-382. considerably shortly after hatching. The RQ GRA NT, G. S., and G . C. WHITTOW. 1983. remained essentially con stant throughout the Metabolic cost of incubation in the Laysan nestling period in both species and most ofthe albatross and Bonin petrel. Compo day- to-day changes in metabolism in the Biochem. Physiol. 74A :77-82. Bonin petrel were due to episodes of fasting IMBER, M . J. 1976. The origin of petrel and feeding . stomach oils-a review. Condor 78: 366­ 369. NICE, M . M . 1962. Development of behavior in precocial birds. Trans. Linnean Soc . ACKNOWLEDGM ENTS N .Y. 8: 1- 211. PALMER, R. S., ed. 1962. H andbook of North C. We are grateful to J. Barnes, command­ American birds. Vol. 1. Yale University ing officer, for assistance during our stay at Press, New Haven. 567 pp . the U.S. Naval Air Facility, Midway Atoll, PETTIT, T. N., G . S. GRANT, and G . C. and to the U.S. and Wildlife Service for WHITTOW. 1982. Body temperatures and gra nting permits for this work. growth of Bonin petrel chicks. Wilson Bull. 94:358-361. PETTIT, T . N., G. S. GRANT, G . C. WHITTOW, H. RAHN, and C. V. PAGAN ELLI. 1982a. LITERA TURE CITED Embryo nic oxygen consumption and BLEM, C. R. 1978. The energetics of young gro wth in the Laysan and black-footed Japanese quai l, Coturnix coturnix japonica. albatross . Amer. J. Physiol. 242:RI2 1- Compo Biochem. Ph ysiol. 59A: 219-223. R 128. . BROWN, C. R., and N. J. ADAMS. 1984: - - -. 1982b. Respirat or y gas exchange and Basal metabolic rate and energy expend!" growth of Bonin petrel embryos. Ph ysiol. ture during incubation in the wandering Zoo l. 55 : 162- 170. albatross (Diomedea ex ulans). Condor 86 : RICKLEFS, R. E. 1974. Energetics of repro­ 182-186. duction in birds. Pages 152- 292 in R. A. CAREY, c., H.RAHN, and P. PARISI. 1980, Paynter, ed. Avian energetics. Publ. Nuttall Calories, water, lipid and yolk in avian Ornithol. Club, No. 15. Cambridge, eggs. Condor 82: 335-343. Massachusetts. FISHER, H. 1972. The nutrition of birds. Pages RICKLEFS, R. E., S. C. WHITE, and J. CULLEN. 431-469 in D. S. Farner and J.R. King, eds. 1980a. Energetics of postnatal gro wth in Avian , vol. 2. Academic Press, New Leach's storm-petrel. Auk 97: 566-575. York. --- . 1980b. Postnatal development of FISHER, H. I. 1967. Body weights in Laysan Leach's storm-petrel. Auk 97 :768-781.

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