Energy Invested in Reproduction by Thick-Billed Murres (Uria Lomvia)

ENERGY INVESTED IN REPRODUCTION BY THICK-BILLED MURRES (URIA LOMVIA)

A. J. GASTON CanadianWildlife Service, Ottawa, Ontario KIA OE7,Canada

A•STR^CT.--Pelagicseabirds that lay single-eggclutches have been thought to invest less energy in reproductionthan inshore-feedingspecies that rear more than one young. To examinethis idea I calculatedtime and energy budgetsfor Thick-billed Murres (Uria lomvia) breeding at two large arctic coloniesand comparedtheir energy expenditure with that of a hypotheticalgroup (shirkers)that wascapable of feedingat the samerate but did not attempt any reproductiveactivity. The differencein energy investmentbetween breedersand shirkers was strongly dependent on the averageforaging range. I also comparedmy resultswith similarestimates for inshore-feedingBlack Guillemots (Cepphus grylle). For the two Thick- billed Murre colonies,energy allocated to reproduction represented30% and 24% of total energyexpenditure during the breedingseason. These values exceed the estimatesfor Black Guillemots. The amount of energy invested by Thick-billed Murres at the coloniesconsid- ered probablyis similar to that investedby other seabirdslaying larger clutchesand rearing heavier young. Received8 December1983, accepted 3 July 1984.

THE allocation of resourcesto reproduction, mainly in offshore waters (Bradstreet 1980, as a fraction of total energy budgets,has been Gastonand Nettleship 1981). regarded as an important componentof life- I adopted a new approachto calculate the historystrategy (Cody 1966,Gadgil and Solbrig amount of energy expendedon reproduction. 1972, Goodman 1974, Wiens and Scott 1975, The energy expenditureof breeding birds was Dunn 1979,Hails and Bryant 1979).Techniques compared with that of a category of non- for quantifying such investmentvary (Calow existentbirds that hypotheticallylived in the 1979). Previous studies of seabirds have de- same area and had the same food-collecting pendedmainly on estimatingthe energeticcost ability as the breeders,but made no effort to of egg productionand chick rearing, although breed. I have coined the term "shirkers" for the authors acknowledgedthat the additional this group to distinguish them from the true flying and feeding involved in reproduction nonbreeding population, which carries out must add significantlyto the total energy cost many activitiesassociated with breeding(flying (Wiens and Scott 1975, Dunn 1979). to and from the breeding colony, occupying Oceanic seabirds,which lay small clutches breeding sites) and therefore makes some in- and have slow-growing chicks, have been vestmenttoward reproductionin future years. thought to make a relatively small investment My intention was not to test the predictionsof in reproduction compared with most birds r- and K-selectiontheory, but to demonstrate (Dunn 1979), and hence considered to fall at that our ideas of "reproductive investment" the "K" end of the r-K strategy continuum may depend heavily on the way in which we (Goodman1974). The assumptionimplicit here choose to measure it. is that smaller clutches and slower-growing To provide some material for comparison,I chicks indicate a lower annual energetic in- estimatedthe reproductiveinvestment of Black vestment by the parents. This in turn is as- Guillemots (Cepphusgrylle) in the same way. sumed to increasetheir residual reproductive This is an inshore-feedingspecies that breeds value by increasingsurvival and the number in the same area as Thick-billed Murres, nor- of subsequentbreeding attempts. mally lays two eggs,and frequently rears two To examine the amount of energy invested chicks. by a long-lived pelagic seabirdwith a single- METHODS egg clutch, I calculatedthe costof reproduction for the Thick-billed Murre (Uria lomvia), an arc- Information on time budgets and foraging ranges tic-nestingalcid that feeds,during the breed- of Thick-billed Murres was drawn from data accu- ing season, on fish and crustaceaobtained mulatedduring CanadianWildlife Servicestudies on

447 The Auk 102:447-458. July 1985 448 A.J. GASTON [Auk, Vol. 102 the large coloniesat Prince Leopold Island, N.W.T. as much as 10% of the entire breeding population. (86,000 pairs, 74ø02'N,90ø00'W; Gaston and Nettle- Sometime on the feeding groundsalso may be spent ship 1981) and DiggesIsland, N.W.T. (180,000pairs, resting.The time during which both membersof a 62ø34'N, 77ø43'W; Gaston et al. 1985). Data on Black pair were presentat the sitesimultaneously amount- Guillemots were obtained at Nuvuk Islands, N.W.T. ed to less than 1 h/day and declined as the season (62ø23'N,78ø05'W; Gaston et al. 1985, Cairns unpubl. progressed,suggesting that lesstime couldbe spared data) about 25 km from the murre colony at Digges for rest in the chick-rearingperiod than during in- Island. Calculationsof energy budgetsare basedon cubation. I therefore estimated time spent resting the energeticsmodel usedby Furness(1978). during daylight as 2 h during the incubationperiods Time budgets.--Informationon time budgets was and 1 h during chickrearing. At DiggesIsland, where obtainedduring 24-h watchescarried out every 5-10 darknessimposes inactivity for a period, I assumed days from before laying until most chicks had left, that one member of each pair was resting during on study plots where the positionof each breeding darkness(T.) and that the other was on the colony. site was mappedand numbered.Thick-billed Murres I assumedthat nonbreeders and shirkers spent the incubate and brood continuously,so one member of dark period resting. eachbreeding pair was alwayspresent on eachsite. (5) Time spent feeding (Tf). The remainderof the The arrival of the other member of the pair was day I assumedwas devotedto feeding.Hence, Tf = marked by a recognizablegreeting display (Gaston 24- (T,+ T,+ T•+ T,). and Nettleship 1981),and the timing of arrivalsand Energy expenditurewas calculatedfor each cate- change-overswas recordedat all sites.The frequency gory, using estimatesbased on equations given by of change-overs/24h was usedto estimatethe mean Kendeigh et al. (1977; hereafter referred to as KDG) number of visits to the colonyby eachbird. and observedmean weights (900 g for Prince Leo- Foragingrange.--Information on distancestraveled pold Islandand 936g for DiggesIsland). The ratefor away from the colony was obtainedfrom aerial sur- T• and T, was assumed to be the same. Becausebirds veys carried out during the chick-rearingperiod at occupyingsites (T•) were inactive,I consideredtheir Prince LeopoldIsland (Nettleship and Gaston1978) rateof energyexpenditure equivalent to the meanof and during the incubation and chick-rearingperiods Standard and ExistenceMetabolism (KDG: Eqs. 5.15 at DiggesIsland (Gastonet al. 1985, Gastonunpubl. and 5.35, Table 1). For resting during daylight (T,), data). Additional information for the prelaying and which included bathing and other maintenanceac- incubation periods at Prince Leopold Island was ob- tivities, I assumeda rate equal to ExistenceMetabo- tained from helicoptersurveys of important feeding lism (KDG: Eq. 5.35). Birds resting away from the areasconducted by Bradstreet(1979). colony during darknesswere assumedto have the Energyexpenditure for breeders.--Tocalculate the en- samerate of energy expenditureas for incubation ergy expenditure of adult murres, their daily activi- (Ti).Expenditure in flight (T,, T•) wascalculated from ties were divided into five categories: KDG Eq. 5.43. The resulting approximation (11.3 x (1) Time spent occupyingthe nest site, including BMR) is close to the rate measured for a 1,026-g incubation,brooding, and guarding the chick (T,). American Black Duck (Anas rubripes),a bird with a Typically, birds occupying sites sat immobile; they rapid,flapping flight similarto that of a murre (Ber- sometimesslept. Preening and interactingwith mates ger et al. 1970),but well below the rate predictedby or neighborsoccupied less than 10%of the total time. Pennycuick's(1969) formula for the power require- The duration of this behavior was determined by di- ments of a bird of the murre's dimensions. Details of rect observation. input parametersare given in Appendix 1. (2) Time spentin flight traveling betweenthe col- Estimatesfor energy expenditureduring feeding ony and the feeding area (Tt). This was estimated presenta problembecause murres feed by pursuing from mean foraging range (L), flight speed(S), and prey underwater,using their wings for propulsion. mean number of visits made to the colony (V) using For the Mallard (Anas platyrhynchos),Prange and the equation Tt = 2VL/S. Schmidt-Nielsen (1970) found the maximum rate of (3) Time spent flying between different locations energyexpenditure required for swimmingwas only within the feeding area (T•). Most murres seen dur- one-third of that used in flight. However, the duck ing aerial surveyswere flying either toward or away wasusing only its leg musclesfor propulsion.In the from their colonies; hence, movement between feed- caseof the murres, becauseof the type of muscular ing areasappears to be small.I estimated0.33 h/day, activity involved, we may anticipatea rate of energy adoptedas a constant,for all classesof birds through- expendituresimilar to that for flight. Betweendives, out the season. which lasted1-2 min, murresspent a similar length (4) Time spent resting (T,). I could not estimate of time on the surface,usually being fairly inactive. what proportionof time away from the colony was I thereforeestimated energy expenditure while feed- spent resting.Birds relieved at the nest site usually ing as 6 x BMR, which is abouthalf the rate of ex- flew to the water closeto the colony to bathe and penditure in flight. This is 3.7 x SMR for a 900-g rest. Numbers on the water sometimes amounted to bird, which is within the range of the 2-4 x SMR July 1985] ReproductiveInvestment by Murres 449

T^BI,E 1. Ratesof energyexpenditure used in calculatingdaily energybudgets for Thick-billedMurres at Prince Leopold Island (PLI) and Digges Island (DI).

Brooding/ incubation Flying Resting Feeding (e,)a (e,,ea) (er) (el) Energy expenditure(kcal/h) for body wt of 900 g (PLI) 6.151 36.420 7.003 19.338 Energyexpenditure (kcal/h) for body wt of 936 g (DI) 6.286 37.430 7.154 19.902 Multiple of BMR 1.9 11.3 2.2 6.0 ' Also restingaway from the colonyat night.

estimatedby Kooymanet al. (1982) for King Pen- (kcal/day).I assumeda value of 1.18for K through- guins (Aptenodytespatagonica). Their estimatespre- out, following Dunn's (1975) estimate for a cormo- sumablyincluded some resting time. Final estimates rant feeding on fish. for energyexpenditure on differentactivities are giv- Energyexpenditure for shirkersand nonbreeders.--For en in Table 1. shirkers I assumeda rate of feeding equal to that Calculationsof energyexpenditure assume an am- calculatedfor breedersat the sameperiod and as- bient temperatureof 0øC.At Prince Leopold Island, sumed that they flew only the 0.33 h required to the mean air temperaturefor the entire seasonwas movebetween feeding places. The remainderof their very closeto 0øC.At DiggesIsland it was 8øC,but the time ! assumedwas spent resting. The time spent seawater, on which murresspent about half of their feeding was calculatedby solving the simultaneous time,was constantly about 0øC, so the approximation equations: probably remains valid. Additionalenergy expended by the femalein pro- 0.33eaK+ T•e•K+ TtetK= RbT• (4) ducingthe eggand by both sexesin incubatingwas and calculatedfrom KDG Eqs.5.51, 5.52, and 5.56. How- ever,the costof incubationestimated in thisway was T, + T• = 23.67, (5) less than 2% of daily averageenergy expenditure, and it thereforehas been ignored. Energy expended where R, = the rate of energyintake of breederswhile in catchingfood for the chickwas introduced by add- feeding. Hence, substituting, ing the energy content of fish delivered to chicksto the estimateof total energy consumedand then us- T• = (0.33e•+ 23.67er)/(RdK+ e, - ef) (6) ing this figure to calculatethe rate at which energy was capturedduring feeding (feeding time being and constant).The costof transportingmeals and lifting them to the nest site was considerednegligible. T, = 23.67 - Tr (7) The generalequation used to calculateaverage daily energy expenditure (ADEE) was: Becausenonbreeders did not occupyfixed siteson the colonyand were not marked, I could not deter- ADEE (kcal) = T,e, + (Tt + Ta)ea mine time budgetsfor these birds by observation.I + T•er+ tref + x, (1) have estimatedtheir time and energy budgetsusing the following assumptions: where T = time (h), e = rate of energy expenditure (kcal/h), and x representsdaily expenditureon egg (1) The most capablenonbreeders could achieve a production.Expressing all e's in terms of BMR, this feeding rate equal to that of the breederswithout the is equivalent to: additional costof egg formation and incubation. (2) The leastcapable nonbreeders were barely able ADEE (kcal) = 3.22 [1.91T• + 11.30(T• + Ta) to maintain their condition in the breeding area at + 2.17T, + 6.00Tf]+ x (2) the mediandate of laying (i.e. all their time wasspent feeding, exceptthe basic2 h for resting and 0.33 h for a 900-g bird. for flying). The rate at which food is captured(R) canthen be (3) The mean feeding rate for nonbreederswas the calculatedfrom the total energyexpenditure and the medianvalue for the mostand leastcapable. time spent feeding: (4) The ratio of the meanfeeding rate of nonbreed- R = ADEE(K + Y)/Te (3) ers to that of breeders remained constant over the season. whereK = a constantrepresenting the efficiencywith (5) Nonbreedersvisited the colonyonly onceevery which the bird convertsfood energy to output en- two days. ergy and Y = the amount of food fed to the chick (6) The rate of energy expenditure of birds on the 450 A.J. GASTON [Auk, Vol. 102 colony was equal to e, (EMR) rather than e•because the mean foraging range was estimated as 100 km they spent more time than breedersmoving about during both incubationand chick-rearing(Gaston et and interacting with other birds (Gastonand Nettie- al. 1985, Gaston unpubl. data). The flight speed of ship 1981). Thick-billed Murres flying between their colony and feeding area is 58 km/h (Bradstreet1982). Becausethe time budget is fixed except for time At Prince Leopold Island birds were active spenton the colony(T•) and time spentfeeding (T•), throughoutthe 24-h day up to the date when 50%of these two parameterscan be derived from the si- chickshad fledged (Gastonand Nettleship 1981). At multaneous equations: DiggesIsland darknessimposed almost total inactiv- T•e• + (T• + 0.33)e•K+ 2e•K+ Tte•K= R•T• (8) ity for an average of 3 h during the early part of incubation, 4 h near the end of incubation, and 5 h and by the middle of the chick-rearingperiod. Valuesadopted for energyestimates.--During the pre- T, + T• = 21.67- T,, (9) laying period I consideredtime spent at the colony (T•) and traveling (T,) to be negligible up to D2o. where Rnb= median rate of energy intake of non- Thereafter, I calculated the mean duration spent at breederswhile feeding and T• = L/S, where L is the same as for breeders. the colonyfrom: The assumptionthat nonbreedersdid not travel to Mean number and from the colony as often as breedersrests on the counted at the hypothesisthat their fitnessis maximizedby maxi- colony D2o-De T, x 24 = 9.6 h/day. mizing the amount of time spenton the colony.Be- Total number causetraveling involvesa high rate of energyexpen- of breeders diture, they shouldtry to minimize the amountof traveling that they do. The lowest rate of exchange This indicatesthat birds averagedabout 41 h at the of breeders observedwas 0.5 visits/day, so I assumed colony at each visit. that nonbreedersmaintained this schedulethrough- I assumedthat, on average,breeders made 7 trips out the season at both colonies. from the feeding area to the colony before the me- Observedvalues for parameters.--Observerswere dian date of laying. Hence, the mean time spent trav- presentat PrinceLeopold Island from the startof the eling duringthe periodD2o-De can be estimatedfrom: seasonin 1976. Birds were seenat the colony for the first time (D•) 50 daysbefore the mediandate of lay- T• = 2VL/[58(De - D20)]= 0.89 h/day. ing (D,), but for the first 20 daysafter D• numbers I assumedthat the rate of energy intake while never exceeded25% of the breedingpopulation. From feeding during the prelayingperiod wasa little low- 30 days before D,, 7 1-2-day peaksof about 50-80% er than that calculated for the start of the incubation attendance alternated with periods when numbers period (45 kcal/day). were low. The mean number counted at the colony For the incubationperiod I usedobserved rates of during the 30 days prior to median laying was 40% exchangeto calculatethe frequencyof visits to the of the total breeding population. Once laying had colonyby breedersand estimatedthe rate of visits begun,however, 50% of the breedersnearly always by nonbreedersto be onceevery two days.I assumed were present.During incubationthe rate of change- that from the median date of fledging onwards, the oversat Prince LeopoldIsland rose from 1 to about meandaily energyexpenditure of breederstook 16 2 changes.egg-•.day -• between De and median daysto fall to the level of shirkers. hatching.At DiggesIsland the correspondingfigures Freshegg weights averaged96.5 g at Prince Leo- were 0.5 and 0.8 changes.egg-•'day-•. During the pold Island and 109 g at DiggesIsland. The mean chick-rearingperiod food was delivered to chicks weight of fish deliveredto chickswas 12.5g at Prince 3-5 timesdaily (• = 4) at PrinceLeopold Island and Leopold Island and 8.9 g at Digges Island (Gaston twice daily at DiggesIsland. and Nettleship 1981,Gaston unpubl. data).Only one The number of birds attending both colonies de- fish was delivered on each visit to the colony. I as- clined from aboutthe mediandate of chickdeparture sumedan energycontent for fishof 1.14kcal/g fresh onwards, so that lessthan 10%of breeding siteswere weight (Dunn 1975).Colony-specific input parame- occupied2 weekslater. During this perioda marked ters are summarized in Appendix 2. diurnal change in attendancesuggested that the re- mainingbirds were visiting the colonyonce a day. The meanforaging range of birdsfrom PrinceLeo- RESULTS pold Island was 110 km during the prelayingand incubationperiods (Bradstreet 1979) and 56 km dur- Energyexpenditure.--Estimated time budgets ing the chick-rearingperiod (Nettleship and Gaston are shown in Table 2. Estimated daily energy 1978,Gaston and Nettleship 1981).At DiggesIsland expenditureby breedingmurres based on these July1985] ReproductiveInvestment byMurres 451

TABLE2. Time budgets used in estimating average daily energy expenditure for Thick-billed Murres (h.bird -•-day -•).

Resting Resting On colony Traveling Flying Feeding (daylight) (night) Prince Leopold Island Breeders Prelayingmale 9.60 0.89 0.33 7.59 5.59 0 Prelayingfemale a 9.60 0.89 0.33 8.08 5.!0 0 Early incubation 12.00 1.90 0.33 7.77 2.00 0 Late incubation 12.00 3.79 0.33 5.88 2.00 0 Chick rearing 12.00 3.86 0.33 6.81 !.00 0 Nonbreeders (average) Early incubation ! 1.25 !.90 0.33 8.52 2.00 0 Late incubation ! !.25 !.90 0.33 8.52 2.00 0 Chick rearing !2.76 0.97 0.33 7.94 2.00 0 Shirkers Prelaying 0 0 0.33 6.89 16.28 0 Early incubation 0 0 0.33 6.!9 !7.48 0 Late incubation 0 0 0.33 3.74 !9.93 0 Chick resring 0 0 0.33 3.96 !9.7! 0 Digges Island Breeders Early incubation !2.00 !.72 0.33 6.45 2.00 !.5 Late incubation !2.00 2.76 0.33 4.9! 2.00 2.0 Chick rearing !2.00 3.45 0.33 4.72 !.00 2.5 Nonbreeders (average) Early incubation 4.96 1.72 0.33 !!.99 2.00 3.0 Late incubation 7.59 1.72 0.33 8.35 2.00 4.0 Chick rearing 7.50 !.72 0.33 7.44 2.00 5.0 Shirkers Prelaying Early incubation 0 0 0.33 5.20 !5.47 3.0 Late incubation 0 0 0.33 3.46 !6.2! 4.0 Chick rearing 0 0 0.33 2.96 !5.7! 5.0 During last !5 days,assuming egg formationextends over !5 daysat a costof !5 kcal/day.

time budgets ranged from 295 to 365 kcal- Ratesof energyintake.--Rates of energy intake bird-•. day-• at PrinceLeopold Island and from during feeding rosefrom 48 kcal/h at the time 304 to 333 kcal.bird-•-day -• at Digges Island of incubationto 67 kcal/h during chick rearing (excludingthe prelaying period,for which no at Prince Leopold Island and from 56 to 86 datawere available).Maximum rates represent kcal/h over the same period at Digges Island. 2.9 and 2.6 x SMR or 4.7 and 4.2 x BMR. Min- Median feeding rates estimatedfor nonbreed- imum rates occurredduring the prelaying pe- ers ranged from 60 to 70% of the rates for riod and maximum rates during chick rearing breeders (Table 3). (Fig. 1). Energyexpenditure by shirkersand the costof Corresponding figures for nonbreeders reproduction.--Energyexpenditure by breeders ranged from 306 to 395 kcal.bird-•-day -• at and shirkers was assumedto be equal at the PrinceLeopold Island and from 324 to 384 kcal. beginning of the prelaying period. Thereafter, bird-'-day -• at Digges Island. Ratesfor "aver- the daily expenditure of shirkers decreased age" nonbreederswere higher than those for while that of breedersincreased (Fig. 1). The breedersat the start of the incubationperiod minimum daily energy expenditureof shirkers at both colonies,failing below them during the was 223 kcal.bird-a.day -• at PrinceLeopold Is- chick-rearingperiod (Fig. 1). land and 215 kcal.bird-a.day -• at Digges Is- 452 A.J. GASTON [Auk, Vol. 102

400 TABLE3. Ratesof energyintake during feeding (kcal/ h).

Start of Chick '"'::::::',,....::::.Locality/status incubation rearing Prince Leopold Island Breeder 48.46 67.48 Nonbreeder 34.50 41.91 Digges Island Breeder 55.71 85.72 Nonbreeder 39.03 53.39

Observations on the amount of fat present on

200 I I I I birds collected suggested that these weight changeswere causedby changesin the amount of stored fat. TIME (days) One gram of fat is equivalent to approxi- Fig. 1. Estimated average daily energy expendi- mately 9.5 kcal of energy (Pennycuick 1975, ture (ADEE) by breeding (solid lines), nonbreeding Kendeigh et al. 1977). Therefore, actual rates of (dottedlines), and shirking (brokenlines) Thick-billed energy intake in the first half of incubationmay Murres at Prince Leopold Island (circles) and Digges have been a minimum of 19 kcal/day greater Island (crosses). than thosepredicted, and subsequentrates may have been about 29 kcal/day lower. If the food supply within foraging range of the colony re- land, giving maximum ratios of 1.61 and 1.55, mainedrelatively stableduring this period, the respectively, for the energy expenditure of observedweight gain and losswould have ef- breeders to that of shirkers (Table 4). fectively evened out the rate of feeding nec- I estimated the energy expenditure of breed- essary to support energy expenditure during ers and shirkers over the entire breeding sea- reproduction. son by calculating the areas below the corre- Changesin weight also would have affected sponding curves in Fig. 1. I then estimated the proportion of energy expenditure devoted to reproductionby subtractingthe area below the TABLE4. Sensitivity of averagedaily energy expen- shirkers' curve from the area below the breed- diture (ADEE) estimates for breeders and ADEE (breeder): ADEE (shirker) ratios to variation in in- ers' curve. I expressed the difference as a per- put parameters. centage of the area below the breeders' curve. This yielded estimatesfor the proportion of en- Deviation of output from ergy expenditure devoted to reproduction of "best" estimate (%) 30%at Prince Leopold Island and 24% at Digges ADEE (breeder): Island. ADEE (breeder) ADEE (shirker) Input Theeffect of changesin bodyweight.--I assumed parameter +25% -25% +25% -25% that birds remained in energy balance e, +11 -11 +11 -11 throughout the season,but this assumption is e, +1 -1 +19 -13 not preciselycorrect. In one year at Prince Leo- ef +7 -7 0 0 pold Island and in two yearsat Digges Sound, e, +7 -7 +4 -4 L +5 -5 +10 -9 Thick-billed Murres showedsignificant weight S -5 +5 -9 +10 losses between laying and the end of chick V (and corre- rearing. Average weights at Digges Island in sponding Y) +5 -5 + 10 -10 1982 rose by 40 g between egg-laying and the 3h Oh 3h Oh middle of the incubation period (20 days) and • -9 +4 0 0 then fell by 120 g/bird by the end of chick lh Oh lh Oh rearing (40 days); hence, average gains were about 2 g/day, and losseswere about 3 g/day. • +4 -2 -4 +3 July1985] ReproductiveInvestment byMurres 453 energy expenditure,particulary in flight. Freed was produced by alteration of the rate of en- (1981) and Norberg (1981) have argued that ergy expenditureon flight, where a 25% vari- weight changes during reproduction may be ation altered the ADEE of breeders by 11%, an adaptive responseto the increased amount nonbreedersby 5%, and shirkers lessthan 1% of flying necessitatedby chick rearing. In the (Table 4). A 25% variation in the rate of energy caseof Thick-billed Murres at Digges Sound, expendedwhile resting(er) resulted in a change the observeddecline in weight between mid- of 15% in the ADEE of shirkers and hence had incubation and the end of chick rearing would a big effecton the ratio ADEE (breeders):ADEE have altered the estimatedflight energy expen- (shirkers).Alterations in the ratesof energy ex- diture from 40.37 to 37.82 kcal/h. Recalculating pended while feeding and incubating had ADEE for incubation and chick rearing using smaller effects on outputs. the weights observedin 1982 (1,043 and 923 g) I also examined the sensitivity of the output gives 395 and 363 kcal/day, a reversal of the to other input parameters. Neither time spent trend in daily energy expenditure predicted as- resting nor time spent flying in the feeding suming a constant weight. area had much effect on the output (Table 4). If the changesin weight are wholly account- However, a 25% change in flight speed (S) or ed for by stored fat, the difference in energy distance traveled (L) altered the ADEE of expenditure is probably less than these calcu- breedersby 5% and the rato breeders: shirkers lations indicate becausefat deposits are likely by 9-10%. to have little effect on BMR. Also, because the Becauseforaging range (L) and the energetic bulk of the fat is stored subcutaneously(pers. costof feeding(el) were poorly estimated,I ex- obs.), it probably helps to improve insulation amined variation in output in relation to these and hence decrease energy expenditure on two parameters in greater detail, using three thermoregulation. The exact magnitude of the valuesfor each (Table 5). Changinge I had a effect of weight changes on energy expendi- large effect on estimatedADEE but had little ture therefore must remain uncertain. How- impact on the ratio ADEE (breeders):ADEE ever, heavier birds inevitably must expend (shirkers). Foraging range had considerable more energy on flight (Pennycuick 1975). impacton ADEE for the casewhere eI was 10 Sensitivityof the modelto variationin inputpa- kcal/h but a much smaller effect for the (prob- rameters.--The effect of variation in constants ably morelikely) caseswhere eI was higher. It derived from energy expenditure equationson had a large effect on the ratio ADEE (breeders): a similar model was examined by Furness ADEE (shirkers)for all values of el, the ratio (1978). He found that output from his model increasingwith foraging range. This is to be (total energy expenditure of an entire colony) expectedbecause as traveling time is reduced, was very strongly affectedby variation in these a greater proportion of time is spent feeding constants.My estimatesof ADEE are likely to and the energy budgetsof breedersand shirk- be similarly affected by these constantsand ers converge, with incubation and brooding should be treated with caution. However, for having energy demands similar to those of comparisons between breeders, nonbreeders, resting. and shirkers, variation in the equation con- Energyexpenditure by BlackGuillemots.--Black stantshas a negligible effect becausethe same Guillemots cease to brood their chicks about 5 body weights are used for all three classes. daysafter hatching,and consequentlythey are The ratio of energy expenditureby breeders, free to feed throughout the daylight period nonbreeders,and shirkersis affectedby the rel- (about 19 h at Nuvuk Islandsin August) during ative rate of energy expenditure on different the remainder of chick rearing. Although they activities. To examine the sensitivity of the make many trips to feed their chickseach day model to variation in the relative values of these (V = 5-10), they forage within 5 km of the parameters, I repeated the model calculations breeding site. Hence, travel time is small com- for the chick-rearing period with values of e, pared to Thick-billed Murres. The combination e•, e, and eI that were 25%greater and smaller of these characteristicsmeans that, although than my best estimates,altering the input val- daily energy expenditure during chick rearing ues one at a time. is 41% greater than during incubation, the rate The greatest effect on the ADEE of breeders at which food has to be found is only slightly 454 A.J. GASTON [Auk, Vol. 102

T^I•I•E5. Averagedaily energyexpenditure by Thick-billedMurres at PrinceLeopold Island in relationto differentestimates of foragingrange and energyexpenditure while feeding.

ef= 10 ef= 19.34 el = 30 Close a Mid Far Close Mid Far Close Mid Far

Incubation Breeders 223.87 260.31 296.75 304.52 328.07 351.63 396.58 405.53 414.29 Shirkers 199.88 192.82 195.23 267.12 239.47 228.33 344.85 293.86 265.57 Breeder/shirker 1.12 1.35 1.52 1.14 1.37 1.54 1.15 1.38 1.56 Chick rearing Breeders 235.97 290.63 345.30 322.73 358.07 393.42 421.79 435.07 448.35 Shirkers 198.29 191.20 185.65 264.53 232.51 209.27 340.15 278.89 237.22 Breeder/shirker 1.19 1.52 1.86 1.22 1.54 1.88 1.24 1.56 1.89 aAverage foraging rangesfor the incubationperiod: close,30 km; mid, 70 km; far, 110 km; and for the chick-rearingperiod: close,20 km; mid, 50 km; far, 80 km.

greater during the chick-rearing period, once and Daan 1980). Measurementsof energy ex- brooding has ceased,than during incubation penditure by breeding Thick-billed Murres at (Table 6). The figures in Table 6 are basedon a Digges Island and breeding Black Guillemots nestcontaining two chicks.For the averagenest, at Nuvuk Islandsduring the incubationperiod containing 1.3 chicks, energy delivered to using the doubly labeled water technique sug- chicks(Y) is 72.8 kcal/day, and the peak rate gest that my estimatesare approximately cor- of energy intake becomes21.85 kcal/h, lower rect (3 incubatingThick-billed Murres, 342-421 than that during incubation. kcal/day; 5 incubating Black Guillemots, 124- According to these estimates, shirkers ex- 183 kcal/day; Pr•,s-Jonesand Gaston in prep.). pend practically the same energy as breeders In terms of SMR these estimates are also similar during the incubationperiod, and even during to thosemade for King Penguins(Kooyman et chick rearing the ratio of ADEE of breedersto al. 1982),another underwater-pursuitpredator. that of shirkers is only 1.45. These estimatesare Second, comparison with our hypothetical lower than the estimates for the Thick-billed shirkers suggeststhat maximum rates of ener- Murres, although differences between the gy expenditure by breeders average 1.5-1.7 speciesfor the chick-rearing period is largely times the level that would sustainthem if they dependent on the difference between the val- made no attempt to visit the colony.Assuming ues I have selectedfor energy expendedwhile that birds remain in energy balance,this sug- foraging(el) and flying (ea).In the termsI have gestsan equivalent increase in the amount of adopted, therefore, the cost of reproduction food consumed. The Pigeon Guillemot (Cep- seems to be lower for the Black Guillemots at phus colurnba,Koelink 1972) and the Double- Nuvuk Islandsthan for the neighboring Thick- crested Cormorant (Phalacrocoraxauritus, Dunn billed Murres at Digges Island, amounting to 1975), two comparablefish-eating seabirdsthat, only a 19% increase over the level estimated on average, rear two young per nesting at- for shirkers (basedon a total colony attendance tempt, had estimatedincreases in feeding rates period of 74 days). during chick rearing twice that of nonbreeders. Third, the estimatedrate of energy intake dur- DISCUSSION ing feeding, which during the chick-rearing period reached 3-5 times the expenditure in- Four points deserveparticular mention from volved, is normal, or perhaps a little higher these results.First, the maximum daily energy than normal, for birds in which the young are expenditure of breeding murres, at 4-5 times fed at the nest (Ricklefs 1974). BMR, is high in comparisonwith other studies Finally, the estimated daily energy expen- on breeding birds (Utter and Lefebvre 1973, diture of nonbreeders is not much different Ricklefs 1974, Hails and Bryant 1979) and may from that of breeders. Although this seems approach the sustainablelimit for birds of 4 counterintuitive, it is quite reasonableif we as- times BMR (Utter, quoted in King 1974; Drent sume (as the model does) that nonbreeders are July1985] ReproductiveInvestment byMurres 455

T^I•LE6. Time budgetsand estimatesof energyexpenditure for breedingBlack Guillemots and shirkers.

Rate of At the Flying Resting, Resting, energy nest (Ta+ T,, Feeding daylight night Totals intake Status Period (Ti,ei) a e•)b (Tt,et)C (T, er)a (T,, e,) (ADEE) (kcal/h)e Breeder Incubation Time (h) 12.0 1.0 7.0 2.0 2.0 Energy (kcal) 47.04 20.68 74.83 9.0 9.0 160.55 22.94 Chick rearing (>5 days) Time (h) 0 1.5 15.5 2.0 5.0 Energy (kcal) 31.02 165.69 9.0 19.60 225.31 24.38 Shirker Incubation Time (h) 0 0.5 6.93 12.57 4.0 Energy (kcal) 10.34 74.08 56.56 18.0 158.98 Chick rearing (>5 days) Time (h) 0 0.5 6.38 12.12 5.0 Energy (kcal) 10.34 68.20 54.54 22.50 155.58 a e• = 3.92 kcal/h. bea = 20.68 kcal/h, "nontravel flying" = 0.5 h. cet = 6 x BMR = 10.69kcal/h. a er = EMR = 4.50 kcal/h. eRb = 1.18ADEE/R t (incubation) and (1.18 ADEE + Y)/Tt (chickrearing), where Y = 112kcal/day (nest contains2 full-grown chicks). less efficient at foraging than breeders (see made by Thick-billed Murres, in comparison Burger 1980). The extra efficiency of breeders with other birds. The maximum rate of energy allows them to invest time in incubation and expenditure for most birds, however, is sus- brooding,which requiresa low rate of energy tained for only a few dayswhen the nestlings expenditure compared to the additional feed- are at their peak weight (Dunn 1975). In the ing that nonbreedersmust do. If nonbreeders Thick-billed Murre feeding rates hardly vary travel from the colony to the feeding areamore with the age of the chick, so the maximum rate frequently than once every two days, as as- of expenditureapplies for the entire 20-25-day sumedby the model, then their energy expen- periodwhen the chickis being fed (Gastonand diture almost certainly will exceed that of Nettleship 1981). Also, Dunn (1975) and Koe- breeders.The possibility that prebreedersac- link (1972) calculated reproductive investment tually might be making a greater investment in a different manner, including the total en- towards reproduction than breeders emerges, ergy delivered to the chicks in the adult's en- although their efforts yield no immediate out- ergy budget instead of only the energy ex- put. The model estimatesthat nonbreeders av- pended on finding and catching the food. erageabout 9 h/day (DiggesIsland) or 13 h/day Estimated in such terms, Thick-billed Murres (Prince Leopold Island) at the colony during make a very small investment in reproduction. the chick-rearing period. Assuming that all of If we compare the Thick-billed Murre with this is in daylight, this suggeststhat half the the Black Guillemot, we find that successful nonbreedingpopulation is presentat any one Black Guillemots at Nuvuk Islands reared an time when we can count them. This accords average of 1.3 chicks to fledging, with a mean fairly well with countsmade at both colonies fledging weight of about 350 g (Gaston et al. and estimates of numbers of nonbreeders as a 1985). In contrast, Thick-billed Murres never proportion of the total population (Birkhead reared more than 1 chick, and averageweights and Hudson 1977, Gaston and Nettleship 1981, at fledging at Digges Island were about 150 g. Gaston et al. 1985). Despite this difference in reproductive output, These observationsgive slightly conflicting the energy expenditureof breedersexceeded impressionsof the investment in reproduction that of shirkers to a greater degree in Thick- 456 A.J. GASTON [Auk, Vol. 102 billed Murres than in Black Guillemots during Shelf Project,and the Departmentsof Transportand both incubation and chick rearing. Hence, the Indian and Northern Affairs Canada. murres make a greater energetic investment than the guillemots but achieve a smaller re- LITERATURE CITED productive profit. BERGER,M., J. HART,& O. Z. ROY. 1970. Respiration, In summary,in terms of energy expenditure, oxygenconsumption, and heart ratein somebirds the Thick-billed Murre appearsto make just as during restand flight. Z. Vergl. Physiol.66: 201- much investment in reproduction as other sea- 214. birds that have life-history strategiesinvolving BIRKHEAD,T. R., & P. J. HUDSON. 1974. Population a higher potential intrinsic rate of increase.As parametersfor the CommonGuillemot Uria aalge. indicated in Table 5, this conclusiondepends Ornis Scandinavica 8: 145-154. heavily on my estimatesof foraging range for BRADSTREET,M. S.W. 1979. Thick-billed Murres and the Thick-billed Murres. Although data on the Black Guillemots in the Barrow Strait area, foraging ranges of birds from the two colonies N.W.T., during spring: distributionand habitat use. Can. J. Zool. 57: 1789-1802. considered are fragmentary, additional evi- --. 1980. Thick-billed Murres and Black Guil- dence from shipboardsurveys by Brown (1980) lemotsin the Barrow Strait area, N.W.T., during in the vicinity of Digges Island supportthe fig- spring:diets and food availabilityalong ice-edges. ures given here. The figures for close foraging Can. J. Zool. 58: 2120-2140. range given in Table 5 are likely to be well --. 1982. Occurrence, habitat use and behavior below the mean foraging range for coloniesthe of seabirds, marine mammals and arctic cod at size of Prince Leopold and Digges islands (see the Pond Inlet ice edge. Arctic 35: 28-40. also Gaston 1985). Otherwise, the results seem BROWN,R. G. B. 1980. The pelagic ecology of sea- fairly robust to variations in input parameters birds. Trans. Linnaean Soc. New York 9: 15-22. within reasonable limits. BURGER,J. 1980. The transitionto independenceand The very long distancesover which Thick- post-fledgingparental care in seabirds.Pp. 367- 448 in Behavior of marine animals. Vol. 4, Ma- billed Murres travel to find food are probably rine birds (J. Burger,B. L. Olla, and H. E. Winn, a consequenceof the very large colonies in Eds.). New York, Plenum Press. which these birds congregate (Gaston et al. C^Low,P. 1979. The costsof reproduction--aphys- 1983). This situation is typical of the species.In iologicalapproach. Biol. Rev. 54: 23-40. the western Atlantic, for instance, more than CODY,M. L. 1966. A general theory of clutch size. 90% of the population breeds in colonies of Evolution 20: 174-184. more than 10,000 pairs (Gaston 1980). DRENT,R. H., & S.D.•,AN. 1980. The prudent parent: I concludethat the reproductiveinvestment energeticadjustments in avian breeding. Ardea 68: 225-252. of seabirdsappears to vary with the way that DUNN, E. H. 1975. Caloric intake of nestling Dou- we choose to measure it. Measured by the ble-crested Cormorants. Auk 92: 553-565. shirker method, it probably is not closely cor- 1979. Time-energy use and life-history related to reproductive rate. The apparently strategiesof northern seabirds.Pp. 141-166 in K-selectedattributes of seabirdsprobably con- Conservation of marine birds of North America stitute a specialcase deriving from the fact that (J.C. Bartonekand D. N. Nettleship,Eds.). Wash- breedingsites are restrictedand hencefood re- ington, D.C., U.S. Fish Wildl. Serv.,Wildl. Rept. sources for reproduction are constrained, as No. 11. suggestedby Ricklefs (1977). FREED,L.A. 1981. Lossof massin breeding wrens: stressor adaptation?Ecology 62:1179-1186. FURNESS,R. W. 1978. Energy requirementsof sea- ACKNOWLEDGMENTS bird communities:a bioenergeticsmodel. J. Anim. Ecol. 47: 39-54. Commentsfrom Tim Birkhead,Hugh Boyd,David G^DGIL,M., & O. T. SOLBRIG.1972. The conceptof Cairns, Graham Cooch, Steve Curtis, Tony Diamond, "r" and "K" selection: evidence from wild flow- Robert PrOs-Jones,and three refereeshelped to im- ers and some theoretical considerations. Amer. prove on earlier drafts of this manuscript.I thank Natur. 106: 14-31. David Cairns for collecting the data on Black Guil- GASTON,A. J. 1980. Populations,movements and lemots.The field researchwas part of the Canadian wintering areas of Thick-billed Murres (Uria Wildlife Serviceprogram "Studies on Northern Sea- lomvia)in easternCanada. Can. Wildl. Serv. Progr. birds." Additional financial and logisticsupport was Note 110. provided by Petro-Canada,the Polar Continental 1985. Developmentof the young. In The July1985] ReproductiveInvestment byMurres 457

Atlantic Alcidae (T. R. Birkhead and D. N. Net- COSTA. 1982. Diving depths and energy re- tleship, Eds.). New York, Academic Press. In quirementsof King Penguins.Science 217: 726- press. 727. --, D. CAIRNS,R. D. ELLIOTT,•z D. G. NOBLE. 1985. NETTLESHIP,D. N., &: A. J. GASTON. 1978. Patterns A natural history of Digges Sound. Can. Wildl. of pelagic distribution of seabirdsin western Serv. Rept. In press. Lancaster Sound and Barrow Strait, N.W.T. Can. --, G. CHAPDELAINE,•z D. G. NOBLE. 1983. The Wildl. Serv. Occ.Pap. No. 39. growth of Thick-billed Murre chicksat colonies NORBERG,A. 1981. Temporary weight decreasein in HudsonStrait: inter- and intra-colonyvaria- breedingbirds may result in morefledged young. tion. Can. J. Zool. 61: 2465-2475. Amer. Natur. 118: 838-850. , & D. N. NETTLESHIP. 1981. The Thick-billed PENN¾CUICK,C.J. 1969. The mechanics of bird mi- Murresof PrinceLeopold Island. Can. Wild. Serv. gration. Ibis 111: 525-556. Monogr. No. 6. 1975. Mechanicsof flight. Pp. 1-76 in Avian GOOr)MAN,D. 1974. Natural selectionand a ceiling biology, vol. 5 (D. S. Earner and J. R. King, Eds.). cost on reproductive effort. Amer. Natur. 108: New York, Academic Press. 247-268. PRANGE, M.D. & K. SCHMIDT-NIELSEN. 1970. The HAILS,C. J., & D. M. BRYANT.1979. Reproductive metaboliccost of swimmingin ducks.J. Exp. Biol. energeticsof a flee-living bird. J.Anim. Ecol.48: 53: 763-777. 471-482. RICKLEES,R. E. 1974. Energeticsof reproduction in KENDEIGH,$. C., V. R. DOL'NIK, &: V. M. GAVRILOV. birds. Pp. 152-292 in Avian energetics(R. A. 1977. Avian energetics.Pp. 127-204 in Graniv- Paynter, Jr., Ed.). Publ. Nuttal! Ornithol. Club orousbirds in ecosystems(J. Pinowskiand S.C. No. 15. Kendeigh, Eds.). Cambridge, England, Cam- 1977. On the evolution of reproductive bridge Univ. Press. strategies in birds: reproductive effort. Amer. KING, J. R. 1974. Seasonal allocation of time and Natur. 111: 453-478. energy resourcesin birds. Pp. 4-85 in Avian en- UTTER,J. M., •z E. A. LEFEBVRE.1973. Daily energy ergetics(R. A. Paynter, Jr., Ed.). Publ. Nuttall expenditureof Purple Martins (Prognesubis) dur- Ornithol. Club No. 15. ing the breeding season:estimates using D20•8 KOELINK,A. F. 1972. Bioenergeticsof growthin the and time-budgetmethods. Ecology 54: 597-603. Pigeon Guillemot. Unpublished M.Sc. thesis. WIENS, J. A., •z J. M. SCOTT. 1975. Model estimation Vancouver, British Columbia, Univ. British Co- of energyflow in Oregoncoastal seabird popu- lumbia. lations. Condor 77: 439-452. KOOYMAN,G. L., R. W. DAVIS,J. P. CROXALL,•z D. P.

APPENDIX1. Input parametersfor model(energy expenditure estimates and formulaefrom Kendeigh et al. 1977).

Egg BM SM EM Flight productionb (5.5)• (5.15) (5.35) (5.43) (5.51, 5.52) Chick foodc Muliplicand 0.5224W 2.624W 4.142W 0.3157W 2.484W Exponent 0.7347 0.5705 0.5444 0.698 0.9574 1.14(fish wt) aFormula number in Kendeighet al. (1977). bDaily investmentin eggproduction (x) is estimatedby dividingthis resultby the numberof daystaken to form an egg(15 days,Gaston and Nettleship1981). cDaily energyfed to chicks(Y) is estimatedby multiplyingthis figureby the numberof visitsduring the chick-rearingperiod (V). 458 A.J. GASTON [Auk, Vol. 102

APPENDIX2. Summary of colony-specificinput parameters(EI = early incubation,LI = late incubation, CR = chick rearing).

Prince Leopold Digges Nuvuk Island Island Islands (TBM) (TBM) (BG) Weight (g) Adult 900 936 400 Egg 96.5 110 -- Fish 12.5 8.9 12.0 Visits. bird -•. day-• (V) EI 0.5 0.25 -- LI 1.0 0.4 -- CR 2.0 1.0 8.0 Foragingrange (L) (kin) EI 110 100 2 LI 110 100 2 CR 56 100 2 Daylight rest (T•) (h) EI 2.0 2.0 2.0 LI 2.0 2.0 2.0 CR 1.0 1.0 2.0 Dark per/od (T,) (h) EI 0 3.0 3.0 LI 0 4.0 4.0 CR 0 5.0 5.0

On 2 April 1985the ICZN gave6 months'notice of the possibleuse of its plenarypower in case#2277, publishedin Bull. Zool. Nomen. 42(1). Commentsare invited and shouldbe addressedto the Secretary ICZN, % British Museum(Natural History), London SW7 5BD, England.

Carpophagaaurorae Peale, 1848, and Serresiusgaleatus Bonaparte, 1855 (Aves): proposed conservation by the suppressionof ColumbaR. ForsteriWagler, 1829.