Allocation of Growth in Food-Stressed Atlantic Puffin Chicks

The Auk 113(4):830-841, 1996

ALLOCATION OF GROWTH IN FOOD-STRESSED ATLANTIC PUFFIN CHICKS

HILDE STOL •JYAN • AND TYCHO ANKER-NILSSEN NorwegianInstitute for NatureResearch, Tungasletta 2, N-7005 Trondheim,Norway

ABSTt•CT.--In long-lived seabirdsthat lay a single-eggclutch, allocation of growth to certain body parts may be advantageousfor the chick if food is limited. To investigatethis, 40 Atlantic Puffin (Fraterculaarctica) hatchlings were distributedin sevengroups that were raisedon differentamounts of food to 38 daysof age.When food intakewas reduced,growth rateswere depressedfor all charactersmeasured (i.e. body massand length of the wing, 2nd primary, forearm, head + bill, culmen, skull, tarsus,and middle toe). Head and wing parts grew preferentiallyrelative to the other characters,and onsetof growth was delayedin the primaries.All chicksaccumulated significant amounts of subcutaneousfat, whereasinternal fat depositswere presentonly in the chicksthat receivedthe mostfood. Received14 July1995, accepted20 March 1996.

ONEWAY that parent birds adjustfor variation The wide variation in chick growth rates in food availability is to vary clutch size (Lack among speciesof alcids has been attributed to 1954,1966, 1968). In long-livedspecies that lay constraintson feeding ecology, such as spe- a single-eggclutch, alteration of chick growth cialized foraging behaviors,unpredictable and rate apparentlyis the only strategyavailable to patchy food distributions, and great distances adjust for variation in food. Slow growth re- between feeding and nesting sites (Lack 1968; duces daily energy requirements and allows Ricklefs 1968, 1984;Ashmole 1971;Sealy 1973; food to be delivered at a lower rate (Lack 1968; Nelson 1977; Birkhead and Harris 1985). Thus, Ricklefs 1968, 1979; Harris 1977; Nelson 1977; chicks of pelagic alcids often face the problem Drent and Daan 1980). Chick abandonment is of being fed at a low rate or even abandoned, likely when food demandscannot be met and because the contribution of an individual chick current offspringcontribute relatively little to to the total lifetime reproductionof its parents total lifetime reproduction (Williams 1966, is fairly small. Goodman 1974, Drent and Daan 1980, Ricklefs The burrow-nesting Atlantic Puffin is a typ- 1983). Variable growth provides a basisfor de- ical alcid. It is long-lived, has delayed sexual velopmental adaptationsin the chick, such as maturity, lays one egg per clutch, and feeds allocationof growth to parts of the body that mainly on pelagicfish (Harris 1984,Harris and would help reduce the nestling period and in- Birkhead1985). Chick-rearing is sharedby both creasethe chancesof survival after fledging. parentsand spans34-74 daysfrom hatchingto Someseabird chicks (e.g. tourres[Uria spp.]and fledging, depending on food supply (Nettle- Razorbills [Alca torda]), escape part of this di- ship 1972,Harris 1984,Harris and Birkhead 1985, lemma by leaving the nest soon after hatching Barrett and Rikardsen 1992). Puffin chicks leave to accompany(and be fed by) their parents at the nest burrow when they are about 60-80% sea(e.g. Lack 1968,Harris and Birkhead1985, of adult body mass(Harris and Birkhead 1985). Ydenberg 1989). In contrast,studies of species They are at risk to abandonmentby their par- that feed their chicks at the nest (e.g. Manx ents becauseadult puffins are specializedfeed- Shearwater[Puffinus puffinus], Harris 1966;At- ers that pursue a variable and patchy food sup- lantic Puffins [Fraterculaarctica], Tschanz 1979, ply (Anker-Nilssen 1987, 1992; Anker-Nilssen Anker-Nilssen 1987;and Yellow-eyed Penguin and Oyan 1995). [Megadyptesantipodes], van Heezik 1990) sug- Our study focusedon identifying adaptations gest that developing chicks faced with food in puffin chicks that may have evolved to re- shortagesallocate resourcespreferentially to duce the length of the nestling period when certain body parts. food supply is limited. We hypothesized that preferential allocation of growth takes place during food shortages.The allocation should E-mail: [email protected] favor body parts that enable the chick to reach

83O October1996] GrowthAllocation inAtlantic Puffins 831

the sea at an earlier physiological age or at a thawed in the eveningbefore being given to the chicks lower mass than "normal" and increase its as four portions supplied one by one at 0900, 1300, chancesof survival during the critical first time 1700 and 2100 (standardtime). A few milligrams of at sea. The charactersinvestigated were body Vitaplex© multivitamin were added to the morning massand growth of the wings, head, and feet. meal every day. The experimentalperiod ended at day 38, and at day 43 the chickswere sacrificedand Fat storagealso was measuredbecause fat could frozen. All carcasses were later dissected. serve as an energy supply during periods of In 1990, chicks were placed into two groups and erraticfood availability and during the firstdays given different amounts of food; diets (different of independence (Lack 1968, Drent and Daan amountsof capelin) were designedto simulate chick 1980, Ricklefs 1990). growth on Rost during a "bad" and a "good" year such that one group (group 3) always receivedhalf STUDY AREA AND METHODS the amount of food as the other (group 6). One stan- dardized equivalent (i.e. 3.33 g) of food was used as Study area.--The study was carried out in the ar- the basisfor the design of the diets. One group was chipelagoof Rost in northern Norway during the startedwith three equivalents,the other with six. In summers of 1990 and 1991. Chicks were collected (un- 1991, five groupswere establishedand given 2, 4, 5, der license from the Directorate of Nature Manage- 6, and 7 equivalents,respectively, from day 1 (Table ment) from nest burrows on the island Hernyken 1). At days 4, 10, and 19, chick diets were increased (67ø26'N, 11ø52'E),which had approximately 55,000 by a number of equivalentscorresponding to their occupiedburrows in 1990.The puffin colony of Rost groupnumber. Due to insufficientsupplies of capelin, amountsto about660,000 pairs and constitutesalmost each chick was fed 50 g of capelin per day from the one-third of the total Norwegian population of At- end of the experimentto day 43, resemblingthe "nor- lantic Puffins(Anker-Nilssen and •lyan 1995). mal" ageat fledgingat Rost(Anker-Nilssen and Oyan Chicks.--In the beginning of each June, 100 acces- 1995). Groupsgiven equal amountsof food (group 6 sible nests containing an egg were checkedevery in both years) acted as controls for possiblediffer- evening throughout the hatching period. When ap- encesin experimental conditionsbetween the years. proximately one-third of the eggs had hatched, 20 Due to a temporaryproblem with saltedcapelin being chicks (less than 24 h old) were collected and ran- given to chicks in group 6 on days 17 to 19 in 1990, domly distributedbetween the experimentalgroups this group was excludedfrom further analysis. (see below). Chicks were collected between 23 June Most chicks ate willingly throughout the experi- and 3 July in 1990 and 25 and 27 June in 1991. The ment, except that chicks in groups 6 and 7, which first day after collectionwas defined as day 1, and were provided with the most abundant food supply, chick massat this day prior to their first meal was occasionallyhad to be force-fedduring the first and taken as the hatching mass.Chicks weighed lessat last 2 to 4 days. This reluctanceto feed probably was hatching in 1990 than in 1991 (t = 2.30, df = 37, P = a consequenceof excessivefeeding, as severalstudies 0.027), but the differencewas only 2 g (i.e. <5% of indicatemuch lower daily food requirementsof wild body mass).Therefore, data from both years were puffin chicks early and late in the nestling period pooled for subsequentanalyses. (Harris 1976, Harris and Hislop 1978,Ashcroft 1979, Experimentaldesign.--Five blocks of four one-chick Anker-Nilssen 1987). cages(21 x 30 x 20 cm) were built of waterproof The quality of random samplesof the capelinwas plywood and wire netting. Aluminum profiles with det•erminedatthe Agricultural University of Norway built-in heatingelements made up the crosswalls of at As (1990) and the State Food Control Authority at the cages.The surfacetemperature of the profileswas Kv•il (1991) accordingto standardmethods for water, regulatedby a voltage regulator (Liibcke R52-220b) crude fat (HC1), protein (Kjeldahl-N), and total ash and kept within the range 34-37øC for the first 10 content. Sample sizes were small, but there was no days,to compensatefor brooding.During the restof indication that protein and fat content of the fish the experiment it was kept at 20-22øC to keep the differed between the two years (Table 2). The mean chicks dry, as excreted salty water tended to accu- energeticvalue for the capelin was about 5.3 kJ/g of mulate on the inner walls of the cages.The roomwas wet mass,which is well within the rangeof 3-11 kJ/g kept dark exceptduring a few hoursof cleaningevery reported by Bradstreetand Brown (1985) and others 1-3 days,and temperaturewas approximately 12-15øC (e.g. Barrett et al. 1987) for food brought to puffin throughoutthe experiment.Disturbance was kept to chicksby their parents. a minimum. Measurements.--In 1990, chicks were measured ev- Chicks were fed on capelin (Mallotusvillosus) that ery morning for the first 26 days,and thereafterevery were caughtand frozen in the BarentsSea each May. secondmorning. In 1991,chicks were measuredeach Capelin were transportedto Rost in blocks of 15-25 morning throughout the experimental period. All kg, which were then thawed, divided into one-day measurementswere done before the first feeding of rations, and stored frozen. Individual rations were the day. Chicks were weighed to the nearest 0.2 g 832 oYAN ANDANKER-NILSSEN [Auk, Vol. 113

TABLE1. Amount of food (g/day and total) given to eachpuffin chick in the variousexperimental groups. The groupnumber indicates the numberof food equivalents(i.e. 3.33g) given at the onsetof the experiment.

No. of chicks Age of chicks(days) Group 1990 1991 1-3 4-9 10-18 19-37 Total 2 -- 4 6.7 13.3 20.0 26.7 787.7 3 10 -- 10.0 20.0 30.0 40.0 1,180.0 4 -- 4 13.3 26.7 40.0 53.3 1,573.3 5 -- 4 16.7 33.3 50.0 66.7 1,966.7 6a 10 4 20.0 40.0 60.0 80.0 2,360.0 7 -- 4 23.3 46.7 70.0 93.3 2,753.3

Group 6 excludedfrom analysesafter day 17 in 1990.See text. using an electronicbalance. Wing length (maximum pc (Complete Statistical System, version 2.1) com- flattenedchord) and, in 1991,length of the 2nd pri- puter package. A simple statistical routine pro- mary (from the tip to the point where the quill ap- grammedin Fortranwas used to calculategroup means pearsfrom the sheath)were measuredto the nearest and SEs,whereas all growth curveswere made using 1 mm using a stoppedruler. Vernier caliperswere SigmaPlot (version 4.02). usedto measure(+__ 0.1 mm) length of culmen,head Two methodswere used to comparegroup means: + bill (Jones et al. 1982), tarsus, and middle toe (1) growth curvesof group means+ 1 SE were com- (Tschanz1979). Skull length was calculatedby sub- pared directly by visual inspection;and (2) a growth tractingculmen length from head + bill, and length index was determined for each characterby compar- of the forearm was calculatedby subtractinglength ing each of groups 2-6 with group 7, which always of 2nd primary from total wing length (as usedhere attained the best growth. Mean hatchling size (all "forearm" refers to the antebrachium plus the ma- groups)and final chick size in each group were con- nus). All measurementswere made by one person. verted to percentageof adult size and comparedfor Tarsusdata from 1990were omitted from the analyses all charactersexcept for length of 2nd primary, fore- due to a changein measuringtechnique. arm, and skull. Skull comparisonswere omitted due The chickswere sexedby dissection.Sex distribu- to the great differencesin bill proportions between tion did not differ betweengroups (X 2 = 7.07,df = 6, adults and chicks. P = 0.314;Table 3). In 1991,the amountsof deposited subcutaneousand internal posteriorfat were ranked from 0 to 3 (seeJones et al. 1982). Also, the maximum RESULTS thickness of the ventral subcutaneousfat depot was measuredusing vernier calipersto the nearest0.1 All chicks survived until the end of the ex- mm, after making an incisionlengthwise from the periment.Retarded growth rates were recorded inside of the skin; internal posteriorfat was excised for all charactersas a consequenceof low food and weighedto the nearest0.01 g on an electronic intake. Body masswas the only characterin balance.During Juneto August1992, 243 adult puf- which growth was approximatelyproportional fins (with at least three bill grooves;Petersen [1976], to the amount of food given (Fig. 1). Harris [1984]) were caught in mist nets at Hernyken Wing characters.--Thetwo groupswith the and measuredby the same person. Except for the lowest food supply lagged behind by day 9 in lengthof 2nd primary,the samecharacters measured on the chicks were measured on adults. total wing length (Fig. 2). Total wing length Statisticalanalyses.--Most statistical calculations and was influencedmainly by growth of the 2nd tests(always two-tailed) were made using the CSS/ primary, which was the only characterwhere a delayed onset of growth was more apparent than reducedgrowth rate (Fig. 3). Primariesap- TABLE2. Protein, fat, and caloric content of capelin (Mallotusvillosus) fed to puffin chicks during ex- pearedto grow approximatelyat a constantrate periments.Data are medians,with samplesizes in parentheses(each sample was derived from several TABLE3. Sex distribution of puffin chickswithin ex- fish). Energyvalues for 1990were obtainedfrom perimental groups. Breivik (1991). Experimentalgroup Variable 1990 1991 Sex 2 3 4 5 6 7 Total Protein (% of dry mass) 60.3 (3) 60.9 (2) Crude fat (% of dry mass) 30.8 (3) 29.8 (2) Females 3 5 2 0 1 3 18 Energy(kJ/g wet mass) 5.7 (3) 4.9 (2) Males 1 5 2 4 3 ! 22 October1996] GrowthAllocation in AtlanticPuffins 833

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4OO 5o 35O cn 300 • 40 • 250

• 200 •3 20

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10 20 o lO 20 30

AGE d AGE d

FIG.1. Growth curvesfor body mass(mean + SE) FIG.3. Growth curvesfor length of 2nd primary of puffin chicks in each experimentalgroup (filled (mean + SE) in puffin chicks in each experimental trianglepointing down, group 2; hollow square,group group. Symbolsare sameas in Figure 1; samplesizes 3; filled square,group 4; filled diamond, group 5; are given in Table 1. filled circle,group 6; filled trianglepointing up, group 7). Samplesizes are given in Table 1. day 22 in group 2. Growth of the forearm in within each group throughout the experiment. group 2 deviated from the others on day 6, and Growth rate was almost identical in groups 4 never obtained an asymptotic value, whereas to 7 (slope of linear regression 1.8, 1.9, 2.0 and all other groups reached almost the same as- 2.0 mm/day, respectively),but it decreasedby ymptotic value (Fig. 4). The growth index for nearly half in group 2 (1.1 mm/day). Primary the forearm in group 2 (42%) was nearly half quills erupted between days 11 and 14 in groups of that in the other groups (79-94%; Table 4). 4 to 7, whereas primaries did not erupt until Head characters.--Culmengrowth in groups

140

80 120

70 100 E E 6O 80

60 40

40 3O

20 2O

0 0 10 20 30 0 10 20 30

AGE d AGE d FIG. 2. Growth cm'vesfor wing length (mean _+ FIG.4. Growth curvesfor length of forearm(mean SE)in puffin chicksin eachexperimental group. Sym- _+SE) in puffin chicksin each experimentalgroup. bols are sameas in Figure 1; samplesizes are given Symbols are same as in Figure 1; sample sizes are in Table 1. given in Table 1. 834 OY•,u.•lqv ANKER-NmssEN [Auk, Vol. 113

TABLE4. Growth indices for morphologicalcharacters in experimentalpuffin chicks.The growth index is the total amountof growth attainedas a percentageof that in group7 (the groupreceiving the mostfood), roundedto the nearestwhole percentage.Within groups,preference orders are in parentheses(preference decreaseswith increasing numbers). Data are plotted in Figure 10. Head + bill and wing length are compositesof other characters.

Experimentalgroup Sumof Overall Character 2 3 4 5 6 7 ranks priority Skull 57 (1) 83 78 (3) 91 (1) 101 (1) 100 6.0 1 Culmen 51 (2) 56 85 (1) 85 (4.5) 96 (2) 100 9.5 2 Forearm 42 (3) -- 79 (2) 87 (3) 94 (3.5) 100 11.5 3 Middle toe 33 (4) 55 74 (4) 90 (2) 94 (3.5) 100 13.5 4 Tarsus 31 (5) -- 69 (5) 85 (4.5) 93 (5) 100 19.5 5 2nd primary 22 (7) -- 66 (6) 75 (6) 87 (6.5) 100 25.5 6 Body mass 23 (6) 39 58 (7) 74 (7) 87 (6.5) 100 26.5 7 Head + bill 54 71 81 89 97 100 -- -- Wing length 36 60 75 83 92 100 -- --

2 and 3 was markedly slower than in the other tarsusdiffered greatly in growth acrossgroups groupsfrom day 9 onwards(Fig. 5), and their (Figs. 8 and 9). Tarsuslength diminished in all growth indiceswere only abouthalf of that in groups shortly after hatching. At day 6, group group 7 (Table 4). Head charactersin groups4 2 split from the rest and displayed markedly to 7 grew at similar rates throughoutthe ex- slower growth than the other groups for the periment.Skull and head + bill were the char- rest of the experiment.Asymptotic values were actersin which differencesin growth between reachedby groups4-7 for tarsus,and by groups groupsapparently was the smallest(Figs. 6 and 6 and 7 for middle toe, although at slightly 7). Nevertheless,group 2 still lagged behind, different levels in each group. Growth indices acquiringa growth index of about55%, whereas varied from 31 to 94% for both characters (Table groups 3 to 6 achievedbetween 83 and 101% 4). for skull length and between 71 and 97% for Comparisonsamong characters.--Characters dif- head + bill length (Table 4). fered in the threshold and degree of reduced Charactersof the feet.--Both middle toe and growth rate. In some characters,most groups

E 30 E z 28 LLI

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Z "' 20 ._1 25 18

16 , I , I , I , 0 10 20 30 ' 1•0 ' 2•0 ' 3; '

AGE d AGE d FIG.5. Growth curvesfor length of culmen(mean FIG. 6. Growth curvesfor length of skull (mean + SE) in puffin chicksin each experimentalgroup. + SE) in puffin chicks in each experimental group. Symbols are same as in Figure 1; sample sizes are Symbols are same as in Figure 1; sample sizes are given in Table 1. given in Table 1. October1996] GrowthAllocation in Atlantic Puffins 835

50 20

0 10 20 3 0 I 20 30

AGE d AGE d FIG. 7. Growth curves for length of head + bill' FIG. 9. Growth curvesfor length of tarsus(mean (mean + SE) in puffin chicks in each experimental + SE) in puffin chicks in each experimental group. group. Symbolsare sameas in Figure 1; samplesizes Symbolsare same as in Figure 1; sample sizes are are given in Table 1. given in Table 1.

exhibited very different growth rates(most ev- ident in middle toe; Fig. 8), whereas in length of 2nd primary and culmen, retarded growth rates were pronounced only in groups 2 and 3 (Figs. 3 and 5). Growth increased with food intake but dif- 90 fered among characters(Fig. 10). The effect of food intake wasmost pronounced for body mass, X 1008OI * , , , , 50 , • . , . , , . E 45 I I U.I - 4.0 :? o 40 u4, : 3s 2030 Iß " 30

percentageof growth in group 7) of morphological ch•amem for each experimentalgroup (hollow •i- •gle pointing up, length of skull; hollow dimond, 10 20 30 length of head + bill; hollow triangle pointing down, length of •lmen; filled triangle pointing up, length AGE d of fore,m; filled dimond, total wing length; filled , FIG. 8. Growth curves for length of middle toe circle, length of middle toe; filled squ•e, length of (mean + SE) in puffin chicks in each experimental tabus; hollow ciTcle,body m•s; filled tffi•gle point- group. Symbolsare sameas in Figure 1; samplesizes ing down, length of 2nd prim•). Staple sizesare are given in Table 1. given in Table 1. 836 o¾•u •ID A_•ram-Nmss•N [Auk,VoL 113

TAnLœ5. Measurementsof adult puffins comparedwith measurementsof chicks(as % of adult size) at day 1 and day 38, the latter separatedby experimental group. Adults Chicks Chicksatday 38 (by experimental group) Character œ SD n at day I 2 3 4 5 6 7 Body mass(g) 451.8 33.4 243 10 30 40 56 68 78 85 Wing (mm) 172.1 3.7 231 12 47 60 69 71 75 77 Culmen (mm) 45.6 1.9 230 40 54 58 65 65 68 70 Head + bill (mm) 81.0 2.1 230 54 72 77 81 83 85 87 Middle toe (mm) 45.7 1.6 55 57 75 85 91 94 97 96 Tarsus (mm) 28.8 1.0 55 68 81 -- 96 97 100 101 where dependenceon amount of food was al- single-egg clutch of Atlantic Puffins (Hudson most linear. Accordingto a simple ranking of 1985) are traits that clearly put this species growthindices within groups,the overallorder among those that give high priority to adult of priority increasedfrom body mass,primary survival. Suchspecies are more likely to with- length, tarsus,middie toe, forearm,and culmen stand long-term environmental stressesthat af- to the skull (Table4). Comparedwith adult size, fect food availability. In speciesdepending on the tarsuswas the mostdeveloped character at highly unpredictablefood sources,the ability hatching,followed by middle toe, head + bill, of adults to breed will be sensitive to changes culmen,wing, and body mass(Table 5). in prey availability. In long-lived specieswith Fatstorage.--Even the chicksthat receivedthe clutchesof one, this sensitivitymay be strength- least amount of food deposited considerable enedby the factthat the singlechick is expected amounts of fat. The amount of subcutaneous fat to contributerelatively little to its parents'fit- varied between scores 2 and 3, whereas internal ness (Clark and Ydenberg 1990). Life history posteriorfat depositswere morevariable (Table theory statesthat risks are assumedin propor- 6). The thicknessof subcutaneousfat was ap- tion to the adults'expectations of mortality be- proximately 40% higher in group 7 than in tween breeding seasons(Linden and Moller groups 2 and 3, and posteriorfat depositsin 1989, Stearns 1992, Martin 1995), which nor- group 7 were approximately 100 times greater mally is only 5-10% in Atlantic Puffins(Harris than those in group 2. and Wanless 1991, Anker-Nilssen and •h•tan 1995). Consequently,food limitation often re- DISCUSSION suits in poor growth, delayed fledging, and in- creasedmortality of chicks,and may even in- Tradeoffs between adult survival and fecun- duce the adults to abandon the nest. Such effects dity are important in the characterizationof a have been demonstrated in Atlantic Puffins and bird's life history strategy(e.g. Linden and in closelyrelated species (Harris 1978;Vermeer Moller 1989, Stearns 1992, Martin 1995). The et al. 1979; Vermeer 1980; Lid 1981; Brown and longevity, delayed onset of reproduction,and Nettleship 1984;Anker-Nilssen 1987,1992; Bar- rett et al. 1987; Martin 1989; Anker-Nilssen and T•a•LE6. Fat depositsin puffin chicksat 43 daysold, Oyan 1995). Apparently,the chick will suffer by experimentalgroup. Fat scoresranged from 0 from starvationunless it is able to developad- to 3 (see Jones et al. 1982). aptations that allow it to leave the nest at an earlier physiologicalage. Experimentalgroup Differential growth as a responseto reduced Variable 2 4 5 6 7 food supply has been reported in many birds, Subcutaneous fat including both altricial and precocial species Median score 2.0 3.0 3.0 3.0 3.0 (Schew 1995, Schew and Ricklefs 1996). Some f thickness (mm) 3.6 3.6 4.1 4.4 5.1 responsesseem to be universal and probably SD thickness (mm) 0.9 0.2 0.2 0.3 0.7 reflect physiologicalconstraints or adaptations Internal posterior fat that are of vital importance to all species.For Median score 1.0 2.0 2.5 3.0 3.0 instance,growth should be allocatedto the ner- f mass(g) 0.04 0.42 1.47 2.16 4.76 vous system and other structuresthat are the SD mass(g) 0.02 0.19 0.42 0.44 1.28 least able to recover from retardation (see Schew October1996] GrowthAllocation inAtlantic Puffins 837 and Ricklefs 1996).Consequently, great caution affectedby their nutritional state,which alsois is needed before claiming that an allocation of in agreementwith resultsof our study. growth is an adaptationto the particular ecol- Our study indicatesthat growth of the head ogy of the speciesin question.Nevertheless, it is given highestpriority in food-stressedAtlan- is important to considerany reasonableecolog- tic Puffin chicks, followed by the wings and ical explanation that could be involved, and lastly the feet. A high preferencefor skull which also may motivate further research. growth agreeswith studiesof Yellow-eyedPen- Our experiment was not designedto identify guins (van Heezik 1990). Furthermore,Schew the extent to which growth restrictionswere (1995) demonstrated that European Starlings merely imposed responses,i.e. a direct and un- (Sturnusvulgaris) and JapaneseQuail (Coturnix avoidable consequenceof reduced supply (cf. japonica)maintained brain growth during pe- Schew and Ricklefs 1996). The gradual retar- riods of food restriction. These preferences dation of growth ratefor mostcharacters among probably reflect the general need for a well- groups,as well aswithin groupsduring periods developed brain and nervous system,but eco- of constantfood supply, indicated that imposed logicaldifferences between species also may be responsesare effective in puffin chicks. Nev- important.Nol (1986) found that the optic lobe ertheless,the heterogeneouseffects of food re- was larger at hatchingin shorebirdchicks that strictionson different charactersstrongly sug- run and catch prey soon after hatching than in gestthat induced,adaptive variation also played those that feed by begging or pecking. Puffin an important role. chicksare independent when they leave their Charactersof greatestimportance for survival burrow (Harris and Birkhead 1985), and they may be expectedto be given preferential allo- are forcedto acquireskills involved in pursuing cation of resourcesand changerelatively little, and capturingprey very quickly. Hence, brain or at least change less than charactersof low developmentshould be relatively independent priority. Thus, our study indicated that body of fluctuationsin body mass.If brain develop- mass,tarsus, and middle toe were of lower pri- ment is independent of body mass, then the ority in puffin chicks,given their large changes effectshould be more apparent in specieswhere in growth with varying food intake. The low- chicksare independentat fledging than in those ranking value of primary length wasdue main- where chicksare accompaniedand fed by their ly to aspectsof the growth index method,which parentsfor a considerabletime after they leave is lessapplicable when a delayin onsetof growth the nest. Another reason for the allocation of is apparent. The fact that the growth rate for energy to growth of the brain is that develop- primaries was approximately the same for ment of other charactersprobably is a function groups4 to 7 demonstratesthat growth of pri- of brain development. Once adequate brain maries is given high priority when first initi- growth is accomplished,resources can be allo- ated. This has been supported by other inves- cated to other components, such as those en- tigations. For instance, Lack and Silva (1949) abling the chickto fledgeearly (despitepossible found that bursting of feather sheathsin nest- low body massand poor condition),if food sup- ling European Robins (Erithacusrubecula) oc- ply is suddenly reduced.To remain in the nest curred independently of body mass,although under these circumstanceswould represent cer- in some"late developers"the burstingof feath- tain death to the chick, whereas nest departure er quills was delayed two days. Harris (1966) could be rewarded by survival. was the first to suggestthat seabirdsput re- Well-developed wings may be particularly sourcesinto wing development before body important in enabling flight from the nest to mass. Anker-Nilssen (1987) found that culmen the sea. Flight, in contrastto walking, makes lengths,but not wing lengths,of puffin fledg- the chick lessvulnerable to predatorygulls and lings were shorter in a poor than in a better also shortensthe time chicksare exposedto this year, and also suggestedthat puffin chicks se- danger.Furthermore, flight allows the chick to lectivelyallocate energy to growth of the wings. move farther out to sea. The time and effort Similarly, Gaston (1985) referred to numerous neededto reach feeding areassolely by swim- studiesof alcidswhere the growth rate of wing ming probablyexceeds the capacityof a chick featherswas unaffectedby nutrition. However, that is already starving. Moreover, the ability he alsoobserved that growth of remigesin un- to pursue and catchprey also is necessaryfor derweightThick-billed Murres (Uria lomvia)was survival. In this context,well-developed wings 838 OYANAND AIqKER-NII_SSEIq [Auk,Vol. 113 could be advantageous,because puffins use their In Leach's Storm-Petrel (Oceanodromaleucor- wings for propulsion under the water. With hoa) chicks, 70-80% of the stored fat is located reference to Uria and Alca species,whose rem- in subcutaneousdeposits (Ricklefs 1974), which iges and rectricesdevelop after nest departure, serve as a buffer against variations in food de- Croxall and Gaston (1988) argued that swim- livery rate (Ricklefs and Schew 1994). The in- ming and finding food were unlikely to be im- sulatoryfunction of thesefat depositsis poorly paired by incompletely grown flight feathers. understood but is believed to provide extra in- Nevertheless,these chicksare fed by their par- sulation in Synthliboramphusmurrelets, which ents long after nest departure, whereas puffin go to seawhen still coveredby down (Croxall chicksare not, suggestingthat well-developed and Gaston 1988). Thus, in newly fledged puf- wings are more important for catchingprey in fins (whose plumage often is not fully devel- puffins than in the latter species.In order to oped),deposition of subcutaneousfat may prove capture and handle prey, the chick also may to be of significance.It is important to stress, need a relatively strongand well-developed bill, however, that fat depositswere measuredat day which could be the reasonwhy length of cul- 43, when all chickshad been fed 50 g daily for men ranked so high in growth allocation. We five days. This rate of food supply was almost realize, however, that the apparent preferential twice the former diet given to chicksin group growth of the bill also may have been an in- 2, and only about half of that previouslygiven evitable result of the bill's intimate connection to group 7. As demonstratedfor cockerels(Os- with the skull (and its rapid development). born and Wilson 1960), it is possiblethat the In growing birds, resources are allocated smallestchicks stored fat becausethey were un- preferentiallyto growth of the componentswith able to take full advantageof the increaseden- the highestcurrent functional priority, with due ergy supply.Conversely, the largestchicks could regard for future needs (O'Connor 1977). Rick- have been forced to deplete their fat deposits lefs (1979) has discussedthe significance of in order to maintain growth of other body parts, highly developed legs at hatching, which he as shown for European Starlings (Schew and attributed to the need for homeothermiccapac- Ricklefs 1996, Schew pers. comm.). Both effects ity becauseleg musclesare the most important would reduce differences in fat deposits be- sourceof heat production early in a chick'slife. tween groups.Moreover, dissectionof wild puf- This argument may explain why charactersof fin chicks found dead on their way to the sea the feet ranked solow in our study despitetheir showed no signs of accumulatedsubcutaneous relatively large size at hatching. The relative or internal fat, despite their having a larger decreasein importance of leg musclesduring body massthan that attainedby the mostpoorly the nestlingstage for non-terrestrialspecies may fed chicksin our experiment (IDyanand Anker- be causedby the gradual developmentof other Nilssenunpubl. data).However, thesebirds may important muscles(e.g. the pectoralis), which have died from starvation following depletion may replace or assistthe leg musclesin heat of fat reservesduring an extended period of production.The importanceof growth and mat- food shortage. A systematic examination of uration of the pectoral musclesin this connec- healthy puffin chickscaptured on their way to tion has been emphasizedfor Willow Ptarmi- the sea would show whether storage of sub- gan (Lagopuslagopus) by Aulie (1976). cutaneousfat, rather that internal deposits,is a Resourcesalso were allocatedfor building up general feature, or if fat deposits in our chicks fat deposits.Despite extremely poor feeding of resulted from the experimental feeding con- somechicks (i.e. groups2 and 3), they still stored ditions. significant amounts of subcutaneousfat. De- We conclude that morphometric parameters position of fat is documentedin the Procellar- in Atlantic Puffin chicks are influenced differ- iiformes, which feed their single chick on a ently by food intake.In particular,when stressed mixture of undigestedfood and an energy-rich for food, growth of the head is given priority oily substance(Ashmole 1971, Ricklefs et al. over the wings, which in turn are favored over 1985, Ricklefs 1987). In contrast, Atlantic Puffins the feet. Preferenceprobably is given to param- feed their chicks mainly on fish that have a eters that are especiallyimportant for survival lower energeticvalue. Nevertheless,our results if premature fledging is required due to inad- give somesupport to Lack's(1968) assertion that equate food or parental abandonment. In an puffin chicksbuild up extensivefat reserves. evolutionary context, preferential growth al- October1996] GrowthAllocation inAtlantic Puffins 839

location in puffins may have arisen as a con- BARRETT,R. T., T. ANKER-NILSSEN,F. RIKARDSEN,K. sequenceof frequentexposure to poorfood sup- V^LDE, N. ROV, AND W. V^DER. 1987. The food, plies, constraintson the feeding ecologyof the growthand fledgingsuccess of NorwegianPuffin parents, and the subsequentrisk to chicks of chicks Fratercula arctica in 1980-1983. Ornis Scan- dinavica 18:73-83. being abandoned. BARRETT,R. T., ANDF. RnOmDSEN.1992. Chick growth, fledging periodsand adult weight lossof Atlantic Puffins Fraterculaarctica during years of pro- ACKNOWLEDGlvlF2qTS longed food stress.Colonial Waterbirds 15:24- 32. This study was affiliated with the long-term puffin BIRKHEAD,T. R., AND M.P. HARRIS. 1985. Ecological researchproject conducted at Rest by the Norwegian adaptationsfor breeding in the Atlantic Alcidae. Institute for Nature Research(NINA) with support Pages205-231 in The Atlantic Alcidae (D. N. Net- from the Directorate of Nature Management. Funds tleship and T. R. Birkhead,Eds.). Academic Press, were receivedfrom the University of Trondheim, the London. World Wide Fund for Nature (Norway), and NINA. BRADSTREET,M. S. W., AND R. G. B. BROWN. 1985. Thanks also are due to the Institute of Marine Re- Feeding ecology of the Atlantic Alcidae. Pages searchin Bergen for providing the capelin and the 263-318 in The Atlantic Alcidae (D. N. Nettleship Norwegian LighthouseAuthorities for permitting us and T. R. Birkhead, Eds.). Academic Press, Lon- free use of the buildings on Skomvlerlighthouse. don. Edward Hough improved the language. We are especiallyindebted to Eivin Roskaftand BREIVIK,M. 1991. Endringer i energiutnyttelsehos John Atle K/ills for fruitful discussions and com- unger av lunde og teist. Cand. real. thesis, Ag- riculturalUniversity of Norway,.•s. ments.Very usefulcomments also were givenby Mike P. Harris, Thomas E. Martin, Robert E. Ricklefs, Wil- BROWN,R. G. B., AND D. N. NETTLESHIP.1984. Cape- lin and seabirdsin the northwestAtlantic. Pages liam A. Schew, and an anonymousreviewer. Geir 184-194 in Marine birds: Their feeding ecology Wing Gabrielsenand Ingar JosteinOien commented and commercial fisheries relationships (D. N. on an early draft of the manuscript.Per Anker-Nils- Nettleship, G. A. Sanger,and P. F. Springer,Eds.). sen, Margrete Breivik, Gunnar Ligaard, Ole Wiggo Canadian Wildlife Service Special Publication, Rostad,and I. J. Oien helped in the field, and O. W. Ottawa. Rostad and Oivind Bakke contributed valuable sta- CLARK, C. W., AND R. C. YDENBERG. 1990. The risks tistical assistance.A specialthanks goesto Egil M. Torsetnes,who constructedthe cages. of parenthood. I. General theory and applica- tions. Evolutionary Ecology4:21-34. CROX•I,I,,J.P., AND A. J. G^STON. 1988. Patterns of reproduction in high-latitude Northern- and LITERATURE CITED Southern-hemisphereseabirds. Pages 1176-1194 ANKER-NILSSKN,T. 1987. The breeding performance in Acta XIX CongressusInternationalis Orni- of Puffins Fratercula arctica on R•st, northern Nor- thologici(H. Ouellet, Ed.). Ottawa, Ontario, 1986. National Museum of Natural Science, Ottawa. way in 1979-1985.Fauna norvegica Series C, Cin- clus 10:21-38. DRENT,R. H., ^ND S. D•N. 1980. The prudent par- ANKr•R-NILSSEN,T. 1992. Food supply as a determi- ent: Energeticadjustments in arian breeding.Ar- dea 68: 225-252. nant of reproduction and population development in NorwegianPuffins Fratercula arctica. D.Sc. G^S7ON,A. J. 1985. Developmentof the young in thesis, University of Trondheim, Trondheim, Atlantic Alcidae. Pages319-354 in The Atlantic Norway. Alcidae (D. N. Nettleship and T. R. Birkhead, ANKER-NILSSEN,T., AND H. S. OYAN. 1995. Long- Eds.). Academic Press, London. term studiesof the breeding biology of Puffins GOODMAN, D. 1974. Natural selection and a cost ceil- at Rost. NINA Fagrapport 15:1-48. ing on reproductiveeffort. AmericanNaturalist ASHCROFT,R. E. 1979. Survival ratesand breeding 108:247-268. biology of Puffinson SkomerIsland, Wales. Ornis HARRIS,M.P. 1966. Breeding biology of the Manx Scandinavica 10:100-110. ShearwaterPuffinus puffinus. Ibis 108:17-33. ASHMOLE,N. P. 1971. Sea bird ecologyand the ma- HARRIS,M.P. 1976. Lack of "desertion period" in rine environment. Pages 223-286 in Avian biol- the nestling life of the Puffin, Fraterculaarctica. ogy, vol. I (D. S. Farner and J. R. King, Eds.). Ibis 118:115-118. Academic Press, New York. HARRIS,M.P. 1977. Comparativeecology ofseabirds AULIE,A. 1976. The pectoral musclesand the de- in the GalapagosArchipelago. Pages65-76 in velopment of thermoregulationin chicksof Wil- Evolutionaryecology (B. Stonehouseand C. Per- low Ptarmigan. Comparative Biochemistryand rins, Eds.). Macmillan, London. PhysiologyA 53:343-346. HARRIS,M.P. 1978. Supplementaryfeeding of young 840 OY•NAND ANKF•R-NILSSEN [Auk,Vol. 113

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