sign in sign up
<<
Home , Frugivore

1080 ShortCommunications [Auk, Vol. 118

NILSSON,J.-•., ANDH. G. SMITH.1988. Effects of dis- SVENSSON,E. 1997. Natural selection on avian breed- persal date on winter flock establishmentand ing time:causality, fecundity-dependent, and fe- social dominance in Marsh Tits Paruspalustris. cundity-independent selection. Evolution 51: Journalof Animal Ecology57:917-928. 1276-1283. NOBLE,D. G. 1990. Factorsaffecting recruitment in VERBOVEN,N., AND M. E. VISSER. 1998. Seasonal var- Thick-billed Murres Uria lornvia on Coats Island, iation in local recruitment of Great Tits: The im- Northwest Territories. M.S. thesis, Queen's Uni- portanceof being early. Oikos 81:511-524. versity, Kingston, Ontario. YDENBERG,R. C. 1989. Growth-mortality trade-offs SEALY,S. G. 1973. Adaptive significanceof post- and the evolutionof juvenile life-historiesin the hatchingdevelopment patterns and growthrates Alcidae. Ecology 70:1494-1506. in the Alcidae. Ornis Scandinavica 4:113-121. YDENBERG,R. C. 1998. Evaluatingmodels of depar- SPEAR,L. B., ANDN. NUR. 1994. Brood size,hatching ture strategiesin alcids.Auk 115:800-801. order and hatchingdate: Effects on four life- his- tory stages from hatching to recruitment in Western Gulls. Journal of Animal Ecology 63: Received15 May 2000, accepted16 April 2001. 283-298. AssociateEditor: D. Nettleship

The Auk 118(4):1080-1088, 2001

Protein Requirementsof a Specialized Frugivore,Pesquet's (Psittrichasfulgidus)

GREGORYS. PRYOR,•,3 DOUGLAS J. LEVEY,• AND ELLEN S. DIERENFELD2 •Departmentof Zoology,University of Florida,Gainesville, Florida 32611-8525, USA; and 2Departmentof WildlifeNutrition, Wildlife Conservation Society, Bronx, New York10460, USA

ABSTRACT.--Forthose few speciesthat are ex- (Morton 1973, White 1974, Berthold 1976, clusivelyfrugivorous, the low proteincontent of Mattson 1980, Snow 1981, Thomas 1984, Jordano is likely a major nutritionalconstraint. Physiological 1992). Furthermore,nonprotein (N) in the mechanismsthat allow strict frugivory remain enig- form of free amino acids and secondarymetabolites matic,but reducedprotein requirements may suffice. is commonin (Herrera 1982,Cipollini and Lev- Weinvestigated protein requirements of Pesquet'sPar- ey 1997)and is not discriminatedfrom protein N in rot (Psittrichasfulgidus), a highly specialized,obligate traditional Kjeldahl analysis (lzhaki 1993). Thus, frugivore.Three isocaloric,fruit-based diets of vary- true proteincontent of fruit is likely evenlower than ing proteincontent (6.1, 3.3, and 2.6% dry masscrude mostpublished estimates. protein) were used in feedingtrials lastingthree to Given the low protein contentof fruits, it is not five days per diet. A minimum dietary protein re- surprisingthat very few speciesof can subsist quirementof 3.2%dry masswas estimatedfrom bal- on a diet of exclusivelyfruits (Berthold1976, Snow ancetrials. Endogenousnitrogen losseswere 0.05 gN 1981,Holthuijzen and Adkisson1984, Bairlein 1987, kg 075day • and nitrogenequilibrium occurred at 0.32 Izhaki and Safriel 1989).Although the physiological gN kg-ø7s day •. Thosevalues are extremelylow com- mechanismsthat allow somebirds to be strictly fru- pared to thoseof granivorousand omnivorousbird givorousare not fully understood,proposed mech- species,but higher than thoseof nectarivorousspe- anismsinclude high ingestionrates (Sorensen1984, cies. In terms of nitrogen lossesand requirements, Bairlein 1987, Izhaki and Safriel 1989, Karasov and Pesquet'sParrot most closely parallels the highlyfru- Levey 1990,Levey and Grajal 1991,Levey and Duke givorousCedar Waxwing (Bombycilla cedrorutn). Thus, 1992, Levey and Karasov 1992), short gut retention reducedprotein requirementsappear to play an im- times (Herrera 1984, Martinez del Rio et al. 1989, portantphysiological role in abilityof highlyfrugiv- orous birds to subsist on fruit diets. Levey and Grajal 1991,Levey and Duke 1992,Levey and Karasov 1994), and low protein requirements Althoughfruits provide a rich sourceof easilyas- (Witmer 1998, Witruer and Van Soest 1998). We in- similated ,they are notoriouslylow in vestigatedprotein requirementsof an obligatefru- givorousbird, Pesquet'sParrot (Psittrichasfulgidus). 3E-mail: [email protected] In particular,we examinedtwo relatedphysiological October2001] ShortCommunications 1081

TABLE1. Compositionof the fruit-baseddiets used in Pesquet'sParrot feedingtrials.

Diet 1 Diet 2 Diet 3

Wet mass Gross energy• Wet mass Gross energya Wet mass Grossenergy • (g) (kcal) (g) (kcal) (g) (kcal) Yam (peeled/cooked) 25.82 32.28 26.21 32.76 33.05 41.31 Apple (cored) 19.90 11.74 20.21 11.92 25.48 15.03 Cantaloupe(seeded/peeled) 14.94 5.23 15.17 5.31 0 0 Banana (peeled) 14.64 13.47 14.87 13.68 18.75 17.25 Grapes (seedless) 9.44 6.42 9.59 6.52 12.09 8.22 Papaya(seeded/peeled) 7.17 2.72 7.28 2.77 9.18 3.49 Avi-pelb 4.78 14.34 0 0 0 0 Chicken egg (hard-boiled, peeled) 3.29 4.84 3.34 4.91 0 0 Sucrose 0 0 3.34 13.16 1.45 5.71 Total 100 g 91.04 kcal 100 g 91.03 kcal 100 g 91.01 kcal Grossenergy (kcal g •, WM) 0.91 0.91 0.91 Grossenergy (kcal g •, DM) 3.78 3.78 3.78 Crude protein (% DM) c 6.1 3.3 2.6 • Calculated total grossenergy of wet massof eachdietary ingredient (after Watt and Merrill 1975). bAvi-pel: custom-formulatedavian maintenancemash, 15% CP (minimum). ßCrude proteincalculated as dietary N contentX 4.05 (after Izhaki 1993). responses(i.e. endogenousN losses,which represent indoor cages(-1 n'l3) and acclimatedfor 10 days.All N lostvia urine and ;and N equilibrium,which cages were disinfected with chlorhexidinebefore occurswhen N intake equalsN excretion)of that ob- use, and food bowls were disinfected with a bleach ligate frugivoreto the low protein contentof fruits. solutionbefore each use. Temperature remained con- Pesquet'sParrot is a highly specialized,obligate stant at 25øC and a natural photoperiod (via sky- frugivorethat feedsonly on a few speciesof figs(For- lights) was supplementedwith daytime fluorescent shaw and Cooper1989, Mack and Wright 1998).This lighting (12 L:12 D). The maintenancediet (Diet i in threatenedspecies is endemicto the highland rain- Table 1) was fed during the acclimationperiod and forests of New Guinea and has a featherless face and between feeding trials. Water was availablead libi- elongatebeak, which are thought to be tum, and birds were in the same room during all for preventing head feathersfrom matting when it phasesof the study. feedson the stickyinterior of large,ripe figs (Horn- Three isocaloricdiets (calculatedGross Energy = berger 1980,Forshaw and Cooper1989). In captivity, 0.91 kcal g-• wet mass [win]; 3.78 kcal g • dry mass Pesquet'sParrots are best maintained and can breed [dm]) of varying crudeprotein (CP) content(6.1, 3.3, when fed a low protein diet comprisingalmost en- and 2.6% dm CP; Table1) were fed asa homogenized tirely fruit (De Jager1976, Hornberger1980, Thurs- slurry to the birds. Thoseprotein levelsapproximate land and Paul 1987, Low 1990, 1991; Sweeney1999). the range reportedfor wild figs (range = 2.1 to 8.8% Thus, we predictedthat Pesquet'sParrot would have dm CP: Janzen1979, Thomas 1984, Wrangham et al. a low dietary protein requirement(i.e. low endoge- 1993). The sequenceand duration of feeding trials nous N lossesand low N equilibrium), relative to was 6.1% (5 days), 2.6% (4 days), and 3.3% (3 days) omnivorous and granivorous species.Because Pes- CP,respectively, with two daysof maintenancediet quet's Parrot evolved from a granivorousancestor (6.1% CP) between trials. and is distantly related to other obligatelyfrugivo- Dietary amino acid levelsfor 18 amino acidswere rous birds (Thompson1899, Dyck 1976, Hornberger determined with an automatic amino acid analyzer 1980, 1991, Van Dongen and De Boer 1984, Forshaw and an external standard. That was necessarybe- and Cooper 1989, Courtney 1997), it provides an op- cause a deficiency of a single essentialamino acid portunity to explore physiological adaptations to can result in increasedN equilibrium, and thus an frugivory in a lineage largely independentof previ- increasedprotein requirement (Maynard et al. 1979, ously examinedlineages. Klasing 1998). Conversely,an excessof nonessential Methods.--Feedingtrials were conductedfrom 15- amino acidscan causeincreased endogenous N loss- 30 May 1997 at the Wildlife ConservationSociety's es. Amino-acid profiles of diets used in this study Wildlife Survival Center, located on St. Catherines were similar but differed from a high quality graniv- Island, Georgia. Three adult, nonmolting Pesquet's orous bird diet (Table 2). That was not considered Parrotswith a mean (-+SD) initial body massof 757 problematic because had been maintained + 58 g were used. Prior to the start of trials, birds for years and reproducedon a diet similar to Diet 1 were moved from large, outdoor enclosuresto three (Tables1, 2) and appeared healthy. 1082 ShortCommunications [Auk, Vol. 118

TABLE2. Amino acid composition(percentage of total protein) of experimentaldiets. Dashesindicate un- detectable levels of amino acids.

Pesquet'sParrot dietsc High protein Medium protein Low protein Amino acid• High quality proteinb 6.1% CP (Diet 1) 3.3% CP (Diet 2) 2.6% CP (Diet 3) GLU 19.3 10.8 15.5 13.5 ASP 8.1 24.8 15.1 18.9 LEU* 7.9 5.4 7.4 6.2 LYS* 7.4 5.6 5.4 6.4 ARG* 7.0 2.5 2.9 3.0 GLY 6.4 8.6 9.4 7.5 VAL* 5.4 7.5 7.0 7.5 PRO 4.9 4.5 6.4 4.8 ILE* 4.7 4.2 4.5 4.5 THR* 4.5 4.4 3.8 4.1 SER 4.4 4.3 4.3 4.9 PHE* 4.3 2.0 2.8 2.1 TYR* 3.8 ------ALA 3.5 10.2 10.8 10.6 HIS* 2.8 3.3 2.7 2.8 MET* 2.5 -- 0.1 -- CYS* 2.0 ------TRP* 1.3 ------Total 100% 98% 98% 97%

Includesessential (*) and nonessentialamino acidsfor birds (after Murphy 1993). Amino acid profile of a syntheticdiet approximatingavian tissues(Murphy 1993). % CP = % N x 4.05 conversion factor (after Izhaki 1993).

Feeding times occurred at 0630, 1200, and 1600 Dry mass of diet and excreta sampleswas deter- EST,and food was removedfor the night at 2100.Di- mined by freeze drying, and N contentof dried sam- ets were prepared daily because they were fruit- ples was determinedby standardKjeldahl technique based and spoiled quickly. To test for evaporative (Associationof Official Analytical Chemists1984). water loss, a control bowl of food was placed in the Instead of using the standard nitrogen-to-protein same room as the caged birds daily and its mass conversion factor of 6.25, which is based on animal monitored. Because water loss from food was not de- tissue (Maynard et al. 1979), we used a conversion tectable during any of the feeding trials, no correc- factor of 4.05 to calculateCP. That was necessarybe- tionswere made for evaporation.Samples of the diet cause fruits have lower conversion factors than ani- were collected daily for N analysis. Uneaten food mal tissues (Izhaki 1993, Conklin-Brittain et al. was collectedat eachfeeding and weighed to deter- 1999). The 4.05 conversionfactor is basedon 27 spe- mine intake. Excreta collections were made from cies of wild fruits (Izhaki 1993). plastic sheetson the cagefloors at eachfeeding and To compare feed intake and excreta among birds when food was removed for the night. Becausepo- and diets, ANOVA were used with Scheffe'spost-hoc tential loss of gaseousN from the alkaline excreta tests. Intake and excreta values were scaled to met- (pH 8.0) was a concern(Brice and Grau 1991),excreta abolic body mass (kgø75) for interspecificcompari- were frozen immediately after collection to mini- sons(Robbins 1993). To detect changesin body mass mize N loss via ammonia volatilization (Manoukas of birds among feeding trials, percentagechange in et al. 1964, Blem 1968, Dawson and Herd 1983). body mass was calculated and arcsin transformed Body mass was monitored during feeding trials. (Sokal and Rohlf 1981). ANOVA with Scheffe'spost- Birds were weighed before first feeding each day, hoctests were then used to comparechanges in body when amount of food in their digestive tracts was mass among diets. minimal. We were concernedthat frequent weigh- To calculate endogenousN lossesand N equilib- ings would stressthe birds becausethey are rarely rium, N excretionwas plotted againstN intake ("N handled. Thus, to weigh a bird, a balancefitted balance plot;" Robbins 1993, Murphy 1993). Nitro- with a perch was placed in the cage.After the bird gen excretion included urinary and fecal compo- moved onto the perch, its body mass was recorded nents,because they are mixed togetherin the cloaca and the balance removed. The birds became accus- of birds before excretionand cannotbe adequately tomed to that routine after a few days and did not separated(Robbins 1993). From the N balanceplot, appear stressed. endogenousN lossesand N equilibrium were deter- October 2001] Short Communications 1083

A 80 10

• 60 a a

• 40

• •o

o high(6.1%) med (3.3%) low (2.6%) high(6.1%) med(3 3%) low (2 6%) Dietary Protein Level DietaryProtein Level

FIG. 1. Mean mass-specific,dry mass intake of FIG.2. Mean changesin body massesof Pesquet's Pesquet'sParrots fed diets varying in protein con- Parrotsamong experimentalfeeding trials. Dietary tent. Dietary protein calculatedas %N (analyzed) x protein calculatedas %N (analyzed)x 4.05 (after Iz- 4.05 (after Izhaki 1993). Error bars representstan- haki 1993).Error bars representstandard deviations. dard deviations. Matching letters indicate similar Matching letters indicate similar means (P > 0.05). means (p > 0.05).

Estimating protein requirementsfor maintenance in birds is complicatedby severalfactors, including mined (Robbins1993, Murphy 1993);minimum en- variabilityin nutrientdigestion and absorption(Kar- dogenousN losses(i.e. theoretical N excretion on a asovand Diamond 1983,Karasov et al. 1987,Levey protein-freediet) are indicated by the y-intercept, and Karasov1989), changes in visceralmorphology and N equilibriumoccurs where N intake equalsN (Drobney 1984,Walsberg and Thompson1990, Klas- excretion.To compareN balanceplots among indi- ing 1998),and ability of birds to adjustto insufficient viduals, ANCOVA were used. or excessivedietary protein (Bairlein1987, Murphy OnceN equilibriumwas determined,CP require- 1993).The presenceof nonproteinN and interference mentsfor maintenanceof body masswere calculated by secondarymetabolites are often ignored,as are for eachbird by regressingpercentage CP in the diet unexplainedN losses(Hegsted 1976, Young 1986, Iz- againstN intake; the point at which percentageCP haki and Safriel 1989,Mack 1990,Sedinger 1990, Iz- = N intake at N equilibrium provided estimated haki 1993).Unmeasured N losses,for examplefrom minimum protein requirement for maintenance sloughedskin and feathers(King and Murphy 1990) (Brice and Grau 1991, Murphy 1993, Robbins1993). or from drying fecal samplesin an oven (Manoukas All statisticalanalyses were conductedwith SPSS v.7.5 software(SPSS Inc., Chicago,Illinois), with al- pha set at 0.05.

Resultsand discussion.--Dry mass intake remained •08 constantamong birds (F = 3.20, df = 2 and 6, P = 0.11) and among diets (F = 1.77, df = 2 and 6, P = 0.25; Fig. 1). The birds did not compensatefor low dietary protein contentby increasingconsumption, as apparentlyoccurs in somefrugivorous birds and •) 04 (Thomas 1984, Izhaki and Safriel 1989). Body z massesremained constant throughout all feedingtri- 0.2 o." ß ß ß als (F = 0.49, df = 2 and 6, P = 0.64; Fig. 2), indi- ß ß ß ß ß cating no net catabolismor anabolism occurred. All ß o birds exhibitedsimilar N balance,as indicatedby 0.2 0.4 0.6 0_8 similar slopes(F = 0.10, df = 2 and 3, P = 0.91) and N Intake(gN kg 'ø75 day -1) y-intercepts(F = 0.87, df = 2 and 5, P = 0.47;Fig. 3). EndogenousN losseswere 0.05 gN kg 0.75day • and FIG. 3. Nitrogen balance among Pesquet'sPar- N equilibrium occurred at 0.32 gN kg 075day-L rots, representedby the solid line, where Y = 0.86X Basedon regressionanalysis and N equilibrium,a + 0.05 (R2 = 0.96; n = 9). Data for different birds are diet containing3.2% dm CP (usinga 4.05 nitrogen- indicated by different symbols. Values below the to-protein conversionfactor) would meet the mini- dashed line (Y = X) indicate net N anabolism, mal requirementsfor maintenancein Pesquet's whereas values above this line indicate net N Parrot. catabolism. 1084 Short Communications [Auk, Vol. 118 October2001] ShortCommunications 1085 et al. 1964, Dawson and Herd 1983), result in an un- Besidesmodifications of the digestive tract, some derestimate of minimum N requirements,because frugivores may obtain additional dietary protein calculatedN equilibrium would actually representN from insectsor seedsin fruits they ingest. Because deficit. Such errors may explain discrepanciesob- Pesquet'sParrots feed exclusivelyon figs, their pro- servedbetween the calculatedamount of dietary N tein intake might be supplementedby fig waspsand needed for N equilibrium and observed amount seeds.However, we doubt that fig waspscontribute neededfor long term maintenanceof body massand significantlyto dietary protein levels.Even if those positiveN balancein severalbird species(Hegsted birds completely digest fig wasps, amount of ad- 1976, Briceand Grau 1991, Murphy 1993). ditional protein contributed by wasps would be For example,Brice and Grau (1991) estimatedthat <3% of their total protein requirement (based on only 0.4% CP was necessaryfor positive N balance data from Herbst 1986). Obtaining protein from fig in Costa'sHummingbird, but observedthat 1.5%CP seeds is also unlikely because Pesquet'sParrot was necessaryto maintain body mass. Likewise, seemsincapable of digestingseeds, due to a poorly Murphy (1993) determined that White-crowned developed, weak, and narrow gizzard (Guntert Sparrowsrequired 8.7% CP for positiveN balance, 1981). When small seeds are offered in their diet, 5.3% CP for N equilibrium, and 7.3% CP for main- the seeds are avoided, discarded, or swallowed in- tenanceof body mass.Because of thoseinconsisten- tact (Homberger 1980, this study). During this cies, as well as various conversion factors used to cal- study, small grape seeds passed undamaged culate CP from measured N levels, it is more through those parrots' digestive tracts. If small fig meaningfulto compareendogenous N lossesand N seeds also pass intact, Pesquet'sParrots could be equilibriumamong species. seeddispersers of the figs on which they specialize. EndogenousN lossesand N equilibrium in Pes- Becauseseeds and insectslikely provide little pro- quet's Parrots are extremely low compared to gra- tein in the diet of this unusual parrot, low protein nivorous and omnivorous birds, but are similar to requirements (i.e. reduced N equilibrium and en- nectarivorousand other frugivorousbirds (Table3). dogenousN losses) appear to play an important Frugivorousand nectarivorousbirds (n = 5 spp. physiologicalrole in the ability of Pesquet'sParrot to subsist on a fruit diet. pooled) have lower endogenousN losses(t = 5.9, p Acknowledgments.--Thisstudy was funded by the = 0.0002) and lower N equilibrium (t = 3.8, p = Wildlife Conservation Society. Laboratory analyti- 0.005) than granivorousand omnivorousbirds (n = cal training was provided by M. Fitzpatrick. We 6 spp.pooled). In terms of endogenousN lossesand thank the staff at the Wildlife Conservation Socie- N equilibrium, Pesquet'sParrot is most similar to an- ty's Wildlife Survival Center on St. Catherines Is- other highly frugivorousbird, the Cedar Waxwing land for assistancein diet preparation, cage con- (Witmer 1998). struction, and handling of Pesquet'sParrots. This Becausegut volume is thought to limit rates of manuscriptwas improved by the valuable sugges- nutrient assimilation from bulky, nutritionally di- tions of L. Gannes and two anonymous reviewers. lute fruit (Worthington 1989, Levey and Grajal 1991, Levey and Duke 1992, Klasing 1998, but see LITERATURE CITED Witruer 1999), a larger gut volume would allow higher net rates of nutrient absorption in frugi- ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTS. vores. Indeed, in some highly specialized frugi- 1984. Official Methods of Analysis of the Asso- vores, intestines are so completely packed with ciation of Official Analytical Chemists.Associ- food that ingestion cannot occur until defecation ation of Official Analytical Chemists,Washing- makesmore spaceavailable (Levey and Duke 1992, ton, D.C. Klasing 1998). In frugivorous Cedar Waxwingsand BAIRLEIN,F. 1987.Nutritional requirementsfor main- Phainopeplas(Phainopepla nitens), a relatively wide tenanceof body weight and fat depositionin the intestinal diameter results in high feed intake, long-distancemigratory Garden Warbler, Sylvia which is associatedwith high rates of nutrient ab- borin(Boddaert). Comparative Biochemistry and sorption(Walsberg 1975, Witmer 1998,Witmer and PhysiologyA 86:337-347. Van Soest 1998). Pesquet'sParrots also have wide BECKERTON,P. R., AND A. L. A. MIDDLETON. 1983. Ef- intestines(Guntert 1981) and high feed intake (one fects of dietary protein levels on body weight, fourth of their total body massper day [wm]; this food consumption,and nitrogen balance in study). Furthermore, rapid nutrient absorption Ruffed Grouse. Condor 85:53-60. likely occursin thoseparrots becausetheir shortin- BERTHOLD,P. 1976. The control and significanceof testineshave extremely long microvilli throughout animal and vegetable nutrition in omnivorous the entire intestinal tract and cloaca (Guntert 1981). songbirds.Ardea 64:140-154. Those modificationsof the digestive tract are con- BLEM,C. 1968.Determination of caloricand nitrogen sistent with very low protein requirements in Pes- content of excretavoided by birds. Poultry Sci- quet's Parrots. ence 47:1205-1208. 1086 ShortCommunications [Auk, Vol. 118

BRICE,A. T., AND C. R. GRAU.1991. Protein require- quier, Ed.). InternationalCouncil for Bird Pres- ments of Costa'sHummingbirds Calyptecostae.. ervation TechnicalPaper no. 1. SmithsonianIn- PhysiologicalZoology 64:611-626. stitution Press,Washington, D.C. CIPOLLINI,M. L., AND D. J. LEVEY.1997. Secondary HOMBERGER,D. G. 1991.The evolutionaryhistory of metabolites of fleshy vertebrate-dispersed parrots and cockatoos:A model for evolution in fruits: Adaptive hypothesesand implicationsfor the Australian avifauna.Pages 398-403 in Acta . American Naturalist 150:346- XX CongressusInternationalis Ornithologici (B. 372. D. Bell, Ed.). Christchurch, New Zealand, 1990. CONKLIN-BRITTAIN, N. L., E. S. DIERENFELD, R. W. New Zealand Ornithological Trust Board, WRANGHAM, M. NORCONK, AND S.C. SILVER. Wellington. 1999. Chemicalprotein analysis:A comparison IZHAKI,I. 1993.Influence of nonproteinnitrogen on of Kjeldahl crude protein and total ninhydrin estimation of protein from total nitrogen in protein from wild, tropicalvegetation. Journal of fleshy fruits. Journalof Chemical Ecology19: ChemicalEcology 25:2601-2622. 2605-2615. COURTNEY,J. 1997.The juvenile food-beggingcalls IZHAKI,I., ANDU. N. SAFR1EL.1989. Why are there so and related behaviour in the Australian "Rose- few exclusivelyfrugivorous birds? Experiments tailed" Parrots Alisterus,Aprosmictus and Poly- on fruit digestibility.Oikos 54:23-32. telis;and a comparisonwith the EclectusParrot JANZEN,D. H. 1979. How to be a fig. Annual Review Eclectusroratus and Pesquet'sParrot Psittrichas of Ecologyand Systematics10:13-51. fulgidus.Australian Bird Watcher17:42-59. JORDANO,P. 1992. Fruits and frugivory. Pages 105- DAWSON,T. J., AND R. M. HERD. 1983. Digestion in the Emu:Low energyand nitrogenrequirements 156 in Seeds:The Ecologyof Regenerationin of this large ratite bird. ComparativeBiochem- Plant Communities (M. Fenner, Ed.). CAB Inter- istry and PhysiologyA 74:41-45. national,Wallingford, Connecticut. DE JAGER,S. F. 1976. Pesquet'sParrot Psittrichasful- KARASOV,W. H., ANDJ. M. DIAMOND.1983. Adaptive gidus:Some observations. Avicultural Magazine regulationof sugar and amino acidtransport by 82:160-163. vertebrateintestine. American Journalof Physi- DROBNEY,R. D. 1984. Effect of diet on visceral mor- ology 245:G443-G462. phologyof breedingWood Ducks.Auk 101:93- KARASOV,W. H., AND D. J. LEVEY.1990. Digestive 98. system trade-offs and adaptationsof frugivo- DYCK,J. 1976.Feather ultrastructure of Pesquet'sPar- rous passerinebirds. PhysiologicalZoology 63: rot Psittrichasfulgidus. Ibis 119:364-366. 1248-1270. FORSHAW,J. M., AND W. T. COOPER.1989. Parrots of KARASOV,W. H., D. H. SOLBERG,AND J. M. DIAMOND. the World, 3rd ed. Kevin Weldon and Associates, 1987. Dependenceof intestinal amino acid up- Willoughby,Australia. take on dietary protein or amino acid levels. GUNTERT,M. 1981.Morphologische Untersuchungen American Journal of Physiology 252:G614- zur adaprivenRadiation des Verdauungstraktes G625. bei Papageien(Psittaci). Zoologisches Jahrbuch KING, J. R., AND M. E. MURPHY. 1990. Estimates of der Anatomie 106:471-526. mass of structures other than plumage pro- HEGSTED,D. M. 1976. Balance studies. Journal of Nu- duced during molt by White-crowned Spar- trition 106:307-311. rows. Condor 92:839-843. HERBST,L. H. 1986. The role of nitrogen from fruit KLASING,K. C. 1998. Comparative Avian Nutrition. pulp in the nutrition of the frugivorousbat Car- CAB International,Wallingford, Connecticut. olliaperspicillata. Biotropica 18:39-44. LEVEY,D. J., AND G. E. DUKE. 1992. How do frugi- HERRERA,C. M. 1982. Seasonalvariation in the qual- voresprocess fruit? Gastrointestinaltransit and ity of fruits and diffuse coevolution between glucoseabsorption in Cedar Waxwings(Bomby- plants and avian dispersers.Ecology 63:773- 785. cilla cedrorum).Auk 109:722-730. HERRERA,C. M. 1984. to frugivory of LEVEY,D. J., AND A. GRAJAL.1991. Evolutionary im- Mediterranean avian seed dispersers.Ecology plicationsof fruit processingand intake limita- 65:609-617. tion in Cedar Waxwings. American Naturalist HOLTHUIJZEN, M. A., AND C. S. ADKISSON. 1984. Pas- 138:171-189. sagerate, energetics, and utilization efficiencyof LEVEY,D. J.,AND W. H. KARASOV.1989. Digestive re- the Cedar Waxwing. Wilson Bulletin 96:680-684. sponsesof temperatebirds switchedto fruit or HOMBERGER,D. G. 1980.Functional morphology and insect diets. Auk 106:657-686. evolutionof the feeding apparatusin parrots, LEVEY,D. J., AND W. H. KARASOV.1992. Digestive with special reference to the Pesquet'sParrot, modulation in a seasonalfrugivore, the Ameri- Psittrichasfulgidus (Lesson).Pages 471-485 in can Robin (Turdusmigratorius). American Jour- Conservation of New World Parrots (R. E Pes- nal of Physiology262:G711-G718. October2001] ShortCommunications 1087

LEVEY,D. J., AND W. H. KARASOV.1994. Gut passage tabolizability of fruits by passerinebirds? A of insectsby EuropeanStarlings and compari- comment on Izhaki and Safriel. Oikos 57:138- sonwith other species.Auk 111:478-481. 140. Low, R. 1990. Breeding Pesquet'sParrot Psittrichas SNOW,B. K. 1981. Tropical frugivorous birds and fulgidus at Loro Parque, Tenerife. International their food plants:A world survey.Biotropica 13: Zoo Yearbook 29:102-108. 1-14. Low, R. 1991.Hand-rearing Parrotsand Other Birds, SOKAL,R. R., ANDF. J. ROHLF. 1981. Biometry, 2nd ed. 2rid ed. Blandford, London. W. H. Freeman, New York. MACK,A. L. 1990.Is frugivory limited by secondary SORENSEN,A. E. 1984.Nutrition, energyand passage compoundsin fruits?Oikos 57:135-138. time: Experimentswith fruit preferencein Eu- MACK, A. L., AND D. D. WRIGHT. 1998. The Vulturine ropean Blackbirds (Turdusmerula). Journal of Parrot, ?sittrichasfulgidus, a threatened New Animal Ecology53:545-557. Guinea endemic:Notes on its biology and con- SWEENEY,R. 1999. Parent-reared Pesquet'sParrots. servation. Bird Conservation International 8: Bird Talk (May): 74-75. 185-194. THOMAS,D. W. 1984.Fruit intake and energybudgets MANOUKAS, A. G., N. E COLOVOS, AND H. A. DAVIS. of frugivorousbats. PhysiologicalZoology 57: 1964. Lossesof energy and nitrogen in drying 457-467. excretaof hens. Poultry Science43:547-549. THOMPSON,D. W. 1899. On characteristicpoints in MARTIN,E. W. 1968.The effectsof dietary protein on the cranialosteology of the parrots.Proceedings the energy and nitrogen balance of the Tree of the ZoologicalSociety of London 67:9-46. Sparrow (Spizellaarborea arborea). Physiological THURSLAND, D., AND L. PAUL. 1987. Parent-reared Zoology 41:313-331. Pesquet'sParrots Psittrichasfulgidus at the Los MARTfNEZ DEL RIO, C., W. H. KARASOV, AND D. J. Angeles Zoo. International Zoo Yearbook 26: LEVEY.1989. Physiologicalbasis and ecological 208-212. consequencesof sugar preferencesin Cedar VAN DONGEN, M. W. M., AND L. E. M. DE BOER. 1984. Waxwings.Auk 106:64-71. Chromosomestudies of eight speciesof parrots MATTSON,W. J. 1980. Herbivory in relation to nitro- of the families Cacatuidaeand Psittacidae(Aves: gen content.Annual Review of Ecologyand Sys- Psittaciformes). Genetica 65:109-117. tematics 11:119-161. WALSBERG,G. E. 1975. Digestive adaptations of MAYNARD, L. A., J. K. LOOSLI,H. E HINTZ, AND R. G. Phainopeplanitens associated with the of WARNER. 1979. Animal Nutrition, 7th ed. Mc- mistletoe . Condor 77:169-174. Graw-Hill, New York. WALSBERG, G. E., AND C. W. THOMPSON. 1990. An- MERRITT,J. J. 1986. The dietary requirement for me- nual changesin gizzard size and function in a thionine and its distribution as influenced by frugivorousbird. Condor 92:794-795. diet in the Dark-eyed Junco (Juncohyemalis). WATT, B. K., AND A. L. MERRILL. 1975. Handbook of Ph.D. dissertation,Bowling Green StateUniver- the Nutritional Contents of Foods. Dover, New sity, Bowling Green, Ohio. York. MORTON,E. S. 1973.On the evolutionaryadvantages WEGLARCZYK,G. 1981.Nitrogen balanceand energy and disadvantagesof fruit eating in tropical efficiency of protein deposition of the House birds. American Naturalist 107:8-22. Sparrow,Passer domesticus (L.). EkologiaPolska MURPHY,M. E. 1993. The protein requirement for 29:519-533. maintenance in the White-crowned Sparrow, WHITE, Z. C. R. 1974. The importanceof a relative Zonotrichialeucophrys gambelii. Canadian Journal shortageof food in animal ecology.Oecologia of Zoology 71:2111-2120. 33:71-86. NATIONAL RESEARCH COUNCIL. 1994. Nutrient Re- WITMER,M. C. 1998.Ecological and evolutionaryim- quirementsof Poultry, 9th ed. National Acade- plicationsof energyand protein requirementsof my Press,Washington, D.C. avian frugivoreseating sugary diets. Physiolog- PATON, D.C. 1982. The diet of the New Holland Hon- ical Zoology 71:599-610. eyeater, Phylidonyrisnovaehollandiae. Australian WITMER, M. C. 1999. Do avian frugivores absorb Journalof Ecology7:279-298. fruit sugarsinefficiently? How dietary nutrient PRYOR,G. S. 1999. Comparative protein require- concentrationcan affect coefficientsof diges- ments and digestive strategiesof three species tive efficiency.Journal of Avian Biology30:159- of parrots with distinct dietary specializations. 164. M.S. thesis, University of Florida, Gainesville. WITMER, M. C., AND P. J. VAN SOEST.1998. Contrast- ROBBINS,C. T. 1993. Wildlife Feedingand Nutrition, ing digestive strategies of fruit-eating birds. 2nd ed. Academic Press, New York. FunctionalEcology 12:728-741. SEDINGER,J. S. 1990. Are plant secondary com- WORTHINGTON,A. n. 1989. Adaptationsfor avian pounds responsiblefor negative apparent me- frugivory: Assimilationefficiency and gut tran- 1088 ShortCommunications [Auk, Vol. 118

sit time of Manacusvitellinus and Pipra mentalis. YOUNG, V. R. 1986. Nutritional balance studies: In- Oecologia80:381-389. dicatorsof human requirementsor of adaptive WRANGHAM, R. W., N. L. CONKLIN, G. ETOT, J. mechanisms? Journal of Nutrition 116:700-703. OBUA, K. D. HUNT, M.D. HAUSER, AND A. P. CLARK.1993. The value of figs to . International Journal of Primatology 14:243- Received29 December1999, accepted 30 April 2001. 256. AssociateEditor: C. Bosque

The Auk 118(4):1088-1095, 2001

Large-ScaleVariation in Growth of Black Brant Goslings Related to Food Availability

JAMESS. SEDINGER,L6 MARK P. HERZOG,1 BRIAN T. PERSON,1 MORGAN T. KIRK, TMTIM OBRITCHKEWITCH,1'5 PHILIP P. MARTIN, 2 AND ALICE A. STICKNEY3 •Instituteof ArcticBiology and Department of Biologyand Wildlife,University of Alaska Fairbanks, Fairbanks, Alaska 99775, USA; 2NorthernAlaska Ecological Services, U.S. Fish and WildlifeService, 101 12th Avenue,Fairbanks, Alaska 99701, USA; and 3ABR Inc., P.O. Box 80410, Fairbanks,Alaska 99709, LISA

ABSTRACT.--Weexamined variation in growth of ulation on the Yukon-Kuskokwim Delta than on the Black Brant (Branta bernicla nigricans) goslings Arctic coast. among two colonieson the Yukon-KuskokwimDelta in southwestern Alaska and the Colville River Delta The growth period of long-lived animals is a pe- on Alaska's Arctic coast. We simultaneouslymea- riod when selectionacts strongly (Rose 1991), likely sured abundanceand quality of a key food plant, because adults have evolved to maintain their sur- Carex subspathacea,and pressure on that vival in variable environments (Charlesworth 1994). plant at the three colonies.Our goal was to measure Furthermore,growing young require diets of higher variationin goslinggrowth in relationto variationin quality than those adequatefor adult maintenance, grazing pressure and food abundance because becausehigher dietary concentrationsof digestible growth of goslingsis directlylinked to first-yearsur- energy and protein are required for tissueproduc- vival, and consequentlyis the principal mechanism tion (O'Conner 1984, Sedinger 1992, 1997). Conse- for density-dependentpopulation regulation. Gos- quently,growth ratesvary considerablyin response lings grew substantiallyfaster on the arcticcoast and to environmental conditions (Cooch et al. 1991, Lars- were nearly 30% larger than those on the Yukon- son and Forslund1991, Sedingerand Flint 1991). Kuskokwim Delta at four to five weeks old. Faster Growing geeseappear to be especiallysusceptible growth on the arctic coast was associatedwith 2x to nutrient limitation during growth, probably be- greaterstanding crop of C. subspathaceaduring brood causethey are small bodied herbivoresand many rearing than on the Yukon-Kuskokwim Delta. Dis- plant foodscontain inadequate concentrations of nu- persalrates are high enough(Lindberg et al. 1998)to trients, especially protein, to support maximum rule out local adaptationand geneticvariation as ex- rates of growth (Sedinger 1992, 1997). Goslings, planationsfor observedvariation in growth. Our re- therefore,are highly selectiveforagers (Sedinger and sults are consistentwith lower survival of goslings Raveling 1984), and preferred foods that will sup- from the Yukon-KuskokwimDelta during their first port rapid growth frequentlymay be depleted(Car- fall migration and strongerdensity-dependent reg- gill and Jefferies1984, Sedinger and Raveling 1986, Person et al. 1998). As a result, several studies have reportedspatial (Aubin et al. 1993,Cooch et al. 1993, 4 Present address: 3291 East Acacia, Fresno, Cali- Leafloor et al. 1998) or temporal (Coochet al. 1991, fornia 93726, USA. Sedingerand Flint 1991, Sedingeret al. 1998)varia- 5 Presentaddress: Northern Alaska EcologicalSer- tion in growth of goslings. vices, U.S. Fish and Wildlife Service, 101 12th Ave- Growth is especiallyimportant in geesebecause nue, Fairbanks, Alaska 99701, USA. size of goslingsat the end of their first summer 6E-mail: [email protected] strongly influences their probability of surviving