The Auk A QuarterlyJournal of Ornithology Vol. 113 No. 4 October 1996

The Auk 113(4):735-743 + frontispiece, 1996

CONSEQUENCES OF AN ALIEN ON THE PLUMAGE COLORATION AND ECOLOGY OF CEDAR

MARK C. WITMER 1 Sectionof Ecologyand Systematics,Corson Hall, CornellUniversity, Ithaca, New York 14853, USA

AI•STRACT.--CedarWaxwings (Bombycillacedrorum) with orange (instead of the normal yellow) tail bandshave appeared in easternNorth Americain the last35 years.Biochemical studieshave implicateda dietary cause(Hudon and Brush 1989),specifically the of Loniceramorrowii (Brush 1990), for this novel color variant. I show that rectricesreplaced while CedarWaxwings are feeding on L. morrowiifruits develop orange tips. Rectrices replaced subsequentto switchingthe diet of molting waxwingsfrom L. morrowiifruits to dog chow wereyellow, showing close temporal correspondence between dietary input of rhodoxanthin and the colorationof growing feathers.In the Ithacavicinity, fruits of L. morrowiiare eaten by wild CedarWaxwings from Juneuntil mid-October.The extendedpattern of availability and consumptionof Lonicerain this regionappears to explainmy uniqueobservations of adult CedarWaxwings growing orange tails during the fall months.Cedar Waxwings main- tained body conditionand moltedwhile on an extendeddiet of L. morrowiifruits (36 days for two and 64 days for two others).Three birds initiated tail molt while on this diet, includingone that moltedall of its flight feathers.These results emphasize the nutritional specializationof CedarWaxwings to a diet of sugary,low-protein fruits, and showthat molt occursin an apparentlynormal manner when birdsare eating a low-proteinfruit diet. Received 30 September1994, accepted 15 April 1995.

CEDARWAXWINGS (Bombycilla cedrorum) nor- Canada (Yunick 1970, Hudon and Brush 1989, mally have a yellow terminal band on their Pittaway 1991, Mulvihill et al. 1992). Carot- tails. Within the past35 years,Cedar Waxwings enoid pigments (i.e. xanthophylls) cause the with orange tail bands have appearedin the yellow tail bands of Cedar Waxwings (Hudon northeastern United States and southeastern and Brush 1989),as well as the red tips of their secondaries (Brush and Allen 1963). The col- •Present address:Department of Zoology and oration of the novel orange-tippedrectrices of Physiology,University of Wyoming, Laramie,Wyo- Cedar Waxwings is causedby the inclusion of ming 82071,USA. E-mail: @uwyo.edu a red carotenoidpigment (rhodoxanthin)in the

FRONTISPIECE.Tail colorsof CedarWaxwings. in upperleft (Bird1) wasfed only Lonicera fruits during tail molt. Bird in upperright (Bird2) wasswitched from Lonicerafruits to chowdiet midwaythrough tail molt. Bird in lower left is wild bird with orangetail band (CornellUniversity Vertebrate Collection [CVC] no. 30194;juvenile male, 9 November1961, Chemung Co., New York). Bird in lower right is wild bird with normal yellow tail band (CVC no. 14422,adult male, I June 1942,Tompkins Co., New York). 735

736 MmucC. WITMER [Auk,Vol. 113 tail bands (Hudon and Brush 1989). Carotenoid eastern United States (Barnes 1972). These are pigments in feathers appear to be derived ex- now commonin the Ithacavicinity (e.g. Stover [1994] clusively from dietary sources,either directly recordedalien honeysuckleshrubs at 7 of 12 pasture or with modification (Goodwin 1984, Hudon sites). Muenscher (1950) reported three exotic hon- and Brush1989). Dietary rhodoxanthinhas been eysucklesin the Ithaca area (native rangesfrom Reh- der 1903): L. morrowii(Japan), L. xylosteum(Europe, reported to be deposited unaltered in the ca- Asia Minor, and western Siberia), and L. tatatica(cen- rotenoid-containing feathers of several birds tral Asia to southern Russia).These speciesare mor- (Vi51ker1955, 1957,1958). Apparently, this pig- phologically similar and are consideredto be closely ment is not distinguishedbiochemically from related (Rehder 1903). Although hybrids are rare the yellow xanthophylls that normally color amongthe speciesof this genusin natural situations these feathers.These findings suggestthat the (native rangesand habitats),L. morrowiiand L. tatatica recent color variant of the is a readily hybridize where they occurtogether as aliens result of a dietary shift to a rhodoxanthin-rich (Rehder1903). I identified localhoneysuckles by food sourceduring the period of tail molt (Hu- pubescence,pedicel length, bractlet size, color, don and Brush1989). Of the sevenrecently in- and filament pubescence(Fernaid 1950, Muenscher 1950). shrubs were surveyedon 24 May troduced in the northeastern United 1993during floweringat sixlocal sites (three in Ithaca Statesanalyzed by Brush (1990), rhodoxanthin and three in rural areas). and L. ta- occurredonly in the fruits of Morrow's honey- tatica can be readily distinguishedat this seasonby suckle (Loniceramorrowii). flower color (white, turning yellow and pink, re- In western Pennsylvania,virtually all Cedar spectively;Fernaid 1950). I did not find L. xylosteum Waxwingswith orangetail bandsare birds with among the shrubsI examined.Lonicera morrowii was juvenal rectrices (Mulvihill et al. 1992). The much more common than L. tatarica.Among three availability of honeysucklefruit (L. morrowiiand transectsin Ithaca, 80.5%(n = 354 shrubs,range 71.6- L. tatarica) coincides with the period during 85.1%, 61-201 shrubs per transect)of honeysuckle which nestlingsare growingtheir tails(late June shrubswere L. morrowii,whereas among three rural transects(two streamside sites and one roadside site), through July) but not with the period during virtually all shrubswere L. morrowii(n = 215 shrubs, which adults replace their rectrices (Dwight range 98.4-100.0%, 37-117 shrubs per transect). Spe- 1900). Mulvihill et al. (1992) suggestedthat this ciesidentity wasbased on morphologicalcriteria, but explainsthe occurrenceof orange-bandedtails in light of the easeof hybridizationamong this group only among young Cedar Waxwings(plumages of shrubs(Rehder 1903, Barnes 1972), the geneticpu- before first completemolt, which occursin fall rity of these plants is uncertain. Rhodoxanthinhas monthsof secondyear). Birds molting from one been reported from fruits of L. morrowii(Brush 1990), color form to the other also have been noted as well as fruits of two other speciesof Lonicera(L. (Hudon and Brush 1989, Mulvihill et al. 1992), webbianaand L. ruprechtiana;Rahman and Egger1973), suggestinga dietary (versusa genetic)basis for suggestingthe widespreadoccurrence of rhodoxan- thin in this genus.I usedfruits from shrubsidentified the phenomenon. asL. morrowii(hereafter, Lonicera) in this study.Voucher In aviary feeding trials, I testedthe influence specimenshave been depositedat the Bailey Horto- of honeysucklefruit consumptionon plumage rium, Cornell University. coloration of molting Cedar Waxwings. Based Housingand foods.--I maintainedCedar Waxwings on work conducted in the vicinity of Ithaca, in unheated aviaries (4.00 x 2.15 m) with exposure New York, I report information on the histor- to natural conditions on the southern side (2.15 m). ical incidence of orange-tailed Cedar Wax- An opaquefiberglass ceiling slanted from a heightof wings, the seasonalphenology of honeysuckle 2.84 m on the southern end to 3.38 m on the northern availability, and Cedar Waxwing con- end. One ceiling panel (0.97 x 2.29 m) was translu- sumptionof this fruit. I alsodescribe body-mass cent. The mesh of the screenedside of the aviary was wide enoughto allow entry of flying ,but in- changesand molt progressionof captive Cedar sect consumption was assumedto be extremely low Waxwings during periods in which they were because insects were uncommon within the cham- fed a diet consistingentirely of honeysuckle bers.Birds were given fresh water and food daily. fruits. The foodsoffered to Cedar Waxwingsin this study were Lonicerafruits and moistened dog chow (Iams METHODS Company,Eukanuba Brand Small BitesPuppy Chow; hereafter referred to as "chow"). I analyzed these Naturalizedhoneysuckles. -- Eurasian are foodsfor hexosesugars (anthrone procedure; Yemm widely establishedoutside of cultivationin thenorth- and Willis 1954),lipids (ethyl ether extraction),and October1996] FruitsAlter Color of WaxwingFeathers 737 nitrogen (Kjeldahl method) as an estimateof protein. tions (CVC). I did not use older specimensbecause Resultsare reported relative to dry matter (dried at of potentialfading. Tail colorsof experimentalbirds 100øCto constantmass) of fruit pulp and skin. Sam- and museumspecimens were matchedwith colorsin ples for sugaranalysis were extractedwith 80%eth- Smithe (1975). Museum specimensin the CVC were anol to excludepolysaccharides. Lonicera fruits were examined to evaluate the historical occurrence of Ce- high in sugar(73.8 + SE of 0.7%,n = 13 shrubs)and dar Waxwingswith orange-tippedrectrices in central low in lipids (<2%, n = 2) and nitrogen (0.53 + 0.01%, New York. Specimensacquired since 1986 were sal- n = 2), whereaschow was low in sugars(1.3%) and vaged birds, representinga haphazardsample. high in lipids (21.7%)and nitrogen(5.78%). Fruits of Dietof wild Cedar Waxwings.--Monthly values of the L. morrowii contain rhodoxanthin (Brush 1990) and proportionof fruit in CedarWaxwing diets were based other carotenoidpigments (Goodwin and Goad1970). on analysisof gut contentrecords from the U.S. Bi- Rhodoxanthinwas presumedto be absentfrom the ologicalSurvey (Witmer 1996).I examinedthese data chowdiet becauseof the lackof ingredientsreported (1885-1950) for records of the fruits of exotic hon- to contain this pigment. The chow diet contained eysucklesin the stomachsof Cedar Waxwings.Con- groundcorn, chicken fat, andwhole eggs, which may temporaryuse of thesefruits by CedarWaxwings in have contributedother C•oxanthophyll carotenoids, the Ithacavicinity was evaluatedby feeding records suchas zeaxanthinand cryptoxanthin(Belyavin and made during daily roadsidesurveys (ca. 4 km) from Marangos 1989). 1988 through 1993. I treated each encounteras a sin- Diet treatments.--SevenCedar Waxwings were used gle sampleof waxwingfeeding, not weightedby flock in the tail-color experiment. Three birds molted all size. I used this approachbecause individuals within rectrices while on a diet of Lonicerafruits, either with a flock are not independent choice measures (Mc- or without supplemental chow. Four others were Pherson 1987). This approachalso reduced bias cre- switched to a chow diet after they initiated rectrix ated by the greaterapparency of larger flocks. molt on a diet that included Lonicera fruits. Bilateral pairs of rectricesare molted from the center outward RESULTS at intervals of about three to four days (Witmer un- publ. data), so the progressionof rectrix molt was Experimentaleffects of diet on plumagecolora- easy to monitor. All birds had been maintained in tion.--Consumption of Lonicerafruits by Cedar captivityfor at leastone year, primarily on a diet of Waxwingsduring tail molt resultedin orange- wild fruits and chow.The diet manipulationsare de- scribed below. tipped rectrices(Frontispiece, Table 1). All four birds that were switched to the chow diet sub- Four adult Cedar Waxwingswere maintained ex- clusivelyon a diet of Lonicerafruits from 30 Julyuntil sequentlygrew yellow-tipped rectrices,where- as each of the three birds not switched contin- 4 September 1992. On 4 September three of these birdswere midway through rectrix molt. Two of these ued growing orange-tipped rectrices(Fisher's three birds were switchedto chow (three-daytran- exact test, P = 0.03, df = 1, n = 7). Two birds sition with both Lonicerafruits and chow offered). The on the diet of only Lonicerafruits also molted other bird undergoingtail molt and the fourth bird flank feathers tinged with orange, instead of that had not begun tail molt remainedon the exclu- the normal yellow flank feathers(Frontispiece). sive fruit diet until 2 October 1992. This fourth wax- Three Cedar Waxwings from this experiment wing did not replaceany rectrices while eatinga fruit- are depositedin the CVC (catalognos. 39056 only diet but molted one rectrix between 3 and 13 October when it was fed Lonicera fruits and chow. [Bird 1], 37981 [Bird 2], and 37554 [Bird 6]). Threeother Cedar Waxwings molted rectrices while Tail bandsof waxwingsfed only Lonicerafruits eating a diet of Lonicerafruits and chow offered si- showedmore red pigmentation(Flame Scarlet multaneouslyin unlimited amounts.These birds se- to ChromeOrange) than did orange-tailedmu- lecteda diet that was about 90% fruit (dry matter). seum specimens(Spectrum Orange in eight Two adults (second-yearbirds) were maintained on birds and Chrome Orange in one). Tail-band this diet from 30 July until 17 September1992. On coloration of birds fed Lonicera fruits and chow 17September one of thesebirds was midway through was similar to that of wild waxwings, but still rectrix molt and was switched to chow. The other showedslightly more red pigmentation(Table bird was alreadygrowing a completeset of new rec- 1). trices.The third waxwing, an adult female,was pro- Most rectricesmolted subsequentto the diet vided the fruit and chowdiet from 30 July through 10 October 1992,during which time she molted all switchfrom Lonicerafruits to chowwere yellow. of her rectrices. Only one rectrix that erupted immediately after I comparedtail colorationof the experimentalbirds the three-day transition from fruit to chow with recent (since 1986) specimensof Cedar Wax- showeda tinge of orangeon the edge of the wings in the Cornell University VertebrateCollec- feather (Frontispiece,Table 1). Thus, the lossof 738 MARKC. WrrME• [Auk,Vol. 113

TABLE1. Colors(in parentheses;after Smithe 1975) of rectrixtips of CedarWaxwings maintained on diets includingLonicera fruits or switchedfrom fruit to dog chowmidway through rectrix molt. "Transition"is a three-dayperiod between diet switch.Rectrices usually were moltedsymmetrically from centeroutward. Unlessnoted otherwise, rectrix numbers refer to bilateralpairs of feathers.Orange colors (in decreasing amountof red):(15) Flame Scarlet; (16) Chrome Orange; (17) Spectrum Orange; (18) Orange Yellow. Yellow color: (56) Straw Yellow.

Rectriceserupted Bird Sex Diet On initial diet During transition After diet switch 1 M Fruit' 1-6 (15-16) 2 M Fruit/chow a Left: 1-2 (16) 3 (16-17) 4-6 (56; orangeedge on 4) Right: 1-2 (16) 3 (16-17) 4-6 (56) 3 F Fruit/chow' 1-4 (16) 5 (18) 6 (56) 4 M Fruit/chowa Right: 6 (16) All others (56) 5 F Fruit 1-6 (17) 6 F Fruit 1-6 (16) 7 F Fruit/chow Left: 1-4 (16) 5-6 (56) Right: 1-3 (16) 4-6 (56) ßFed only Lonicerafruits for extendedperiod (see text). Bird no. 4 moltedno rectriceson the fruit-onlydiet but moltedone rectrix on the fruit/ chow diet between 3 and 13 October.

rhodoxanthinpigmentation from the plumage tentsof CedarWaxwings collected in the north- correspondedvery closelywith the timing of eastern United States from 1885 to 1950 (n = the diet switch. The yellow rectricesof exper- 212; Witmer 1996). Many of these birds (142) imental birds were duller (Straw Yellow; Fron- were taken from Junethrough October,the pe- tispiece, Table 1) than those of wild birds (14 riod during which Lonicerafruits are available specimenswith SpectrumYellow tails). All ex- in central New York. Fruits of a native hon- perimental birds had very little yellow pig- eysuckle,L. caerulea,occurred in 20 of 30 wax- mentation in their belly feathers. wings collectedin Maine in July 1949and 1950. Molt ona fruit-only diet.--Cedar Waxwings that Fruits of L. caeruleaare bluish-black (Muenscher were fed only Lonicerafruits maintained good 1950)and probablywere not confusedwith the body condition (Fig. 1) and molted varying red-fruited Eurasianhoneysuckles. In contrast, amountsof plumage while on this diet. Two fruits of alien honeysucklesare eaten by wax- birdsthat were fed this diet for 36 daysinitiated wings from mid-Juneuntil mid-Octoberin the prebasicmolt and showed a slight (Bird 2) or Ithaca vicinity (57% of fruit diet, 46% of whole moderate(Bird 3) lossof bodymass (Fig. 1, Table diet; Fig. 2). 1). Two other waxwingsfed only Lonicerafruits Adult waxwingsmolting orangetails.--I ob- for 64 days showed much different molting served flocksof waxwings feeding heavily on schedules from each other, but exhibited sim- Lonicerafruits from 23 Septemberuntil 8 Oc- ilar patternsof body-masschange (Fig. 1). One tober 1993on sevendays. I judgedbirds as adults of these(Bird 1) molted all of its flight feathers by the presenceof molting rectrices(an un- during this period (Table 1). This bird molted ambiguousindicator of adult status)or by adult at a faster rate than two other waxwings that body plumage with distinct red waxy tips on were at a similar stageof molt on 4 September, the secondariesand a wide tail band (Pyle et and were switched from the fruit-only diet to al. 1987). Among adult birds, 79% (n = 53) had the chow diet on this date (Bird 1 replaced 23 someor all of their rectricestipped with orange. flight feathersduring this period,whereas Birds All orange-tailed adults were undergoing tail 2 and 3 replaced 18 and 10 flight feathers,re- molt, whereas most yellow-tailed adults were spectively).The other waxwing fed only Lonic- not. Among juvenile waxwings, 39% (n = 97) erafruits for 64 days(Bird 4) molted fewer flight had orange-tippedrectrices. These observations feathers than the other three fruit-only birds corroborateprevious field observations(1989- by 4 September, and during the subsequent 1991) of orange-tailedadults in fall flocksthat month molted only one primary per wing. were feedingon Lonicerafruits (12 of 18 orange- Historicaldietary changes.--Fruitsof intro- tailed birds were adults). duced honeysucklesdid not occur in gut con- Historical occurrenceof orange-tailedwax- October1996] FruitsAlter Color of WaxwingFeathers 739

45' 100 4 I 1714 7 / • Bird4 ß Lonicera fruits • ...... _._._._....-e ß Bird23

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Jan Feb Ma' Apr May Jun Jul Aug Sep Oct Nov Dec

25 egg dates 11 Aug 4 Sept 2 Oct molt period FIG. 1. Body masschanges of birds fed only Lo- FIG. 2. Frequencyof occurrenceof Lonicerafruits nicerafruits for extended periods (solid lines); diet in diet of wild Cedar Waxwingsfrom recent roadside initiated on 30 July. On 4 September, all birds were surveysnear Ithaca,New York. Monthly estimatesof molting; they were midway through wing molt and proportion of fruit in diet are from analysisof records three had begun tail molt (see Table 1). At this time of stomach contents; fruit in diet is represented by two birds were switched to chow diet for remainder bars (Witmet 1996). Egg datesfrom Bull (1974); molt of molt period (dashed lines). period from Dwight (1900) and Pyle et al. (1987). wings.--All Cedar Waxwings in the CVC from sistent with the immediate absence of rhodox- 1878 to 1950 (n = 47 birds) and from 1951 to anthin in growing feathersupon the removal 1960 (n = 17 birds) had yellow tail bands. A of Lonicera fruits from the diet, the reddish col- Cedar Waxwing collectedin 1961 was the first oration of the tail bands of the experimental record of the orange-tailed variant (see Fron- waxwings comparedwith wild birds suggests tispiece);seven other waxwings from this de- a positive relationshipbetween dietary intake cade had yellow tails. This phenomenon ap- of rhodoxanthin-lacedfood and deposition of pears to have arisen in other areasof the north- this pigment in growing feathers. east at about this time; Mulvihill et al. (1992) The capacityof Cedar Waxwingsto storeca- first noted orange-tailed Cedar Waxwings in rotenoidsis unknown, but the skin on the legs, western Pennsylvaniain 1964. The incidence and the subcutaneousfat, of two experimental of orange-tailedCedar Waxwingssubsequently birds were reddish (Birds 1 and 2). Chickens are has increased(2 of 16 specimensfrom 1986 to known to deposit carotenoidsin subcutaneous 1990,and 7 of 13 specimensfrom 1991to 1993). fat and egg yolks (Goodwin 1984). Cedar Wax- Mulvihill et al. (1992) also reported an increas- wings showedno evidencethat they mobilized ing incidenceof orange-tailedCedar Waxwings storedrhodoxanthin for feather pigmentation. from the early 1960sto 1985. Of recent speci- Hill (1992) found no visible effect of stored mens (1986 to present) that had tails grown as carotenoids on plumage coloration in male adults,12 waxwings salvaged during the breed- House Finches(Carpodacus mexicanus) that were ing season(May to September)had yellow rec- fed a carotenoid-deficient diet just prior (-<1 trices,and one waxwing salvagedin November month) to the initiation of prebasic molt. In had some orange rectrices. contrast,Kritzler (1943) induced molt of display feathersin three speciesof weaver finchesafter DISCUSSION maintaining them on a carotenoid-freediet for about three months; these birds grew feathers Experimentaleffects of diet on plumagecolora- with normal amountsof yellow pigments but tion.--Pigment deposition in the tail bands of with much diluted amounts of red pigments. Cedar Waxwings was strongly influenced by Test (1969) maintained Northern Flickers (Co- dietary inputs of rhodoxanthin at the time of laptesauratus) on a carotenoid-deficientdiet and feathergrowth. Wild waxwingsprobably never observeda steadydecline in the amount of yel- consumeLonicera fruits to the extent that any low pigmentation in remigesmolted over a 2.5- of the experimentalbirds did. Birdsin the wild month period; red pigments were lost imme- eat someanimal prey during the prebasicmolt diately, however. Test also observedan imme- period (Septemberto November; Witmer 1996) diate (within hours) effect of the addition of and would likely eat a mixture of fruits. Con- dietary carotenoidson feather color.Similarly, 740 MARIeC. WITMI•R [Auk, Vol. 113

Kritzler (1943) induced orange feathersin nor- ers, and protracted molt; Murphy and King mally yellow-featheredfinches (Euplectes spp.) 1991).This resultwith captiveCedar Waxwings by feeding them paprika, which containscap- is consistentwith the predominantlyfruit diet santhin,a pigment foreign to their normal diet. of wild waxwings during their prebasicmolt V/51ker(1955, 1957) demonstrated strong effects (see Fig. 2). of dietary rhodoxanthinon feather coloration Granivorous American Tree Sparrows (Spi- in Common Canaries (Serinuscanaria) and Red zella arborea)require a dietary protein level Crossbills (Loxiacurvirostra). higher than 4% for maintenance(Martin 1968). The experiments noted above indicate that The ability of Cedar Waxwings to thrive on dietary inputs of carotenoidsoften appear im- sugary fruit diets is paralleled by the perfor- mediately in molting carotenoid-containing mance of hummingbirds eating sugary, low- feathers,but the effectsof dietary deprivation proteindiets (1.5% protein; Brice and Grau 1991). of carotenoidsvary amongspecies in their rates Murphy and King (1984,1991) found that molt of disappearance.There appearsto be variation in White-crowned Sparrows (Zonotrichialeuco- in the responseof plumage pigmentation to di- phrys)occurs normally at low dietary protein etary inputs due to the amount and/or type of and sulfur amino acid levels. carotenoid involved, both in the food and in Ecologyof an introducedshrub and nativefrugi- the plumage.Carotenoid deposition in chicken vore.--Fruits of L. morrowii have increased dra- egg yolks also is strongly affected by dietary maticallyin the diet of CedarWaxwings within carotenoid content (Goodwin 1984). Quantita- the last 40 years,at least in somelocalities. In tive depositionof dietary carotenoidsin feath- centralNew York, this fruit is locally abundant ers as a function of their availability in the en- and persistsuntil October,well into the period vironment affectsplumage color variation in during which adult Cedar Waxwings replace Great Tits (Parusmajor; Slagsvoid and Lifjeld their rectrices(Sherburne 1972, Witmer unpubl. 1985,Partali et al. 1987)and appearsresponsible data). Captive Cedar Waxwings perform well for habitat-associatedcolor morphs of Tristan on a diet of Lonicerafruits, and wild waxwings Buntings (Nesospizaacunhae; Ryan et al. 1994). in Ithaca include much of this fruit in their diet If the size and coloration of the tail are im- from July to mid-October.As a consequenceof portantin mateselection (see Burley et al. 1982, thesedietary patterns,adult and juvenile Cedar Hill 1990), then orange tail colorationmay be Waxwings produce orange-tipped tails in the affecting the attractiveness of waxwings as Ithaca area. Hudon and Brush (1989) and Mul- mates. Mountjoy and Robertson (1988) found vihill et al. (1992) reportedseveral adult Cedar that Cedar Waxwing matestend to associateby Waxwing specimenswith some orange rectri- the number of secondarieswith red waxy tips. ces. The demonstration that adult waxwings, Molt on an exclusivefruit diet.--The perfor- both captive and wild, develop orangetails un- manceof molting Cedar Waxwingseating a diet der the influence of diet eliminates hypotheses of only Lonicerafruits (ca. 2.33%protein based that suggest that nestling waxwings are more on a nitrogen-to-protein conversion factor of susceptibleto this effectbecause of the idiosyn- 4.4; Milton and Dintzis 1981) underscores the craciesof nestling nutrition and growth (Hu- nutritional specializationof waxwingsto a diet don and Brush 1989). The apparent rarity of of sugary, low-protein fruits (Witmer 1994, adult Cedar Waxwingswith orange tail bands 1996).Captive Cedar Waxwingsfed an array of in other areas of the northeastern United States fruits maintained stable body massover a 27- (Mulvihill et al. 1992) suggeststhat the phe- day period (Holthuijzen and Adkisson 1984). nomenon in central New York is local. The con- Similarly, Berthold(1976) found that Bohemian tinued predominanceof breeding adults with Waxwings (B. garrulus)maintained body mass yellow tail bands in the Ithaca area (Witmer when fed fruit diets over periods of 10 to 18 unpubl. data) may reflect a dilution effectdue days.The adequacyof this diet for moltingwax- to the lack of philopatry in Cedar Waxwings wings is remarkablebecause of the protein and (Bruggeret al. 1994). sulfur amino-acid costsof molt (Robbins 1993). Populationsof honeysuckleshrubs (Lonicera Lonicera fruits are low in sulfur amino acids spp.) most likely spread in the northeastern (Witruerunpubl. data), but Cedar Waxwings did United States during the middle part of this not showsigns of proteinor sulfuramino-acid centurybecause of increasesin availablehabitat deficiency(e.g. loss of bodymass, shorter feath- coupled with aggressiveplanting programs. October1996] FruitsAlter Color of WaxwingFeathers 741

Eurasian honeysuckleswere introduced into Reservewither by mid-August(Mulvihill et al. North Americalong ago (L. morrowiiin 1875,L. 1992, R. Mulvihill pers. comm.). Barnes(1972) tataricain 1752;Wyman 1949).By the early 1900s, reported a similar phenology of fruit persis- morrowiiand tataricahad escapedcultivation and tence in Wisconsin. The contrast between cen- were widely naturalizedin New England(Reh- tral New York and westernPennsylvania shows der 1903).The abandonmentof agriculturalland that the ecologicalinteractions between in the 1920s and 1930s, however, appears to dispersersand fruiting plants can vary over rel- have createdlarge areasof suitablehabitat for atively short distances,contingent upon local theseshrubs (Hauser 1966). Honeysuckle shrubs fruiting phenology and frugivore abundance. thrive in disturbed sites, such as roadsides, old The ecological interactions between Cedar fields,and streambanks(Barnes 1972). Dispersal Waxwingsand alien honeysuckles,along with of Eurasian honeysuckles throughout the the ramifications that this new food has had on northeastern and midwestern United States was the plumage coloration of waxwings, under- facilitated by governmentagencies that prop- scorethe unanticipated consequencesthat ex- agatedand dispensedthese shrubs because they oticscan have on native organisms.The extent were deemed to be beneficial to wildlife (Cook to which introduced honeysucklesmay influ- and Edminster 1944, Edminster 1950, Edminster ence the ecology and behavior of Cedar Wax- and May 1951,Smith 1964,Mulvihill et al. 1992). wings remains to be determined. Loniceramorrowii and L. tataricaappeared in the naturalized Illinois flora between 1922 and 1955 ACK•OWLEDGMI•ITS (Henry and Scott 1981). These shrubswere nat- Cedar Waxwings were held under U.S. Fish and uralized in Michigan by the late 1940s,with Wildlife Service Permit PRT-721267 and New York their hybrid, L. x bella,establishing by 1957 StateDepartment of EnvironmentalConservation Fish (Hauser 1966). Mulvihill et al. (1992) reported and Wildlife LicenseLCP92-054. I thank Ann Herzig that L. morrowiiand L. tataricawere planted at for feeding the birds during a critical week of the their studysite in westernPennsylvania in 1960. experiment. Kevin McGowan provided accessto Ce- Thus, Eurasianhoneysuckles have expanded dar Waxwing specimensin the Cornell University over large areas of North America within the VertebrateCollections. Bob Dirig and Ed Cope of the last 50 years. The first appearanceof orange- BaileyHorrorlure provided access to specimens tailed Cedar Waxwingsin the early 1960s,and and usefulliterature. Ray Davis,Mike Matthews,and the increasingoccurrence of this plumage vari- JohnSolan of the New York Departmentof Environ- mental Conservationoffered helpful informationon ant since then, suggeststhat heavy consump- shrub-plantingprograms by New York State. Peter tion of honeysucklefruits by waxwingshas fol- Van Soestgenerously provided facilities and supplies lowed the plant'swidespread establishment by for chemicalanalysis of foods.Cedar Waxwing spec- human influences (Mulvihill et al. 1992). The imenswere photographedby SRSUnlimited Photog- cultivation and spread of alien honeysuckle raphy. I thank Peter Marks, DeedraMcClearn, Kevin shrubs in North America have resulted in an McGowan, Peter Van Soest, David Winklet, and abundanceof the fruits of these shrubs,an ap- LaReesaWoolfenbarger for providing helpful sug- parent characteristicof many of the foodseaten gestionson drafts of this paper. I also thank John by Cedar Waxwings (McPherson 1987, Witruer Reissfor translating the German literature. Jocelyn 1996). Although consumptionof honeysuckle Hudon, JamesMountjoy, and Robert Mulvihill of- fered helpful commentson this paper. fruits by Cedar Waxwingsand other fruit-eat- ing birds is importantin the dispersalof these LITERATURE CITED plants,frugivorous birds do not appearto have beenprimarily responsiblefor the rapid spread BARNES,W. J. 1972. The autecologyof the Lonicera of Eurasian shrub honeysuckles in North x bellacomplex. Ph.D. dissertation,University of America. Wisconsin, Madison. BœLYAVIN,C. G., ANr• A. G. MARANC.OS. 1989. Natural The large differencein the fruiting phenol- productsfor egg yolk pigmentation.Pages 239- ogy of honeysuckleshrubs between western 260 in Recentdevelopments in poultry nutrition Pennsylvania and central New York is inter- (D. J. A. Cole and W. Haresign, Eds.). Butter- esting, considering that these two locales are worths, London. relatively closegeographically and share sim- BœRTHOLr•,P. 1976. The control and significanceof ilar climate,soil, and vegetation(Vankat 1979). animal and vegetable nutrition in omnivorous Honeysuckle fruits at the Powdermill Nature songbirds.Ardea 64:140-154. 742 MmucC. WITMER [Auk,Vol. 113

BPaCE,A. T., ANDC. R. GRAU. 1991. Protein require- basisof a color variant of the Cedar Waxwing. mentsof Costa'sHummingbirds Calypte costae. Journal of Field Ornithology 60:361-368. PhysiologicalZoology 64:611-626. KRrrZLER,H. 1943. Carotenoids in the display and BRUGGER,K. E., L. N. ARraN, AND J. M. GRmaMCH. eclipseplumages of bishop birds. Physiological 1994. Migration patternsof CedarWaxwings in Zoology 16:241-255. the eastern United States. Journal of Field Or- MARTIN,E. W. 1968. The effectsof dietary protein nithology 65:381-387. on the energy and nitrogen balanceof the Tree BRUSH,A. H. 1990. A possible source for the rho- Sparrow (Spizellaarborea arborea). Physiological doxanthinin someCedar Waxwing tails. Journal Zoology41:313-331. of Field Ornithology 61:355. McPHImSON,J.M. 1987. A field study of winter fruit BRUSH, A. H., AND K. ALLEN. 1963. Astaxanthin in preferencesof CedarWaxwings. Condor 89:293- the Cedar Waxwing. Science142:47-48. 306. BtmLEY, N., G. KPOA•rrzBERG,AND P. PADMAN. 1982. MILTON,K., AND F. R. DntrzIs. 1981. Nitrogen-to- Influence of colour-bandingon the conspecific protein conversionfactors for tropical plant sam- preferencesof Zebra Finches. Animal Behaviour pies. Biotropica13:177-181. 30:444-455. MOUNTIOY,J., AND R. J. ROBERTSON.1988. Why are BULL, J. 1974. Birds of New York state. Cornell Uni- waxwings"waxy"? Delayed plumage maturation versity Press,Ithaca, New York. in the Cedar Waxwing. Auk 105:61-69. COOK D. B., AND F. C. EDMINSTER. 1944. Survival and MUENSCHER,W.C. 1950. Keysto woody plants.Cor- growth of shrubs planted for wildlife in New nell University Press,Ithaca, New York. York.Journal of Wildlife Management8:185-191. MULVII-IILL, R. S., K. C. PARKES,R. C. LL•BERMAN,AND DWIGHT,J., JR.1900. The sequenceof plumagesand D. S. WOOD. 1992. Evidencesupporting a di- moults of the passerinebirds of New York. An- etary basisfor orange-tippedrectrices in the Ce- nals of the New York Academyof Sciences13: dar Waxwing. Journalof Field Ornithology 63: 73-360. 212-216. EDMINSTER,F. C. 1950. Useof shrubsin developing MURPHY,M. E., ANDJ. R. KING. 1984. Dietary sulfur farm wildlife habitat. Transactions of the North amino acid availability and molt dynamicsin American Wildlife Conference 15:519-550. White-crowned Sparrows. Auk 101:164-167. EDMINSTER,F. C., ANDR. M. MAY. 1951. Shrub plant- MURPHY,M. E., AND J. R. K•G. 1991. Protein intake ings for soil conservationand wildlife cover in and the dynamics of the postnuptial molt in the Northeast.U.S. Department of Agriculture White-crowned Sparrows, Zonotrichialeucophrys Circular No. 887. gambelii.Canadian Journal of Zoology 69:2225- FERNALD,M. L. 1950. Gray's manual of botany. 2229. AmericanBook Company, New York. PARTALl,V., S. LIAAEN-JENsEN,T. SLAGSVOLD,AND J. GOODWIN,T. W. 1984. The biochemistry of the ca- T. LIFIELD. 1987. Carotenoids in food chain stud- rotenoids:, vol. 2. Chapman and Hall, ies.II. The food chainof Parusspp. monitored by New York. carotenoidanalysis. Comparative Biochemistry GOODWIN,T. W., AND L. J. GOAD. 1970. Carotenoids and PhysiologyB ComparativeBiochemistry 87: and triterpenoids.Pages 305-368 in The biochem- 885-888. istry of fruits and their products(A. C. Hulme, PITTAwAY,R. 1991. Orange-bandedvariant of the Ed.). Academic Press, London. CedarWaxwing. Ontario Birds9:7-8. HAUSER,E. J.P. 1966. The natural occurrence of a PYLE, P., S. N. G. HOWELL, R. P. YUhnCK, AND D. F. hybrid honeysuckle(Lonicera x bella)in Ohio and DESANTE.1987. Identification guide to North Michigan. Michigan Botanist5:211-217. American passetines.Slate Creek Press,Bolinas, HENRY, R. D., AND A. R. SCOTT. 1981. Time of intro- California. duction of the alien component of the sponta- RAHMAN, A.-K., AND K. EC•Fm. 1973. Ketocaroti- neous Illinois vascular flora. American Midland noide in den Friichten yon Lonicera webbiana und Naturalist 106:318-324. .Zeitschrift •r Naturfor- HILL, G. E. 1990. Female House Finches prefer col- schung C 28:434-436. ourful males: Sexual selection for a condition- REHDER,A. 1903. Synopsisof the genus Lonicera. dependent trait. Animal Behaviour 40:563-572. Missouri Botanical Garden, St. Louis. HILL, G.E. 1992. Proximate basis of variation in ca- ROBBINS,C.T. 1993. Wildlife feeding and nutrition. rotenoid pigmentation in male House Finches. Academic Press, New York. Auk 109:1-12. RYAN, P. G., C. L. MOLONL:Y,AND J. HUDON. 1994. HOLTHUIJZEN, A.M. A., AND C. S. ADKISSON. 1984. Color variation and hybridization amongNesos- Passagerate, energetics,and utilization efficiency pizabuntings on InaccessibleIsland, Tristan da of the Cedar Waxwing. Wilson Bulletin 96:680- Cunha. Auk 111:314-327. 684. SHERBURN•,J. A. 1972. Effectsof seasonalchanges HUDON,J., ANDA. H. BRUSH.1989. Probabledietary in the abundance and chemistry of the fleshy October1996] FruitsAlter Color of WaxwingFeathers 743

fruits of northeastern woody shrubs on patterns V•SLI