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Carotenoid Pigments in Male House Finch Plumage in Relation to Age, Subspecies, and Ornamental Coloration

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Carotenoid Pigments in Male House Finch Plumage in Relation to Age, Subspecies, and Ornamental Coloration The Auk 118(4):900-915, 2001 CAROTENOID PIGMENTS IN MALE HOUSE FINCH PLUMAGE IN RELATION TO AGE, SUBSPECIES, AND ORNAMENTAL COLORATION CARON Y. INOUYE,L6 GEOFFREYE. HILL, 2'5RICCARDO D. STRADI,3 AND ROBERT MONTGOMERIE 4 •Departmentof OrganismicBiology, Ecology and Evolution, University of California,P.O. Box 951606, Los Angeles, California90095-1606, USA; 2Departmentof BiologicalSciences and Alabama Agricultural Experiment Station, 331 FunchessHall, AuburnUniversity, Auburn, Alabama 36849, USA; 3Institutodi ChimicaOrganica, Universita Degli Studidi Milano,Milano, MI 20133,Italy; and 4Departmentof Biology,Queenk University, Kingston, Ontario K7L 3N6, Canada ABSTRACT.--Likemales of many bird species,male House Finches(Carpodacus mexicanus) havepatches of featherswith ornamentalcoloration that are due to carotenoidpigments. With- in populations,male HouseFinches vary in expressionof ornamentalcoloration from paleyel- low to bright red, which previousresearch suggested was the result of variationin typesand amountsof carotenoidpigments deposited in feathers.Here we usedimproved analytical tech- niquesto describetypes and amountsof carotenoidpigments present in thatplumage. We then used thosedata to make comparisonsof carotenoidcomposition of feathersof male House Finchesat three levels:among individual maleswith different plumagehue and saturation, betweenage groupsof malesfrom the samepopulation, and betweenmales from two sub- speciesthat differ in extent of ventral carotenoidpigmentation (patch size): large-patched C. m.frontalis from coastalCalifornia and small-patchedC. m.griscomi from Guerrero,Mexico. In all age groupsand populations,the ornamentalplumage coloration of male HouseFinches resultedfrom the same13 carotenoidpigments, with 3-hydroxyechinenone and luteinbeing the mostabundant carotenoid pigments. The compositionof carotenoidsin featherssuggested that House Finchesare capableof metabolictransformation of dietary forms of carotenoids. The hue of male plumagedepended on componentcarotenoids, their relativeconcentrations, and total concentrationof all carotenoids.Most 4-keto (red) carotenoidswere positivelycor- related with plumage redness,and most yellow carotenoidpigments were negativelyassoci- ated with plumageredness, although the strengthof the relationshipfor specificcarotenoid pigmentsvaried amongage groupsand subspecies.Using age and subspeciesas factorsand concentrationof eachcomponent carotenoid as dependentvariables in a MANOVA, we found a distinctivepigment profile for eachage group within eachsubspecies. Amongfrontalis males, hatch-yearbirds did not differ from adultsin meanplumage hue, but theyhad a significantly lower proportionof red pigmentsin their plumage,and significantlylower levelsof the red pimentsadonirubin and astaxanthin,but significantlyhigher levels of the yellow pigmentze- axanthin, than adult males. Among griscomimales, hatch-year birds differed from adultsin plumagehue but not significantlyin pigment composition,though in generaltheir feathers had lower concentrationsof red pigmentsand higherconcentrations of yellow pigmentsthan adult males.Both adult and hatch-yearfrontalismales differed from griscomimales in having significantlyhigher levelsof most yellow carotenoidpigments and significantlylower levels of mostred carotenoidpigments. Variation in pigmentprofiles of subspecies and ageclasses may reflectdifferences among the groupsin carotenoidmetabolism, in dietary accessto ca- rotenoids,or in exposureto environmentalfactors, such as parasites, that may affectpigmen- tation. Received18 January1999, accepted 11 June2001. CAROTENOIDPIGMENTS ARE responsiblefor plumage.Birds obtainthose carotenoids exclu- the bright red, orange,and yellow colorationof sively through their diet. No animal has been shownunequivocally to be capableof in vivo s Addresscorrespondence to this author. synthesisof carotenoids(Goodwin 1984,1986; E-mail: [email protected] Schiedt 1990). In birds, dietary carotenoids 6Present address:Department of BiologicalSci- may either be depositeddirectly into feathers ences, California State University, Hayward, 25800 or chemically changed from ingested forms Carlos Bee Boulevard, Hayward, California 94542, prior to pigment deposition,typically by ad- USA. dition or elimination of oxygen groupsto one 900 October2001] HouseFinch Carotenoids 901 or both end rings of the molecule(Davies 1985, males in expression of these displays (Hill Goodwin 1986, Tyzckowski and Hamilton 1992, 1996a, 2002). 1986a, b; Brush 1990, Schiedt 1990). Feedingexperiments conducted with captive The House Finch (Carpodacusmexicanus) is a House Finches have demonstrated that varia- sexually dichromaticpasserine bird speciesin tion among males in plumage hue and satura- which males display bright, carotenoid-based tion is dependentupon carotenoidaccess dur- patches of color on their crowns, throats, ing molt (Brush and Power 1976, Hill 1992, breasts,and rumps, and male House Finches 1993a).When malesare held in flight cagesand vary in expressionof that ornamental colora- fed a standardized diet, variation in ornamen- tion from a bright red to a dull yellow (Mich- tal plumage colorationis minimized (Hill 1992, ener and Michener 1931, Hill 1990, 1993a). The 1993a).Moreover, after molting in captivity un- carotenoid pigments responsiblefor colorful der conditions of standardized carotenoid ac- plumage in the House Finch and the pigmen- cess,males from populationsthat are typically tary basisfor variationamong males in expres- drab in colorationgrow ornamentalplumage sion of that coloration were first studied by coloration that is indistinguishablefrom that Brushand Power(1976). They attributedplum- grown by malesfrom populationsthat are typ- age colorvariation to differencesin constituent ically bright in coloration (Hill 1993a). How- carotenoids in feathers. Red birds had the most ever, the degree to which accessto dietary ca- complexassemblage of pigments,consisting of rotenoids affects expression of carotenoid- B-carotene,a group of unidentifiedmixed xan- basedplumage colorationin the wild remains thophylls, orange isocryptoxanthin,and red controversial (Hill 1994c, 2002; Hudon 1994a, echinenone;orange birds had the same subset Thompson et al. 1997, Inouye 1999). Birds are of carotenoidswithout echinenone;and yellow capableof endogenousmodification of ingest- birds lacked both echinenoneand isocryptox- ed carotenoidsprior to depositioninto target anthin. Recent analysesof severalcongeneric tissues (Fox et al. 1969, Davies 1985, Schiedt et finch speciesof the PalearcticCarduelinae done al. 1985,Tyczkowski and Hamilton 1986b,c, d; by Stradiet al. (1995a,b; 1996,1997), using new Brush 1990, Hencken 1992). Therefore, mecha- analyticaltechniques, revealed a more complex nisms involved in the digestion, absorption, pattern that differed substantiallyfrom that de- transport, modification,and depositionof die- scribedby Brushand Power (1976). tary carotenoidsmay contribute to plumage The proximate basis of variation in caroten- color variation (Hill 1999, 2002). Furthermore, oid-basedplumage coloration in HouseFinches viral, bacterial, and coccidial infectionsmay is of interestbeyond improved understanding have a significant effect on expressionof or- of the physiologicalcontrol of avian pigmen- namental plumage colorationby male House tation. Plumageredness in House Fincheshas Finches (Thompson et al. 1997, Nolan et al. been shown to be a primary criterion used by 1998, Hill and Brawner 1998, Brawner et al. females in choosingmates (Hill 1990, 1991, 2000). 1994a). In addition, plumage brightness in There is substantial variation in expression male House Finches is correlated with overwin- of ornamental plumage coloration in House ter survival (Hill 1991), nutritional condition Finchesnot just among males within popula- during molt (Hill and Montgomerie1994), par- tions,but alsoamong populations and subspe- asiteload (Thompsonet al. 1997,Brawner et al. cies (Moore 1939, Hill 1993a). There are ap- 2000), and provisioningof femalesduring in- proximately 15 subspeciesof House Finchesin cubation(Hill 1991).It has been proposedthat North America (Moore 1939, Hill 1996b), each male plumagebrightness is an honestsignal of of which has had a unique evolutionaryhistory male condition, becausecarotenoids may be for thousandsof years(Moore 1939).Each sub- scarce resources in the environment and carot- speciesis characterizedby specificplumage enoid-basedcolor displays may be costly to traits, some of which involve carotenoid color- produce(Hill 1994b,1996a, 2002). A thorough ation (Moore 1939,Hill 1996b).Two subspecies understandingof the signal content of carot- are studied in this paper: C. m.frontalis, origi- enoid-basedornamental displays can only be nally native to coastalCalifornia but now in- achieved,however, through an understanding troduced to the Hawaiian Islands and the east- of the proximate control of variation among ern United States and Canada, and C. m. 902 INOUYEET AL. [Auk, Vol. 118 griscomi,found in a relatively small region of sis for differencesbetween subspeciesin carot~ southern Mexico. Male House Finches from the enoid display,we comparedtheir patch sizes frontalispopulation have much more extensive and mean hues, total carotenoid abundances, ventral carotenoidpigmentation (larger patch and carotenoidcomposition of their feathers. size) than thosefrom the griscomipopulation (Moore 1939, Hill 1993a), but some adult male METHODS griscomihave more intense red colorationthan any malefrontalis
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