{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T23:51:25Z","timestamp":1792713085212,"version":"4.5.0"},"reference-count":77,"publisher":"The Royal Society","issue":"1452","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Proc. R. Soc. Lond. B"],"published-print":{"date-parts":[[2000,8,7]]},"DOI":"10.1098\/rspb.2000.1174","type":"journal-article","created":{"date-parts":[[2002,7,26]],"date-time":"2002-07-26T19:55:43Z","timestamp":1027713343000},"page":"1525-1531","source":"Crossref","is-referenced-by-count":265,"title":["Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration"],"prefix":"10.1098","volume":"267","author":[{"given":"Kevin J.","family":"McGraw","sequence":"first","affiliation":[{"name":"Department of Biological Sciences and Alabama Agricultural Experiment Station, 331 Funchess Hall, Auburn University, Auburn, AL 36849, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Geoffrey E.","family":"Hill","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences and Alabama Agricultural Experiment Station, 331 Funchess Hall, Auburn University, Auburn, AL 36849, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"175","published-online":{"date-parts":[[2000,8,7]]},"reference":[{"key":"p_1","first-page":"319","article-title":"E\u00a1ect of Eimeria acervulina infection on chick (Gallus domesticus) high density lipoprotein composition","volume":"87","author":"Allen P. C.","year":"1987","journal-title":"Comp. Biochem. Ph siol. B"},{"key":"p_2","first-page":"45","article-title":"E\u00a1ect of Eimeria acervulina infection on apolipoprotein A-1 synthesis in chick intestine","volume":"67","author":"Allen P. C.","year":"1988","journal-title":"Poult. Sci."},{"key":"p_3","doi-asserted-by":"crossref","unstructured":"Allen P. C. 1992 E\u00a1ect of coccidiosis on the distribution of dietary Iutein in the chick. Poult. Sci. 71 1457^1463.","DOI":"10.3382\/ps.0711457"},{"key":"p_4","doi-asserted-by":"crossref","unstructured":"Augustine P. C. & Ru\u00a1 M. D. 1983 Changes in carotenoid and vitamin A levels in young turkeys infected with Eimeria meleagrimitis or E. adenoides. Avian Dis. 27 963^971.","DOI":"10.2307\/1590197"},{"key":"p_5","doi-asserted-by":"crossref","unstructured":"Badyaev A. V. & Hill G. E. 2000 Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based plumage coloration. Biol. J. Linn. Soc. 69 153^172.","DOI":"10.1111\/j.1095-8312.2000.tb01196.x"},{"key":"p_6","doi-asserted-by":"crossref","unstructured":"Baker D. G. Speer C. A. Yamaguchi A. Gri\u00a1ey S. M. & Dubey J. P. 1996 An unusual coccidian parasite causing pneumonia in a northern cardinal (Cardinalis cardinalis). J. Wildl. Dis. 32 130^132.","DOI":"10.7589\/0090-3558-32.1.130"},{"key":"p_7","doi-asserted-by":"crossref","unstructured":"Brawner III W. R. & Hill G. E. 1999 Temporal variation in shedding of coccidial oocysts: implications for sexual selection studies. Can. J. Zool. 77 347^350.","DOI":"10.1139\/z98-207"},{"key":"p_8","doi-asserted-by":"crossref","unstructured":"Brawner III W. R. Hill G. E. & Sundermann C. A. 2000 E\u00a1ects of coccidial and mycoplasmal infection on carotenoidbased plumage pigmentation in male house \u00a2nches. Auk. (In the press.)","DOI":"10.1642\/0004-8038(2000)117[0952:EOCAMI]2.0.CO;2"},{"key":"p_9","doi-asserted-by":"crossref","unstructured":"Brooks R. 1996 Melanin as a visual signal ampli\u00a2er in male guppies. Naturwissenschaften 83 39^41.","DOI":"10.1007\/s001140050245"},{"key":"p_10","doi-asserted-by":"crossref","unstructured":"Brooks R. & Couldridge V. 1999 Multiple sexual ornaments coevolve with multiple mating preferences. Am. Nat. 154 38^45.","DOI":"10.1086\/303219"},{"key":"p_11","unstructured":"Brush A. H. 1978 Avian pigmentation. In Chemical zoolog . X. Aves (ed. A. H. Brush) pp. 141^161. New York: Academic Press."},{"key":"p_12","doi-asserted-by":"crossref","unstructured":"Brush A. H. 1981 Carotenoids in wild and captive birds. In Carotenoids as colorants and vitamin A precursors (ed. J. C. Bauerfeind) pp. 539^562. New York: Academic Press.","DOI":"10.1016\/B978-0-12-082850-0.50012-3"},{"key":"p_13","doi-asserted-by":"crossref","unstructured":"Butcher G. S. & Rohwer S. 1989 The evolution of conspicuous and distinctive colouration for communication in birds. Curr. Ornithol. 6 51^108.","DOI":"10.1007\/978-1-4757-9918-7_2"},{"key":"p_14","unstructured":"Cohen J. 1988 Statistical power anal sis for the behavioral sciences. Hillsdale NJ: Lawrence Erlbaum."},{"key":"p_15","doi-asserted-by":"crossref","unstructured":"Darwin C. 1871 The descent of man and selection in relation to sex. London UK: John Murray.","DOI":"10.5962\/bhl.title.24784"},{"key":"p_16","doi-asserted-by":"crossref","unstructured":"Eckert C. G. & Weatherhead P. J. 1987 Ideal dominance distributions: a test using red-winged blackbirds (Agelaius phoeniceus). Behav. Ecol. Sociobiol. 20 43^52.","DOI":"10.1007\/BF00292165"},{"key":"p_17","unstructured":"Figuerola J. & Gutie rrez R. 1998 Sexual di\u00a1erences in levels of blood carotenoids in cirl buntings Emberiza cirlus. Ardea 86 245^248."},{"key":"p_18","doi-asserted-by":"crossref","unstructured":"Fox D. L. 1976 Animal biochromes and structural colours. Berkeley CA: University of California Press.","DOI":"10.1525\/9780520339422"},{"key":"p_19","unstructured":"Fox D. L. & Vevers G. 1960 The nature of animal colours. New York: Macmillan."},{"key":"p_20","doi-asserted-by":"crossref","unstructured":"Giacomo R. Stefania P. Ennio T. Giorgina V. C. Giovanni B. & Giacomo R. 1997 Mortality in black siskins (Carduelis atrata) with systemic coccidiosis. J. Wildl. Dis. 33 152^157.","DOI":"10.7589\/0090-3558-33.1.152"},{"key":"p_21","unstructured":"Goodwin T. W. 1984 The biochemistr of the carotenoids vol. 2. London UK: Chapman & Hall."},{"key":"p_22","doi-asserted-by":"crossref","unstructured":"Gray D. A. 1996 Carotenoids and sexual dichromatism in North American passerine birds. Am. Nat. 148 453^480.","DOI":"10.1086\/285935"},{"key":"p_23","doi-asserted-by":"crossref","unstructured":"Gri\u00a4th S. C. Owens I. P. F. & Burke T. 1999 Environmental determination of a sexually selected trait. Nature 400 358^360.","DOI":"10.1038\/22536"},{"key":"p_24","doi-asserted-by":"crossref","unstructured":"Grubb Jr T. C. 1995 Ptilochronology: a review and prospectus. Curr. Ornithol. 12 89^114.","DOI":"10.1007\/978-1-4615-1835-8_3"},{"key":"p_25","doi-asserted-by":"crossref","unstructured":"Hamilton W. D. & Zuk M. 1982 Heritable true \u00a2tness and bright birds: a role for parasites? Science 218 384^387.","DOI":"10.1126\/science.7123238"},{"key":"p_26","doi-asserted-by":"crossref","unstructured":"Hasson O. 1989 Ampli\u00a2ers and the handicap principle in sexual selection: a di\u00a1erent emphasis. Proc. R. Soc. Lond. B 235 383^406.","DOI":"10.1098\/rspb.1989.0006"},{"key":"p_27","doi-asserted-by":"crossref","unstructured":"Hasson O. 1991 Sexual displays as ampli\u00a2ers: practical examples with an emphasis on feather decorations. Behav. Ecol. 2 189^197.","DOI":"10.1093\/beheco\/2.3.189"},{"key":"p_28","unstructured":"Helman R. G. Jensen J. M. & Russell R. G. 1984 Systemic protozoal disease in zebra \u00a2nches. J. Am. Vet. Med. Assoc. 169 1400^1401."},{"key":"p_29","doi-asserted-by":"crossref","unstructured":"Hill G. E. 1992 Proximate basis of variation in carotenoid pigmentation in male house \u00a2nches. Auk 109 1^12.","DOI":"10.2307\/4088262"},{"key":"p_30","doi-asserted-by":"crossref","unstructured":"Hill G. E. 1993 Geographic variation in the carotenoid plumage pigmentation of male house \u00a2nches (Carpodacus mexicanus). Biol. J. Linn. Soc. 49 63^86.","DOI":"10.1006\/bijl.1993.1023"},{"key":"p_31","doi-asserted-by":"crossref","unstructured":"Hill G. E. 1995 Ornamental traits as indicators of environmental health. BioScience 45 25^31.","DOI":"10.2307\/1312532"},{"key":"p_32","doi-asserted-by":"crossref","unstructured":"Hill G. E. 1996 Redness as a measure of the production cost of ornamental coloration. Ethol. Ecol. Evol. 8 157^175.","DOI":"10.1080\/08927014.1996.9522926"},{"key":"p_33","unstructured":"Hill G. E. 1998 An easy inexpensive method to quantify plumage coloration. J. Field Ornithol. 69 353^363."},{"key":"p_34","unstructured":"Hill G. E. 1999 Mate choice male quality and carotenoidbased plumage coloration. In Proceedings of the International Ornithological Congress vol. 22 (ed. N. J. Adams & R. H. Slotow) pp. 1654^1668. Johannesburg South Africa: BirdLife South Africa."},{"key":"p_35","doi-asserted-by":"crossref","unstructured":"Hill G. E. 2000 Energetic constraints on expression of carotenoid-based plumage coloration. J. Avian Biol. (In the press.)","DOI":"10.1034\/j.1600-048X.2000.310415.x"},{"key":"p_36","doi-asserted-by":"crossref","unstructured":"Hill G. E. & Brawner III W. R. 1998 Melanin-based plumage coloration in the house \u00a2nch is una\u00a1ected by coccidial infection. Proc. R. Soc. Lond. B 265 1105^1109.","DOI":"10.1098\/rspb.1998.0405"},{"key":"p_37","doi-asserted-by":"crossref","unstructured":"Hill G. E. & Montgomerie R. 1994 Plumage colour signals nutritional condition in the house \u00a2nch. Proc. R. Soc. Lond. B 258 47^52.","DOI":"10.1098\/rspb.1994.0140"},{"key":"p_38","doi-asserted-by":"crossref","unstructured":"Houde A. E. & Torio A. J. 1992 E\u00a1ect of parasitic infection on male color pattern and female choice in guppies. Behav. Ecol. 3 346^351.","DOI":"10.1093\/beheco\/3.4.346"},{"key":"p_39","doi-asserted-by":"crossref","first-page":"654","DOI":"10.5962\/p.358279","article-title":"Non-melanin schizochroism in Alberta evening grosbeaks Coccothraustes vespertinus","volume":"111","author":"Hudon J.","year":"1997","journal-title":"Can. Field-Nat."},{"key":"p_40","doi-asserted-by":"crossref","unstructured":"Johnson K. Dalton R. & Burley N. 1993 Preferences of female American gold\u00a2nches (Carduelis tristis) for natural and arti\u00a2- cial male traits. Behav. Ecol. 4 138^143.","DOI":"10.1093\/beheco\/4.2.138"},{"key":"p_41","doi-asserted-by":"crossref","unstructured":"Johnson S. G. 1991 E\u00a1ects of predation parasites and phylogeny on the evolution of bright coloration in North American male passerines. Evol. Ecol. 5 52^62.","DOI":"10.1007\/BF02285245"},{"key":"p_42","doi-asserted-by":"crossref","unstructured":"Johnstone R. A. 1995 Honest advertisement of multiple qualities using multiple signals. J.Theor. Biol. 177 87^94.","DOI":"10.1016\/S0022-5193(05)80006-2"},{"key":"p_43","doi-asserted-by":"crossref","unstructured":"Johnstone R. A. 1996 Multiple displays in animal communication: `backup signals' and `multiple messages'. Phil. Trans. R. Soc. Lond. B 351 329^338.","DOI":"10.1098\/rstb.1996.0026"},{"key":"p_44","doi-asserted-by":"crossref","unstructured":"Linville S. U. & Breitwisch R. 1997 Carotenoid availability and plumage coloration in a wild population of northern cardinals. Auk 114 796^800.","DOI":"10.2307\/4089305"},{"key":"p_45","doi-asserted-by":"crossref","unstructured":"McGraw K. J. & Hill G. E. 2000a Plumage brightness and breeding-season dominance in the house \u00a2nch: a negatively correlated handicap? Condor 102 457^462.","DOI":"10.1650\/0010-5422(2000)102[0456:PBABSD]2.0.CO;2"},{"key":"p_46","doi-asserted-by":"crossref","unstructured":"McGraw K. J. & Hill G. E. 2000b Carotenoid-based ornamentation and status signaling in the house \u00a2nch. Behav. Ecol. (In the press.)","DOI":"10.1093\/beheco\/11.5.520"},{"key":"p_47","doi-asserted-by":"crossref","unstructured":"Marler P. 1955 Studies of \u00a2ghting in cha\u00a4nches. 2. The e\u00a1ect on dominance relations of disguising females as males. Br. J. Anim. Behav. 3 137^146.","DOI":"10.1016\/S0950-5601(55)80052-4"},{"key":"p_48","doi-asserted-by":"crossref","unstructured":"Maynard Smith J. & Harper D. C. G. 1988 The evolution of aggression: can selection generate variability? Phil. Trans. R. Soc. Lond. B 319 557^570.","DOI":"10.1098\/rstb.1988.0065"},{"key":"p_49","doi-asserted-by":"publisher","DOI":"10.2307\/4512067"},{"key":"p_50","doi-asserted-by":"crossref","unstructured":"Middleton A. L. A. 1993 American gold\u00a2nch (Carduelis tristis). In The birds of North America vol. 80 (ed. A. Poole & F. Gill) pp. 1^24. Philadelphia PA: Academy of Natural Sciences.","DOI":"10.2173\/bna.80"},{"key":"p_51","doi-asserted-by":"crossref","unstructured":"Milinski M. & Bakker T. C. M. 1990 Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344 330^333.","DOI":"10.1038\/344330a0"},{"key":"p_52","doi-asserted-by":"crossref","unstructured":"M\u00d6ller A. P. 1989 Natural and sexual selection on a plumage signal of status and on morphology in house sparrows Passer domesticus. J. Evol. Biol. 2 125^140.","DOI":"10.1046\/j.1420-9101.1989.2020125.x"},{"key":"p_53","doi-asserted-by":"crossref","unstructured":"M\u00d6ller A. P. & Pomiankowski A. 1993 Why have birds got multiple sex ornaments? Behav. Ecol. Sociobiol. 32 167^176.","DOI":"10.1007\/BF00173774"},{"key":"p_54","doi-asserted-by":"crossref","unstructured":"Mundinger P. C. 1972 Annual testicular cycle and bill color change in the eastern American gold\u00a2nch. Auk 89 403^419.","DOI":"10.2307\/4084214"},{"key":"p_55","doi-asserted-by":"crossref","unstructured":"Norris K. 1993 Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature 362 537^539.","DOI":"10.1038\/362537a0"},{"key":"p_56","unstructured":"Olson V. A. 1996 Coccidia and sexual selection in the American gold\u00a2nch (Carduelis tristis): a test of the Hamilton^ Zuk hypothesis. MSc thesis University of Guelph Ontario Canada."},{"key":"p_57","doi-asserted-by":"crossref","unstructured":"Olson V. A. & Owens I. P. F. 1998 Costly sexual signals: are carotenoids rare risky or required? Trends Ecol. Evol. 13 510^514.","DOI":"10.1016\/S0169-5347(98)01484-0"},{"key":"p_58","unstructured":"Otter K. & Ratcli\u00a1e L. 1999 Relationship of bib size to age and sex in the black-capped chickadee. J. Field Ornithol. 70 567^577."},{"key":"p_59","doi-asserted-by":"crossref","unstructured":"Rice W. R. 1989 Analyzing tables of statistical tests. Evolution 43 223^225.","DOI":"10.1111\/j.1558-5646.1989.tb04220.x"},{"key":"p_60","doi-asserted-by":"crossref","unstructured":"Rohwer S. 1975 The social signi\u00a2cance of avian winter plumage variability. Evolution 29 593^610.","DOI":"10.1111\/j.1558-5646.1975.tb00853.x"},{"key":"p_61","doi-asserted-by":"crossref","unstructured":"Roulin A. Richner H. & Ducrest A. L. 1998 Genetic environmental and condition-dependent e\u00a1ects on female and male ornamentation in the barn owl T to alba. Evolution 52 1451^1460.","DOI":"10.1111\/j.1558-5646.1998.tb02026.x"},{"key":"p_62","doi-asserted-by":"crossref","unstructured":"Ru\u00a1 M. D. Reid W. M. & Johnson J. K. 1974 Lowered blood carotenoid levels in chickens infected with coccidia. Poult. Sci. 53 1801^1809.","DOI":"10.3382\/ps.0531801"},{"key":"p_63","doi-asserted-by":"crossref","unstructured":"Ryan P. G. Moloney C. L. & Hudon J. 1994 Color variation and hybridization among Neospiza buntings on Inaccessible Island Tristan da Cunha. Auk 111 314^327.","DOI":"10.2307\/4088596"},{"key":"p_64","doi-asserted-by":"crossref","unstructured":"Savalli U. M. 1995 The evolution of bird coloration and plumage elaboration: a review of hypotheses. Curr. Ornithol. 12 141^190.","DOI":"10.1007\/978-1-4615-1835-8_5"},{"key":"p_65","doi-asserted-by":"crossref","unstructured":"Searcy W. A. 1979 Morphological correlates of dominance in captive male red-winged blackbirds. Condor 81 417^420.","DOI":"10.2307\/1366971"},{"key":"p_66","unstructured":"Senar J. C. 1999 Plumage coloration as a signal of social status. In Proceedings of the International Ornithological Congress vol. 22 (ed. N. J. Adams & R. H. Slotow) pp. 1669^1686. Johannesburg South Africa: BirdLife South Africa."},{"key":"p_67","doi-asserted-by":"crossref","unstructured":"Senar J. C. & Camerino M. 1998 Status signalling and the ability to recognize dominants: an experiment with siskins (Carduelis spinus). Proc. R. Soc. Lond. B 265 1515^1520.","DOI":"10.1098\/rspb.1998.0466"},{"key":"p_68","doi-asserted-by":"crossref","unstructured":"Senar J. C. Camerino M. Copete J. L. & Metcalfe N. B. 1993 Variation in black bib of the Eurasian siskin (Carduelis spinus) and its role as a reliable badge of dominance. Auk 110 924^927.","DOI":"10.2307\/4088649"},{"key":"p_69","doi-asserted-by":"crossref","unstructured":"Shawcross J. E. & Slater P. J. B. 1984 Agonistic experience and individual recognition in male Quelea quelea. Behav. Process. 9 49^60.","DOI":"10.1016\/0376-6357(84)90007-X"},{"key":"p_70","doi-asserted-by":"crossref","unstructured":"Slagsvold T. & Lif jeld J. T. 1985 Variation in plumage coloration in the great tit Parus major in relation to habitat season and food. J. Zool. 206A 321^328.","DOI":"10.1111\/j.1469-7998.1985.tb05661.x"},{"key":"p_71","doi-asserted-by":"crossref","unstructured":"Slagsvold T. & Lif jeld J. T. 1992 Plumage color is a conditiondependent sexual trait in male pied \u00a3ycatchers. Evolution 46 825^828.","DOI":"10.1111\/j.1558-5646.1992.tb02087.x"},{"key":"p_72","doi-asserted-by":"crossref","unstructured":"Swayne D. E. Getzy D. Siemons R. D. Bocetti C. & Kramer L. 1991 Coccidiosis as a cause of transmural Iymphocytic enteritis and mortality in captive Nashville warblers (Vermivora ru\u00a2capilla). J. Wildl. Dis. 27 615^620.","DOI":"10.7589\/0090-3558-27.4.615"},{"key":"p_73","doi-asserted-by":"crossref","unstructured":"Thompson C. W. Hillgarth N. Leu M. & McClure H. E. 1997 High parasite load in house \u00a2nches (Carpodacus mexicanus) is correlated with reduced expression of a sexually selected trait. Am. Nat. 149 270^294.","DOI":"10.1086\/285990"},{"key":"p_74","doi-asserted-by":"crossref","unstructured":"Tyczkowski J. K. Hamilton P. B. & Ru\u00a1 M. D. 1991 Altered metabolism of carotenoids during pale-bird syndrome in chicks infected with Eimeria acervulina. Poult. Sci. 70 2074^2081.","DOI":"10.3382\/ps.0702074"},{"key":"p_75","doi-asserted-by":"crossref","unstructured":"Veiga J. P. & Puerta M. 1996 Nutritional constraints determine the expression of a sexual trait in the house sparrow Passer domesticus. Proc. R. Soc. Lond. B 263 229^234.","DOI":"10.1098\/rspb.1996.0036"},{"key":"p_76","doi-asserted-by":"crossref","unstructured":"Wolfenbarger L. L. 1999 Is red coloration of male northern cardinals bene\u00a2cial during the nonbreeding season?: a test of status signaling. Condor 101 655^663.","DOI":"10.2307\/1370195"},{"key":"p_77","unstructured":"Zar J. H. 1984 Biostatistical anal sis. Englewood Cli\u00a1s NJ: Prentice Hall."}],"container-title":["Proceedings of the Royal Society of London. Series B: Biological Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2000.1174","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,8]],"date-time":"2024-12-08T07:03:51Z","timestamp":1733641431000},"score":1,"resource":{"primary":{"URL":"https:\/\/royalsocietypublishing.org\/doi\/10.1098\/rspb.2000.1174"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2000,8,7]]},"references-count":77,"journal-issue":{"issue":"1452","published-online":{"date-parts":[[2000,8,7]]},"published-print":{"date-parts":[[2000,8,7]]}},"alternative-id":["10.1098\/rspb.2000.1174"],"URL":"https:\/\/doi.org\/10.1098\/rspb.2000.1174","relation":{},"ISSN":["0962-8452","1471-2954"],"issn-type":[{"value":"0962-8452","type":"print"},{"value":"1471-2954","type":"electronic"}],"subject":[],"published":{"date-parts":[[2000,8,7]]}}}