Hidden carotenoids in the powder down of herons

Abstract

Vivid plumage colors are some of the best examples of elaborate trait evolution resulting from sexual selection. Bird feathers often contain high concentrations of pigment or intricate microstructures for reflecting light at distal feather tips, in order to maximize color presentation to intended viewers (e.g., prospective mates, rivals). However, here we describe a rare form of “hidden” plumage coloration, whereby several species of heron (Pelecaniformes: Ardeidae) have powder down tracts liberally coated in yellow pigments that are hidden from view underneath contour feathers. We show using Raman spectroscopy and high-performance liquid chromatography that the yellow coloration is due to carotenoid pigmentation. We also show that fatty acids and carotenoids co-occur in samples and discuss the possible evidence and implications for the presence of esterified carotenoids in powder down. Our study of hidden feather coloration is in apparent contrast with the traditional view of carotenoid pigmentation in plumage, which holds that carotenoids are costly pigments that are displayed to advertise individual quality. We hypothesize that carotenoid pigments are transferred onto powder down as a consequence of the chemical affinity that these pigments have to lipoid secretions associated with subcutaneous fat. Further investigation may identify functions for carotenoid pigmentation in powder down (e.g., signaling, microbiological protection), but we cannot rule out the possibility that the powder down of herons may provide the first evidence for carotenoid coloration in feathers being a non-adaptive by-product of other processes.

Zusammenfassung

Versteckte Carotinoide in den Puderdunen von Reihern

Leuchtende Gefiederfarben gehören zu den besten Beispielen für die Evolution aufwendiger Merkmale durch sexuelle Selektion. Vogelfedern enthalten oft hohe Pigmentkonzentrationen oder besitzen komplexe lichtreflektierende Mikrostrukturen an den distalen Federspitzen, um die Wirkung der Farben auf die beabsichtigten Betrachter (beispielsweise mögliche Partner oder Rivalen) zu maximieren. Hier allerdings beschreiben wir eine seltene Form „versteckter Gefiederfärbung”, bei der verschiedene Reiherarten (Pelecaniformes: Ardeidae) Fluren reichlich mit gelben Pigmenten bedeckter Puderdunen aufweisen, welche unter dem Deckgefieder den Blicken verborgen bleiben. Mittels Raman-Spektroskopie und Hochleistungs-Flüssigkeitschromatografie zeigen wir, dass die Gelbfärbung auf Carotinoidpigmenten beruht. Außerdem zeigen wir, dass Fettsäuren und Karotinoide gemeinsam in den Proben vorkommen und erörtern die möglichen Belege für die Existenz veresterter Carotinoide in Puderdunen und deren eventuelle Konsequenzen. Unsere Untersuchung “versteckter” Gefiederfärbung steht in offenkundigem Gegensatz zur traditionellen Ansicht über carotinoidbasierte Gefiederpigmentierung, welche besagt, dass Carotinoide kostspielige Pigmente sind, die präsentiert werden, um die individuelle Qualität zu demonstrieren. Wir stellen die Hypothese auf, dass Carotinoidpigmente in Folge ihrer chemischen Affinität zu lipoiden Sekreten, welche im Zusammenhang mit subkutanem Fett stehen, auf die Puderdunen übertragen werden. Weitergehende Studien könnten Funktionen der carotinoidbasierten Pigmentierung der Puderdunen aufzeigen (beispielsweise Signalwirkung oder mikrobiologische Schutzfunktion), wir können allerdings die Möglichkeit nicht ausschließen, dass die Puderdunen der Reiher der erste Beleg dafür sind, dass Carotinoidfärbung bei Federn als ein nicht-adaptives Nebenprodukt anderer Prozesse entsteht.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Amat JA, Rendón MA, Garrido-Fernández J, Garrido A, Rendón-Martos M, Pérez-Gálvez A (2011) Greater Flamingos Phoenicopterus roseus use uropygial secretions as make-up. Behav Ecol Sociobiol 65:665–673. https://doi.org/10.1007/s00265-010-1068-z

    Article  Google Scholar 

  2. Brockmann H, Volker O (1934) Federfarbstoff des Kanarienvogels (Serinus canaria canaria [L.]) und das vorkommen von Carotinoiden bei Vögeln. Z Physiol Chem 224:193–215

    Article  CAS  Google Scholar 

  3. Burtt EH, Schroeder MR, Smith LA, Sroka JE, McGraw KJ (2010) Colourful parrot feathers resist bacterial degradation. Biol Lett 7:214–216. https://doi.org/10.1098/rsbl.2010.0716

    Article  PubMed  PubMed Central  Google Scholar 

  4. Camplani A, Saino N, Møller AP (1999) Carotenoids, sexual signals and immune function in Barn Swallows from Chernobyl. Proc R Soc Lond B 266:1111–1116. https://doi.org/10.1098/rspb.1999.0751

    Article  CAS  Google Scholar 

  5. De Gelder J, De Gussem K, Vandenabeele P, Moens L (2007) Reference database of Raman spectra of biological molecules. J Raman Spectrosc 38:1133–1147. https://doi.org/10.1002/jrs.1734

    Article  CAS  Google Scholar 

  6. Delhey K, Peters A, Kempenaers B (2007) Cosmetic coloration in birds: occurrence, function, and evolution. Am Nat 169:S145–S158. https://doi.org/10.1086/510095

    Article  PubMed  Google Scholar 

  7. Dumbacher JP, Fleischer RC (2001) Phylogenetic evidence for colour pattern convergence in toxic pitohuis: Müllerian mimicry in birds? Proc R Soc Lond B 268:1971–1976. https://doi.org/10.1098/rspb.2001.1717

    Article  CAS  Google Scholar 

  8. Elder WH (1954) The oil gland of birds. Wilson Bull 66:6–31

    Google Scholar 

  9. García-de Blas E, Mateo R, Viñuela J, Pérez-Rodríguez L, Alonso-Alvarez C (2013) Free and esterified carotenoids in ornaments of an avian species: the relationship to color expression and sources of variability. Physiol Biochem Zool 86:483–498. https://doi.org/10.1086/671812

    Article  PubMed  CAS  Google Scholar 

  10. García-de Blas E, Mateo R, Alonso-Alvarez C (2015) Accumulation of dietary carotenoids, retinoids and tocopherol in the internal tissues of a bird: a hypothesis for the cost of producing colored ornaments. Oecologia 177:259–271. https://doi.org/10.1007/s00442-014-3163-8

    Article  PubMed  Google Scholar 

  11. Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc B 205:581–598. https://doi.org/10.1098/rspb.1979.0086

    Article  CAS  Google Scholar 

  12. Heinen-Kay JL, Morris KE, Ryan NA, Byerley SL, Venezia RE, Peterson MN, Langerhans RB (2015) A trade-off between natural and sexual selection underlies diversification of a sexual signal. Behav Ecol 26:533–542. https://doi.org/10.1093/beheco/aru228

    Article  Google Scholar 

  13. Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339. https://doi.org/10.1038/350337a0

    Article  Google Scholar 

  14. Hofmann CM, McGraw KJ, Cronin TW, Omland KE (2007) Melanin coloration in New World orioles. I. Carotenoid masking and pigment dichromatism in the Orchard Oriole complex. J Avian Biol 38:163–171. https://doi.org/10.1111/j.2006.0908-8857.03803.x

    Article  Google Scholar 

  15. Hsu SL, Moore WH, Krimm S (1976) Vibrational spectrum of the unordered polypeptide chain: a Raman study of feather keratin. Biopolymers 15:1513–1528. https://doi.org/10.1002/bip.1976.360150807

    Article  PubMed  CAS  Google Scholar 

  16. Husak JF, Swallow JG (2011) Compensatory traits and the evolution of male ornaments. Behaviour 148:1–29

    Article  Google Scholar 

  17. Jacob J, Pomeroy DE (1979) The feather lipids of the Marabou Stork (Leptoptilos crumeniferus). Comp Biochem Physiol B 64:301–303. https://doi.org/10.1016/0305-0491(79)90148-2

    Article  Google Scholar 

  18. Koch RE, Hill GE (2017) An assessment of techniques to manipulate oxidative stress in animals. Funct Ecol 31:9–21. https://doi.org/10.1111/1365-2435.12664

    Article  Google Scholar 

  19. Lucas AM, Stettenheim PR (1972) Avian anatomy—integument. Agriculture handbook 362. US Department of Agriculture, Washington, DC

    Google Scholar 

  20. Marshall KLA, Philpot KE, Stevens M (2015) Conspicuous male coloration impairs survival against avian predators in Aegean Wall Lizards, Podarcis erhardii. Ecol Evol 5:4115–4131. https://doi.org/10.1002/ece3.1650

    Article  PubMed  PubMed Central  Google Scholar 

  21. Massaro M, Davis LS, Darby JT (2003) Carotenoid-derived ornaments reflect parental quality in male and female Yellow-eyed Penguins (Megadyptes antipodes). Behav Ecol Sociobiol 55:169–175

    Article  Google Scholar 

  22. McGraw KJ (2004) European Barn Swallows use melanin pigments to color their feathers brown. Behav Ecol 15:889–891. https://doi.org/10.1093/beheco/arh109

    Article  Google Scholar 

  23. McGraw KJ (2005a) Interspecific variation in dietary carotenoid assimilation in birds: links to phylogeny and color ornamentation. Comp Biochem Physiol B 142:245–250. https://doi.org/10.1016/j.cbpb.2005.07.012

    Article  PubMed  CAS  Google Scholar 

  24. McGraw KJ (2005b) The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Anim Behav 69:757–764. https://doi.org/10.1016/j.anbehav.2004.06.022

    Article  Google Scholar 

  25. McGraw KJ (2006) Mechanics of carotenoid-based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration: mechanisms and measurements, vol 1. Harvard University Press, Cambridge, pp 177–242

    Google Scholar 

  26. McGraw KJ, Hardy LS (2006) Astaxanthin is responsible for the pink plumage flush in Franklin’s and Ring-billed Gulls. J Field Ornithol 77:29–33. https://doi.org/10.1111/j.1557-9263.2006.00008.x

    Article  Google Scholar 

  27. McGraw KJ, Toomey MB, Nolan PM, Morehouse NI, Massaro M, Jouventin P (2007) A description of unique fluorescent yellow pigments in penguin feathers. Pigment Cell Res 20:301–304. https://doi.org/10.1111/j.1600-0749.2007.00386.x

    Article  PubMed  CAS  Google Scholar 

  28. Menon GK, Menon J (2000) Avian epidermal lipids: functional considerations and relationship to feathering. Am Zool 40:540–552. https://doi.org/10.1093/icb/40.4.540

    CAS  Article  Google Scholar 

  29. Negro JJ, Figuerola J, Garrido J, Green AJ (2001) Fat stores in birds: an overlooked sink for carotenoid pigments? Funct Ecol 15:297–303. https://doi.org/10.1046/j.1365-2435.2001.00526.x

    Article  Google Scholar 

  30. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514. https://doi.org/10.1016/S0169-5347(98)01484-0

    Article  PubMed  CAS  Google Scholar 

  31. Ortonne JP (2002) Photoprotective properties of skin melanin. Br J Dermatol 146:7–10. https://doi.org/10.1046/j.1365-2133.146.s61.3.x

    Article  PubMed  CAS  Google Scholar 

  32. Pérez-Gálvez A, Mínguez-Mosquera MI (2005) Esterification of xanthophylls and its effect on chemical behavior and bioavailability of carotenoids in the human. Nutr Res 25:631–640. https://doi.org/10.1016/j.nutres.2005.07.002

    Article  CAS  Google Scholar 

  33. Smith DG (1972) The role of the epaulets in the Red-Winged Blackbird, (Agelaius phoeniceus) social system. Behaviour 41:251–268

    Article  Google Scholar 

  34. Surai PF, Speake BK, Sparks NHC (2001) Carotenoids in avian nutrition and embryonic development. 1. Absorption, availability and levels in plasma and egg yolk. J Poult Sci 38:1–27. https://doi.org/10.2141/jpsa.38.1

    Article  CAS  Google Scholar 

  35. Teyssier J, Saenko SV, van der Marel D, Milinkovitch MC (2015) Photonic crystals cause active colour change in chameleons. Nat Commun 6:6368. https://doi.org/10.1038/ncomms7368

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Thomas DB, McGoverin CM, McGraw KJ, James HF, Madden O (2013) Vibrational spectroscopic analyses of unique yellow feather pigments (spheniscins) in penguins. J R Soc Interface 10:20121065. https://doi.org/10.1098/rsif.2012.1065

    Article  PubMed  PubMed Central  Google Scholar 

  37. Thomas DB, McGraw KJ, Butler MW, Carrano MT, Madden O, James HF (2014a) Ancient origins and multiple appearances of carotenoid-pigmented feathers in birds. Proc R Soc B 281:20140806. https://doi.org/10.1098/rspb.2014.0806

    Article  PubMed  Google Scholar 

  38. Thomas DB, McGraw KJ, James HF, Madden O (2014b) Non-destructive descriptions of carotenoids in feathers using Raman spectroscopy. Anal Methods 6:1301–1308. https://doi.org/10.1039/c3ay41870g

    Article  CAS  Google Scholar 

  39. Tuma R (2005) Raman spectroscopy of proteins: from peptides to large assemblies. J Raman Spectrosc 36:307–319. https://doi.org/10.1002/jrs.1323

    Article  CAS  Google Scholar 

  40. Tyczkowski JK, Hamilton PB (1987) Altered metabolism of carotenoids during aflatoxicosis in young chickens. Poult Sci 66:1184–1188. https://doi.org/10.3382/ps.0661184

    Article  PubMed  CAS  Google Scholar 

  41. Völker O (1938) Porphyrin in Vogelfedern. J Ornithol 86:436–456

    Article  Google Scholar 

  42. Warren IA, Gotoh H, Dworkin IM, Emlen DJ, Lavine LC (2013) A general mechanism for conditional expression of exaggerated sexually-selected traits. BioEssays 35:889–899. https://doi.org/10.1002/bies.201300031

    PubMed  Article  Google Scholar 

  43. Weaver RJ, Koch RE, Hill GE (2017) What maintains signal honesty in animal colour displays used in mate choice? Phil Trans R Soc B 372:20160343. https://doi.org/10.1098/rstb.2016.0343

    Article  PubMed  Google Scholar 

  44. Wetmore A (1920) The function of powder downs in herons. Condor 22:168–170. https://doi.org/10.2307/1362391

    Article  Google Scholar 

  45. Wolfenbarger LL (1999) Red coloration of male Northern Cardinals correlates with mate quality and territory quality. Behav Ecol 10:80–90. https://doi.org/10.1093/beheco/10.1.80

    Article  Google Scholar 

  46. Zhong L, Gustavsson K-E, Oredsson S, Głąb B, Yilmaz JL, Olsson ME (2016) Determination of free and esterified carotenoid composition in rose hip fruit by HPLC-DAD-APCI+-MS. Food Chem 210:541–550. https://doi.org/10.1016/j.foodchem.2016.05.002

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank H. F. James for specimen access and comments on a draft manuscript, C. Gebhard, National Museum of Natural History, Smithsonian Institution for collecting samples, and the Museum Conservation Institute, Smithsonian Institution for providing access to Raman instrumentation.

Funding

D. B. T. was funded by a Peter Buck Fellowship administered by the Smithsonian Institution.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Daniel B. Thomas.

Ethics declarations

Ethics statement

All analyses were on feathers from deceased birds that had not been specifically killed for this study. Analyses were performed in, and adhered to the laws of, the United States of America.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by K. C. Klasing.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 28605 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Thomas, D.B., McGraw, K.J. Hidden carotenoids in the powder down of herons. J Ornithol 159, 785–792 (2018). https://doi.org/10.1007/s10336-018-1554-z

Download citation

Keywords

  • Ardeidae
  • Green Heron
  • High-performance liquid chromatography
  • Carotenoid pigments
  • Plumage
  • Raman spectroscopy