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Journal of Chemical Ecology

, Volume 45, Issue 1, pp 37–45 | Cite as

Wax Ester Composition of Songbird Preen Oil Varies Seasonally and Differs between Sexes, Ages, and Populations

  • Leanne A. GrievesEmail author
  • Mark A. Bernards
  • Elizabeth A. MacDougall-Shackleton
Article

Abstract

Chemical signaling has been well studied in invertebrates and mammals but less so in birds, due to the longstanding misconception that olfaction is unimportant or even non-existent in this taxon. However, recent findings suggest that olfaction plays an important role in avian mate choice and reproductive behavior, similar to other taxa. The leading candidate source for compounds involved in avian chemical communication is preen oil, a complex mixture secreted from the uropygial gland. Preen oil contains volatile compounds and their potential wax ester precursors, and may act as a reproductive chemosignal. Reproductive signals are generally sexually dimorphic, age-specific, seasonally variable, and may also vary geographically. We tested whether preen oil meets these expectations by using gas chromatography to examine the wax ester composition of preen oil in song sparrows (Melospiza melodia). We found that the wax ester composition of preen oil was significantly different between sexes, age classes, seasons, and populations. Collectively, our results suggest that song sparrow preen oil meets the criteria of a chemical cue that may influence mate choice and reproduction. Our findings in song sparrows, which are sexually monomorphic in plumage, also parallel patterns described for dark-eyed juncos (Junco hyemalis), a closely related songbird with sexually dimorphic plumage. Behavioral tests are needed to confirm that song sparrows attend to the cues present in preen oil, but our findings support the increasingly accepted idea that chemical communication is common and widespread in birds as it is in other taxa.

Keywords

Infochemicals Melospiza melodia Preen oil Reproductive chemosignal Chemical communication Song sparrow Uropygial gland 

Notes

Acknowledgments

We thank the rare Charitable Research Reserve and the Queen’s University Biological Station (QUBS) for access to their land and research facilities. We further acknowledge that the land we used is on the traditional territories of the Anishinabek and Haudenosauneega (Iroquois) peoples, Haldimand Treaty and Simcoe Patent Treaty lands (Cambridge) and on the traditional territories of the Anishinabek, Huron-Wendat, and Mohawk peoples and Crawford Purchase lands (Newboro). We thank Tosha Kelly and Ross Dickson for field assistance and sample collection. This research was supported by an Ontario Graduate Scholarship and a Vanier Scholarship to LAG, and NSERC Discovery Grants to MAB and EAMS.

Compliance with Ethical Standards

All birds were captured under permission from the Canadian Wildlife Service (banding subpermits 10691B, E, F). All animal procedures were approved by The University of Western Ontario Animal Use Subcommittee (protocol # 2016–017).

Supplementary material

10886_2018_1033_MOESM1_ESM.docx (42 kb)
Table S1 (DOCX 42 kb)
10886_2018_1033_Fig6_ESM.png (30 kb)
Fig. S1

Complete wax ester composition of breeding stage adult song sparrow preen oil at Newboro (Nfemales = 3, Nmales = 3, mean ± SD). Peaks that were at least 0.1% of the total chromatogram area were retained for analysis, while peaks that were <0.1% were counted as zero (see text for details). (PNG 30 kb)

10886_2018_1033_MOESM2_ESM.tif (331 kb)
High resolution image (TIF 331 kb)
10886_2018_1033_Fig7_ESM.png (44 kb)
Fig. S2

Selected wax ester composition of breeding stage adult song sparrow preen oil at Newboro (Nfemales = 3, Nmales = 3, mean ± SD). For complete wax ester composition, see Supplementary Material, Fig. S1. (PNG 43 kb)

10886_2018_1033_MOESM3_ESM.tif (311 kb)
High resolution image (TIF 311 kb)
10886_2018_1033_Fig8_ESM.png (25 kb)
Fig. S3

Complete wax ester composition of song sparrow preen oil from post-breeding stage adults and juveniles (sexes pooled for juveniles; sampled at Newboro). Peaks that were at least 0.1% of the total chromatogram area were retained for analysis, while peaks that were <0.1% were counted as zero (see text for details). (PNG 25 kb)

10886_2018_1033_MOESM4_ESM.tif (340 kb)
High resolution image (TIF 339 kb)
10886_2018_1033_Fig9_ESM.png (32 kb)
Fig. S4

Complete wax ester composition of breeding-stage song sparrow preen oil at Newboro and Cambridge (NNewboro males = 3, NNewboro females = 3, NCambridge males = 3, NCambridge females = 3, mean ± SD). Peaks that were at least 0.1% of the total chromatogram area were retained for analysis, while peaks that were <0.1% were counted as zero (see text for details). (PNG 31 kb)

10886_2018_1033_MOESM5_ESM.tif (332 kb)
High resolution image (TIF 332 kb)
10886_2018_1033_Fig10_ESM.png (86 kb)
Fig. S5

Selected wax ester composition of breeding-stage song sparrow preen oil at Newboro and Cambridge (NNewboro males = 3, NNewboro females = 3, NCambridge males = 3, NCambridge females = 3, mean ± SD). For complete wax ester composition, see Supplementary Material, Fig. S4. (PNG 85 kb)

10886_2018_1033_MOESM6_ESM.tif (974 kb)
High resolution image (TIF 973 kb)
10886_2018_1033_Fig11_ESM.png (32 kb)
Fig. S6

Complete wax ester composition of adult song sparrow preen oil sampled during breeding and post-breeding stages at Newboro (Nearly-season females = 3, Nlate-season females = 2, Nearly-season males = 3, Nlate-season males = 3, mean ± SD). Peaks that were at least 0.1% of the total chromatogram area were retained for analysis, while peaks that were <0.1% were counted as zero (see text for details). (PNG 31 kb)

10886_2018_1033_MOESM7_ESM.tif (338 kb)
High resolution image (TIF 337 kb)
10886_2018_1033_Fig12_ESM.png (102 kb)
Fig. S7

Selected wax ester composition of adult song sparrow preen oil sampled during breeding and post-breeding stages at Newboro (Nearly-season females = 3, Nlate-season females = 2, Nearly-season males = 3, Nlate-season males = 3, mean ± SD). For complete wax ester composition, see Supplementary Material, Fig. S6. (PNG 101 kb)

10886_2018_1033_MOESM8_ESM.tif (963 kb)
High resolution image (TIF 962 kb)

References

  1. Amo L, Avilés JM, Parejo D, Peña A, Rodríguez J, Tomás G (2012a) Sex recognition by odour and variation in the uropygial gland secretion in starlings. J Anim Ecol 81:605–613.  https://doi.org/10.1111/j.1365-2656.2011.01940.x CrossRefGoogle Scholar
  2. Amo L, López-Rull I, Pagán I, Garcia CM (2012b) Male quality and conspecific scent preferences in the house finch, Carpodacus mexicanus. Anim Behav 84:1483–1489CrossRefGoogle Scholar
  3. Andersson MB (1994) Sexual selection. Princeton University Press, Princeton.Google Scholar
  4. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302CrossRefGoogle Scholar
  5. Azzani L, Rasmussen JL, Gieseg SP, Briskie JV (2016) An experimental test of the effect of diet on preen wax composition in New Zealand silvereyes (Zosterops lateralis). In: Schulte BA, Goodwin TE, Ferkin MH (eds) Chemical Signals in Vertebrates 12. Springer, New York, pp 511–525Google Scholar
  6. Balthazart J, Schoffeniels E (1979) Pheromones are involved in the control of sexual behaviour in birds. Naturwissenschaften 66:55–56Google Scholar
  7. Balthazart J, Taziaux M (2009) The underestimated role of olfaction in avian reproduction? Behav Brain Res 200:248–259.  https://doi.org/10.1016/j.bbr.2008.08.036 CrossRefGoogle Scholar
  8. Bonadonna F, Nevitt GA (2004) Partner-specific odor recognition in an Antarctic seabird. Science 306:835–835.  https://doi.org/10.1126/science.1103001 CrossRefGoogle Scholar
  9. Campagna S, Mardon J, Celerier A, Bonadonna F (2012) Potential semiochemical molecules from birds: a practical and comprehensive compilation of the last 20 years studies. Chem Senses 37:3–25CrossRefGoogle Scholar
  10. Caro SP, Balthazart J (2010) Pheromones in birds: myth or reality? J Comp Physiol A 196:751–766.  https://doi.org/10.1007/s00359-010-0534-4 CrossRefGoogle Scholar
  11. Caro SP, Balthazart J, Bonadonna F (2015) The perfume of reproduction in birds: chemosignaling in avian social life. Horm Behav 68:25–42CrossRefGoogle Scholar
  12. Caspers BA, Krause ET (2013) Intraspecific olfactory communication in zebra finches (Taeniopygia guttata): potential information apart from visual and acoustic cues. In: East ML, Dehnhard M (eds) Chemical Signals in Vertebrates 12. Springer, New York, pp 341–351Google Scholar
  13. Clarke KR (1999) Nonmetric multivariate analysis in community-level ecotoxicology. Environ Toxicol Chem 18:118–127.  https://doi.org/10.1002/etc.5620180205 CrossRefGoogle Scholar
  14. Dekker MH, Piersma T, Damsté JSS (2000) Molecular analysis of intact preen waxes of Calidris canutus (Aves: Scolopacidae) by gas chromatography/mass spectrometry. Lipids 35:533–541CrossRefGoogle Scholar
  15. Dixon P, Palmer MW (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930CrossRefGoogle Scholar
  16. Fischer I, Haliński LP, Meissner W, et al (2017) Seasonal changes in the preen wax composition of the Herring gull Larus argentatus. Chemoecology 27:127–139Google Scholar
  17. Gabirot M, Raux L, Dell’Ariccia G et al (2016) Chemical labels differ between two closely related shearwater taxa. J Avian Biol 47:540–551CrossRefGoogle Scholar
  18. Gill FB (2007) Ornithology, 3rd edn. W. H. Freeman, New YorkGoogle Scholar
  19. Grieves LA, Kelly TR, Bernards MA, MacDougall-Shackleton EA (2018) Malarial infection alters wax ester composition of preen oil in songbirds: results of an experimental study. Auk 135:767–776.  https://doi.org/10.1642/AUK-17-242.1 CrossRefGoogle Scholar
  20. Griffiths R, Double MC, Orr K, Dawson RJ (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075CrossRefGoogle Scholar
  21. Hagelin JC, Jones IL (2007) Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication? Auk 124:741–761. https://doi.org/10.1642/0004-8038(2007)124[741:BOAOCS]2.0.CO;2Google Scholar
  22. Hagelin JC, Jones IL, Rasmussen LEL (2003) A tangerine-scented social odour in a monogamous seabird. Proc R Soc Lond B Biol Sci 270:1323–1329CrossRefGoogle Scholar
  23. Haribal M, Dhondt AA, Rosane D, Rodriguez E (2005) Chemistry of preen gland secretions of passerines: different pathways to same goal? Why? Chemoecology 15:251–260CrossRefGoogle Scholar
  24. Jacob J, Balthazart J, Schoffeniels E (1979) Sex differences in the chemical composition of uropygial gland waxes in domestic ducks. Biochem Syst Ecol 7:149–153CrossRefGoogle Scholar
  25. Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289.  https://doi.org/10.1111/j.1469-185X.2007.00009.x CrossRefGoogle Scholar
  26. Leclaire S, Merkling T, Raynaud C, Giacinti G, Bessière JM, Hatch SA, Danchin É (2011) An individual and a sex odor signature in kittiwakes? Study of the semiochemical composition of preen secretion and preen down feathers. Naturwissenschaften 98:615–624CrossRefGoogle Scholar
  27. Leclaire S, Merkling T, Raynaud C, Mulard H, Bessiere JM, Lhuillier E, Hatch SA, Danchin E (2012) Semiochemical compounds of preen secretion reflect genetic make-up in a seabird species. Proc R Soc B Biol Sci 279:1185–1193.  https://doi.org/10.1098/rspb.2011.1611 CrossRefGoogle Scholar
  28. LeMaster MP, Mason RT (2003) Pheromonally mediated sexual isolation among denning populations of red-sided garter snakes, Thamnophis sirtalis parietalis. J Chem Ecol 29:1027–1043CrossRefGoogle Scholar
  29. Martín J, López P (2006) Interpopulational differences in chemical composition and chemosensory recognition of femoral gland secretions of male lizards Podarcis hispanica: implications for sexual isolation in a species complex. Chemoecology 16:31–38CrossRefGoogle Scholar
  30. Moreno-Rueda G (2017) Preen oil and bird fitness: a critical review of the evidence. Biol Rev 92:2131–2143CrossRefGoogle Scholar
  31. R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  32. Reneerkens J, Piersma T, Damsté JSS (2002) Sandpipers (Scolopacidae) switch from monoester to diester preen waxes during courtship and incubation, but why? Proc R Soc Lond B Biol Sci 269:2135–2139CrossRefGoogle Scholar
  33. Reneerkens J, Piersma T, Damsté JSS (2005) Switch to diester preen waxes may reduce avian nest predation by mammalian predators using olfactory cues. J Exp Biol 208:4199–4202.  https://doi.org/10.1242/jeb.01872 CrossRefGoogle Scholar
  34. Salibian A, Montalti D (2009) Physiological and biochemical aspects of the avian uropygial gland. Braz J Biol 69:437–446CrossRefGoogle Scholar
  35. Slade JWG, Watson MJ, Kelly TR, Gloor GB, Bernards MA, MacDougall-Shackleton EA (2016) Chemical composition of preen wax reflects major histocompatibility complex similarity in songbirds. Proc R Soc B Biol Sci 283:20161966CrossRefGoogle Scholar
  36. Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102(77):77–97CrossRefGoogle Scholar
  37. Soini HA, Schrock SE, Bruce KE, Wiesler D, Ketterson ED, Novotny MV (2007) Seasonal variation in volatile compound profiles of preen gland secretions of the dark-eyed junco (Junco hyemalis). J Chem Ecol 33:183–198.  https://doi.org/10.1007/s10886-006-9210-0 CrossRefGoogle Scholar
  38. Soini HA, Whittaker DJ, Wiesler D, Ketterson ED, Novotny MV (2013) Chemosignaling diversity in songbirds: chromatographic profiling of preen oil volatiles in different species. J Chromatogr A 1317:186–192CrossRefGoogle Scholar
  39. Stoffel MA, Caspers BA, Forcada J, Giannakara A, Baier M, Eberhart-Phillips L, Müller C, Hoffman JI (2015) Chemical fingerprints encode mother–offspring similarity, colony membership, relatedness, and genetic quality in fur seals. Proc Natl Acad Sci 112:E5005–E5012CrossRefGoogle Scholar
  40. Thomas RH, Price ER, Seewagen CL et al (2010) Use of TLC-FID and GC-MS/FID to examine the effects of migratory state, diet and captivity on preen wax composition in white-throated sparrows Zonotrichia albicollis. Ibis 152:782–792CrossRefGoogle Scholar
  41. Tuttle EM, Sebastian PJ, Posto AL, Soini HA, Novotny MV, Gonser RA (2014) Variation in preen oil composition pertaining to season, sex, and genotype in the polymorphic white-throated sparrow. J Chem Ecol 40:1025–1038CrossRefGoogle Scholar
  42. Whittaker DJ, Soini HA, Atwell JW, Hollars C, Novotny MV, Ketterson ED (2010) Songbird chemosignals: volatile compounds in preen gland secretions vary among individuals, sexes, and populations. Behav Ecol 21:608–614.  https://doi.org/10.1093/beheco/arq033 CrossRefGoogle Scholar
  43. Whittaker DJ, Richmond KM, Miller AK, Kiley R, Bergeon Burns C, Atwell JW, Ketterson ED (2011) Intraspecific preen oil odor preferences in dark-eyed juncos (Junco hyemalis). Behav Ecol 22:1256–1263.  https://doi.org/10.1093/beheco/arr122 CrossRefGoogle Scholar
  44. Zhang J-X, Wei W, Zhang J-H, Yang W-H (2010) Uropygial gland-secreted alkanols contribute to olfactory sex signals in budgerigars. Chem Senses 35:375–382CrossRefGoogle Scholar
  45. Zink RM, Dittmann DL (1993) Gene flow, refugia, and evolution of geographic variation in the song sparrow (Melospiza melodia). Evolution 47:717–729CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyThe University of Western OntarioLondonCanada

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