Pigeon odor varies with experimental exposure to trace metal pollution
Trace metals are chemical pollutants that have well-known noxious effects on wildlife and that are current major environmental issues in urban habitats. Previous studies have demonstrated their negative (e.g. lead) or positive (e.g. zinc) effects on body condition, immunity and reproductive success. Because of their effects on condition, trace metals are likely to influence the production of condition-dependent ornaments. The last decade has revealed that bird odors, like mammal odors, can convey information on individual quality and might be used as secondary sexual ornaments. Here, we used solid-phase microextraction headspace sampling with gas chromatography—mass spectrometry to investigate whether plumage scent varied with experimental supplementation in lead and/or zinc in feral pigeons. Zinc supplementation (alone or in combination with lead) changed the proportion of several volatiles, including an increase in the proportion of hydroxy-esters. The production of these esters, that most likely originate from preen gland secretions, may be costly and might thus be reduced by stress induced by zinc deficiency. Although lead is known to negatively impact pigeon condition, it did not statistically affect feather scent, despite most of the volatiles that increased with zinc exposure tended to be decreased in lead-supplemented pigeons. Further studies should evaluate the functions of plumage volatiles to predict how trace metals can impact bird fitness.
KeywordsScent Zinc Lead Birds Dove
We thank the “Mairie de Paris” (Thomas Charachon) for allowing the capture of birds and the Centre de Recherche en Ecologie Experimentale et Predictive (CEREEP) which provided logistic support for the field work of this study. We are very thankful to T. Gayet, S. Pollet, S. Hasnaoui, F. Lorente, S. Perret and B. Decenciere for their help in field work.
This work was financed by grants from the local government (Ile-de-France: Sustainable Development Network R2DS, No. 2012–11 to JG), and from the “Agence Nationale de la Recherche” (No. ANR-13-PDOC-0002 to SL).
Compliance with ethical standards
All experiments were carried out in strict accordance with the recommendations of the “European Convention for the Protection of vertebrate Animals used for Experimental and Other Scientific Purposes” and were conducted under the authorizations of the “Ministère de l’éducation nationale, de l’enseignement supérieur et de la recherche” (authorization N_00093.02) and the “Direction Departementale des Services Veterinaires de Seine-et-Marne” (authorization N_ 77-05).
Conflict of interest
The authors declare that they have no conflict of interest.
- Borges LMF, de Oliveira Filho JG, Ferreira LL, Louly CCB, Pickett JA, Birkett MA (2015) Identification of non-host semiochemicals for the brown dog tick, Rhipicephalus sanguineus sensu lato (Acari: Ixodidae), from tick-resistant beagles, Canis lupus familiaris. Ticks Tick-borne Dis 6:676–682CrossRefGoogle Scholar
- Chatelain M, Gasparini J, Jacquin L, Frantz A (2014) The adaptive function of melanin-based plumage coloration to trace metals. Biol Lett 10 https://doi.org/10.1098/rsbl.2014.0164
- Chatelain M, Pessato A, Frantz A, Gasparini J, Leclaire S (2017) Do trace metals influence visual signals? Effects of trace metals on iridescent and melanic feather colouration in the feral pigeon. OikosGoogle Scholar
- Datnoff LE, Elmer WH, Huber DM (2007) Mineral nutrition and plant disease. American Phytopathological Society (APS Press), St Paul, USAGoogle Scholar
- Demayo A, Taylor MC, Taylor KW, Hodson PV, Hammond PB (1982) Toxic effects of lead and lead compounds on human health, aquatic life, wildlife plants, and livestock. Crit Rev Environ Sci Technol 12:257–305Google Scholar
- Gabirot M, Buatois B, Müller CT, Bonadonna F (2018) Odour of King Penguin feathers analysed using direct thermal desorption discriminates between individuals but not sexes. IbisGoogle Scholar
- Goodwin TE et al. (2016) The role of bacteria in chemical signals of elephant musth: Proximate causes and biochemical pathways. In: Schulte BA (ed) Chemical signals in vertebrates 13. Springer, Cham, pp 63–85Google Scholar
- Goutte A et al. (2014) Demographic consequences of heavy metals and persistent organic pollutants in a vulnerable long-lived bird, the wandering albatross. Proc R Soc Lond B: Biol Sci 281:20133313Google Scholar
- Leclaire S, Merkling T, Raynaud C, Giacinti G, Bessière JM, Hatch SA, Danchin E (2011) An individual and a sex odor signature in kittiwakes? Study of the semiochemical composition of preen secretion and preen down feathers. Naturwissenschaften 98:615–624. https://doi.org/10.1016/j.yhbeh.2008.07.002 CrossRefGoogle Scholar
- Leclaire S, Pierret P, Chatelain M, Gasparini J (2014a) Feather bacterial load affects plumage condition, iridescent color, and investment in preening in pigeons. Behav Ecol: aru109, 25:1192–1198Google Scholar
- Leclaire S, Strandh M, Mardon J, Westerdahl H, Bonadonna F (2017) Odour-based discrimination of similarity at the major histocompatibility complex in birds. In: Proc. R. Soc. B, vol 1846. The Royal Society, p 20162466Google Scholar
- Leclaire S et al. (2014b) Preen secretions encode information on MHC similarity in certain sex-dyads in a monogamous seabird. Sci Rep 4:6920Google Scholar
- McGraw KJ, Mackillop EA, Dale J, Hauber ME (2002) Different colors reveal different information: how nutritional stress affects the expression of melanin-and structurally based ornamental plumage. J Exp Biol 205:3747–3755Google Scholar
- Oksanen J et al. (2013) Package ‘vegan’ Community ecology package, version 2Google Scholar
- Oteiza PI, Olin KL, Fraga CG, Keen CL (1995) Zinc deficiency causes oxidative damage to proteins, lipids and DNA in rat testes. J Nutr 125:823Google Scholar
- Papanikolaou NC, Hatzidaki EG, Belivanis S, Tzanakakis GN, Tsatsakis AM (2005) Lead toxicity update. A brief review. Med Sci Monit 11:RA329–RA336Google Scholar
- R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
- Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. In: Luch A (ed) Molecular, clinical and environmental toxicology. Springer, Basel pp 133–164Google Scholar
- Troïanowski M, Mondy N, Dumet A, Arcanjo C, Lengagne T (2017) Effects of traffic noise on tree frog stress levels, immunity, and color signaling. Conserv BiolGoogle Scholar
- von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition–dependent sexual signals. Proc R Soc Lond B: Biol Sci 266:1–12Google Scholar
- Wallraff HG (2005) Avian navigation: pigeon homing as a paradigm. Springer Science & Business Media, BerlinGoogle Scholar
- Whittaker DJ, Rosvall KA, Slowinski SP, Soini HA, Novotny MV, Ketterson ED (2017) Songbird chemical signals reflect uropygial gland androgen sensitivity and predict aggression: implications for the role of the periphery in chemosignaling. J Comparative Physiol A:1–11Google Scholar
- Whittaker DJ, Theis KR (2016) Bacterial communities associated with junco preen glands: Preliminary ramifications for chemical signaling. In: Schulte BA, Goodwin TE, Ferkin MH (eds) Chemical Signals in Vertebrates 13. Springer International Publishing, Cham, pp 105–117 https://doi.org/10.1007/978-3-319-22026-0_8CrossRefGoogle Scholar
- Wyatt TD (2014) Pheromones and animal behavior: chemical signals and signatures. Cambridge University Press, CambridgeGoogle Scholar
- Zahavi A, Zahavi A (1999) The handicap principle: a missing piece of Darwin’s puzzle. Oxford University Press, OxfordGoogle Scholar
- Zhang J-X, Sun L, Zuo M (2009) Uropygial gland volatiles may code for olfactory information about sex, individual, and species in Bengalese finches Lonchura striata. Curr Zool 55:357–365Google Scholar