Potential Semiochemical Molecules from Birds: A Practical and Comprehensive Compilation of the Last 20 Years Studies

Chem. Senses 37: 3–25, 2012 doi:10.1093/chemse/bjr067 Advance Access publication July 27, 2011 Potential Semiochemical Molecules from Birds: A Practical and Comprehensive Compilation of the Last 20 Years Studies Sylvie Campagna1,2, Jérôme Mardon1, Aurélie Celerier1 and Francesco Bonadonna1 1 CNRS, UMR 5175 CEFE, Behavioral Ecology Group, F-34293 Montpellier, Cedex 5, France and Université de Nimes, F-30021 Nimes Cedex 1, France 2 Correspondence to be sent to: Sylvie Campagna, Behavioral Ecology Group, Centre d’Ecologie Fonctionnelle et Evolutive—CNRS UMR 5175, Montpellier, France. e-mail: Accepted June 27, 2011 During the past 2 decades, considerable progress has been made in the study of bird semiochemistry, and our goal was to review and evaluate this literature with particular emphasis on the volatile organic constituents. Indeed, since the importance of social chemosignaling in birds is becoming more and more apparent, the search for molecules involved in chemical communication is of critical interest. These molecules can be found in different sources that include uropygial gland secretions, feather-surface compounds, and molecules from feces and skin. Although many studies have examined the chemical substances secreted by birds, research on bird chemical communication is still at the start, so new strategies for collecting samples and development of new methods of analysis are urgently required. As a first step, we built a database that brings together potential semiochemicals, using a unique chemical nomenclature for comparing different bird species and also for referencing the different classes of substances that can be found in order to adapt future parameters of analysis. The most important patterns of the wax fraction of preen secretions are highlighted and organized in an ordered table. We also draw up a list of various combinations of sampling and analytical techniques, so that each method can be compared at a glance. Key words: bird olfaction, chemical communication, feathers, feces, uropygial gland Introduction Avian olfactory communication is a poorly explored area of study, although it is now established that most birds possess a fully functional olfactory system. The number and diversity of avian genes coding for olfactory receptors and the presence of a proper olfactory bulb indicate that birds may use their smell more than previously thought (Steiger et al. 2008, 2009). Indeed, birds can use chemical signals from the environment for foraging (Hutchison and Wenzel 1980; Smith and Paselk 1986; Nevitt 2000), navigation (Papi 1991; Wallraff 2001, 2004; Gagliardo et al. 2009, 2011), nest material selection (Clark and Mason 1985, 1987; Clark and Smeraski 1990; Petit et al. 2002; Gwinner and Berger 2008; Mennerat 2008), homing (Minguez 1997; Bonadonna and Bretagnolle 2002; Bonadonna et al. 2003, 2004), and predator avoidance (Amo et al. 2008; Roth et al. 2008). Birds also have scent-producing organs (uropygial gland, cloacal gland, and epidermal cells) that could be involved, at least in some taxa, in social behavior via chemical communication (for review, see: Hagelin 2007). Although birds apparently do not possess vomeronasal receptors, as neither the genes nor pseudogenes for such receptors are found in the chicken genome (Shi and Zhang 2007), they are still able to integrate olfactory information for social and reproductive behaviors. Some pheromonal responses can be mediated by the main olfactory system or possibly the septal organ. For example, some receptors from the main olfactory system have been associated with pheromone detection and belong to the trace-amine associated family of receptors (Liberles and Buck 2006), some members of which are present in the chicken genome (Lagerstrom et al. 2006; Hashiguchi and Nishida 2007; Mueller et al. 2008) and in other birds (Antarctic prion, blue and snow petrel unpublished results). The first study that linked olfaction to social behaviors was carried out in the late 70s on sexual behavior in mallards (Balthazart and Schoffeniels 1979). The role of chemosignals in the sexual behavior of birds was suggested by the difference in the chemical composition of the preen gland secretion between male and female ducks during the ª The Author 2011. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: Abstract 4 S. Campagna et al. Molecules from the uropygial gland The uropygial gland (or preen gland) in birds is located dorsally, above the last vertebrae of the pygostyle. The external morphology (size, shape, and proportions) of this holocrine secretory organ greatly varies among species but is usually relatively constant at the intraspecific level except among the Psittaciformes, Galliformes, and Anseriformes (Jacob and Ziswiler 1982; Johnston 1988). The gland can be completely absent or reduced as in the Struthionidae, Rheidae, Casuariidae, and Dromaiidae; and in a few species of Columbidae and Psittacidae (Johnston 1988). More anatomical and histological informations about this gland are available in other reviews (Haahti et al. 1964; Kolattukudy 1981; Jacob and Ziswiler 1982; Salibian and Montalti 2009). Because the gland produces a large amount of volatile and nonvolatile compounds that are spread on feathers, uropygial secretions are generally considered key sources of avian body scent. Moreover, the important variability of the chemical composition of these secretions across species (Jacob and Ziswiler 1982) suggests that the uropygial gland may be involved in a variety of functions (for review, see: Salibian and Montalti 2009; Rajchard 2010). Large esters The chemical composition of preen waxes from various birds has been extensively reviewed, mainly in the 70’s and 80’s (Haahti et al. 1964; Saito and Gamo 1972, 1973; Kolattukudy 1981; Jacob and Ziswiler 1982). The gland produces a greasy material that is mainly composed of unusual lipids that vary significantly from order to order (Jacob and Ziswiler 1982). Different factors have been shown to influence the content of the fatty acid fraction of the secretions such as age of the birds, that is, sexual maturity (Kolattukudy and Sawaya 1974; Sandilands et al. 2004), breeding stage (Kolattukudy et al. 1987; Piersma et al. 1999; Sinninghe Damste et al. 2000; Reneerkens et al. 2002; Reneerkens, Piersma, et al. 2007), sex (Zhang et al. 2009; Mardon et al. 2010), individuality (Zhang et al. 2009; Mardon et al. 2010), and diet (Thomas et al. 2010). In adult birds, natural esters are made up of an extraordinary mixture of fatty acids and long-chain alcohols. The main components are usually monoester waxes made of fatty acids (nearly always saturated) with different degrees of methyl branching and long-chain monohydroxy fatty alcohols. In some groups of birds, diester waxes containing hydroxy fatty acids and/or alkanediols are also present. Other compounds such as alkanes, triglycerides, free fatty acids, and (...truncated)