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 Abstract 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: 4 S. Campagna et al. reproductive season (Jacob et al. 1979). Furthermore, the sexual behavior of male domestic ducks (Anas platyrhynchos) was significantly disrupted when the birds were rendered anosmic through cutting their olfactory nerves, whereas neither their aggressive behaviors nor their plasma levels of pituitary–gonadal hormones were affected (Balthazart and Schoffeniels 1979). Following this early study, the role of avian olfaction was examined in different social contexts such as territoriality, parent-offspring recognition, environmental familiarity, and species recognition (Jones and Roper 1997; Roper 1999; Hagelin 2007; Hagelin and Jones 2007; Rajchard 2007, 2010; Balthazart and Taziaux 2009). Recent experimental evidence further suggested that olfaction influences mate choice in domestic chickens (Gallus gallus domesticus), in which the female’s uropygial gland appears to act as a source of sexual chemosignals (Hirao et al. 2009). Although the importance of social chemosignaling in some bird taxa is becoming more and more apparent, the exact nature of the chemical cues involved remains largely undocumented. This is probably due to the difficulties of collecting body odor samples and/or extracting volatile molecules from biological samples for chromatographic analyses, as well as adequately processing these data. The exact identification of molecules emitted by avian secretory organs is, however, of critical importance for understanding the role of olfaction in the social life of birds. This review compiles information published in the last 20 years on avian chemical compounds in the form of a database that should prove particularly useful for colleagues, whether theystudy the chemical/chromatographic or behavioral aspects of chemical communication. In this compilation, the names of chemical compounds all use the International Union of Pure and Applied Chemistry (IUPAC) nomenclature to avoid the disparity observed in the literature that might lead to difficulties when comparing species. The most interesting patterns based on behavioral ecology and observed in the lipidic fraction of the uropygial secretion are organized in a separate table (Table 1). Furthermore, to compare data, we bring together details of various methods of the studies that we review (Table 5). 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 rel (...truncated)