Songbird chemosignals: volatile compounds in preen gland secretions vary among individuals, sexes, and populations

Danielle J. Whittaker 0 2 Helena A. Soini 0 1 Jonathan W. Atwell 0 2 Craig Hollars 0 1 Milos V. Novotny 0 1 Ellen D. Ketterson 0 2 0 The Author 2010. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions , please 1 Institute for Pheromone Research and Department of Chemistry, Indiana University , 800 East Kirkwood Avenue, Bloomington, IN 47405 , USA 2 Department of Biology, Indiana University , 1001 East Third Street, Bloomington, IN 47405 , USA Chemical signaling has been documented in many animals, but its potential importance in avian species, particularly songbirds, has received far less attention. We tested whether volatile compounds in the preen oil of a songbird (Junco hyemalis) contain reliable information about individual identity, sex, or population of origin by repeated sampling from captive male and female juncos originating from 2 recently diverged junco populations in southern California. One of the populations recently colonized an urban environment; the other resides in a species-typical montane environment. The birds were field-caught as juveniles, housed under identical conditions, and fed the same diet for 10 months prior to sampling. We used capillary gas chromatography-mass spectrometry to quantify the relative abundance of 19 volatile compounds previously shown to vary seasonally in this species. We found individual repeatability as well as significant sex and population differences in volatile profiles. The persistence of population differences in a common environment suggests that preen oil chemistry likely has a genetic basis and may thus evolve rapidly in response to environmental change. These finding suggest that songbird preen oil odors have the potential to function as chemosignals associated with mate recognition or reproductive isolation. Key words: birds, chemical communication, Junco hyemalis, olfaction, pheromones. [Behav Ecol 21:608-614 (2010)] - Rplay an important role in reproductive behavior in birds; ecent studies indicate that olfactory communication may most work to date has focused on seabirds of the order Procellariiformes (Bonadonna and Nevitt 2004; Hagelin 2007) and fowl in the order Galliformes (Taziaux et al. 2008; Hirao et al. 2009). These olfactory signals may be transmitted via compounds present in preen oil secreted from the uropygial gland (Hirao et al. 2009). Birds spread this oil onto their plumage where it has been thought to function primarily to protect the feathers from environmental degradation, enhance their insulative capacity, and to ward off ectoparasites such as feather lice (Jacob and Ziswiler 1982; but see Moyer et al. 2003). Preen oil is now known to contain volatile compounds that contribute to an odor (Haribal et al. 2005, 2009; Douglas 2006; Soini et al. 2007). In some species, the odor from this oil may serve to repel predators (Burger et al. 2004; Douglas et al. 2004; Hagelin and Jones 2007). Behavioral studies suggest odor may also be important in intraspecific communication in seabirds (Hagelin et al. 2003; Bonadonna and Nevitt 2004; Hagelin 2007), chickens (Hirao et al. 2009), and even in passerines (Whittaker et al. 2009). Concentrations of volatile compounds in preen oil vary seasonally, perhaps in relation to hormonal status (Piersma et al. 1999; Soini et al. 2007; Douglas et al. 2008), and the compounds themselves differ among species (Haribal et al. 2005, 2009). At least one study has found that seabird odor is variable among individuals and that individual odor is repeatable (Bonadonna et al. 2007). In songbirds, the use of chemical signals is virtually unexplored, although at least one study suggests that songbirds are capable of distinguishing between preen oil odors from conspecifics and heterospecifics (Whittaker et al. 2009). The order Passeriformes is the most speciose group of birds with over 6000 species and displays enormous diversity in visual and auditory signals (Gill 2006), yet only a few studies have addressed interspecific variation in the volatile compounds found in preen oil (Haribal et al. 2005, 2009) or seasonal variation (Soini et al. 2007). No prior study has examined either individual repeatability or intraspecific variation in songbird preen gland secretions. We examined the volatile content of preen oil from a wellstudied songbird, the dark-eyed junco (Junco hyemalis), to evaluate its potential utility as a chemosignal. Volatile compounds in junco preen oil have been previously described and are known to vary with season (day length) and to increase during the breeding season (Soini et al. 2007), suggesting a potential role in reproductive behavior. We asked whether volatile compounds in the preen oil of juncos would meet several of the prescribed criteria for compounds that might serve as reproductive chemosignals (Johansson and Jones 2007); specifically, we tested the hypotheses that they would: 1) be repeatable within an individual (e.g., individuals should have distinct chemical signatures), 2) differ consistently between males and females, and 3) differ among geographically disjunct populations of the same species. We compared preen oil volatile composition between dark-eyed juncos that were originally captured from 2 recently diverged populations in San Diego County, CA, following one populations unique colonization of a novel urban environment. These birds were captured as young juveniles and held in a captive common garden experiment under identical conditions for 10 months prior to sampling. Details of the study system are described below. MATERIALS AND METHODS Study system and sample collection A small number of breeding pairs of Oregon juncos (J. hyemalis thurberi) colonized the University of California, San Diego (UCSD) campus in the early 1980s; since that time this population has remained isolated geographically and genetically, about 70 km from the nearest breeding population with low levels of immigration (Rasner et al. 2004; Yeh and Price 2004). Several morphological and behavioral changes have occurred in this short period of time, including cessation of migration, reduced wing length, reduction of a sexually selected plumage characteristic, shifts in reproductive behavior including a longer breeding season, reduced territorial aggression, and increased exploratory boldness compared with juncos in the presumptive ancestral range (Rasner et al. 2004; Yeh 2004; Yeh and Price 2004; Newman et al. 2006; Yeh et al. 2007; Price et al. 2008; Atwell JW, unpublished data). Data from common garden experiments suggest that changes in plumage traits and exploratory boldness may have a genetic basis (Yeh 2004; Atwell JW, unpublished data). Juncos in this study were originally captured from the UCSD campus (lat 32 40#N, long 117 10#W; elevation 30 m) and the Laguna Mountain Recreation Area in the Cleveland National Forest (lat 32 52#N, long 116 25#W; elevation 1700 m). These (...truncated)