Pheromones in birds: myth or reality?

Abstract

Birds are anosmic or at best microsmatic… This misbelief persisted until very recently and has strongly influenced the outcome of communication studies in birds, with olfaction remaining neglected as compared to acoustic and visual channels. However, there is now clear empirical evidence showing that olfaction is perfectly functional in birds and birds use olfactory information in a variety of ethological contexts. Although the existence of pheromones has never been formally demonstrated in this vertebrate class, different groups of birds, such as petrels, auklets and ducks have been shown to produce specific scents that could play a significant role in within-species social interactions. Behavioral experiments have indeed demonstrated that these odors influence the behavior of conspecifics. Additionally, in quail, deprivation of olfactory inputs decreases neuronal activation induced by sexual interactions with a female. It seems therefore well established that birds enjoy a functional sense of smell and a fast growing body of experimental evidence suggests that they use this channel of olfactory communication to control their social life. The unequivocal identification of an avian pheromone is, however, still ahead of us but there are now many exciting opportunities to unravel the behavioral and physiological particularities of chemical communication in birds.

Figure 1

A. Seasonal variation (December to June) of the percentage of male (left) or female (right) domestic ducks synthesizing two types of lipids in their uropygial gland: branched ester waxes and diester axes. Prominent seasonal changes are seen in females but not in males. B. Behavior frequencies recorded during four hours of observations during January in male ducks that had their olfactory nerves sectioned bilaterally (NO-X; black bars) and in control subjects (Ctrl; open bars). A marked decrease in the expression of social displays and sexual behaviors was detected after the nerves section but aggressive behaviors were not affected. Abbreviations: GW: grunt-whistle; HU: head-up tail-up; NG: neck grab; M: mount; COP: copulation; TH: threat; PE: peck; CH: chase. Redrawn from data in Jacob et al. (1979) and Balthazart and Schoffeniels (1979).

Figure 2

Occlusion of the nostrils in Japanese quail (A) does not lead to any significant change in sexual behavior (B) but alters the expression of immediate early gene fos in their brain (C). A. Photographs of the head of a male Japanese quail in which the nostrils were blocked by dental cement (arrow). B. Frequencies (± SEM) of mount attempts and cloacal contact movements recorded during a 10 min test in males that were either used as control (open columns; SEX) or had their nose blocked by dental cement (black columns; SEX/PLUGGED). C. Numbers of Fos-immunoreactive (Fos-ir) cells (±SEM) observed in the caudal medial preoptic area (mPOA) and rostral bed nucleus striae terminalis, medial part (BSTM) of male quail that had been allowed to copulate with a female either in the normal condition (SEX) or after their nose was blocked with dental cement (SEX/PLUGGED). The dotted lines and grey area represent the mean (±SEM) numbers of Fos-ir cells in control birds that stayed in their home cage and were not exposed to a female (Ctrl). Redrawn from data in Taziaux et al. (2008).

Figure 3

A. Percentage of time (mean ± SEM) spent by crested auklets in the arm of a T-maze next to a specific odor cue (black bars) as compared to the control arm containing no odor. A 50% choice (horizontal dashed line) would be expected in the absence of any attraction/repulsion by the odor. Significant preferences are observed for the auklet natural and synthetic odor, but not for biologically irrelevant odors such as amyl acetate (a chemical compound with a smell similar to banana) or mammalian musk. B. Percentage of male or female crested auklets that approached male or female decoys that had been scented or not with artificial scent (mixture of aldehydes) reproducing the tangerine-like odor produced by auklets during the breeding season. Redrawn from data in Hagelin et al. (2003), Jones et al. (2004) and Hagelin (2007b).

Figure 4

Experimental maze used to investigate olfactory orientation towards the burrow in Antarctic prions (A) and results of the choice tests performed in a variety of conditions (B). A. A flexible T-maze was located in front of two burrows and the end of one arm was connected to the entrance of the burrow of the bird being tested while the other arm was connected to the entrance of a neighboring burrow. In control experiments, the same maze was used and placed in front of burrows but the end of each arm was closed so that no olfactory stimulus could be detected in the maze. B. Results of these maze orientation experiments performed in a variety of conditions: birds were either untreated (left) or were made anosmic by injection of zinc sulphate in the olfactory chambers (middle) or were tested in a control situation in which the end of the arms were closed so that olfactory stimuli from the burrows could not enter the maze (right). Black= choice of the correct arm leading to the nest, Light grey= wrong choice (neighbor’s burrow), Dark grey = no choice. Redrawn from data in Bonadonna et al. (2003b).