Avian olfaction: a review of the recent literature

Abstract

Birds can smell. Despite early assumptions that birds had little or no sense of smell (Audubon, 1826; Hill, 1905; Stager, 1964), there is now abundant evidence that they are endowed with all the anatomical and neurobiological components necessary for a functional olfactory sense (Balthazart & Taziaux, 2009; Caro, Balthazart, & Bonadonna, 2015), and morphologically the olfactory systems of birds closely resembles those of amphibians, reptiles, and mammals (Kare & Mason, 1986; Wenzel, 1987). Most birds have paired external nares through which they breathe air, internal nasal cavities that contain olfactory epithelium, functional olfactory receptors, and a neuronal connection to the olfactory bulb in the forebrain (Jones & Roper, 1997). Moreover, they have been shown to use odor cues for tasks as diverse as foraging (e.g., Healy & Guilford, 1990; Nevitt, Loosekoot, & Weimerskirch, 2008; Potier, Duriez, Celerier, Liegeois, & Bonadonna, 2019), recognizing eggs (Leclaire, Bourret, & Bonadonna, 2017), selecting nest material (e.g., Gwinner, 2013), and avoiding predation (e.g., Amo, Galvan, Tomás, & Sanz, 2008), as well as in social contexts such as species (e.g., Krause et al., 2014), kin (e.g., Bonadonna & Sanz-Aguilar, 2012; Coffin, Watters, & Mateo, 2011; Krause et al., 2012), and mate recognition (e.g., Bonadonna & Nevitt, 2004). However, we argue that even today there is a tendency for researchers to underappreciate the possible role olfaction plays in birds’ everyday lives. Compelling evidence shows that vision and, to a lesser extent, hearing are the primary avian senses (Martin, 2017). By contrast, few bird species smell noticeably to humans (although there are notable exceptions, such as Crested auklets [Aethia cristatella]; Hagelin, Jones, & Rasmussen, 2003), and they do not typically engage in any overt olfactory behavior, such as sniffing. However, this should not be taken to mean that olfaction is of limited importance to them. To put birds’ sense of smell in perspective, it is useful to provide a comparison with humans. In humans, as in birds, olfaction is commonly considered to be the least acute sense; despite this, it has been estimated that humans with intact olfactory systems can detect (Amoore, 1977) and discriminate (Bushdid, Magnasco, Vosshall, & Keller, 2014) virtually