Introduction
Plants attacked by herbivorous arthropods release volatiles (herbivore-induced plant volatiles, HIPVs) that might be used by natural enemies of the herbivores to locate prey or host (Dicke et al. 1990, Vet & Dicke 1992, Takabayashi & Dicke 1996, Dicke et al. 2009, Dicke 2015). The HIPVs that plants release in response to herbivory vary with the plant and insect species (De Moraes et al. 1998, Dicke et al. 1998, Mumm & Dicke 2010, Hare 2011), and the herbivore density (Girling et al. 2011, Pisani Gareau et al. 2013, Cai et al. 2014). For many predators, it remains unknown whether the ability to find the prey with the aid of olfactory signals is innate or learned. Previous experience was shown to modulate olfactory responses in insects (Vet & Dicke 1992, Steidle & Van Loon 2003), rabbits (Semke et al. 1995) and fish (Nevitt & Dittman 1998). In contrast, use of olfaction in searching for their hosts was shown to be an innate trait in parasitoids (Dicke & van Loon 2000, Dicke 2015). It was not known until 2004 that also birds are attracted to trees infested by defoliator larvae, without the need to see larvae or physical damage they cause to foliage (Mäntylä et al. 2004, Mäntylä et al. 2008, Mäntylä et al. 2016, 2020). The mechanism of use of olfactory signals by birds searching for prey were not disentangled until recently (Amoet al. 2013a, Koski et al.2015, but see Koski et al. 2015). Rigid experimental work on bird’s innate abilities to recognize odours, or to learn them, is missing.
Reportedly, some bird species need previous experience with volatile compounds before they are able to associate them with a particular food (Sneddon et al. 1998, Mennerat et al. 2005, Gwinner & Berger 2008, Cunningham & Nevitt 2011, Caspers et al. 2013). In contrast, use of olfaction in foraging was shown to be innate in some procellariform bird species (Bonadonnaet al. 2006, Amo et al.2013b). A rare experimental work, with naïve birds exposed to visual and olfactorial signals separately, implied that naïve birds did not show any preference for olfactory signal of herbivore-induced apple saplings compared to olfactory signal of uninfested control saplings (Amo et al. 2016). In contrast, when the naïve birds were allowed to gain some experience with foraging for caterpillars in trees, they exhibited a preference for olfactory signal of caterpillar infested trees (Amoet al. 2013a).
While the innate detection of HIPVs may be under strong selection pressure for specialized species (e.g. parasitoids), generalist predators may need to adapt their foraging behaviour in response to changes in the availability, distribution and abundance of prey species (e.g. Murakami 1998, 2002). Under these circumstances, natural selection may have favoured the ability to adaptively associate different scents with the food resource in order to maximise the foraging effort for different plant and insect species (Royama 1970), rather than having this ability innately (Amo et al. 2016).
To our knowledge, no previous study tested the response of birds to evolutionarily familiar and unfamiliar HIPVs. In our experiment, we aimed to investigate whether the great tits (Parus major ) are able to learn various HIPVs, how quickly, and whether they are able to associate the evolutionarily unfamiliar and familiar plant volatile compounds with prey.