The role of associative learning process on the response of fledgling great tits (Parus major) to mobbing calls

Abstract

When they detect a predator, many species emit antipredator vocalizations. In some cases, they emit mobbing calls, which are associated with the caller approaching and harassing the predator while attracting others to join it. Surprisingly, although mobbing has been widely reported in adults of numerous species, there has been no test of the role of learning in mobbing call recognition, especially during ontogeny. Here, we exposed wild great tit (Parus major) nestlings to playbacks of an unthreatening, novel sound either associated with conspecific mobbing calls (experimental treatment) or with another unthreatening novel sound (control treatment). We then tested them as nestlings and fledglings to see how responses to the novel sound compared to conspecific mobbing calls. Results revealed that fledglings in the experimental treatment behaved similarly to conspecific mobbing calls and the novel sound associated with conspecific mobbing calls. Because mobbing efficiency is often linked to interspecific communication, associative learning should be used by heterospecifics as a mobbing calls recognition mechanism. Regardless of treatment during the nestling phase, fledglings always were sensitive to the playback of conspecific mobbing calls.However, fledglings from the control group were more likely to approach the loudspeaker than those from the experimental group when mobbing calls were played, suggesting that overexposure during the nestling phase altered mobbing learning. Overall, these results suggest that learning could play a role in the recognition of calls, like heterospecific mobbing calls, when paired with conspecific mobbing, and that mobbing is perceived as a threatening stimulus from a very young age.

Great tits (Parus major) adequately respond to both allopatric combinatorial mobbing calls and their isolated parts

“…Tests were carried out between 06:00 and 13:00 hr during calm and dry days. To avoid pseudoreplication, all selected focal birds were distant from one another by at least 100 m (Dutour, Léna, et al., 2019; Dutour et al, 2020). Two or three different calling males were usually detected within 100 m, we never went on the same path twice, and we made sure that no bird was following us.…”

“…Studies about the mechanisms underlying heterospecific communication suggest that both learning and innate processes are in place: associative learning has been evidenced both in the adult response to mobbing calls and in the ontogeny of mobbing behaviour in fledglings (Carlson et al., 2019; Dutour, Léna, et al., 2019; Magrath et al., 2015; Potvin et al., 2018). This could well explain higher responsiveness towards sympatric species than towards allopatric ones (Wheatcroft & Price, 2013).…”

“…Although the use of a combinatory call sequence in eliciting mobbing behaviour of a conspecific receiver has been evidenced in several passerine birds (Dutour et al., 2019; Engesser et al., 2016; Suzuki et al., 2016), until now, little has been done to understand to which extent this process also applies to heterospecific mobbing sequences. Yet, such test may bring information on how birds perceive and deal with combinations and shed light on whether it could be considered semantic compositionality in the human sense (Dutour, Léna, et al., 2019). Semantic compositionality (also termed compositional syntax by some authors) occurs when a combination of words has a meaning emerging from its individual parts (each part having its own meaning), and when the order of such parts is important (Engesser & Townsend, 2019; Suzuki et al., 2019; Zuberbühler, 2019).…”

Social learning of acoustic anti-predator cues occurs between wild bird species

“…if calls are acoustically similar among species [26][27][28]), or learned [24,29], which may occur as early as the embryonic stage in birds [30]. In addition to learning heterospecific alarm calls, recent experimental evidence has shown that birds and mammals can learn to associate unfamiliar acoustic cues with perceived predation risk [14,31,32], adding to a growing body of literature suggesting that associative learning may be the mechanism underpinning the recognition of heterospecific alarm calls. Recent research has also shown that birds can learn to associate novel sounds with heterospecific alarm calls [15], suggesting that a behavioural response to an acoustic cue can be socially transmitted, even when the cue is not initially recognized as an alarm call.…”

Eavesdropping of an African ground squirrel on the heterospecific alarm calls of a noisy ground‐nesting bird

“…The response to alarm calls may be to run to shelter, increase vigilance or mob the potential predator (Dutour et al., 2019; Sherman, 1985), and the ability to respond appropriately to a call can be either innate (e.g., white‐browed scrubwren, Sericornis frontali, Platzen & Magrath, 2004) or learned (e.g., Belding's ground squirrels, Urocitellus beldingi , Mateo & Holmes, 1997). In addition to information gained from conspecific alarm calls, information on potential predators may also be gained by eavesdropping on the signals or cues made by heterospecific individuals (Magrath et al., 2015; Meise et al., 2018).…”