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Japanese tits nest in tree cavities with a small entrance, and males and females enter the nest one at a time. We noticed that Japanese tits carrying a food item often fluttered their wings in front of their mates when they were also perched near their nest cavity with a food item (Figure 1A and Video S1). We hypothesized that this visual display functions as a gesture that prompts mates to enter the nest first. Following previous animal studies4,6,7, we define gestures as movements of a body part that are expressed in the presence of the target recipient, are goal-directed — i.e., a signaler waits for a response after the signal has been produced — do not act as a direct physical agent and receive a specific response.
4.
Hobaiter, C. ∙ Byrne, R.W.
The meanings of chimpanzee gestures
Curr. Biol. 2014; 24:1596-1600
6.
Pika, S. ∙ Bugnyar, T.
The use of referential gestures in ravens (Corvus corax) in the wild
Nat. Commun. 2011; 2:560
7.
Vail, L. ∙ Manica, A. ∙ Bshary, R.
Referential gestures in fish collaborative hunting
Nat. Commun. 2013; 4:1765
Video S1. Wing-fluttering by a female Japanese tit
First, we observed 321 nest visitations to feed nestlings by male and female Japanese tits that were breeding using nestboxes (16 individuals, 8 pairs). We found that parents adjusted wing-fluttering according to social contexts: they exhibited wing-fluttering when they encountered their mate at the nest site (defined as within five meters of the nestbox) but never when they arrived at the nest site alone (Figure 1B; Generalized Linear Mixed Model: N = 321, Z = 5.35, p < 0.0001). There was a significant effect of sex on wing-fluttering behavior (Figure 1B; N = 321, Z = –2.39, p = 0.017). Six out of 8 females exhibited wing-fluttering, accounting for 14% (24/169) of all nest visitations and 42% (24/57) of nest visitations when accompanied by a mate. In contrast, only one out of eight males displayed wing-fluttering, accounting for 1% (2/152) of all nest visitations and 6% (2/33) of nest visitations when with a mate. In all observed cases (26/26), the tits performed wing-fluttering with their chests facing their mates from a location that should be visible to their mates. In most cases (23/26), they ceased wing-fluttering after their mates had entered the nestbox.
Next, we analyzed the effect of wing-fluttering on the order of nest entry. As most wing-fluttering was observed in females, we focused on nest visitations by females that encountered a male before entering their nestbox (N = 57). When females fluttered their wings, males usually entered their nestbox before the females (Video S2). However, when females did not flutter their wings, they usually entered the nestbox before males (Figure 1C; GLMM: N = 57, Z = 3.50, p = 0.0005). For 23% (13/57) of the visitations, females arrived at the nest site first and stayed on a perch until the male arrived, whereas for 77% (44/57) of the visitations, males arrived at the nest site first. However, the order in which parents arrived at the nest site did not affect the order in which they entered the nest (N = 57, Z = –1.14, p = 0.25).
Video S2. Wing-fluttering by a female Japanese tit prompts a male to enter the nest first
A more detailed analysis revealed that females’ wing-fluttering shortened the latency of males to enter the nest cavity, i.e., the delay between the time when males encountered females at the nest site and the time when the males entered (Figure 1D; Cox mixed-effects model: N = 33, Z = 2.92, p = 0.0035). The order of arrival by males (first arrival: 15/33) and females (first arrival: 18/33) did not have a significant effect on the male’s latency to enter the nest (N = 33, Z = 0.84, p = 0.40). Therefore, females’ wing-fluttering has an independent effect on prompting males to enter the nestbox.
The wing-fluttering behavior of Japanese tits fulfills the criteria of gestures4,6,7, as it is produced in the presence of their mate, ceases after the mate has entered the nestbox, and elicits nest entry without any direct physical contact. Notably, Japanese tits direct this behavior toward their mate, prompting them to enter the nest first, rather than fluttering their wings toward the nest entrance as if indicating its location. Thus, wing-fluttering in Japanese tits is not a deictic gesture that simply directs receivers’ attention to objects, but a symbolic gesture conveying a specific message, such as a request (‘after you’); this classification aligns with that of human gestures1. We observed a clear pattern of females exhibiting wing-fluttering more frequently than males, but its ecological significance remains an intriguing subject for future research.
4.
Hobaiter, C. ∙ Byrne, R.W.
The meanings of chimpanzee gestures
Curr. Biol. 2014; 24:1596-1600
6.
Pika, S. ∙ Bugnyar, T.
The use of referential gestures in ravens (Corvus corax) in the wild
Nat. Commun. 2011; 2:560
7.
Vail, L. ∙ Manica, A. ∙ Bshary, R.
Referential gestures in fish collaborative hunting
Nat. Commun. 2013; 4:1765
1.
Goodwyn, S.W. ∙ Acredolo, L.P. ∙ Brown, C.A.
Impact of symbolic gesturing on early language development
J. Nonverbal Behav. 2000; 24:81-103
While previous studies have shown that many birds use various wing displays in interactions between two individuals, such as courtship2, our findings indicate that Japanese tits can use wing-fluttering not only as a symbolic gesture but also in a triadic context involving a signaler, a recipient, and a specific goal (i.e., nest entry) — a prominent feature of human communication8. In addition, Japanese tits have evolved a variety of call types and use them to indicate external referents (e.g., predator types)9 and to create compositional messages10. Further comparative studies may elucidate how cognitive mechanisms underlying visual and vocal communication have co-evolved in birds, which may shed new light on theories of language evolution.
2.
Bradbury, J.W. ∙ Vehrencamp, S.L.
Principles of Animal Communication
Sinauer Associates, Inc., Sunderland, MA, 2011
8.
Tomasello, M.
Origins of Human Communication
MIT Press, Cambridge, MA, 2010
9.
Suzuki, T.N.
Alarm calls evoke a visual search image of a predator in birds
Proc. Natl. Acad. Sci. USA. 2018; 115:1541-1545
10.
Suzuki, T.N. ∙ Matsumoto, Y.K.
Experimental evidence for core-Merge in the vocal communication system of a wild passerine
Nat. Commun. 2022; 13:5605
Acknowledgments
We are grateful to Nora V. Carlson, Yui K. Matsumoto, and three anonymous reviewers for their comments on the manuscript. This work was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI (Grant Number JP20H03325 to T.N.S.) and the Japan Science and Technology Agency (JST) FOREST Program (Grant Number JPMJFR2149 to T.N.S.).
Author contributions
T.N.S. designed research and wrote the paper; T.N.S. and N.S. performed research and analyzed data.
Declaration of interests
The authors declare no competing interests.
Data availability
The dataset and R codes used in this study have been deposited at Mendeley Data doi: 10.17632/256z7k654k.1.
Supplemental information (1)
Document S1. Experimental procedures
References
Goodwyn, S.W. ∙ Acredolo, L.P. ∙ Brown, C.A.
Impact of symbolic gesturing on early language development
J. Nonverbal Behav. 2000; 24:81-103
Bradbury, J.W. ∙ Vehrencamp, S.L.
Principles of Animal Communication
Sinauer Associates, Inc., Sunderland, MA, 2011
Kaplan, G.
Pointing gesture in a bird- merely instrumental or a cognitively complex behavior?
Curr. Zool. 2011; 57:453-467
Pika, S. ∙ Bugnyar, T.
The use of referential gestures in ravens (Corvus corax) in the wild
Nat. Commun. 2011; 2:560
Vail, L. ∙ Manica, A. ∙ Bshary, R.
Referential gestures in fish collaborative hunting
Nat. Commun. 2013; 4:1765
Suzuki, T.N.
Alarm calls evoke a visual search image of a predator in birds
Proc. Natl. Acad. Sci. USA. 2018; 115:1541-1545
Suzuki, T.N. ∙ Matsumoto, Y.K.
Experimental evidence for core-Merge in the vocal communication system of a wild passerine
Nat. Commun. 2022; 13:5605
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Document S1. Experimental procedures
