Songbirds never forget: long-lasting behavioural change triggered by a single playback event

in Behaviour
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Many behavioural studies rely on playback experiments. While it is known that songbirds decrease behavioural responses after short-term repeated stimulation, long-term behavioural changes due to playbacks are unknown. We studied the response to playbacks in a free-living songbird in the long-term, while also studying the repeatability of the behaviour. Locomotor behaviour (a proxy of aggressiveness) decreased one year after first exposure to a single playback. Song response, however, remained consistent, suggesting that these two behaviours may provide different information. Locomotor behaviour was less repeatable than the song response to playback, the latter showing significant between-years repeatability. To the best of our knowledge, our study is the first to report long-term decrease in response to playbacks in a songbird, and that some aspects of the response to playback are repeatable. Similar studies in other species or populations of the great tit are important, to examine the generality of our findings.

Songbirds never forget: long-lasting behavioural change triggered by a single playback event

in Behaviour



AmrheinV.JohannessenL.E.KristiansenL.SlagsvoldT. (2008). Reproductive strategy and singing activity: blue tit and great tit compared. — Behav. Ecol. Sociobiol. 62: 1633-1641. GoedeP.NaguibM. (2010). Effects of personality on territory defence in communication networks: a playback experiment with radio-tagged great tits. — Proc. Roy. Soc. Lond. B: Biol. Sci. 277: 3685-3692.

BellA.M. (2007). Future directions in behavioural syndromes research. — Proc. Roy. Soc. Lond. B: Biol. Sci. 274: 755-761.

BellA.M.HankisonS.J.LaskowskiK.L. (2009). The repeatability of behaviour: a meta-analysis. — Anim. Behav. 77: 771-783.

BoeckleM.BugnyarT. (2012). Long-term memory for affiliates in ravens. — Curr. Biol. 22: 801-806.

ChewS.J.MelloC.NottebohmF.JarvisE.VicarioD.S. (1995). Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain. — Proc. Natl. Acad. Sci. USA 92: 3406-3410.

ConwayC.J. (2011). Standardized North American marsh bird monitoring protocol. — Waterbirds 34: 319-346.

DeeckeV.B.SlaterP.J.B.FordJ.K.B. (2002). Selective habituation shapes acoustic predator recognition in harbour seals. — Nature 420: 171-173.

DongS.ClaytonD.F. (2009). Habituation in songbirds. — Neurobiol. Learn. Mem. 92: 183-188.

DongS.ReplogleK.L.HasadsriL.ImaiB.S.YauP.M.Rodriguez-ZasS.SoutheyB.R.SweedlerJ.V.ClaytonD.F. (2009). Discrete molecular states in the brain accompany changing responses to a vocal signal. — Proc. Natl. Acad. Sci. USA 106: 11364-11369.

DouglasS.B.MennillD.J. (2010). A review of acoustic playback techniques for studying avian vocal duets. — J. Field Ornithol. 81: 115-129.

FallsJ.B. (1992). Playback — a historical-perspective. — In: Playback and studies of animals communication: problems and prospects ( McGregorP.K. ed.). PlenumNew York, NY p.  11-33.

GaramszegiL.Z.CalhimS.DochtermannN.HegyiG.HurdP.L.JorgensenC.KutsukakeN.LajeunesseM.J.PollardK.A.SchielzethH.SymondsM.R.E.NakagawaS. (2009). Changing philosophies and tools for statistical inferences in behavioral ecology. — Behav. Ecol. 20: 1363-1375.

GaramszegiL.Z.EensM.TorokJ. (2008). Birds reveal their personality when singing. — PLoS ONE 3: e2647.

GodardR. (1991). Long-term memory of individual neighbors in a migratory songbird. — Nature 350: 228-229.

HemmiJ.M.MerkleT. (2009). High stimulus specificity characterizes anti-predator habituation under natural conditions. — Proc. Roy. Soc. Lond. B: Biol. Sci. 276: 4381-4388.

KrebsJ.R.AshcroftR.WebberM. (1978). Song repertoires and territory defence in the great tit. — Nature 271: 539-542.

KrebsJ.R. (1976). Habituation and song repertoires in great tit. — Behav. Ecol. Sociobiol. 1: 215-227.

KrebsJ.R.AshcroftR.VanorsdolK. (1981). Song matching in the great tit Parus major L.Anim. Behav. 29: 918-923.

LambrechtsM.M. (1992). Male quality and playback in the great tit. — In: Playback and studies of animals communication: problems and prospects ( McGregorP.K. ed.). PlenumNew York, NY p.  135-152.

LeeW.LeeS.-I.ChoeJ.JablonskiP. (2011). Wild birds recognize individual humans: experiments on magpies, Pica pica. — Anim. Cogn. 14: 817-825.

LessellsC.M.BoagP.T. (1987). Unrepeatable repeatabilities: a common mistake. — Auk 104: 116-121.

LeveyD.J.LondonoG.A.Ungvari-MartinJ.HiersouxM.R.JankowskiJ.E.PoulsenJ.R.StraceyC.M.RobinsonS.K. (2009). Urban mockingbirds quickly learn to identify individual humans. — Proc. Natl. Acad. Sci. USA 106: 8959-8962.

LinhartP.FuchsR.PolakovaS.SlabbekoornH. (2012). Once bitten twice shy: long-term behavioural changes caused by trapping experience in willow warblers Phylloscopus trochilus. — J. Avian Biol. 43: 186-192.

McGregorP.K.AveryM.I. (1986). The unsung songs of great tits (Parus major) — learning neighbors songs for discrimination. — Behav. Ecol. Sociobiol. 18: 311-316.

McGregorP.K.HornA.G. (1992). Strophe length and response to playback in great tits. — Anim. Behav. 43: 667-676.

McGregorP.K.KrebsJ.R. (1982). Song types in a population of great tits (Parus major) — their distribution, abundance and acquisition by individuals. — Behaviour 79: 126-152.

McGregorP.K.KrebsJ.R.PerrinsC.M. (1981). Song repertoires and lifetime reproductive success in the great tit (Parus major). — Am. Nat. 118: 149-159.

NakagawaS.SchielzethH. (2010). Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. — Biol. Rev. 85: 935-956.

PeakeT.M.TerryA.M.R.McGregorP.K.DabelsteenT. (2001). Male great tits eavesdrop on simulated male-to-male vocal interactions. — Proc. Roy. Soc. Lond. B: Biol. Sci. 268: 1183-1187.

PeakeT.M.TerryA.M.R.McGregorP.K.DabelsteenT. (2002). Do great tits assess rivals by combining direct experience with information gathered by eavesdropping?Proc. Roy. Soc. Lond. B: Biol. Sci. 269: 1925-1929.

PeekeH.V.S. (1984). Habituation and the maintenance of territorial boundaries. — In: Habituation sesitization and behavior ( PeekeH.PetrinovichL. eds). Academic PressNew York, NY p.  393-421.

RankinC.H.AbramsT.BarryR.J.BhatnagarS.ClaytonD.F.ColomboJ.CoppolaG.GeyerM.A.GlanzmanD.L.MarslandS.McSweeneyF.K.WilsonD.A.WuC.-F.ThompsonR.F. (2009). Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. — Neurobiol. Learn. Mem. 92: 135-138.

Rivera-GutierrezH.F.PinxtenR.EensM. (2010). Multiple signals for multiple messages: great tit, Parus major, song signals age and survival. — Anim. Behav. 80: 451-459.

Rivera-GutierrezH.F.PinxtenR.EensM. (2011a). Difficulties when assessing birdsong learning programmes under field conditions: a re-evaluation of song repertoire flexibility in the great tit. — PLoS ONE 6: e16003.

Rivera-GutierrezH.F.PinxtenR.EensM. (2011b). Songs differing in consistency elicit differential aggressive response in territorial birds. — Biol. Lett. 7: 339-342.

Rivera-GutierrezH.F.PinxtenR.EensM. (2012). Tuning and fading voices in songbirds: age-dependent changes in two acoustic traits across the life span. — Anim. Behav. 83: 1279-1283.

SearcyW.A.AndersonR.C.NowickiS. (2006). Bird song as a signal of aggressive intent. — Behav. Ecol. Sociobiol. 60: 234-241.

SearcyW.A.BeecherM.D. (2009). Song as an aggressive signal in songbirds. — Anim. Behav. 78: 1281-1292.

SihA.BellA.JohnsonJ.C. (2004). Behavioral syndromes: an ecological and evolutionary overview. — Trends Ecol. Evol. 19: 372-378.

TemelesE.J. (1994). The role of neighbours in territorial systems: when are they ‘dear enemies’?Anim. Behav. 47: 339-350.

TibbettsE.A.DaleJ. (2007). Individual recognition: it is good to be different. — Trends Ecol. Evol. 22: 529-537.

Van DuyseE.PinxtenR.EensM. (2000). Does testosterone affect the trade-off between investment in sexual/territorial behaviour and parental care in male great tits?Behaviour 137: 1503-1515.

YdenbergR.C.GiraldeauL.A.FallsJ.B. (1988). Neighbours, strangers, and the asymmetric war of attrition. — Anim. Behav. 36: 343-347.


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    Spectrographic representation of great tit song. The figure depicts examples of complete strophes of two different song types (a, two notes song type; b, three notes song type), indicating what constitutes a note and a phrase.

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    Behavioural responses during playback tests in two consecutive years for (a) PC locomotor behaviour (number of flights around speaker and closest approach distance) and (b) PC singing behaviour (number of strophes sung in response to the playback and proportion of overlapping strophes). Filled circles represent individuals tested three times (solid line), and unfilled triangles represent individuals that were tested only two times within a season in 2009 (dashed line).

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