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Male Great Tits (Parus major) adjust dear enemy effect expression in different breeding stages

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Abstract

Many territorial animals are less aggressive towards neighbours than to strangers, a phenomenon known as the ‘dear enemy effect’. However, there has been little research on changes in this behaviour in songbirds across the breeding season. In this study, we followed changes in the dear enemy effect during the breeding season in Great Tits, Parus major. We simulated neighbour and stranger intrusions at three breeding stages corresponding to key ecological and social situations, egg-laying, incubation and nestling stages, and examined the territorial songs and physical responses of territory owners. Our results suggest that neighbours are dear enemies in the egg-laying and incubation stages, when territories are stable, but not at the nestling stage when territories become unstable. In addition, physical responses were more effective as warning signals than territorial songs when dear enemy effects were expressed. We conclude that the dear enemy effect is expressed flexibly, rather than in a fixed way, by territorial male Great Tits in our study area.

Zusammenfassung

Männliche Kohlmeisen (Parus major) stimmen die Ausprägung des „Lieber-Feind-Effekts“ auf das Brutstadium ab

Viele territoriale Tiere sind gegenüber Nachbarn weniger aggressiv als gegenüber fremden Artgenossen, ein Phänomen, das als „Lieber-Feind-Effekt“ bekannt ist. Allerdings haben nur wenige Studien untersucht, inwieweit sich dieser Effekt im Laufe der Brutsaison verändert. In der vorliegenden Studie haben wir Veränderungen im „Lieber-Feind-Effekt“ im Laufe der Brutsaison bei Kohlmeisen, Parus major, untersucht. Wir haben das Eindringen von Nachbarn und fremden Tieren ins Revier simuliert, in drei verschiedenen Brutstadien, die entscheidenden ökologischen und sozialen Situationen entsprechen, nämlich Lege-, Bebrütungs- und Nestlingsstadium, und haben die Reviergesänge und körperlichen Antworten von Revierinhabern untersucht. Unsere Ergebnisse deuten darauf hin, dass Nachbarn während des Lege- und Bebrütungsstadiums, wenn die Reviergrenzen stabil sind, als „liebe Feinde“ betrachtet werden, nicht jedoch während des Nestlingsstadiums, wenn die Reviergrenzen instabil werden. Außerdem waren körperliche Antworten effektivere Warnsignale als Reviergesänge, wenn der „Lieber-Feind-Effekt“ zum Ausdruck gebracht wurde. Wir schlussfolgern, dass bei territorialen männlichen Kohlmeisen in unserem Untersuchungsgebiet der „Lieber-Feind-Effekt“ flexibel und nicht starr ausgeprägt ist.

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References

  • Akçay Ç, Searcy WA, Campbell SE, Reed VA, Templeton CN, Hardwick KM, Beecher MD (2011) Who initiates extrapair mating in song sparrows? Behav Ecol 23:44–50

    Google Scholar 

  • Akçay Ç, Swift RJ, Reed VA, Dickinson JL (2013) Vocal kin recognition in kin neighborhoods of western bluebirds. Behav Ecol 24:898–905

    Google Scholar 

  • Akçay Ç, Anderson RC, Nowicki S, Beecher MD, Searcy WA (2015) Quiet threats: soft song as an aggressive signal in birds. Anim Behav 105:267–274

    Google Scholar 

  • Amy M, Sprau P, de Goede P, Naguib M (2010) Effects of personality on territory defence in communication networks: a playback experiment with radio-tagged great tits. P Roy Soc B Bio 277:3685–3692

    Google Scholar 

  • Baker TM, Wilson DR, Mennill DJ (2012) Vocal signals predict attack during aggressive interactions in black-capped chickadees. Anim Behav 84:965–974

    Google Scholar 

  • Baldassarre DT, Greig EI, Webster MS (2016) The couple that sings together stays together: duetting, aggression and extra-pair paternity in a promiscuous bird species. Biol Lett 12:20151025

    PubMed  PubMed Central  Google Scholar 

  • Bee MA (2003) A test of the" dear enemy effect" in the strawberry dart-poison frog (Dendrobates pumilio). Behav Ecol Sociobiol 54:601–610

    Google Scholar 

  • Beletsky LD, Orians GH (1989) Familiar neighbors enhance breeding success in birds. P Nati Acad Sci USA 86:7933–7936

    CAS  Google Scholar 

  • Blakey JK (1994) Genetic evidence for extra-pair fertilizations in a monogamous passerine, the great tit Parus major. Ibis 136:457–462

    Google Scholar 

  • Booksmythe I, Jennions MD, Backwell PR (2010) Investigating the ‘dear enemy’ phenomenon in the territory defence of the fiddler crab, Uca mjoebergi. Anim Behav 79:419–423

    Google Scholar 

  • Boucaud ICA, ValÈre PA, Aguirre Smith MLN, Doligez B, Cauchard L, Rybak F, Vignal C (2016) Interactive vocal communication at the nest by parent great tits Parus major. Ibis 158:630–644

    Google Scholar 

  • Bradley DW, Mennill DJ (2009) Strong ungraded responses to playback of solos, duets and choruses in a cooperatively breeding Neotropical songbird. Anim Behav 77:1321–1327

    Google Scholar 

  • Briefer E, Rybak F, Aubin T (2008) When to be a dear enemy: flexible acoustic relationships of neighbouring skylarks, Alauda arvensis. Anim Behav 76:1319–1325

    Google Scholar 

  • Brun J, Epplen J, Strohbach S, Lubjuhn T, Gerken T (1999) Extra-pair paternity in great tits (Parus major)-a long term study. Behaviour 136:1157–1172

    Google Scholar 

  • Budka M, Osiejuk TS (2014) Individually specific call feature is not used to neighbour-stranger discrimination: the corncrake case. PLoS ONE 9:e104031

    PubMed  PubMed Central  Google Scholar 

  • Camfield AF (2006) Resource value affects territorial defense by broad-tailed and rufous hummingbirds. J Field Ornithol 77:120–125

    Google Scholar 

  • Christensen C, Radford AN (2018) Dear enemies or nasty neighbors? Causes and consequences of variation in the responses of group-living species to territorial intrusions. Behav Ecol 29:1004–1013

    Google Scholar 

  • Courvoisier H, Camacho-Schlenker S, Aubin T (2014) When neighbours are not 'dear enemies' a study in the winter wren, Troglodytes troglodytes. Anim Behav 90:229–235

    Google Scholar 

  • Cramp S, Perrins CM (1993) Parus major Great tit. Handbook of the birds of europe, the middle east and north africa: the birds of the Western Palearctic. Oxford Univsity Press, Oxford, pp 255–281

    Google Scholar 

  • Demko AD, Mennill DJ (2018) Male and female signaling behavior varies seasonally during territorial interactions in a tropical songbird. Behav Ecol Sociobiol 72:1–13

    Google Scholar 

  • Eliassen S, Jørgensen C (2014) Extra-pair mating and evolution of cooperative neighbourhoods. PLoS ONE 9:e99878

    PubMed  PubMed Central  Google Scholar 

  • Fisher J (1954) Evolution and bird sociality. In: Huxley J, Hardy AC, Ford EB (eds) Evolution as a Process. Allen & Unwin, London, pp 71–83

    Google Scholar 

  • Fogo BR, Sanches FHC, Costa TM (2019) Testing the dear enemy relationship in fiddler crabs: is there a difference between fighting conspecific and heterospecific opponents? Behav Process 162:90–96

    Google Scholar 

  • Getty T (1987) Dear enemies and the prisoner's dilemma: why should territorial neighbors form defensive coalitions? Am Zool 27:327–336

    Google Scholar 

  • Getty T (1989) Are dear enemies in a war of attrition? Anim Behav 37:337–339

    Google Scholar 

  • Godard R (1993) Tit for tat among neighboring hooded warblers. Behav Ecol Sociobiol 33:45–50

    Google Scholar 

  • Gong Y, Qin B, Qin YF, Sun W, Wang HT (2020) Playback of male song advanced onset of nest building but not initial egg date or breeding synchrony in the great tit Parus major. J Ornithol 161:585–588

    Google Scholar 

  • Gorissen L, Gorissen M, Eens M (2006) Heterospecific song matching in two closely related songbirds (Parus major and P. caeruleus): great tits match blue tits but not vice versa. Behav Ecol Sociobiol 60:260–269

    Google Scholar 

  • Grabowska-Zhang AM, Sheldon BC, Hinde CA (2012) Long-term familiarity promotes joining in neighbour nest defence. Biol Lett 8:544–546

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gullberg A, Tegelstrom H, Gelter HP (1992) DNA fingerprinting reveals multiple paternity in families of great and blue tits (Parus major and P. caeruleus). Hereditas 117:103–108

    Google Scholar 

  • Hill SD, Brunton DH, Anderson MG, Ji W (2018) Fighting talk: complex song elicits more aggressive responses in a vocally complex songbird. Ibis 160:257–268

    Google Scholar 

  • Itzkowitz M, Leiser J (1999) The benefits of dear enemy recognition in three-contender convict cichlid (Cichlasoma nigrofasciatum) contests. Behaviour 136:983–1003

    Google Scholar 

  • Kerbs JR (1971) Territory and breeding density in the great tit, Parus major L. Ecology 52:2–22

    Google Scholar 

  • Kolesnikova Y, Liu M, Kang Z, Opaev A (2019) Song does not function as a signal of direct aggression in two Leaf-warbler species. Ornithol Sci 18:17–26

    Google Scholar 

  • Lachish S, Goldizen AW (2004) Responses to neighbours and non-neighbours in the buff-banded rail (Gallirallus philippensis): no dear-enemy relationships. Aust J Zool 52:369–378

    Google Scholar 

  • Lesbarrèresa D, Lodé T (2002) Variations in male calls and responses to an unfamiliar advertisement call in a territorial breeding anuran, Rana dalmatina: evidence for a "dear enemy" effect. Ethol Ecol Evol 14:287–295

    Google Scholar 

  • López JS-L, Gómez JMG, Mennill DJ (2016) Divergence in mating signals correlates with genetic distance and behavioural responses to playback. J Evol Biol 29:306–318

    Google Scholar 

  • Losin N, Drury JP, Peiman KS, Storch C, Grether GF (2016) The ecological and evolutionary stability of interspecific territoriality. Ecol Lett 19:260–267

    PubMed  Google Scholar 

  • Lovell SF, Lein MR (2004) Neighbor-stranger discrimination by song in a suboscine bird, the alder flycatcher, Empidonax alnorum. Behav Ecol 15:799–804

    Google Scholar 

  • Maciej P, Patzelt A, Ndao I, Hammerschmidt K, Fischer J (2013) Social monitoring in a multilevel society: a playback study with male Guinea baboons. Behav Ecol Sociobiol 67:61–68

    PubMed  Google Scholar 

  • McGregor PK, Avery MI (1986) The unsung songs of great tits (Parus major): learning neighbours' songs for discrimination. Behav Ecol Sociobiol 18:311–316

    Google Scholar 

  • Moser-Purdy C, Mennill DJ (2016) Large vocal repertoires do not constrain the dear enemy effect: a playback experiment and comparative study of songbirds. Anim Behav 118:55–64

    Google Scholar 

  • Moser-Purdy C, MacDougall-Shackleton EA, Mennill DJ (2017) Enemies are not always dear: male song sparrows adjust dear enemy effect expression in response to female fertility. Anim Behav 126:17–22

    Google Scholar 

  • Müller CA, Manser MB (2007) 'Nasty neighbours' rather than 'dear enemies' in a social carnivore. P Roy Soc B Bio 274:959–965

    Google Scholar 

  • Naguib M, Kazek A, Schaper SV, Van Oers K, Visser ME (2010) Singing activity reveals personality traits in great tits. Ethology 116:763–769

    Google Scholar 

  • Newey PS, Robson SKA, Crozier RH (2010) Weaver ants Oecophylla smaragdina encounter nasty neighbors rather than dear enemies. Ecology 91:2366–2372

    PubMed  Google Scholar 

  • Osborne L (2005) Rival recognition in the territorial tawny dragon (Ctenophorus decresii). Acta Ethol 8:45–50

    Google Scholar 

  • Peake T, Terry AMR, McGregor PK, Dabelsteen T (2001) Male great tits eavesdrop on simulated male–to–male vocal interactions. P Roy Soc Lond B Bio 268:1183–1187

    CAS  Google Scholar 

  • Perneger TV (1998) What's wrong with Bonferroni adjustments. Brit Med J 316:1236–1238

    CAS  PubMed  Google Scholar 

  • Pratt AE, McLain DK (2006) How dear is my enemy: intruder-resident and resident-resident encounters in male sand fiddler crabs (Uca pugilator). Behaviour 143:597–617

    Google Scholar 

  • Ritschard M, van Oers K, Naguib M, Brumm H (2012) Song amplitude of rival males modulates the territorial behaviour of great tits during the fertile period of their mates. Ethology 118:197–202

    Google Scholar 

  • Rosell F, Bjørkøyli T (2002) A test of the dear enemy phenomenon in the Eurasian beaver. Anim Behav 63:1073–1078

    Google Scholar 

  • Sandoval L (2011) Male–male vocal interactions in a territorial neotropical quail: which song characteristics predict a territorial male's response? Behaviour 148:1103–1120

    Google Scholar 

  • Searcy WA, Akçay C, Nowicki S, Beecher MD (2014) Aggressive signaling in song sparrows and other songbirds. In: Naguib M, Barrett L, Brockmann HJ, et al. (eds) Advances in the study of behavior. Academic Press, Burlington, pp 89–125

    Google Scholar 

  • Siracusa ER, Boutin S, Dantzer B, Lane JE, Coltman DW, McAdam AG (2019) Familiar neighbors, but not relatives, enhance fitness in a territorial mammal. bioRxiv.https://doi.org/10.1101/589002:589002

  • Slagsvold T, Dale S, SÆTRE G-P (1994) Dawn singing in the great tit (Parus major): mate attraction, mate guarding, or territorial defence? Behaviour 131:115–138

    Google Scholar 

  • Snijders L, van der Eijk J, van Rooij EP, De Goede P, van Oers K, Naguib M (2015) Song trait similarity in great tits varies with social structure. PLoS ONE 10:e0116881

    PubMed  PubMed Central  Google Scholar 

  • Stoddard PK (1996) Vocal recognition in territorial passerines. In: Kroodsma DE, Miller EH (eds) Ecology and evolution of acoustic communication in birds. Cornell Univ Press, Ithaca, pp 356–374

    Google Scholar 

  • Strohbach S, Curio E, Bathen A, Epplen J, Lubjuhn T (1998) Extrapair paternity in the great tit (Parus major): a test of the "good genes" hypothesis. Behav Ecol 9:388–396

    Google Scholar 

  • Szymkowiak J, Kuczyński L (2017) Song rate as a signal of male aggressiveness during territorial contests in the wood warbler. J Avian Biol 48:275–283

    Google Scholar 

  • Temeles EJ (1989) The effect of prey consumption on territorial defense by harriers: differential responses to neighbors versus floaters. Behav Ecol Sociobiol 24:239–243

    Google Scholar 

  • Temeles EJ (1994) The role of neighbours in territorial systems: when are they 'dear enemies'? Anim Behav 47:339–350

    Google Scholar 

  • Wei M, Lloyd H, Zhang Y (2011) Neighbour-stranger discrimination by yellow-bellied Tit Parus venustulus: evidence for the "dear-enemy" effect. J Ornithol 152:431–438

    Google Scholar 

  • Wilson EO (1975) Sociobiology: the new synthe sis. Harvard Univ. Press, Cambridge

    Google Scholar 

  • Wood WE, Yezerinac SM (2006) Song sparrow (Melospiza melodia) song varies with urban noise. Auk 123:650–659

    Google Scholar 

  • Yoon J, Sillett TS, Morrison SA, Ghalambor CK (2012) Breeding density, not life history, predicts interpopulation differences in territorial aggression in a passerine bird. Anim Behav 84:515–521

    Google Scholar 

  • You YY et al (2009) Variation in egg size and nestling growth rate in relation to clutch size and laying sequence in great tits Parus major. Prog Nat Sci 19:427–433

    Google Scholar 

  • Zollinger SA, Slater PJB, Nemeth E, Brumm H (2017) Higher songs of city birds may not be an individual response to noise. P Roy Soc B Bio 284:20170602

    Google Scholar 

  • Zwart MC, Dunn JC, McGowan PJK, Whittingham MJ (2015) Wind farm noise suppresses territorial defense behavior in a songbird. Behav Ecol 27:101–108

    Google Scholar 

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Acknowledgements

This research was supported by the National Natural Science Foundation of China (Grant Nos. 31570390, 31770419), and a project funded by China Postdoctoral Science Foundation (2018M631854). We thank Hongwei Xu and Yusheng Wei for their invaluable field assistance. We thank Harry Taylor, PhD, from Liwen Bianji, Edanz Editing China (https://www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

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  1. Jilin Engineering Laboratory for Avian Ecology and Conservation Genetics, School of Life Sciences, Northeast Normal University, 5268 Renmin Street, Changchun, China

    Longru Jin, Jingnan Liang, Qianxi Fan, Jiangping Yu & Haitao Wang

  2. Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University, 2555 Jingyue Street, Changchun, China

    Longru Jin, Jingnan Liang, Qianxi Fan, Jiangping Yu, Keping Sun & Haitao Wang

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  1. Longru Jin
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Jin, L., Liang, J., Fan, Q. et al. Male Great Tits (Parus major) adjust dear enemy effect expression in different breeding stages. J Ornithol 162, 221–229 (2021). https://doi.org/10.1007/s10336-020-01815-3

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