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Comparative Study of Aggressive Signaling in Three Closely-Related Warbler Species

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Abstract

Songbirds are known to use several different ways to signal aggression, and even closely-related species can differ in this respect. It is not clear why the variability exists among species. Here, we used playback experiments to compare the vocal behavior of three closely-related songbird species (Phylloscopus omeiensis, P. tephrocephalus and P. valentin) during simulated territorial intrusion. First of all, we analyzed spontaneous singing of each species and found that species differed quantitatively but not qualitatively. P. valentini sang with fewer song types and with more diverse song type sequencing patterns than both P. tephrocephalus and P. omeiensis. Species differed in how much they modified their spontaneous singing while responding to playback. P. valentini males modified singing the most as they increased song type switching rate and tended to sequence song types according to a fixed linear order while responding to playback. P. omeiensis increased song type switching rate, and P. tephrocephalus modified singing the least. We correlated singing in the two contexts (playback vs. spontaneous) both between and within each species. We found that species/males that tended to produce song types according to a fixed sequence and switch after every song type modified their singing less in aggressive contexts (e.g., P. tephrocephalus).

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REFERENCES

  1. Akçay, K., Porsuk, Y.K., Avşar, A., Çabuk, K., and Bilgin, C.C., Song overlapping, noise, and territorial aggression in great tits, Behav. Ecol., 2020, vol. 31, no. 3, pp. 807–814.

    Article  Google Scholar 

  2. Alström, P. and Olsson, U., The golden–spectacled warbler: a complex of sibling species from Sichuan Province, China, Ibis, 1999, vol. 141, pp. 545–568.

    Article  Google Scholar 

  3. Alström, P. and Olsson, U., Golden-spectacled Warbler systematics, Ibis, 2000, vol. 142, pp. 495–500.

    Article  Google Scholar 

  4. Alström, P., Olsson, U., and Lei, F., A review of the recent advances in the systematic of the avian superfamily Sylvioidea, Chin. Birds, 2013, vol. 4, pp. 99–131.

    Article  Google Scholar 

  5. Baker, T., Wilson, D., and Mennill, D., Vocal signals predict attack during aggressive interactions in black-capped chickadees, Anim. Behav., 2012, vol. 84, pp. 965–974.

    Article  Google Scholar 

  6. Bates, D., Maechler, M., Bolker, B., and Walker, S., Fitting linear mixed-effects models using lme4, J. Stat. Soft., 2015, vol. 67, pp. 1–48.

    Article  Google Scholar 

  7. Bhattacharya, H., Cirillo, J., Subba, B.R., and Todt, D., Song performance rules in the oriental magpie robin (Copsychus salauris). Our Nat., 2007, vol. 5, pp. 1–13.

    Google Scholar 

  8. Briefer, E., Osiejuk, T., Rybak, F., and Aubin, T., Are bird song complexity and song sharing shaped by habitat structure? An information theory and statistical approach, J. Theor. Biol., 2010, vol. 262, pp. 151–164.

    Article  PubMed  ADS  Google Scholar 

  9. Burt, J.M. and Beecher, M.D., The social interaction role of song in song sparrow: implication for signal design, Comp. Cong. Behav. Rev., 2008, vol. 3, pp. 86–98.

    Google Scholar 

  10. Byers, E.B. and Kroodsma, E.D., Female mate choice and songbird repertoires, Anim. Behav., 2009, vol. 77, pp. 13–22.

    Article  Google Scholar 

  11. Carlson, N.V., Healy, S.D., and Templeton, C.H., A comparative study of how British tits encode predator threat in their mobbing calls, Anim. Behav., 2017, vol. 125, pp. 77–92.

    Article  Google Scholar 

  12. Catchpole, C.K. and Slater, P.J.B., Bird Song: Biological Themes and Variations, Cambridge: Cambridge Univ. Press, 2008.

    Book  Google Scholar 

  13. Collins, S.A., Is female preference for male repertoires due to sensory bias?, Proc. R. Soc. B, 1999, vol. 266, pp. 2309–2314.

    Article  PubMed Central  Google Scholar 

  14. Collins, S.A., Vocal fighting and flirting: the functions of birdsong, in Nature’s Music: The Science of Birdsong, Marler, P. and Slabbekoorn, H., Eds., Amsterdam: Elsevier Academic Press, 2004, pp. 39–79.

    Google Scholar 

  15. Darolová, A., Krištofik, J., Knauer, F., and Hoi, H., Behavioural response of Eurasian Blackcaps to acoustically simulated conspecific and heterospecific male intruders, J. Ornithol., 2020, vol. 161, pp. 447–458.

    Article  Google Scholar 

  16. Dobson, C.W. and Lemon, R.E., Markov sequences in songs of American thrushes, Behaviour, 1978, vol. 68, pp. 86–104.

    Article  Google Scholar 

  17. Falls, J.B. and D’Agincourt, L.G., Why do meadowlarks switch song types?, Can. J. Zool., 1982, vol. 60, pp. 3400–3408.

    Article  Google Scholar 

  18. Ficken, M.S. and Ficken, R.W., Comparative ethology of the chestnut-sided warbler, yellow warbler, and American redstart, Wilson Bull., 1965, vol. 77, pp. 363–375.

    Google Scholar 

  19. Flower, T.P., Gribble, M., and Ridley, A.R., Deception by flexible alarm mimicry in an African bird, Science, 2014, vol. 344, pp. 513–516.

    Article  CAS  PubMed  ADS  Google Scholar 

  20. Gentner, T., Mechanisms of temporal auditory pattern learning in song birds, Lang. Learn. Dev., 2007, vol. 3, pp. 1–22.

    Article  Google Scholar 

  21. Gil, D. and Slater, P.J.B., Song organization and singing patterns of the willow warbler, Phylloscopus trochilus, Behaviour, 2000, vol. 137, pp. 759–782.

    Article  Google Scholar 

  22. Goretskaia, M.I., Song structure variability in passerine birds: random variation or direct informative changes, Biol. Bull. (Moscow), 2013, vol. 40, pp. 748–759.

    Article  Google Scholar 

  23. Grieves, L.A., Logue, D.M., and Quinn, J.S., Ready to fight: reliable predictors of attack in a cooperatively breeding, non-passerine bird, Ethology, 2015, vol. 121, pp. 1154–1165.

    Article  Google Scholar 

  24. Hammer, Ø., Harper, D.A.T., and Ryan, P.D., PAST—paleontological statistics, 2001. http://www.toyen.uio.no/~ohamm er/past.

  25. Hesler, N., Mundry, R., and Dabelsteen, T., Does song repertoire size in common blackbirds play a role in an intra-sexual context?, J. Ornithol., 2011, vol. 152, pp. 591–601.

    Article  Google Scholar 

  26. Hill, S.D., Brunton, D.H., Anderson, M., and Ji, W., Fighting talk: complex song elicits more aggressive responses in a vocally complex songbird, Ibis, 2018, vol. 160, pp. 257–268.

    Article  Google Scholar 

  27. del Hoyo, J. and Collar, N.J., HBW and BirdLife International Checklist of the Birds of the World, Barcelona: Lynx Edicions, 2016.

    Google Scholar 

  28. Hurlbert, S.H., Pseudoreplication and the design of ecological field experiments, Ecol. Monogr., 1984, vol. 54, pp. 187–211.

    Article  Google Scholar 

  29. Ivanitskii, V.V., Marova, I.M., and Malykh, I.M., Between order and chaos: contrasting syntax in the advertising song of dusky (Phylloscopus fuscatus) and Radde’s (Ph. schwarzi) warblers, J. Ornithol., 2012, vol. 153, pp. 337–346.

    Article  Google Scholar 

  30. Ivanitskii, V.V., Marova, I.M., and Antipov, V.A., Sequential organization in the song of (Luscinia luscinia): clustering and sequential order of the song types, Bioacoustics, 2017, vol. 26, pp. 199–215.

    Article  Google Scholar 

  31. Johansson, U.S., Alström, P., Olsson, U., Ericson, P.G., Sundberg, P., and Price, T.D., Build-up of the Himalayan avifauna through immigration: a biogeographical analysis of the Phylloscopus and Seicercus warblers, Evolution, 2007, vol. 61, pp. 324–333.

    Article  PubMed  Google Scholar 

  32. Kolesnikova, Y., Liu, M., Kang, Z., and Opaev, A., Song does not function as a signal of direct aggression in two leaf-warbler species, Ornithol. Sci., 2019, vol. 18, pp. 17–26.

    Article  Google Scholar 

  33. Krebs, J.R., Habituation and song repertoires in the great tit, Behav. Ecol. Sociobiol., 1976, vol. 1, pp. 215–227.

    Article  Google Scholar 

  34. Krebs, J.R., Song and territory in the great tit, in Evolutionary Ecology, Stonehouse, B. and Perrins, C., Eds., New York: Macmillan, 1977, pp. 47–62.

    Google Scholar 

  35. Krebs, J.R., Ashcroft, R., and Orsdol, K.V., Song matching in the great tit Parus major L., Anim. Behav., 1981, vol. 29, pp. 918–923.

    Article  Google Scholar 

  36. Kroodsma, D.E., Continuity and versatility in bird song: support for the monotony-threshold hypothesis, Nature, 1978, vol. 274, pp. 681–683.

    Article  ADS  Google Scholar 

  37. Kroodsma, D.E., Suggested experimental designs for song playbacks, Anim. Behav., 1989, vol. 37, pp. 600–609.

    Article  Google Scholar 

  38. Kroodsma, D.E. and Verner, J., Complex singing behaviors among Cistothorus wrens, Auk, 1978, vol. 95, pp. 703–716.

    Google Scholar 

  39. Kroodsma, D.E., Byers, B.E. Goodale, E., Johnson, S., and Lui, W.-C., Pseudoreplication in playback experiments, revisited a decade later, Anim. Behav., 2001, vol. 61, pp. 1029–1033.

    Article  Google Scholar 

  40. Kuznetsova, A., Brockhoff, P.B., and Christensen, R.H.B., lmerTest package: tests in linear mixed effects models, J. Stat. Soft., 2017, vol. 82, pp. 1–26.

    Article  Google Scholar 

  41. Leitão, A., ten Cate, C., and Riebel, K., Within-song complexity in a songbird is meaningful to both male and female receivers, Anim. Behav., 2006, vol. 71, pp. 1289–1296.

    Article  Google Scholar 

  42. Lemon, R.E., Cotter, R., MacNally, R.C., and Monette, S., Song repertoires and song sharing by American redstarts, Condor, 1985, vol. 87, pp. 457–470.

    Article  Google Scholar 

  43. Lemon, R.E., Dobson, C.W., and Clifton, P.G., Songs of American redstarts (Setophaga ruticilla): sequencing rules and their relationships to repertoire size, Ethology, 1993, vol. 93, pp. 198–210.

    Article  Google Scholar 

  44. Linhart, P., Slabbekoorn, H., and Fuchs, R., The communicative significance of song frequency and song length in territorial chiffchaffs, Behav. Ecol., 2012, vol. 23, pp. 1338–1347.

    Article  Google Scholar 

  45. McGregor, P.K., Playback experiments: design and analysis, Acta Ethol., 2000, vol. 3, pp. 3–8.

    Article  Google Scholar 

  46. McGregor, P.K., Dablesteen, T., Shepherd, M., and Pedersen, S.B., The signal value of matched singing in great tits: evidence from interactive playback experiments, Anim. Behav., 1992, vol. 43, pp. 987–998.

    Article  Google Scholar 

  47. Marler, P. and Slabbekoorn, H., Nature’s Music, The Science of Birdsong, San Diego: Academic, 2004.

    Google Scholar 

  48. Martens, J., A preliminary review of the leaf warbler genera Phylloscopus and Seicercus, Br. Ornithol. Club Occas. Publs., 2010, vol. 5, pp. 41–116.

    Google Scholar 

  49. Martens, J., Eck, S., Päckert, M., and Sun, Y.-H., The golden-spectacled warbler Seicercus burkii: a species swarm (Aves: Passeriformes: Sylviidae). Part 1, Zool. Abh. (Dresden), 1999, vol. 50, pp. 282–327.

    Google Scholar 

  50. Martens, J., Eck, S., Päckert, M., and Sun, Y.-H., Methods of systematic and taxonomic research on passerine birds: the timely example of the Seicercus burkii complex (Sylviidae). Part 2, Bonner Zool. Beitr., 2003, vol. 51, pp. 109–118.

    Google Scholar 

  51. Mennill, D.J. and Ratcliffe, L.M., Overlapping and matching in the song contests of black-capped chickadees, Anim. Behav., 2004, vol. 67, pp. 441–450.

    Article  Google Scholar 

  52. Molles, L.E., Singing complexity of the banded wren Thryothorus pleurostictus: do switching and song-type diversity send different messages?, Auk, 2006, vol. 123, pp. 991–1003.

    Google Scholar 

  53. Naguib, M., Effects of song overlapping and alternating on nocturnally singing nightingales, Anim. Behav., 1999, vol. 58, pp. 1061–1067.

    Article  CAS  PubMed  Google Scholar 

  54. Nowicki, S., Searcy, W.A., and Hughes, M., The territory defense function of song in song sparrows: a test with the speaker occupation design, Behaviour, 1998, vol. 135, pp. 615–628.

    Article  Google Scholar 

  55. Okanoya, K., Finite–state song syntax in Bengalese finches: sensorimotor evidence, developmental processes, and formal procedures for syntax extraction, in Birdsong, Speech, and Language. Exploring the Evolution of Mind and Brain, Bolhuis, J.J. and Everaert, M., Eds., London: The MIT Press, 2013, pp. 229–242.

    Google Scholar 

  56. Opaev, A., Relationships between repertoire size and organization of song bouts in the grey-crowned warbler (Seicercus tephrocephalus), J. Ornithol., 2016, vol. 157, pp. 949–960.

    Article  Google Scholar 

  57. Opaev, A.S. and Kolesnikova, Y.A., The role of song rate and song bout’s complexity in the territorial behavior of Radde’s warbler (Phylloscopus schwarzi), Zool. Zh., 2019a, vol. 98, pp. 319–331.

    Google Scholar 

  58. Opaev, A. and Kolesnikova, Y., Lack of habitat segregation and no interspecific territoriality in three syntopic cryptic species of the golden-spectacled warblers Phylloscopus (Seicercus) burkii complex, J. Avian. Biol., 2019b, vol. 50, pp. 1–9.

    Article  Google Scholar 

  59. Opaev, A., Kolesnikova, Y., Liu, M., and Kang, Z., Singing of Claudia’s leaf-warbler (Phylloscopus claudiae) in aggressive contexts: role of song rate, song type diversity and song type transitional pattern, J. Ornithol., 2019, vol. 160, pp. 297–304.

    Article  Google Scholar 

  60. Päckert, M., Martens, J., Sun, Y.-H., and Veith, M., The radiation of the Seicercus burkii complex and its congeners (Aves: Sylviidae): molecular genetics and bioacoustics, Org. Div. Evol., 2004, vol. 4, pp. 341–364.

    Article  Google Scholar 

  61. Päckert, M., Sun, Y.-H., Peterson, T., Holt, P., Strutzenberger, P., and Martens, J., Integrative taxonomy of Seicercus spectacled warblers for mapping species’ distribution, Atlas Verbr. Palaearkt. Vogel, 2016, vol. 22, pp. 1–7.

    Google Scholar 

  62. Pitt, S.M.G., Why sing so many songs? Testing the function of song type repertoires in rock wrens using playback experiments and behavioral observations, Master of Science Thesis, University of Northern Colorado, 2018.

  63. R Core Team, R: A Language and Environment for Statistical Computing, Vienna: R Found. Stat. Comp., 2020. https://www.R-project.org.

  64. Randler, C., A possible phylogenetically conserved urgency response of great tits (Parus major) towards allopatric mobbing calls, Behav. Ecol. Sociobiol., 2012, vol. 66, pp. 675–681.

    Article  Google Scholar 

  65. Riebel, K. and Slater, P.J.B., Song type switching in the chaffinch, Fringilla coelebs: timing or counting?, Anim. Behav., 1999, vol. 57, pp. 655–661.

    Article  CAS  PubMed  Google Scholar 

  66. Sasahara, K., Cody, M.L., Cohen, D., and Taylor, C., Structural design principles of complex bird songs: a network-based approach, PLoS One, 2012, vol. 7, p. e44446.

    Article  ADS  Google Scholar 

  67. Schank, J.C. and Koehnle, T.J., Pseudoreplication is a pseudoproblem, J. Comp. Psychol., 2009, vol. 123, pp. 421–433.

    Article  PubMed  Google Scholar 

  68. Scharff, C. and Nottebohm, F., A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implication for vocal learning, J. Neurosci., 1991, vol. 11, pp. 2896–2913.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Scordato, E.S.C., Geographic variation in male territory defense strategy in an avian ring species, Anim. Behav., 2017, vol. 126, pp. 153–162.

    Article  Google Scholar 

  70. Searcy, W.A. and Beecher, M.D., Song as an aggressive signal in songbirds, Anim. Behav., 2009, vol. 78, pp. 1281–1292.

    Article  Google Scholar 

  71. Searcy, W.A. and Yasukawa, K., Use of the song repertoire in intersexual and intrasexual context by male red-winged blackbirds, Behav. Ecol. Sociobiol., 1990, vol. 27, pp. 123–128.

    Article  Google Scholar 

  72. Searcy, W.A., Nowicki, S., and Hogan, C., Song type variants and aggressive context, Behav. Ecol. Sociobiol., 2000, vol. 48, pp. 358–363.

    Article  Google Scholar 

  73. Searcy, W.A., Anderson, R.C., and Nowicki, S., Bird song as a signal of aggressive intent, Behav. Ecol. Sociobiol., 2006, vol. 60, pp. 234–241.

    Article  Google Scholar 

  74. Spector, D.A., The singing behaviour of yellow warblers, Behaviour, 1991, vol. 117, pp. 29–52.

    Article  Google Scholar 

  75. Spedicato, G.A., Kang, T.S., Yalamanchi, S.B., Thoralf, M., Yadav, D., Castillo, N.C., and Jain, V., Easy handling discrete time Markov chains, 2017. https://cran.r-project.org/web/packages/markovchain.

  76. Suzuki, T.N., Semantic communication in birds: evidence from field research over the past two decades, Ecol. Res., 2016, vol. 31, pp. 307–319.

    Article  Google Scholar 

  77. Szymkowiak, J. and Kuczyński, L., Song rate as a signal of male aggressiveness during territorial contests in the wood warbler, J. Avian Biol., 2017, vol. 48, pp. 275–283.

    Article  Google Scholar 

  78. Todt, D. and Hultsch, H., How songbirds deal with large amounts of serial information: retrieval rules suggest a hierarchical song memory, Biol. Cybern., 1998, vol. 79, pp. 487–500.

    Article  Google Scholar 

  79. Todt, D. and Naguib, M., Vocal interactions in birds: the use of song as a model in communication, Adv. Study Behav., 2000, vol. 29, pp. 247–296.

    Article  Google Scholar 

  80. Vehrencamp, S.L. Handicap, index, and conventional signal elements of bird song, in Animal Signals: Signalling and Signal Design in Animal Communication, Espmark, Y., Amundsen, T., Rosenqvist, G., Eds., Trondheim: Tapir Publishers, 2000, pp. 277–300.

    Google Scholar 

  81. Vehrencamp, S.L., Hall, M.L., Bohman, E.R., Depeine, C.D., and Dalziel, A.H., Song matching, overlapping, and switching in the banded wren: the sender’s perspective, Behav. Ecol., 2007, vol. 18, pp. 849–859.

    Article  PubMed  Google Scholar 

  82. Weiss, M., Hultsch, H., Adam, I., Scharff, C., and Kipper, S., The use of network analysis to study complex animal communication systems: a study on nightingale song, Proc. R. Soc. B, 2014, vol. 281, p. 20140460.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Woolley, S.M.N. and Rubel, E.W., Bengalese finches Lonchura striata domestica depend upon auditory feedback for the maintenance of adult song, J. Neurosci., 1997, vol. 17, pp. 6380–6390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

The authors thank Shurong Tian, Meishi Liu and Zujie Kang for their support during field study.

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The study was supported by the Russian Science Foundation (grant no. 20-14-00058-P).

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Kolesnikova, Y.A., Opaev, A.S. Comparative Study of Aggressive Signaling in Three Closely-Related Warbler Species. Biol Bull Russ Acad Sci 50 (Suppl 3), S415–S427 (2023). https://doi.org/10.1134/S1062359023602495

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