Learning mimetic cuckoo call innovations from neighbors in a Chinese songbird.

Changjian Fu, Xiaochun Wang, Fiona Backhouse, Zhongqiu Li
Author Information
  1. Changjian Fu: Lab of Animal Behavior and Conservation, School of Life Sciences, Nanjing University, No. 163 Xianlin Avenue, Qixia District, Nanjing, 210023, Jiangsu, China. ORCID
  2. Xiaochun Wang: Lab of Animal Behavior and Conservation, School of Life Sciences, Nanjing University, No. 163 Xianlin Avenue, Qixia District, Nanjing, 210023, Jiangsu, China. ORCID
  3. Fiona Backhouse: Cornell Lab of Ornithology, Cornell University, Ithaca, NY, 14850, USA. ORCID
  4. Zhongqiu Li: Lab of Animal Behavior and Conservation, School of Life Sciences, Nanjing University, No. 163 Xianlin Avenue, Qixia District, Nanjing, 210023, Jiangsu, China. lizq@nju.edu.cn.

Abstract

Some oscine passerines incorporate heterospecific sounds into their repertoires, including vocalizations of other bird species, sounds of other fauna, and even anthropogenic sounds, through vocal mimicry. However, few studies have investigated whether mimics learn heterospecific sounds from model species or from conspecific tutors. Here, we investigate mimicry acquisition using innovation in Cuculidae calls imitated by the Chinese blackbird (Turdus mandarinus). If the mimicry innovation arises and spreads among several neighbors and is not produced by model species, the mimicry must be acquired partially from conspecifics. We found that: (1) Cuculidae calls imitated by blackbirds were reasonably accurate, but with some differences between mimetic and real calls in acoustic structures. (2) We identified four unique mimetic units (mimicry innovation or copy errors), and these units only occurred at certain sites and were shared by several neighbors. In aggregate, frequency parameters (the first principal component) of unique mimetic units were higher than usual mimetic units (p < 0.001). Our findings provide further evidence that mimetic units can be partially learnt from conspecifics based on four cases of unique mimetic units. Our study and approach provide a reference and theoretical basis for the future understanding of social learning and development of vocal mimicry.

Keywords

References

  1. Goller, M. & Shizuka, D. Evolutionary origins of vocal mimicry in songbirds. Evol. Lett.2 (4), 417-426. https://doi.org/10.1002/evl3.62 (2018). [DOI: 10.1002/evl3.62]
  2. Hamao, S. & Eda-Fujiwara, H. Vocal mimicry by the black-browed reed warbler Acrocephalus bistrigiceps: objective identification of mimetic sounds. Ibis. 146 (1), 61-68. https://doi.org/10.1111/j.1474-919X.2004.00226.x (2004). [DOI: 10.1111/j.1474-919X.2004.00226.x]
  3. Dalziell, A. H., Welbergen, J. A. & Magrath, R. D. Male superb lyrebirds mimic functionally distinct heterospecific vocalizations during different modes of sexual display. Anim. Behav.188, 181-196. https://doi.org/10.1016/j.anbehav.2022.04.002 (2022). [DOI: 10.1016/j.anbehav.2022.04.002]
  4. Gammons, D. E. & Lyon, R. P. An acoustic comparison of mimetic and non-mimetic song in northern mockingbirds Mimus polyglottos. Ardea. 105 (1), 37-42. https://doi.org/10.5253/arde.v105i1.a1 (2017). [DOI: 10.5253/arde.v105i1.a1]
  5. Dalziell, A. H., Maisey, A. C., Magrath, R. D. & Welbergen, J. A. Male lyrebirds create a complex acoustic illusion of a mobbing flock during courtship and copulation. Curr. Biol.31 (9), 1970-1976.e (1974). https://doi.org/10.1016/j.cub.2021.02.003 (2021).
  6. Gammon, D. E. & Corsiglia, A. M. Mockingbirds imitate frogs and toads across North America. Behav. Processes169, 103982. https://doi.org/10.1016/j.beproc.2019.103982 (2019). [DOI: 10.1016/j.beproc.2019.103982]
  7. Dalziell, A. H., Welbergen, J. A., Igic, B. & Magrath, R. D. Avian vocal mimicry: a unified conceptual framework. Biol. Rev.90 (2), 643-668. https://doi.org/10.1111/brv.12129 (2015). [DOI: 10.1111/brv.12129]
  8. Langmore, N. E., Maurer, G., Adcock, G. J. & Kilner, R. M. Socially acquired host-specific mimicry and the evolution of host races in Horsfield’s bronze-cuckoo Chalcites Basalis. Evolution. 62 (7), 1689-1699. https://doi.org/10.1111/j.1558-5646.2008.00405.x (2008). [DOI: 10.1111/j.1558-5646.2008.00405.x]
  9. Kelley, L. A. & Healy, S. D. Vocal mimicry in male bowerbirds: who learns from whom? Biol. Lett.6 (5), 626-629. https://doi.org/10.1098/rsbl.2010.0093 (2010). [DOI: 10.1098/rsbl.2010.0093]
  10. Backhouse, F., Dalziell, A. H., Magrath, R. D. & Welbergen, J. A. Higher-order sequences of vocal mimicry performed by male Albert’s lyrebirds are socially transmitted and enhance acoustic contrast. Proc. R. Soc. B289 20212498. (1970). https://doi.org/10.1098/rspb.2021.2498 (2022).
  11. Riegert, J. & Juzlova, Z. Vocal mimicry in the song of Icterine warblers (Hippolais icterina): possible functions and sources of variability. Ethol. Ecol. Evol.30 (5), 430-446. https://doi.org/10.1080/03949370.2017.1412356 (2018). [DOI: 10.1080/03949370.2017.1412356]
  12. Putland, D. A., Nicholls, J. A., Noad, M. J. & Goldizen, A. W. Imitating the neighbours: vocal dialect matching in a mimic-model system. Biol. Lett.2 (3), 367-370. https://doi.org/10.1098/rsbl.2006.0502 (2006). [DOI: 10.1098/rsbl.2006.0502]
  13. Backhouse, F., Welbergen, J. A., Magrath, R. D. & Dalziell, A. H. Depleted cultural richness of an avian vocal mimic in fragmented habitat. Divers. Distrib.29 (1), 109-122. https://doi.org/10.1111/ddi.13646 (2023). [DOI: 10.1111/ddi.13646]
  14. Baker, M. C., Baker, M. S. A. & Baker, E. M. Rapid evolution of a novel song and an increase in repertoire size in an island population of an Australian songbird. Ibis. 145 (3), 465-471. https://doi.org/10.1046/j.1474-919X.2003.00190.x (2003). [DOI: 10.1046/j.1474-919X.2003.00190.x]
  15. Dowsett-Lemaire, F. Imitative range of the song of the marsh warbler Acrocephalus palustris, with special reference to imitations of African birds. Ibis. 121 (4), 453-468. https://doi.org/10.1111/j.1474-919X.1979.tb06685.x (1979). [DOI: 10.1111/j.1474-919X.1979.tb06685.x]
  16. Zheng, G. M. A Checklist on the Classification and Distribution of the Birds of China Fourth edn (Science, 2023).
  17. del Hoyo, J., Collar, N. & Christie, D. A. Birds of the World Version 1.0 (Cornell Lab of Ornithology, 2020).
  18. Mei, J. J., Puswal, S. M., Wang, M. & Liu, F. L. Diurnal and seasonal patterns of calling activity of seven Cuculidae species in a forest of Eastern China. Diversity-Basel. 14 (4), 249. https://doi.org/10.3390/d14040249 (2022). [DOI: 10.3390/d14040249]
  19. Xia, C. et al. The function of three main call types in common cuckoo. Ethology. 125 (9), 652-659. https://doi.org/10.1111/eth.12918 (2019). [DOI: 10.1111/eth.12918]
  20. Slabbekoorn, H. & Smith, T. B. Bird song, ecology and speciation. Philos. Trans. R Soc. Lond. Ser. B-Biol Sci.357 (1420), 493-503. https://doi.org/10.1098/rstb.2001.1056 (2002). [DOI: 10.1098/rstb.2001.1056]
  21. Payne, R. B., Woods, J. L., Siddall, M. E. & Parr, C. S. Randomization analyses: mimicry, geographic variation and cultural evolution of song in brood-parasitic straw-tailed whydahs, Vidua fischeri. Ethology. 106 (3), 261-282. https://doi.org/10.1046/j.1439-0310.2000.00528.x (2000). [DOI: 10.1046/j.1439-0310.2000.00528.x]
  22. Moskát, C. & Hauber, M. E. Syntax errors do not disrupt acoustic communication in the common cuckoo. Sci. Rep.12 (1), 1568. https://doi.org/10.1038/s41598-022-05661-6 (2022). [DOI: 10.1038/s41598-022-05661-6]
  23. Catchpole, C. K. & Slater, P. J. B. Bird song: Biological Themes and Variations (Cambridge University Press, 1995).
  24. Tchernichovski, O., Feher, O., Fimiarz, D. & Conley, D. How social learning adds up to a culture: from birdsong to human public opinion. J. Exp. Biol.220 (1), 124-132. https://doi.org/10.1242/jeb.142786 (2017). [DOI: 10.1242/jeb.142786]
  25. Wei, C. et al. Geographic variation in the calls of the common cuckoo (Cuculus canorus): isolation by distance and divergence among subspecies. J. Ornithol.156 (2), 533-542. https://doi.org/10.1007/s10336-014-1153-6 (2015). [DOI: 10.1007/s10336-014-1153-6]
  26. Wang, Y., Huang, Q., Lan, S., Zhang, Q. & Chen, S. Common blackbirds Turdus merula use anthropogenic structures as nesting sites in an urbanized landscape. Curr. Zool.61 (3), 435-443. https://doi.org/10.1093/czoolo/61.3.435 (2015). [DOI: 10.1093/czoolo/61.3.435]
  27. Hesler, N., Mundry, R. & Dabelsteen, T. Are there age-related differences in the song repertoire size of eurasian blackbirds? acta Ethologica. 15 (2), 203-210. https://doi.org/10.1007/s10211-012-0127-z (2012). [DOI: 10.1007/s10211-012-0127-z]
  28. Hesler, N., Mundry, R. & Dabelsteen, T. Does song repertoire size in common blackbirds play a role in an intra-sexual context? J. Ornithol.152 (3), 591-601. https://doi.org/10.1007/s10336-010-0618-5 (2011). [DOI: 10.1007/s10336-010-0618-5]
  29. Huang, W., Xu, S., Liang, W. & Xia, C. Daily vocal pattern of large Hawk cuckoo (Hierococcyx sparverioides). Chin. J. Zool.52 (6), 945-953 (2017).
  30. K. Lisa Yang Center for Conservation Bioacoustics. Revan Pro: interactive sound analysis software (Version 1.6.4) [Computer software]. Ithaca, NY: The Cornell Lab of Ornithology. Available from (2023). https://ravensoundsoftware.com/
  31. Yu, G. Using ggtree to visualize data on tree-like structures. Curr. Protocols Bioinf.69 (1), e96. https://doi.org/10.1002/cpbi.96 (2020). [DOI: 10.1002/cpbi.96]
  32. Yu, G. C., Smith, D. K., Zhu, H. C., Guan, Y. & Lam, T. T. Y. GGTREE: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol.8 (1), 28-36. https://doi.org/10.1111/2041-210x.12628 (2017). [DOI: 10.1111/2041-210x.12628]
  33. Yu, G. C., Lam, T. T. Y., Zhu, H. C. & Guan, Y. Two methods for mapping and visualizing associated data on phylogeny using ggtree. Mol. Biol. Evol.35 (12), 3041-3043. https://doi.org/10.1093/molbev/msy194 (2018). [DOI: 10.1093/molbev/msy194]
  34. Wang, L. G. et al. Treeio: an R package for phylogenetic tree input and output with richly annotated and associated data. Mol. Biol. Evol.37 (2), 599-603. https://doi.org/10.1093/molbev/msz240 (2020). [DOI: 10.1093/molbev/msz240]
  35. Zann, R. & Dunstan, E. Mimetic song in superb lyrebirds: species mimicked and mimetic accuracy in different populations and age classes. Anim. Behav.76 (3), 1043-1054. https://doi.org/10.1016/j.anbehav.2008.05.021 (2008). [DOI: 10.1016/j.anbehav.2008.05.021]
  36. Dalziell, A. H. & Magrath, R. D. Fooling the experts: accurate vocal mimicry in the song of the superb lyrebird, Menura novaehollandiae. Anim. Behav.83 (6), 1401-1410. https://doi.org/10.1016/j.anbehav.2012.03.009 (2012). [DOI: 10.1016/j.anbehav.2012.03.009]
  37. Khan, A. A. & Qureshi, I. Z. Vocalizations of adult male Asian koels (Eudynamys scolopacea) in the breeding season. PLoS ONE. 12 (10), e0186604. https://doi.org/10.1371/journal.pone.0186604 (2017). [DOI: 10.1371/journal.pone.0186604]
  38. Møller, A. P., Morelli, F., Mousseau, T. A. & Tryjanowski, P. The number of syllables in Chernobyl cuckoo calls reliably indicate habitat, soil and radiation levels. Ecol. Indic.66, 592-597. https://doi.org/10.1016/j.ecolind.2016.02.037 (2016). [DOI: 10.1016/j.ecolind.2016.02.037]
  39. Ansell, D., Magrath, R. D. & Haff, T. M. Song matching in a long-lived, sedentary bird with a low song rate: the importance of song type, song duration and intrusion. Ethology. 126 (12), 1098-1110. https://doi.org/10.1111/eth.13090 (2020). [DOI: 10.1111/eth.13090]
  40. King, S. L. & McGregor, P. K. Vocal matching: the what, the why and the how. Biol. Lett.12 (10), 20160666. https://doi.org/10.1098/rsbl.2016.0666 (2016). [DOI: 10.1098/rsbl.2016.0666]
  41. Harcus, J. L. The functions of mimicry in the vocal behaviour of the chorister robin. Z. für Tierpsychologie. 44 (2), 178-193. https://doi.org/10.1111/j.1439-0310.1977.tb00992.x (1977). [DOI: 10.1111/j.1439-0310.1977.tb00992.x]
  42. Danner, J. E. et al. Female, but not male, tropical sparrows respond more strongly to the local song dialect: implications for population divergence. Am. Nat.178 (1), 53-63. https://doi.org/10.1086/660283 (2011). [DOI: 10.1086/660283]
  43. O’Loghlen, A. L. & Beecher, M. D. Mate, neighbour and stranger songs: a female song sparrow perspective. Anim. Behav.58 (1), 13-20. https://doi.org/10.1006/anbe.1999.1125 (1999). [DOI: 10.1006/anbe.1999.1125]
  44. Jagielski, P. M. & Foote, J. R. Local and range-wide distribution of song types suggest ovenbirds (Seiurus aurocapilla) have song neighborhoods but not macro-dialects. Avian Res.14, 100096. https://doi.org/10.1016/j.avrs.2023.100096 (2023). [DOI: 10.1016/j.avrs.2023.100096]
  45. Wu, L. et al. Limited song mixing without genomic gene flow in a contact zone between two songbird species. Mol. Biol. Evol.40 (3), msad053. https://doi.org/10.1093/molbev/msad053 (2023). [DOI: 10.1093/molbev/msad053]
  46. Beecher, M. D. & Brenowitz, E. A. Functional aspects of song learning in songbirds. Trends Ecol. Evol.20 (3), 143-149. https://doi.org/10.1016/j.tree.2005.01.004 (2005). [DOI: 10.1016/j.tree.2005.01.004]
  47. Gammon, D. E. Seasonal patterns of vocal mimicry in northern mockingbirds Mimus polyglottos. J. Avian Biol.45 (6), 545-550. https://doi.org/10.1111/jav.00414 (2014). [DOI: 10.1111/jav.00414]

Grants

  1. 2022YFC3202104/National Key Research and Development Program of China
  2. BK20211151/Natural Science Foundation of Jiangsu Province
  3. NGS-CG-CS-2022116/Survey Project of Banqiao Provincial Nature Reserve, Ningguo, Anhui Province

MeSH Term

Animals
China
Imitative Behavior
Learning
Songbirds
Vocalization, Animal

Word Cloud

Created with Highcharts 10.0.0mimicrymimeticunitssoundsspeciesinnovationcallsChineseneighborsuniqueheterospecificvocalmodelCuculidaeimitatedblackbirdseveralpartiallyconspecificsfourprovidecalloscinepasserinesincorporaterepertoiresincludingvocalizationsbirdfaunaevenanthropogenicHoweverstudiesinvestigatedwhethermimicslearnconspecifictutorsinvestigateacquisitionusingTurdusmandarinusarisesspreadsamongproducedmustacquiredfoundthat:1 Cuculidaeblackbirdsreasonablyaccuratedifferencesrealacousticstructures2 Weidentifiedcopyerrorsoccurredcertainsitessharedaggregatefrequencyparametersfirstprincipalcomponenthigherusualp < 0001findingsevidencecanlearntbasedcasesstudyapproachreferencetheoreticalbasisfutureunderstandingsociallearningdevelopmentLearningcuckooinnovationssongbirdBirdsongmatingInnovationSocialtransmissionVocal

Similar Articles

Cited By

No available data.