Cultural divergence and morphological variation of isolated remnant populations of the endangered Floreana mockingbird
Enzo M. R. Reyes
A * , Michelle M. Roper A E , Christian Sevilla B , Danny Rueda B , Dianne H. Brunton A E , Adam N. H. Smith C and Luis Ortiz-Catedral D
A
B
C
D
E Present Address:
Abstract
Cultural divergence refers to changes over time in behavioural traits. These cultural changes could have important implications for conservation planning, and impact the success of conservation efforts such as translocations.
Here, we investigate the extent, and potential impacts, of cultural divergence in two isolated populations of the Floreana mockingbird (Mimus trifasciatus) on the Galápagos Islands.
Using contemporary recordings of vocalisations we test for spatial vocal differentiation between mockingbird populations. Furthermore, we explore the potential drivers of change using morphological measurements and historical recordings of the species.
We found evidence of spatial and temporal differentiation in vocalisations between the two populations of the Floreana mockingbird. We accurately classified over 75% of the birds to the correct populations based on multivariate measures of audio recordings using canonical analysis of principal coordinates (CAP). We also found significant differences in morphometrics between populations; specifically, beak depth was associated with frequency modulation, an acoustic measure that is significantly different between populations. Furthermore, we found evidence of change in the complexity of the vocalisations over a period of 57 years.
Cultural divergence was found in the two remaining populations of this endangered species. Factors such as changes in morphology and cultural drift might have been influenced the change in vocalisation across time and populations.
We highlight the importance of considering behavioural factors when planning reintroductions of endangered species where there is a need to minimise the risk of assortative mating so as to maximise genetic diversity.
Keywords: conservation, cultural divergence, cultural drift, Floreana mockingbird, Galapagos, morphology, reintroduction, vocalisations.
References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26(1), 32-46.
| Crossref | Google Scholar |
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62(1), 245-253.
| Crossref | Google Scholar | PubMed |
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84(2), 511-525.
| Crossref | Google Scholar |
Aplin L (2016) Understanding the multiple factors governing social learning and the diffusion of innovations. Current Opinion in Behavioral Sciences 12, 59-65.
| Crossref | Google Scholar |
Aplin LM (2019) Culture and cultural evolution in birds: a review of the evidence. Animal Behaviour 147, 179-187.
| Crossref | Google Scholar |
Baker MC (1975) Song dialects and genetic differences in white-crowned sparrows (Zonotrichia leucophrys). Evolution 29(2), 226-241.
| Crossref | Google Scholar | PubMed |
Baker MC, Baker EM, Baker MSA (2001) Island and island-like effects on vocal repertoire of singing honeyeaters. Animal Behaviour 62(4), 767-774.
| Crossref | Google Scholar |
Bell D, Slabbekoorn H, Jesse A (2003) Microgeographic song variation in island populations of the white-crowned sparrow (Zonotrichia leucophrys nutalli): innovation through recombination. Behaviour 140(7), 947-963.
| Crossref | Google Scholar |
Benedict L, Najar NA (2019) Are commonly used metrics of bird song complexity concordant? The Auk 136(1), uky008.
| Crossref | Google Scholar |
Bollmer JL, Sanchez T, Cannon MD, Sanchez D, Cannon B, Bednarz JC, de Vries T, Struve MS, Parker PG (2003) Variation in morphology and mating system among island populations of Galápagos hawks. The Condor 105(3), 428-438.
| Crossref | Google Scholar |
Botero CA, Vehrencamp SL (2007) Responses of male tropical mocking birds (Mimus gilvus) to variation in within-song and between-song versatility. The Auk 124(1), 185-196.
| Crossref | Google Scholar | PubMed |
Botero CA, Rossman RJ, Caro LM, Stenzler LM, Lovette IJ, de Kort SR, Vehrencamp SL (2009) Syllable type consistency is related to age, social status and reproductive success in the tropical mockingbird. Animal Behaviour 77(3), 701-706.
| Crossref | Google Scholar |
Bozzuto C, Hoeck PEA, Bagheri HC, Keller LF (2017) Modelling different reintroduction strategies for the critically endangered Floreana mockingbird. Animal Conservation 20(2), 144-154.
| Crossref | Google Scholar |
Bradley DW, Molles LE, Waas JR (2014) Post-translocation assortative pairing and social implications for the conservation of an endangered songbird. Animal Conservation 17(3), 197-203.
| Crossref | Google Scholar |
Briefer E, Osiejuk TS, Rybak F, Aubin T (2010) Are bird song complexity and song sharing shaped by habitat structure? An information theory and statistical approach. Journal of Theoretical Biology 262(1), 151-164.
| Crossref | Google Scholar | PubMed |
Crates R, Langmore N, Ranjard L, Stojanovic D, Rayner L, Ingwersen D, Heinsohn R (2021) Loss of vocal culture and fitness costs in a critically endangered songbird. Proceedings of the Royal Society B: Biological Sciences 288(1947), 20210225.
| Crossref | Google Scholar |
Curry RL (1986) Whatever happened to the Floreana mockingbird? Noticias de Galápagos 43, 13-15.
| Google Scholar |
Curry RL (1988a) Group structure, within-group conflict and reproductive tactics in cooperatively breeding Galápagos mockingbirds, Nesomimus parvulus. Animal Behaviour 36(6), 1708-1728.
| Crossref | Google Scholar |
Curry RL (1988b) Influence of kinship on helping behavior in Galápagos mockingbirds. Behavioral Ecology and Sociobiology 22, 141-152.
| Crossref | Google Scholar |
Curry RL (1989) Geographic variation in social organization of Galápagos mockingbirds: ecological correlates of group territoriality and cooperative breeding. Behavioral Ecology and Sociobiology 25, 147-160.
| Crossref | Google Scholar |
de Kort SR, Eldermire ERB, Cramer ERA, Vehrencamp SL (2009) The deterrent effect of bird song in territory defense. Behavioral Ecology 20(1), 200-206.
| Crossref | Google Scholar | PubMed |
Deem SL, Parker PG, Cruz MB, Merkel J, Hoeck PEA (2011) Comparison of blood values and health status of Floreana mockingbirds (Mimus trifasciatus) on the islands of Champion and Gardner-by-Floreana, Galápagos Islands. Journal of Wildlife Diseases 47(1), 94-106.
| Crossref | Google Scholar | PubMed |
Demery A-JC, Burns KJ, Mason NA (2021) Bill size, bill shape, and body size constrain bird song evolution on a macroevolutionary scale. Ornithology 138(2), 1-11.
| Crossref | Google Scholar |
Demko AD, Mennill DJ (2019) Rufous-capped Warblers Basileuterus rufifrons show seasonal, temporal and annual variation in song use. Ibis 161(3), 481-494.
| Crossref | Google Scholar |
Derrickson KC (1987) Yearly and situational changes in the estimate of repertoire size in northern mockingbirds (Mimus polyglottos). The Auk 104(2), 198-207.
| Crossref | Google Scholar |
Derrickson KC, Breitwisch R (1992) Northern mockingbird. The Birds of North America 1(7), 1-26.
| Google Scholar |
Derryberry EP (2007) Evolution of bird song affects signal efficacy: an experimental test using historical and current signals. Evolution 61(8), 1938-1945.
| Crossref | Google Scholar | PubMed |
Derryberry EP, Seddon N, Claramunt S, Tobias JA, Baker A, Aleixo A, Brumfield RT (2012) Correlated evolution of beak morphology and song in the neotropical woodcreeper radiation. Evolution 66(9), 2784-2797.
| Crossref | Google Scholar | PubMed |
Derryberry EP, Seddon N, Derryberry GE, Claramunt S, Seeholzer GF, Brumfield RT, Tobias JA (2018) Ecological drivers of song evolution in birds: disentangling the effects of habitat and morphology. Ecology and Evolution 8(3), 1890-1905.
| Crossref | Google Scholar | PubMed |
Ey E, Fischer J (2009) The “acoustic adaptation hypothesis” – a review of the evidence from birds, anurans and mammals. Bioacoustics 19(1–2), 21-48.
| Crossref | Google Scholar |
Freeberg TM (2006) Social complexity can drive vocal complexity: group size influences vocal information in Carolina chickadees. Psychological Science 17(7), 557-561.
| Crossref | Google Scholar | PubMed |
Freeberg TM, Dunbar RIM, Ord TJ (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Philosophical Transactions of the Royal Society B: Biological Sciences 367(1597), 1785-1801.
| Crossref | Google Scholar |
Friedman NR, Miller ET, Ball JR, Kasuga H, Remeš V, Economo EP (2019) Evolution of a multifunctional trait: shared effects of foraging ecology and thermoregulation on beak morphology, with consequences for song evolution. Proceedings of the Royal Society B: Biological Sciences 286(1917), 20192474.
| Crossref | Google Scholar |
Friis JI, Sabino J, Santos P, Dabelsteen T, Cardoso GC (2022) Ecological adaptation and birdsong: how body and bill sizes affect passerine sound frequencies. Behavioral Ecology 33(4), 798-806.
| Crossref | Google Scholar |
Fukuzawa Y, Webb WH, Pawley MDM, Roper MM, Marsland S, Brunton DH, Gilman A (2020) Koe: web-based software to classify acoustic units and analyse sequence structure in animal vocalizations. Methods in Ecology and Evolution 11(3), 431-441.
| Crossref | Google Scholar |
Galeotti PR, Appleby BM, Redpath SM (1996) Macro and microgeographical variations in the ‘hoot’ of Italian and English tawny owls (Strix aluco). Italian Journal of Zoology 63(1), 57-64.
| Crossref | Google Scholar |
Gammon DE (2014) Seasonal patterns of vocal mimicry in northern mockingbirds Mimus polyglottos. Journal of Avian Biology 45(6), 545-550.
| Crossref | Google Scholar |
Gammon DE (2020) Are northern mockingbirds classic open-ended song learners? Ethology 126(11), 1038-1047.
| Crossref | Google Scholar |
Gammon DE, Stracey CM (2022) First documentation of vocal mimicry in female northern mockingbirds. Journal of Ornithology 163, 749-756.
| Crossref | Google Scholar |
Garamszegi LZ, Eens M, Erritzøe J, Møller AP (2005) Sexually size dimorphic brains and song complexity in passerine birds. Behavioral Ecology 16(2), 335-345.
| Crossref | Google Scholar |
García NC, Tubaro PL (2018) Dissecting the roles of body size and beak morphology in song evolution in the “blue” cardinalids (Passeriformes: Cardinalidae. Auk 135(2), 262-275.
| Google Scholar |
Garland EC, Goldizen AW, Rekdahl ML, Constantine R, Garrigue C, Hauser ND, Poole M M, Robins J, Noad MJ (2011) Dynamic horizontal cultural transmission of humpback whale song at the ocean basin scale. Current Biology 21(8), 687-691.
| Crossref | Google Scholar | PubMed |
Geist D (1996) On the emergence and submergence of the Galápagos Islands. Noticias de Galápagos 56, 5-9.
| Google Scholar |
Goodale E, Podos J (2010) Persistence of song types in Darwin’s finches, Geospiza fortis, over four decades. Biology Letters 6(5), 589-592.
| Crossref | Google Scholar | PubMed |
Grant BR, Grant PR (1989) Natural selection in a population of Darwin’s finches. The American Naturalist 133(3), 377-393.
| Crossref | Google Scholar |
Grant BR, Grant PR (1993) Evolution of Darwin’s finches caused by a rare climatic event. Proceedings of the Royal Society of London. Series B: Biological Sciences 251(1331), 111-117.
| Crossref | Google Scholar |
Grant PR, Curry RL, Grant BR (2000) A remnant population of the Floreana mockingbird on Champion Island, Galápagos. Biological Conservation 92(3), 285-290.
| Crossref | Google Scholar |
Hardt B, Benedict L (2021) Can you hear me now? A review of signal transmission and experimental evidence for the acoustic adaptation hypothesis. Bioacoustics 30(6), 716-742.
| Crossref | Google Scholar |
Hill SD, Pawley MDM, Ji W (2017) Local habitat complexity correlates with song complexity in a vocally elaborate honeyeater. Austral Ecology 42(5), 590-596.
| Crossref | Google Scholar |
Hoeck PEA, Beaumont MA, James KE, Grant RB, Grant PR, Keller LF (2010a) Saving Darwin’s muse: evolutionary genetics for the recovery of the Floreana mockingbird. Biology Letters 6(2), 212-215.
| Crossref | Google Scholar |
Hoeck PEA, Bollmer JL, Parker PG, Keller LF (2010b) Differentiation with drift: a spatio-temporal genetic analysis of Galápagos mockingbird populations (Mimus spp.). Philosophical Transactions of the Royal Society B: Biological Sciences 365(1543), 1127-1138.
| Crossref | Google Scholar |
Howard RD (1974) The influence of sexual selection and interspecific competition on mockingbird song (Mimus polyglottos). Evolution 28(3), 428-438.
| Crossref | Google Scholar | PubMed |
Huber SK, Podos J (2006) Beak morphology and song features covary in a population of Darwin’s finches (Geospiza fortis). Biological Journal of the Linnean Society 88(3), 489-498.
| Crossref | Google Scholar |
Irwin DE, Bensch S, Price TD (2001) Speciation in a ring. Nature 409(6818), 333-337.
| Crossref | Google Scholar | PubMed |
Jarvis ED, Ribeiro S, da Silva ML, Ventura D, Vielliard J, Mello CV (2000) Behaviourally driven gene expression reveals song nuclei in hummingbird brain. Nature 406(6796), 628-632.
| Crossref | Google Scholar | PubMed |
Kazemi A, Kesba M, Provini P (2023) Realistic three-dimensional avian vocal tract model demonstrates how shape affects sound filtering (Passer domesticus). Journal of the Royal Society Interface 20, 20220728.
| Crossref | Google Scholar |
Kershenbaum A (2014) Entropy rate as a measure of animal vocal complexity. Bioacoustics 23(3), 195-208.
| Crossref | Google Scholar |
Kershenbaum A, Blumstein DT, Roch MA, et al. (2016) Acoustic sequences in non-human animals: a tutorial review and prospectus. Biological Reviews 91(1), 13-52.
| Crossref | Google Scholar | PubMed |
Kipper S, Kiefer S (2010) Age-related changes in birds’ singing styles: on fresh tunes and fading voices? Advances in the Study of Behavior 41, 77-118.
| Crossref | Google Scholar |
Krishnan A (2023) Biomechanics illuminates form-function relationships in bird bills. Journal of Experimental Biology 226(1), jeb245171.
| Crossref | Google Scholar |
Kroodsma DE (1985) Geographic variation in songs of the Bewick’s wren: a search for correlations with avifaunal complexity. Behavioral Ecology and Sociobiology 16(2), 143-150.
| Crossref | Google Scholar |
Laiolo P, Jovani R (2007) The emergence of animal culture conservation. Trends in Ecology & Evolution 22(1), 5.
| Crossref | Google Scholar | PubMed |
Laiolo P, Tella JL (2007) Erosion of animal cultures in fragmented landscapes. Frontiers in Ecology and the Environment 5(2), 68-72.
| Crossref | Google Scholar |
Laiolo P, Vögeli M, Serrano D, Tella JL (2008) Song diversity predicts the viability of fragmented bird populations. PLoS ONE 3(3), e1822.
| Crossref | Google Scholar | PubMed |
Laland KN, Janik VM (2006) The animal cultures debate. Trends in Ecology & Evolution 21(10), 542-547.
| Crossref | Google Scholar | PubMed |
Leader N, Wright J, Yom-Tov Y (2000) Microgeographic song dialects in the orange-tufted sunbird (Nectarinia osea). Behaviour 137(12), 1613-1627.
| Crossref | Google Scholar |
Leader N, Geffen E, Mokady O, Yom-Tov Y (2008) Song dialects do not restrict gene flow in an urban population of the orange-tufted sunbird, Nectarinia osea. Behavioral Ecology and Sociobiology 62(8), 1299-1305.
| Crossref | Google Scholar |
Logan CA (1985) Mockingbird use of chatbursts with neighbors versus strangers. Journal of Field Ornithology 56(1), 69-71.
| Google Scholar |
Logan CA, Budman PD, Fulk KR (1983) Role of chatburst versus song in the defense of fall territory in mockingbirds (Mimus polyglottos). Journal of Comparative Psychology 97(4), 292.
| Crossref | Google Scholar |
Loning H, Verkade L, Griffith SC, Naguib M (2023) The social role of song in wild zebra finches. Current Biology 33(2), 372-380.e3.
| Crossref | Google Scholar | PubMed |
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. Journal of Statistical Software 25(1), 1-18.
| Crossref | Google Scholar |
Marler P (1970) A comparative approach to vocal learning: song development in white-crowned sparrows. Journal of Comparative and Physiological Psychology 71(2p2), 1-25.
| Crossref | Google Scholar |
Martins BA, Rodrigues GSR, de Araújo CB (2018) Vocal dialects and their implications for bird reintroductions. Perspectives in Ecology and Conservation 16(2), 83-89.
| Crossref | Google Scholar |
Martínez TM, Logue DM (2020) Conservation practices and the formation of vocal dialects in the endangered Puerto Rican parrot, Amazona vittata. Animal Behaviour 166, 261-271.
| Crossref | Google Scholar |
Mesoudi A (2017) Pursuing Darwin’s curious parallel: prospects for a science of cultural evolution. Proceedings of the National Academy of Sciences 114(30), 7853-7860.
| Crossref | Google Scholar |
Morton ES (1975) Ecological sources of selection on avian sounds. The American Naturalist 109(965), 17-34.
| Crossref | Google Scholar |
Mundinger PC (1980) Animal cultures and a general theory of cultural evolution. Ethology and Sociobiology 1(3), 183-223.
| Crossref | Google Scholar |
Nietlisbach P, Wandeler P, Parker PG, Grant PR, Grant BR, Keller LF, Hoeck PEA (2013) Hybrid ancestry of an island subspecies of Galápagos mockingbird explains discordant gene trees. Molecular Phylogenetics and Evolution 69(3), 581-592.
| Crossref | Google Scholar | PubMed |
Ortiz-Catedral L, Lichtblau A, Anderson MG, Sevilla C, Rueda D (2021) First report of co-ocurrence of two species of mockingbirds in the Galápagos Islands: a San Cristobal mockingbird Mimus melanotis in a population of Floreana mockingbird M. trifasciatus. Galapagos Research 70, 41-44.
| Google Scholar |
Ortiz-Ramírez MF, Andersen MJ, Zaldívar-Riverón A, Ornelas JF, Navarro-Sigüenza AG (2016) Geographic isolation drives divergence of uncorrelated genetic and song variation in the Ruddy-capped Nightingale-Thrush (Catharus frantzii; Aves: Turdidae). Molecular Phylogenetics and Evolution 94, 74-86.
| Crossref | Google Scholar | PubMed |
Otter KA, Mckenna A, LaZerte SE, Ramsay SM (2020) Continent-wide shifts in song dialects of white-throated sparrows. Current Biology 30(16), 3231-3235.e3.
| Crossref | Google Scholar | PubMed |
O’Grady JJ, Brook BW, Reed DH, Ballou JD, Tonkyn DW, Frankham R (2006) Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biological Conservation 133(1), 42-51.
| Crossref | Google Scholar |
O’Loghlen AL, Rothstein SI (1995) Culturally correct song dialects are correlated with male age and female song preferences in wild populations of brown-headed cowbirds. Behavioral Ecology and Sociobiology 36(4), 251-259.
| Crossref | Google Scholar |
Parker KA, Hauber ME, Brunton DH (2010) Contemporary cultural evolution of a conspecific recognition signal following serial translocations. Evolution 64(8), 2431-2441.
| Google Scholar | PubMed |
Parker KA, Anderson MJ, Jenkins PF, Brunton DH (2012) The effects of translocation-induced isolation and fragmentation on the cultural evolution of bird song. Ecology Letters 15(8), 778-785.
| Crossref | Google Scholar | PubMed |
Paxton KL, Sebastián-González E, Hite JM, Crampton LH, Kuhn D, Hart PJ (2019) Loss of cultural song diversity and the convergence of songs in a declining Hawaiian forest bird community. Royal Society Open Science 6(8), 190719.
| Crossref | Google Scholar | PubMed |
Peckre L, Kappeler PM, Fichtel C (2019) Clarifying and expanding the social complexity hypothesis for communicative complexity. Behavioral Ecology and Sociobiology 73(11), 1-19.
| Google Scholar |
Podos J (1997) A performance constraint on the evolution of trilled vocalizations in a songbird family (Passeriformes: Emberizidae). Evolution 51(2), 537-551.
| Crossref | Google Scholar | PubMed |
Podos J, Nowicki S (2004) Beaks, adaptation, and vocal evolution in Darwin’s finches. BioScience 54(6), 501-510.
| Crossref | Google Scholar |
Podos J, Warren PS (2007) The evolution of geographic variation in birdsong. Advances in the Study of Behavior 37, 403-458.
| Crossref | Google Scholar |
Reyes EMR, Smith ANH, Rueda D, Sevilla C, Brunton DH, Ortiz-Catedral L (2022) Sexing of the endangered Floreana mockingbird (Mimus trifasciatus) using morphometric measurements. Notornis 69, 257-264.
| Google Scholar |
Rose EM, Prior NH, Ball GF (2022) The singing question: re-conceptualizing birdsong. Biological Reviews 97, 326-342.
| Crossref | Google Scholar | PubMed |
Rowe SJ, Bell BD (2007) The influence of geographic variation in song dialect on post-translocation pair formation in North Island kokako (Callaeas cinerea wilsoni). Notornis 54(1), 28-37.
| Google Scholar |
Ryan SJ (2006) The role of culture in conservation planning for small or endangered populations. Conservation Biology 20(4), 1321-1324.
| Crossref | Google Scholar | PubMed |
Santiago-Alarcon D, Tanksley SM, Parker PG (2006) Morphological variation and genetic structure of Galápagos Dove (Zenaida galapagoensis) populations: issues in conservation for the Galápagos bird fauna. The Wilson Journal of Ornithology 118(2), 194-207.
| Crossref | Google Scholar |
Slabbekoorn H, Smith TB (2000) Does bill size polymorphism affect courtship song characteristics in the African finch Pyrenestes ostrinus? Biological Journal of the Linnean Society 71(4), 737-753.
| Crossref | Google Scholar |
Slabbekoorn H, Smith TB (2002) Bird song, ecology and speciation. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 357(1420), 493-503.
| Crossref | Google Scholar |
Slarkin M (1985) Gene flow in natural populations. Annual Review of Ecology and Systematics 16(1), 393-430.
| Crossref | Google Scholar |
Snowberg LK, Benkman CW (2007) The role of marker traits in the assortative mating within red crossbills, Loxia curvirostra complex. Journal of Evolutionary Biology 20(5), 1924-1932.
| Crossref | Google Scholar | PubMed |
Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences 101(42), 15261-15264.
| Crossref | Google Scholar |
Tanimoto AM, Hart PJ, Pack AA, Switzer R, Banko PC, Ball DL, Sebastián-Gonzálz E, Komarczyk L, Warrington MH (2017) Changes in vocal repertoire of the Hawaiian crow, Corvus hawaiiensis, from past wild to current captive populations. Animal Behaviour 123, 427-432.
| Crossref | Google Scholar |
ten Cate C, Fullagar PJ (2021) Vocal imitations and production learning by Australian musk ducks (Biziura lobata). Philosophical Transactions of the Royal Society B: Biological Sciences 376(1836), 20200243.
| Crossref | Google Scholar |
Tracy LN, Wallis GP, Efford MG, Jamieson IG (2011) Preserving genetic diversity in threatened species reintroductions: how many individuals should be released? Animal Conservation 14(4), 439-446.
| Crossref | Google Scholar |
Vitousek MN, Adelman JS, Gregory NC, Clair JJHS (2007) Heterospecific alarm call recognition in a non-vocal reptile. Biology Letters 3(6), 632-634.
| Crossref | Google Scholar |
Voigt C, Leitner S, Gahr M (2007) Socially induced brain differentiation in a cooperatively breeding songbird. Proceedings of the Royal Society B: Biological Sciences 274(1626), 2645-2652.
| Crossref | Google Scholar |
Whitehead H, Rendell L, Osborne RW, Würsig B (2004) Culture and conservation of non-humans with reference to whales and dolphins: review and new directions. Biological Conservation 120(3), 427-437.
| Crossref | Google Scholar |
Wildenthal JL (1965) Structure in primary song of the mockingbird (Mimus polyglottos). The Auk 82(2), 161-189.
| Crossref | Google Scholar |
Williams H, Lachlan RF (2022) Evidence for cumulative cultural evolution in bird song. Philosophical Transactions of the Royal Society B: Biological Sciences 377(1843), 20200322.
| Crossref | Google Scholar |
Wyles JS, Kunkel JG, Wilson AC (1983) Birds, behavior, and anatomical evolution. Proceedings of the National Academy of Sciences 80(14), 4394-4397.
| Crossref | Google Scholar |
