Variation within and between courts in visual components of Swallow-tailed Manakin (Chiroxiphia caudata) display

Abstract

Birds are well known for displaying courtship exhibitions shaped by sexual selection that involve combinations of visual, motor, and acoustic components. Among such multifaceted exhibitions are those of male piprids, which can perform coordinated or cooperative displays to attract females. Here we focus on the Swallow-tailed Manakin (Chiroxiphia caudata), endemic to the Atlantic Forest, whose displays include two or more males executing a cartwheel-type movement (“cooperative display”) and solo exhibitions. We used videography to describe and analyze male maneuvers and to test differences in display parameters between courts (where adult males perform coordinated/cooperative displays in groups of two to six individuals within an arena) and between dominant and subordinate males. We recorded displays of individuals from four courts in southern Brazil during two breeding seasons. We identified nine male display elements, five in cooperative, three in solo formations and one in other contexts, in addition to two elements performed exclusively by females. Sequences of male display elements were highly stereotyped, but three display parameters differed between courts: vertical flight height, distance from which males approached females and cartwheel velocity. Moreover, subordinates flew longer vertical flights than dominants. This variability suggests that females may evaluate courts based on display parameters, leading to their decision to remain at the perch, attend the solo display and eventually copulate. The vertical flight duration can also be a signal used during intrasexual communication, such as for hierarchy establishment. Our detailed description of male display attributes provides essential evidence that courts differ in motor parameters, and opens an avenue for further studies on sexual selection mechanisms in the Swallow-tailed Manakin and other manakins.

Zusammenfassung

Variation visueller Komponenten der Schaubalz beim Blaubrustpipra ( Chiroxiphia caudata ) innerhalb und zwischen Balzarenen.

Vögel sind bekannt für ihr auffälliges, durch sexuelle Selektion geformtes Balzverhalten, welches Kombinationen aus visuellen, motorischen und akustischen Komponenten umfasst. Zu diesen facettenreichen Darbietungen gehören die der männlichen Schnurrvögel, welche zur Anlockung von Weibchen koordiniertes oder kooperatives Schaubalzverhalten ausführen können. Hier betrachten wir den für den Atlantischen Regenwald endemischen Blaubrustpipra (Chiroxiphia caudata), bei dem als Teil der Schaubalz zwei oder mehr Männchen einen radschlagähnlichen Bewegungsablauf („kooperative Schaubalz“) sowie Einzeldarbietungen zeigen. Mittels Videoaufnahmen beschrieben und analysierten wir die Manöver der Männchen und untersuchten diese auf Unterschiede bezüglich der Parameter des Balzverhaltens zwischen verschiedenen Balzarenen sowie zwischen dominanten und untergeordneten Männchen. Über zwei Brutsaisons hinweg nahmen wir Schaubalzen von Individuen aus vier Balzarenen in Südbrasilien auf. Wir identifizierten neun Schaubalzelemente bei den Männchen, fünf davon in kooperativen, drei in einzelnen Darbietungen sowie eine weitere in anderem Kontext auftretende; zusätzlich noch zwei Elemente, die ausschließlich von den Weibchen ausgeführt wurden. Die Abfolge der Schaubalzelemente war bei den Männchen hochgradig stereotyp, drei Parameter unterschieden sich jedoch zwischen den Balzarenen: vertikale Flughöhe, der Abstand, bis zu dem die Männchen sich den Weibchen näherten, und die Geschwindigkeit des Radschlags. Außerdem führten untergeordnete Vögel längere vertikale Flüge aus als dominante. Diese Variabilität legt nahe, dass die Weibchen die Arenen möglicherweise aufgrund der Darbietungsparameter bewerten, woraufhin sie entscheiden, ob sie auf der Sitzwarte bleiben, der Einzelvorstellung zuschauen und schließlich kopulieren. Die Dauer des Vertikalfluges kann auch ein Signal im Rahmen der intrasexuellen Kommunikation darstellen und zum Beispiel der Hierarchiefindung dienen. Unsere detaillierte Beschreibung der Attribute des männlichen Balzverhaltens liefert entscheidende Belege dafür, dass sich die Arenen hinsichtlich der motorischen Parameter unterscheiden und bereitet den Weg für weiterführende Untersuchungen zu den Mechanismen der sexuellen Selektion beim Blaubrustpipra und anderen Schnurrvögeln.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Andersson M (1994) Sexual selection. Princeton University Press, NJ

    Google Scholar 

  2. Barske J, Schlinger BA, Wikelski M, Fusani L (2011) Female choice for male motor skills. Proc R Soc B Biol Sci 278:3523–3528

    Article  Google Scholar 

  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  4. Bodony D, Day L, Friscia A, Fusani L, Kharon A, Swenson G, Wikelski M, Schlinger B (2016) Determination of the wingsnap sonation mechanism of the Golden-collared Manakin (Manacus vitellinus). J Exp Biol 219:1524–1534

    Article  PubMed  Google Scholar 

  5. Boscolo D, Metzger JP (2009) Is bird incidence in Atlantic forest fragments influenced by landscape patterns at multiple scales? Landscape Ecol 24:907–918

    Article  Google Scholar 

  6. Bostwick KS, Prum RO (2005) Courting bird sings with stridulating wing feathers. Science 309:736

    Article  CAS  PubMed  Google Scholar 

  7. Brodt MSC, Della-Flora F, Cáceres N (2013) Non-linear ascension in a reproductive hierarchy of the Blue Manakin (Chiroxiphia caudata). Acta Ethol 17:181–185

    Article  Google Scholar 

  8. Byers J, Hebets E, Podos J (2010) Female mate choice based upon male motor performance. Anim Behav 79:771–778

    Article  Google Scholar 

  9. Cárdenas-Posada G, Cadena CD, Blake JG, Loiselle BA (2018) Display behaviour, social organization and vocal repertoire of Blue-backed Manakin Chiroxiphia pareola napensis in northwest Amazonia. Ibis 160:269–282

    Article  Google Scholar 

  10. Coccon F, Schlinger BA, Fusani L (2012) Male Golden-collared Manakins Manacus vitellinus do not adapt their courtship display to spatial alteration of their court. Ibis 154:173–176

    Article  Google Scholar 

  11. Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Curr Biol 16:R755–R765

    Article  CAS  PubMed  Google Scholar 

  12. Darwin C (1871) The descent of man, and selection in relation to sex. Murray, London

    Google Scholar 

  13. DuVal EH (2007a) Cooperative display and lekking behavior of the Lance-tailed Manakin (Chiroxiphia lanceolata). Auk 124:1168–1185

    Article  Google Scholar 

  14. DuVal EH (2007b) Social organization and variation in cooperative alliances among male Lance-tailed Manakins. Anim Behav 73:391–401

    Article  Google Scholar 

  15. Foster MS (1977) Odd couples in manakins: a study of social organization and cooperative breeding in Chiroxiphia linearis. Am Nat 11:845–853

    Article  Google Scholar 

  16. Foster MS (1981) Cooperative behavior and social organization of the Swallow-tailed Manakin (Chiroxiphia caudata). Behav Ecol Sociobiol 9:167–177

    Article  Google Scholar 

  17. Foster MS (1987) Delayed maturation, neoteny, and social system differences in two manakins of the genus Chiroxiphia. Evolution 41:547–558

    Article  PubMed  Google Scholar 

  18. Francisco MR, Gibbs HL, Galetti PM, Lunardi VO, Galetti Junior PM (2007) Genetic structure in a tropical lek-breeding bird, the Blue Manakin (Chiroxiphia caudata) in the Brazilian Atlantic Forest. Mol Ecol 16:4908–4918

    Article  PubMed  Google Scholar 

  19. Francisco MR, Gibbs HL, Galetti PM Jr (2009) Patterns of individual relatedness at Blue Manakin (Chiroxiphia caudata) leks. Auk 126:47–53

    Article  Google Scholar 

  20. Fusani L, Schlinger BA (2012) Proximate and ultimate causes of male courtship behavior in Golden-collared Manakins. J Ornithol 153:119–124

    Article  Google Scholar 

  21. Fusani L, Giordano M, Day LB, Schlinger BA (2007) High-speed video analysis reveals individual variability in the courtship displays of male Golden-collared Manakins. Ethology 113:964–972

    Article  Google Scholar 

  22. Girard MB, Kasumovic MM, Elias DO (2011) Multi-modal courtship in the Peacock Spider, Maratus volans (OP-Cambridge, 1874). PLoS One 6:e25390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Gomez D, Richardson C, Lengagne T, Plenet S, Joly P, Léna JP, Théry M (2009) The role of nocturnal vision in mate choice: females prefer conspicuous males in the European Tree Frog (Hyla arborea). Proc R Soc B Biol Sci 276:2351–2358

    Article  Google Scholar 

  24. Hasui E, Gomes VSM, Kiefer MC, Tamashiro J, Silva WR (2009) Spatial and seasonal variation in niche partitioning between Blue Manakin (Chiroxiphia caudata) and Greenish Schiffornis (Schiffornis virescens) in southeastern Brazil. Stud Neotrop Fauna Environ 44:149–159

    Article  Google Scholar 

  25. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  Google Scholar 

  26. Keyser AJ, Hill GE (2010) Structurally based plumage coloration is an honest signal of quality in male Blue Grosbeaks. Behav Ecol 11:202–209

    Article  Google Scholar 

  27. LeBas NR, Marshall NJ (2000) The role of colour in signalling and male choice in the agamid lizard Ctenophorus ornatus. Proc R Soc B Biol Sci 267:445–452

    Article  CAS  Google Scholar 

  28. Lill A (1974) Sexual behavior of the lek-forming White-bearded Manakin (Manacus manacus trinitalis Hartert). Z Tierpsychol 36:1–36

    Article  CAS  PubMed  Google Scholar 

  29. Lindsay WR, Houck JT, Giuliano CE, Day LB (2015) Acrobatic courtship display coevolves with brain size in manakins (Pipridae). Brain Behav Evol 85:29–36

    Article  PubMed  Google Scholar 

  30. Loiselle BA, Graham CH, Goerck JM, Ribeiro MC (2010) Assessing the impact of deforestation and climate change on the range size and environmental niche of bird species in the Atlantic forests, Brazil. J Biogeogr 37:1288–1301

    Article  Google Scholar 

  31. Lukianchuk KC, Doucet SM (2014a) Cooperative courtship display in Long-tailed Manakins Chiroxiphia linearis: predictors of courtship success revealed through full characterization of display. J Ornithol 155:729–743

    Article  Google Scholar 

  32. Lukianchuk KC, Doucet SM (2014b) A young manakin knows his place: evidence for an age-graded dominance hierarchy among Long-tailed Manakins. Ethology 120:693–701

    Article  Google Scholar 

  33. Mallet-Rodrigues F, Dutra R (2012) Acquisition of definitive adult plumage in male Blue Manakins Chiroxiphia caudata. Cotinga 34:24–27

    Google Scholar 

  34. Manica LT, Graves JA, Podos J, Macedo RH (2016) Multimodal flight display of a Neotropical songbird predicts social pairing but not extrapair mating success. Behav Ecol Sociobiol 70:2039–2052

    Article  Google Scholar 

  35. Manica LT, Macedo RH, Graves JA, Podos J (2017) Vigor and skill in the acrobatic mating displays of a Neotropical songbird. Behav Ecol 28:164–173

    Article  Google Scholar 

  36. Marques Silva S, Eduardo Agne C, Aleixo A, Bonatto SL (2018) Phylogeny and systematics of Chiroxiphia and Antilophia manakins (Aves, Pipridae). Mol Phylogenet Evol 127:706–711

    Article  Google Scholar 

  37. Møller AP, Birkhead TR (1994) The evolution of plumage brightness in birds is related to extrapair paternity. Evolution 48:1089–1100

    Article  PubMed  Google Scholar 

  38. Nowicki S, Peters S, Podos J (1998) Song learning, early nutrition and sexual selection in songbirds. Am Zool 38:179–190

    Article  Google Scholar 

  39. Ota N, Gahr M, Soma M (2015) Tap dancing birds: the multimodal mutual courtship display of males and females in a socially monogamous songbird. Sci Rep 5:16614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Patricelli GL, Uy JAC, Walsh G, Borgia G (2002) Sexual selection: male displays adjusted to female’s response. Nature 415:279–280

    Article  CAS  Google Scholar 

  41. Prum RO (1994) Phylogenetic analysis of the evolution of alternative social behavior in the manakins (Aves: Pipridae). Evolution 48:1657–1675

    Article  PubMed  Google Scholar 

  42. Prum RO (1997) Phylogenetic tests of alternative intersexual selection mechanisms: trait macroevolution in a polygynous clade (Aves: Pipridae). Am Nat 149:668–692

    Article  Google Scholar 

  43. Prum RO (1998) Sexual selection and the evolution of mechanical sound production in manakins (Aves: Pipridae). Anim Behav 55:977–994

    Article  CAS  PubMed  Google Scholar 

  44. R Core Team (2015) R: a language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria. http://www.R-project.org

  45. Reginato M, Goldenberg R (2007) Análise florística, estrutural e fitogeográfica da vegetação em região de transição entre as Florestas Ombrófilas Mista e Densa Montana, Piraquara, Paraná, Brasil. Hoehnea 34:349–364

    Article  Google Scholar 

  46. Rueden CT et al (2017) ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinform 18:529

    Article  Google Scholar 

  47. Ryder TB, Durães R (2005) It’s not easy being green: using molt and morphological criteria to age and sex green-plumage manakins (Aves: Pipridae). Ornithol Neotrop 16:481–491

    Google Scholar 

  48. Scholes E (2006) Courtship ethology of Carola’s Parotia (Parotia carolae). Auk 123:967–990

    Google Scholar 

  49. Scholes E (2008) Structure and composition of the courtship phenotype in the bird of paradise Parotia lawesii (Aves: Paradisaeidae). Zoology 111:260–278

    Article  PubMed  Google Scholar 

  50. Schaedler M, Ribeiro PHL, Guaraldo AC, Manica LT (2019) Acoustic signals and repertoire complexity in Swallow-tailed Manakins (Chiroxiphia caudata, Aves: Pipridae). Bioacoustics. https://doi.org/10.1080/09524622.2018.1563870

    Article  Google Scholar 

  51. Scholes E, Gillis JM, Laman TG (2017) Visual and acoustic components of courtship in the bird-of-paradise genus Astrapia (Aves: Paradisaeidae). PeerJ 5:e3987

    Article  PubMed  PubMed Central  Google Scholar 

  52. Sick H (2001) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro

    Google Scholar 

  53. Snow DW (1963) The display of the Blue-backed Manakin, Chiroxiphia pareola, in Tobago, WI. Zoologica 48:167–176

    Google Scholar 

  54. Tello JG (2001) Lekking behavior of the Round-tailed Manakin. Condor 103:198–321

    Article  Google Scholar 

  55. Uezu A, Metzger JP, Vielliard JME (2005) Effects of structural and functional connectivity and patch size on the abundance of seven Atlantic Forest bird species. Biol Conserv 123:507–519

    Article  Google Scholar 

  56. Vanderbilt CC, Kelley JP, DuVal EH (2015) Variation in the performance of cross-contextual displays suggests selection on dual-male phenotypes in a lekking bird. Anim Behav 107:213–219

    Article  Google Scholar 

  57. Zahavi A (1980) Ritualization and the evolution of movement signals. Behaviour 72:77–80

    Article  Google Scholar 

  58. Zima PV, Perrella DF, Biagolini-Jr CH, Ribeiro-Silva L, Francisco MR (2017) Breeding behavior of the Atlantic Forest endemic Blue Manakin (Chiroxiphia caudata). Wilson J Ornithol 129:53–61

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to all field and lab assistants who helped collect and process the data. We are also grateful to Laura M. Schaedler, Jeff Podos and anonymous referees for valuable comments and suggestions, to members of the Manakins Research Coordination Network for productive discussions regarding manakin species, to Miguel Â. Marini, Marco Pizo, Alex Jahn and IdeaWild for equipment donation and sharing and to Instituto Ambiental do Paraná, Chico Mendes Institute for Biodiversity Conservation and National Center for Bird Conservation (ICMBio/CEMAVE) for research permits.

Funding

This study was funded by the Conselho de Aperfeiçoamento de Pessoal de Nível Superior (Capes/Brazil) by a scholarship granted to P. H. L. R. and A. C. G.; the National Council for Scientific and Technological Development (CNPq/Brazil, grant to L. T. M. no. 455908/2014-1); the Animal Behavior Society for the Student Research Grant to P. H. L. R.; the Fundação de Amparo à Pesquisa do Distrito Federal (FAP-DF/Brazil, grant no. 193.000.845 to R. H. M.).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Lilian T. Manica.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in the studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (license nos.: Sistema de Autorização e Informação em Biodiversidade no. 44439, Centro Nacional de Pesquisa e Conservação de Aves Silvestres no. 1195110 and Ethics Commitee of the Universidade Federal do Paraná no. 820).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by F. Bairlein.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1. Repertoire of male and female Swallow-tailed Manakin displays

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ribeiro, P.H.L., Guaraldo, A.C., Macedo, R.H. et al. Variation within and between courts in visual components of Swallow-tailed Manakin (Chiroxiphia caudata) display. J Ornithol 160, 485–496 (2019). https://doi.org/10.1007/s10336-019-01627-0

Download citation

Keywords

  • Atlantic forest
  • Lekking
  • Motor display
  • Pipridae
  • Sexual selection