Defending as a unit: sex- and context-specific territorial defence in a duetting bird

Abstract

Behaviours such as territorial defence represent functionally integrated traits that underlie multiple behavioural variables such as physical and acoustic responses. Characterizing the multivariate structure of such traits is fundamental to understand their evolution. In bird species that form stable pair bonds and are territorial year-round, both sexes are expected to defend their territory; however, the role that each sex plays in defending their shared territory remains largely unknown. Evidence for the sex-roles during territorial defence is mixed and sex- and context-specific characterizations of territorial defence embracing the multivariate nature of the trait are currently lacking. Here, we investigated sex- and context-specific variation in a hypothesised latent variable called ‘territorial defence’ and tested whether duets were part of territorial defence in a wild population of rufous hornero (Furnarius rufus). To do so, we combined a simulated territorial intrusion approach during nest building and provisioning contexts with a structural equation modelling approach. Our results showed that, in males and females, the six measured behavioural variables were linked by a single latent trait, territorial defence, in both contexts. Flights over the decoy and duet songs were equally good proxies of territorial defence. Although males were defending more the territory than females, pair members showed a positive correlation in their behaviour. The structural equation modelling framework enabled us to capture a complex correlation pattern among behavioural variables, expanding upon a classic body of research on territorial defence. Thus, the combination of classical behavioural approaches with sophisticated statistical analyses brings new exciting possibilities to the field of behavioural ecology.

Significance statement

Territorial defence is a key behaviour in territorial species as it plays a major role in an individual’s reproductive success and survival. Additionally, territorial defence has been proposed as one possible evolutionary driver of duetting behaviour, one of the most fascinating vocal behaviours in birds. As behaviours are evolutionary characters, they must be studied in a multivariate framework. In this study, we focused on characterizing territorial defence during a simulated territorial intrusion in an integrative manner using a structural equation modelling framework. We did so in male and female rufous horneros (Aves: Furnaridae) across two breeding contexts, while simultaneously testing theoretical predictions about the role of duetting behaviour as key part of territorial defence. Overall, our study provides for the first time a sex- and context-comparison of the multivariate, latent variable ‘territorial defence’ in duetting birds, while highlighting the potential of combining field behavioural approaches with structural equation modelling.

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

Fig. 1
Fig. 2
Fig. 3

Data availability

The datasets generated and/or analysed during the current study are available in the open repository: Mendeley Data (https://data.mendeley.com/datasets/7ztwn539jd/1).

References

  1. Adreani NM, Goymann W, Mentesana L (2018) Not one hormone or another: aggression differentially affects progesterone and testosterone in a South American ovenbird. Horm Behav 105:104–109

    CAS  PubMed  Google Scholar 

  2. Apfelbeck B, Goymann W (2011) Ignoring the challenge? Male black redstarts (Phoenicurus ochruros) do not increase testosterone levels during territorial conflicts but they do so in response to gonadotropin-releasing hormone. Proc R Soc Lond B 278:3233–3242

    CAS  Google Scholar 

  3. Araya-Ajoy YG, Dingemanse NJ (2013) Characterizing behavioural “characters”: an evolutionary framework. Proc R Soc B 281:20132645

    PubMed  Google Scholar 

  4. Bard SC, Hau M, Wikelski M, Wingfield JC (2002) Vocal distinctiveness and response to conspecific playback in the spotted antbird, a neotropical suboscine. Condor 104:387–394

    Google Scholar 

  5. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. https://cran.r-project.org/web/packages/lme4/index.html

  6. Bollen KA (2002) Latent variables in psychology and the social sciences. Annu Rev Psychol 53:605–634

    PubMed  Google Scholar 

  7. Burnham KP, Anderson DR (2004) Multimodel inference. Sociol Methods Res 33:261–304

    Google Scholar 

  8. Card NA, Little TD (2007) Studying agression with structural equation modeling. In: Flannery DJ, Vazsonyi AT, Waldman ID (eds) The Cambridge handbook of violent behavior and aggression. Cambridge University Press, New York, pp 727–739

    Google Scholar 

  9. Carter AJ, Feeney WE (2012) Taking a comparative approach: analysing personality as a multivariate behavioural response across species. PLoS One 7:e42440

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Clutton-Brock TH, Vincent ACJ (1991) Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60

    CAS  PubMed  Google Scholar 

  11. Demko AD, Mennill DJ (2018) Male and female signaling behavior varies seasonally during territorial interactions in a tropical songbird. Behav Ecol Sociobiol 72:84

    Google Scholar 

  12. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54

    PubMed  Google Scholar 

  13. Diniz P, Ribeiro PHL, Rech GS, Macedo RH (2016) Monochromatism, cryptic sexual dimorphism and lack of assortative mating in the Rufous Hornero, Furnarius rufus albogularis. Emu 116:294–300

    Google Scholar 

  14. Diniz P, Júnior EF d S, Webster MS, Macedo RH (2018) Duetting behavior in a Neotropical ovenbird: sexual and seasonal variation and adaptive signaling functions. J Avian Biol 49:jav–01637

    Google Scholar 

  15. Diniz P, Macedo RH, Webster MS (2019) Duetting correlates with territory quality and reproductive success in a suboscine bird with low extra-pair paternity. Auk 136:1–13

    Google Scholar 

  16. Diniz P, Rech G, Ribeiro PH, Webster MS, Macedo RH (2020) Partners coordinate territorial defence against simulated intruders in a duetting ovenbird. Ecol Evol 10:81–89

    PubMed  Google Scholar 

  17. Douglas SB, & Mennill DJ (2010) A review of acoustic playback techniques for studying avian vocal duets. J Field Ornithol 81(2):115–129

  18. Dowling J, Webster MS (2016) An experimental test of duet function in a fairy-wren (Malurus) with moderate cuckoldry rates. Behav Ecol 27:228–236

    Google Scholar 

  19. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    CAS  PubMed  Google Scholar 

  20. Farabaugh SM (1982) The ecological and social significance of duetting. In: Kroodsma DE, Miller EH (eds) Acoustic communication in birds, vol 2. Academic Press, New York, pp 85–124

    Google Scholar 

  21. Fedy BC, Stutchbury BJM (2005) Territory defence in tropical birds: are females as aggressive as males? Behav Ecol Sociobiol 58:414–422

    Google Scholar 

  22. Fraga RM (1980) The breeding of Rufous Horneros (Furnarius rufus). Condor 82:58–68

    Google Scholar 

  23. Freeman BG, Montgomery GA, Schluter D (2017) Evolution and plasticity: divergence of song discrimination is faster in birds with innate song than in song learners in Neotropical passerine birds. Evolution 71:2230–2242

    PubMed  Google Scholar 

  24. Garcia JT, Arroyo BE (2002) Intra- and interspecific agonistic behaviour in sympatric harriers during the breeding season. Anim Behav 64:77–84

    Google Scholar 

  25. Gelman A, Yu-Sung S (2015) arm: data analysis using regression and multilevel/hierarchical models. R package version 1.8-5, https://cran.r-project.org/web/packages/arm/arm.pdf

  26. Gill SA, Alfson ED, Hau M (2007) Context matters: female aggression and testosterone in a year-round territorial neotropical songbird (Thyrothorus leucotis). Proc R Soc Lond B 274:2187–2194

    CAS  Google Scholar 

  27. Greenberg R, Gradwohl J (1983) Sexual roles in the dot-winged antwren (Microrhopias quixensis), a tropical forest passerine. Auk 100:920–925

    Google Scholar 

  28. Hall ML (2004) A review of hypotheses for the functions of avian duetting. Behav Ecol Sociobiol 55:415–430

    Google Scholar 

  29. Hall ML (2009) A review of vocal duetting in birds. Adv Study Behav 40:67–121

    Google Scholar 

  30. Hall ML, Peters A (2008) Coordination between the sexes for territorial defence in a duetting faire-wren. Anim Behav 76:65–73

    Google Scholar 

  31. Harris MR, Siefferman L (2014) Interspecific competition influences fitness benefits of assortative mating for territorial aggression in eastern bluebirds (Sialia sialis). PLoS One 9:e88668

    PubMed  PubMed Central  Google Scholar 

  32. Harrison XA (2009) Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2:e616

    Google Scholar 

  33. Houle D, Pélabon C, Wagner GP, Hansen TF (2011) Measurement and meaning in biology. Q Rev Biol 86:3–34

    PubMed  Google Scholar 

  34. Huntingford FA (1976) An investigation of the territorial behaviour of the three-spined stickleback (Gasterosteus aculeatus) using principal components analysis. Anim Behav 24:822–834

    Google Scholar 

  35. Koloff J, Mennill DJ (2013) The responses of duetting antbirds to stereo duet playback provide support for the joint territory defence hypothesis. Ethology 119:462–471

    Google Scholar 

  36. Korner-Nievergelt F, Roth T, von Felten S, Guélat J, Almasi B, Korner-Nievergelt P (2015) Bayesian data analysis in ecology using linear models with R, BUGS, and Stan. Academic Press, New York

    Google Scholar 

  37. Langmore NE (1998) Functions of duet and solo songs of female birds. Trends Ecol Evol 13:136–140

    CAS  PubMed  Google Scholar 

  38. Logue DM (2005) Cooperative defence in duet singing birds. Cognition, Brain, Behavior

  39. Massoni V, Reboreda JC, López GC, Aldatz MF (2012) High coordination and equitable parental effort in the Rufous Hornero. Condor 114:564–570

    Google Scholar 

  40. Mentesana L, Adreani NM (2020) Is aggression costly? Acute aggressive behavior increases oxidative stress independently of testosterone. bioRxiv. https://doi.org/10.1101/2020.04.06.027029

  41. Morton ES, Derrickson KC (1996) Song ranging by the dusky antbird, Cercomacra tyrannina: ranging without song learning. Behav Ecol Sociobiol 39:195–201

    Google Scholar 

  42. Morton ES, Derrickson KC, Stutchbury BJM (2000) Territory switching behavior in a sedentary tropical passerine, the dusky antbird (Cercomacra tyrannina). Behav Ecol 11:648–653

    Google Scholar 

  43. Naguib M, Mennill DJ (2010) The signal value of birdsong: empirical evidence suggests song overlapping is a signal. Anim Behav 80:e11–e15

    Google Scholar 

  44. Nilsson JÅ, Råberg L (2001) The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128:187–192

    PubMed  Google Scholar 

  45. Odom KJ, Logue DM, Studds CE, Monroe MK, Campbell SK, Omland KE (2017) Duetting behavior varies with sex, season, and singing role in a tropical oriole (Icterus icterus). Behav Ecol 28:1256–1265

    Google Scholar 

  46. Owens IPF, Thompson DBA (1994) Sex differences, sex ratios and sex roles. Proc R Soc Lond B 258:93–99

    CAS  Google Scholar 

  47. Quinard A, Cézilly F (2012) Sex roles during conspecific territorial defence in the Zenaida dove, Zenaida aurita. Anim Behav 83:47–54

    Google Scholar 

  48. Quirós-Guerrero E, Janeiro MJ, Lopez-Morales M, Cresswell W, Templeton CN (2017) Riverside wren pairs jointly defend their territories against simulated intruders. Ethology 123:949–956

    Google Scholar 

  49. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  50. Robinson A (1949) The biological significance of bird song in Australia. Emu 48:291–315

    Google Scholar 

  51. Roper JJ (2005) Sexually distinct songs in the duet of the sexually monomorphic Rufous Hornero. J Ornithol 76:234–236

    Google Scholar 

  52. Schuett W, Tregenza T, Dall SRX (2010) Sexual selection and animal personality. Biol Rev 85:217–246

    PubMed  Google Scholar 

  53. Searcy WA, Beecher MD (2009) Song as an aggressive signal in songbirds. Anim Behav 78:1281–1292

    Google Scholar 

  54. Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455

    Google Scholar 

  55. Sosa-López JR, Mennill DJ, Renton K (2017) Sexual differentiation and seasonal variation in response to conspecific and heterospecific acoustic signals. Ethology 123:460–466

    Google Scholar 

  56. Sprenger D, Dingemanse NJ, Dochtermann NA, Theobald J, Walker SP (2012) Aggressive females become aggressive males in a sex-changing reef fish. Ecol Lett 15:986–992

    PubMed  Google Scholar 

  57. Stamps JA, Krishnan VV (1997) Functions of fights in territory establishment. Am Nat 150:393–405

    CAS  PubMed  Google Scholar 

  58. Tobias JA, Sheard C, Seddon N, Meade A, Cotton AJ, Nakagawa S (2016) Territoriality, social bonds, and the evolution of communal signaling in birds. Front Ecol Evol 4:74

    Google Scholar 

  59. Topp SM, Mennill DJ (2008) Seasonal variation in the duetting behaviour of rufous-and-white wrens (Thryothorus rufalbus). Behav Ecol Sociobiol 62:1107–1117

    Google Scholar 

  60. Warner RR, Hoffman SG (1980) Population density and the economics of territorial defence in a coral reef fish. Ecology 61:772–780

    Google Scholar 

  61. Wickler W, Seibt U (1980) Vocal dueting and the pair bond. Z Tierpsychol 52:217–226

    Google Scholar 

  62. Willis EO (1972) The behavior of ocellated antbirds. Ornithol Monogr 10:1–162

    Google Scholar 

  63. Wingfield JC (1994) Regulation of territorial behavior in the sedentary song sparrow, Melospiza melodia morphna. Horm Behav 28:1–15

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Klaus Pichler for his help to prepare the STI and all the ‘INIA Las Brujas’ staff for supporting us with accommodation and equipment during fieldwork. We also thank Facultad de Ciencias and the Ethology lab from Universidad de la República and Juan Carlos Reboreda and the ‘Laboratorio de Ecología y Comportamiento Animal’ at the Universidad de Buenos Aires for the logistical support, and Pablo Tubaro from the Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’ (MACN) for providing us with the mounted hornero. We are grateful to Manfred Gahr and Michaela Hau for their valuable support. We also thank Yimen Araya-Ajoy, Glenn Cockburn, Luke Eberhart-Phillips and Wolfgang Wickler for constructive criticism on previous versions of the manuscript. Finally, we want to thank the anonymous reviewers for constructive feedback on the manuscript.

Funding

This work was funded by the International Max Planck Research School (IMPRS) for Organismal Biology, and by Idea Wild that provided field equipment.

Author information

Affiliations

Authors

Contributions

NMA, LM and MM share first authorship and names are ordered at random. NMA and LM conceived the study and designed the study. BT provided logistic support. NMA, LM, EG and EC collected the data. NMA, LM and MM analysed the data. NMA, LM and MM wrote the manuscript with input from all authors.

Corresponding author

Correspondence to Nicolas M. Adreani.

Ethics declarations

Ethical approval

The experimental procedures of this study have approval by the Ethics Committee of Animal Experimentation (CEUA) of the Facultad de Ciencias of the Universidad de la República, Uruguay (Protocol number 186, file 2400-11000090-16).

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

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

Communicated by D. Rubenstein

Electronic supplementary material

ESM 1

(DOCX 161 kb).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mentesana, L., Moiron, M., Guedes, E. et al. Defending as a unit: sex- and context-specific territorial defence in a duetting bird. Behav Ecol Sociobiol 74, 111 (2020). https://doi.org/10.1007/s00265-020-02891-4

Download citation

Keywords

  • Territorial aggression
  • Duets
  • Behavioural character
  • Phenotypic integration
  • Female aggression
  • Structural equation analysis