Vocal variation in Chiroxiphia boliviana (Aves; Pipridae) along an Andean elevational gradient

  • Mariana Villegas
  • John G. Blake
  • Kathryn E. Sieving
  • Bette A. Loiselle
Original Paper

Abstract

Bird vocalizations are likely shaped both by natural and sexual selection. Here we test the sensory-drive hypothesis, which states that communication signals diverge as a direct adaptation to the signaling environment and can evolve to minimize degradation and maximize transmission. We examined the effects of elevation and other habitat variables on variation in vocalizations of Chiroxiphia boliviana (Aves, Pipridae) along an elevational gradient (1300–2500 m) in cloud and humid montane forests in the Andes of Bolivia. We also conducted sound transmission experiments to determine if reverberation and attenuation changed along the gradient. Reverberation increased at higher elevations, and attenuation decreased at higher elevations and increased for higher frequencies. We recorded vocalizations from ~ 50 individuals throughout the elevational gradient and examined variation in duration and bandwidth of short calls (used as contact calls between males), 2 display calls (advertisement for females) and 2 types of male–male duets (including interval times between males). Duration of short calls, display 1 and duet 1 increased with elevation. Bandwidth of short calls increased at mid-elevation categories and decreased at high elevations, whereas bandwidth of display 1 and duet 1 decreased with elevation. We also directly related the transmission properties to vocalizations and found that bandwidth of short calls decreased with reverberation and attenuation, bandwidth of display 2 decreased with reverberation, and duration of duet 1 both increased and decreased with attenuation (at 3 and 4 kHz, respectively). This study suggests that vocalizations by C. boliviana may be adapted to the habitat transmission properties along the elevational gradient; and perhaps that increasing song length and concentrating energy within a narrow bandwidth may lead to an increase in amplitude and improvement in transmission. Overall, our results support the sensory-drive hypothesis and suggest that this form of selection is likely common along tropical elevational gradients.

Keywords

Andes Bolivia Lek Manakins Sensory-drive Suboscines Vocalizations 

Notes

Acknowledgements

We thank M. Symonds, two anonymous reviewers and an associate editor, whose comments and suggestions greatly improved this manuscript. We would like to thank R. Kimball and J. Austin for their advice and valuable insights on previous versions of the manuscript. We also thank J. Lucas for an interesting discussion and assistance in the use of Praat. We are grateful to the Dirección General de Biodiversidad y Áreas Protegidas from Bolivia for providing research permits (MMAyA-VMA-DGBAP No. 490/11). M. Villegas would like to thank M. Gonzalez, E. Quenta, V. Lazo, D. Morón, A. C. Paca, A. Rojas, D. Torrico and M. Villegas for their much appreciated assistance in the field. This research was partially funded by the College for Agricultural and Life Sciences (CALS) at the University of Florida.

Compliance with ethical standards

Conflict of interests

The authors declare that they have no conflicts of interest.

Supplementary material

10682_2018_9934_MOESM1_ESM.docx (1.1 mb)
Supplementary material 1 (DOCX 1081 kb)

References

  1. Abbey-Lee RN, Kaiser A, Mouchet A, Dingemanse NJ (2016) Immediate and carry-over effects of perceived predation risk on communication behavior in wild birds. Behav Ecol 27:708–716CrossRefGoogle Scholar
  2. Badyaev AV, Ghalambor CK (2001) Evolution of life histories along elevational gradients: trade-off between parental care and fecundity. Ecology 82:2948–2960CrossRefGoogle Scholar
  3. Barker NK (2008) Bird song structure and transmission in the Neotropics: trends, methods and future directions. Ornitol Neotrop 19:175–199Google Scholar
  4. Barve S, Dhondt AA, Mathur VB, Cheviron ZA (2016) Life-history characteristics influence physiological strategies to cope with hypoxia in Himalayan birds. Proc R Soc B Biol Sci 283:20162201CrossRefGoogle Scholar
  5. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48Google Scholar
  6. Blumstein DT, Turner AC (2005) Can the acoustic adaptation hypothesis predict the structure of Australian birdsong? Acta Ethol 8:35–44CrossRefGoogle Scholar
  7. Boersma P, Weenik D (2016) Praat: doing phonetics by computer [Computer program]. Version 6.0.13. http://www.praat.org/. Accessed 5 Feb 2016
  8. Boncoraglio G, Saino N (2007) Habitat structure and the evolution of bird song: a meta-analysis of the evidence for the acoustic adaptation hypothesis. Funct Ecol 21:134–142CrossRefGoogle Scholar
  9. Boughman JW (2002) How sensory drive can promote speciation. Trends Ecol Evol 17:571–577CrossRefGoogle Scholar
  10. Boyle WA, Sandercock BK, Martin K (2016) Patterns and drivers of intraspecific variation in avian life history along elevational gradients: a meta-analysis. Biol Rev 91:469–482CrossRefGoogle Scholar
  11. Brumm H, Naguib M (2009) Environmental acoustics and the evolution of bird song. Adv Study Behav 40:1–33CrossRefGoogle Scholar
  12. Caro LM, Caycedo-Rosales PC, Bowie RCK, Slabbekoorn H, Cadena CD (2013) Ecological speciation along an elevational gradient in a tropical passerine bird? J Evol Biol 26:357–374CrossRefPubMedGoogle Scholar
  13. Dingle C, Halfwerk W, Slabbekoorn H (2008) Habitat-dependent song divergence at subspecies level in the grey-breasted wood-wren. J Evol Biol 21:1079–1089CrossRefPubMedGoogle Scholar
  14. Dingle C, Poelstra JW, Halfwerk W, Brinkhuizen DM, Slabbekoorn H (2010) Asymmetric response patterns to subspecies-specific song differences in allopatry and parapatry in the gray-breasted wood-wren. Evolution 64:3537–3548CrossRefPubMedGoogle Scholar
  15. Dooling RJ (2004) Audition: can birds hear everything they sing? In: Marler P, Slabbekoorn H (eds) Nature’s music, the science of birdsong. Elsevier Academic Press, San Diego, pp 206–224Google Scholar
  16. Doutrelant C, Lambrechts MM (2001) Macrogeographic variation in song: a test of competition and habitat effects in Blue Tits. Ethology 107:533–544CrossRefGoogle Scholar
  17. Dubay SG, Witt CC (2014) Differential high-altitude adaptation and restricted gene flow across a mid-elevation hybrid zone in Andean tit-tyrant flycatchers. Mol Ecol 23:3551–3565CrossRefPubMedGoogle Scholar
  18. DuVal EH (2007) Cooperative display and lekking behavior of the Lance-Tailed Manakin (Chiroxiphia lanceolata). Auk 124:1168–1185CrossRefGoogle Scholar
  19. Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153CrossRefGoogle Scholar
  20. Endler JA (1993) Some general comments on the evolution and design of animal communication systems. Philos Trans Biol Sci 340:215–225CrossRefGoogle Scholar
  21. Ey E, Fischer J (2009) The “acoustic adaptation hypothesis”: a review of the evidence from birds, anurans and mammals. Bioacoustics 19:21–48CrossRefGoogle Scholar
  22. Fitzsimmons LP, Barker NK, Mennill DJ (2008) Individual variation and lek-based vocal distinctiveness in songs of the Screaming Piha (Lipaugus vociferans), a suboscine songbird. Auk 125:908–914CrossRefGoogle Scholar
  23. Forrest TG (1994) From sender to receiver: propagation and environmental effects on acoustic signals. Am Zool 34:644–654CrossRefGoogle Scholar
  24. Gilliard ET (1959) Notes on the courtship behavior of the Blue-backed Manakin (Chiroxiphia pareola). Am Mus Novit 1942:1–20Google Scholar
  25. Graves GR, Robbins MB, Remsen JVJ (1983) Age and sexual difference in spatial distribution and mobility in Manakins (Pipridae): inferences from mist-netting. J Field Ornithol 54:407–412Google Scholar
  26. Kirschel ANG, Blumstein DT, Cohen RE, Buermann W, Smith TB, Slabbekoorn H (2009) Birdsong tuned to the environment: green hylia song varies with elevation, tree cover, and noise. Behav Ecol 20:1089–1095CrossRefGoogle Scholar
  27. Kirwan GM, Green G (2012) Cotingas and Manakins. Princeton University Press, PrincetonGoogle Scholar
  28. Londoño GA (2013) Avian life history diversification along an Andean elevation gradient: a nesting perspective. Dissertation, University of FloridaGoogle Scholar
  29. Maan ME, Seehausen O (2011) Ecology, sexual selection and speciation. Ecol Lett 14:591–602CrossRefPubMedGoogle Scholar
  30. Macleod R, Ewing SK, Herzog SK et al (2005) First ornithological inventory and conservation assessment for the yungas forests of the Cordilleras Cocapata and Mosetenes, Cochabamba, Bolivia. Bird Conserv Int 15:361–382CrossRefGoogle Scholar
  31. Marten K, Quine D, Marler P (1977) Sound transmission and its significance for animal vocalization: II Tropical forests habitats. Behav Ecol Sociobiol 2:291–302CrossRefGoogle Scholar
  32. Mason NA, Burns KJ (2015) The effect of habitat and body size on the evolution of vocal displays in Thraupidae (tanagers), the largest family of songbirds. Biol J Linn Soc 114:538–551CrossRefGoogle Scholar
  33. Mathevon N, Aubin T, Vielliard J, da Silva ML, Sebe F, Boscolo D (2008) Singing in the rain forest: how a tropical bird song transfers information. PLoS ONE 3:e1580CrossRefPubMedCentralPubMedGoogle Scholar
  34. Maynard-Smith J, Harper D (2003) Animal signals. Oxford University Press, OxfordGoogle Scholar
  35. Merkord CL (2010) Seasonality and elevational migration in an Andean bird community. Dissertation, University of Missouri, ColumbiaGoogle Scholar
  36. Milá B, Wayne RK, Fitze P, Smith TB (2009) Divergence with gene flow and fine-scale phylogeographical structure in the wedge-billed woodcreeper, Glyphorynchus spirurus, a neotropical rainforest bird. Mol Ecol 18:2979–2995CrossRefPubMedGoogle Scholar
  37. Montaño-Centellas FA, Garitano-Zavala Á (2015) Andean bird responses to human disturbances along an elevational gradient. Acta Oecol 65–66:51–60CrossRefGoogle Scholar
  38. Morton ES (1975) Ecological sources of selection on avian sounds. Am Nat 109:17–34CrossRefGoogle Scholar
  39. Mougeot F, Bretagnolle V (2000) Predation as a cost of sexual communication in nocturnal seabirds: an experimental approach using acoustic signals. Anim Behav 60:647–656CrossRefPubMedGoogle Scholar
  40. Nemeth E, Dabelsteen T, Pedersen SB, Winkler H (2006) Rainforests as concert halls for birds: are reverberations improving sound transmission of long song elements? J Acoust Soc Am 119:620–626CrossRefPubMedGoogle Scholar
  41. Nowicki S (1987) Vocal tract resonances in oscine bird sound production: evidence from birdsongs in a helium atmosphere. Nature 325:53–55CrossRefPubMedGoogle Scholar
  42. Nyári AS (2007) Phylogeographic patterns, molecular and vocal differentiation, and species limits in Schiffornis turdina (Aves). Mol Phylogenet Evol 44:154–164CrossRefPubMedGoogle Scholar
  43. Podos J (2014) Sexual selection and the evolution of vocal mating signals: lessons from neotropical songbirds. In: Macedo RH, Machado G (eds) Sexual selection: perspectives and models from the neotropics. Elsevier Inc., Amsterdam, pp 341–363Google Scholar
  44. Podos J, Huber SK, Taft B (2004) Bird song: the interface of evolution and mechanism. Annu Rev Ecol Evol Syst 35:55–87CrossRefGoogle Scholar
  45. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  46. Raposo MA, Hofling E (2003) Overestimation of vocal characters in Suboscine taxonomy (Aves: Passeriformes: Tyranni): causes and implications. Lundiana 4:35–42Google Scholar
  47. Richards DG, Wiley RH (1980) Reverberations and amplitude fluctuations in the propagation of sound in a forest: implications for animal communication. Am Nat 115:381CrossRefGoogle Scholar
  48. Ryan MJ, Brenowitz EA (1985) The role of body size, phylogeny, and ambient noise in the evolution of bird song. Am Nat 126:87–100CrossRefGoogle Scholar
  49. Saranathan V, Hamilton D, Powell GVN, Kroodsma DE, Prum RO (2007) Genetic evidence supports song learning in the three-wattled bellbird Procnias tricarunculata (Cotingidae). Mol Ecol 16:3689–3702CrossRefPubMedGoogle Scholar
  50. Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380CrossRefPubMedGoogle Scholar
  51. Schneider CJ, Smith TB, Larison B, Moritz C (1999) A test of alternative models of diversification in tropical rainforests: ecological gradients versus rainforest refugia. Proc Natl Acad Sci USA 96:13869–13873CrossRefPubMedCentralPubMedGoogle Scholar
  52. Schulenberg TS, Stotz DF, Lane DF et al (2007) Birds of Peru. Princeton University Press, PrincetonGoogle Scholar
  53. Seddon N (2005) Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds. Evolution 59:200–215CrossRefPubMedGoogle Scholar
  54. Slabbekoorn H (2004) Singing in the wild: the ecology of birdsong. In: Marler P, Slabbekoorn H (eds) Nature’s music, the science of birdsong. Elsevier Academic Press, San Diego, pp 178–205Google Scholar
  55. Slabbekoorn H, Smith TB (2002a) Habitat-dependent song divergence in the little greenbul: an analysis of environmental selection pressures on acoustic signals. Evolution 56:1849–1858CrossRefPubMedGoogle Scholar
  56. Slabbekoorn H, Smith TB (2002b) Bird song, ecology and speciation. Philos Trans R Soc Lond B Biol Sci 357:493–503CrossRefPubMedCentralPubMedGoogle Scholar
  57. Slabbekoorn H, Ellers J, Smith TB (2002) Birdsong and sound transmission: the benefits of reverberations. Condor 104:564–573CrossRefGoogle Scholar
  58. Smith TB, Schneider CJ, Holder K (2001) Refugial isolation versus ecological gradients. Testing alternative mechanisms of evolutionary divergence in four rainforest vertebrates. Genetica 112–113:383–398CrossRefPubMedGoogle Scholar
  59. Snell-Rood EC, Badyaev AV (2008) Ecological gradient of sexual selection: elevation and song elaboration in finches. Oecologia 157:545–551CrossRefPubMedGoogle Scholar
  60. Snow DW (2004) Family Pipridae (Manakins). In: del Hoyo J, Elliot A, Christie DA (eds) Handbook of birds of the world. Cotingas to pipits and wagtails, vol 9. Lynx Editions, Barcelona, pp 110–169Google Scholar
  61. Stein AC, Uy JAC (2006) Unidirectional introgression of a sexually selected trait across an avian hybrid zone: a role for female choice? Evolution 60:1476–1485PubMedGoogle Scholar
  62. Swenson JJ, Young BE, Beck S et al (2012) Plant and animal endemism in the eastern Andean slope: challenges to conservation. BMC Ecol 12:1–18CrossRefPubMedCentralPubMedGoogle Scholar
  63. Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21CrossRefGoogle Scholar
  64. Terborgh J (1977) Bird species diversity on an Andean elevational gradient. Ecology 58:1007–1019CrossRefGoogle Scholar
  65. Tobias JA, Aben J, Brumfield RT, Derryberry EP, Halfwerk W, Slabbekoorn H, Seddon N (2010) Song divergence by sensory drive in Amazonian birds. Evolution 64:2820–2839PubMedGoogle Scholar
  66. Trainer JM, McDonald DB (1993) Vocal repertoire of the long-tailed Manakin and its relation to male–male cooperation. Condor 95:769–781CrossRefGoogle Scholar
  67. Trainer JM, McDonald DB, Learn WA (2002) The development of coordinated singing in cooperatively displaying long-tailed manakins. Behav Ecol 13:65–69CrossRefGoogle Scholar
  68. Trillo PA, Athanas KA, Goldhill DH, Hoke KL, Funk WC (2013) The influence of geographic heterogeneity in predation pressure on sexual signal divergence in an Amazonian frog species complex. J Evol Biol 26:216–222CrossRefPubMedGoogle Scholar
  69. Weir JT, Wheatcroft DJ, Price TD (2012) The role of ecological constraint in driving the evolution of avian song frequency across a latitudinal gradient. Evolution 66:2773–2783CrossRefPubMedGoogle Scholar
  70. Wiley RH, Richards DG (1978) Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behav Ecol Sociobiol 3:69–94CrossRefGoogle Scholar
  71. Wilkins MR, Seddon N, Safran RJ (2013) Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol Evol 28:156–166CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Wildlife Ecology and ConservationUniversity of FloridaGainesvilleUSA
  2. 2.Center for Latin American StudiesUniversity of FloridaGainesvilleUSA
  3. 3.Instituto de EcologíaUniversidad Mayor de San AndrésLa PazBolivia

Personalised recommendations