Advertisement

Oecologia

, Volume 186, Issue 4, pp 931–938 | Cite as

Intraspecific variation in exploratory behavior and elevational affinity in a widely distributed songbird

  • Yanina Poblete
  • Víctor Gutiérrez
  • Valeska Cid
  • Seth D. Newsome
  • Pablo Sabat
  • Rodrigo A. Vasquez
Behavioral ecology –original research

Abstract

Populations of the same species can vary substantially in their behavioral and morphometric traits when they are subject to different environmental pressures, which may lead to the development of different adaptive strategies. We quantified variation in exploratory behavior and morphometric traits among two rufous-collared sparrow populations that occur at low and high elevations in central Chile. Moreover, we used census and δ2H values of feather and blood to evaluate migration. We found that individual sparrows inhabiting high elevations were larger and showed more intense exploratory behavior in comparison with those that were captured at lower elevation. Moreover, we observed a steady decline in sparrow abundance during the winter and similar δ2H values for blood collected in the winter and summer at this site, which were significantly lower than blood δ2H values observed at low elevation. This pattern suggests that individuals do not move long distances during winter, and likely they remain at similar elevations in refuge habitats. As predicted, our results support the existent of different adaptive strategies among populations of the same species, and suggest that the combination of behavioral, morphometric, and stable isotope data is a novel and robust integrative approach to assess differences in adaptation across environmental gradients.

Keywords

Exploratory behavior Migration Zonotrichia capensis δ2

Notes

Acknowledgements

We are grateful to R. Zuñiga, C. Venegas, P. Espíndola, and C. Flores for field assistance. Research was funded by FONDECYT- Chile 1140548 (RAV), 1160115 (PS), Institute of Ecology and Biodiversity (ICM-P05-002-Chile, and PFB-23-CONICYT-Chile), Fondo Basal FB 0002-2014 (PS) and Y.P. acknowledges support from a doctoral scholarship (21130127 CONICYT-Chile). Birds were captured under a permit issued by the Servicio Agricola Ganadero, Chile.

Author contribution statement

YP conceived the ideas, led the analysis, and wrote the manuscript. VG assisted with the field work and contributed to the development of the ideas. VC assisted with the field work and edited the manuscript. SDN contributed to the ideas, provided assistance with the analysis and editing of the manuscript. PS contributed to the ideas, provided assistance with the analysis, and edited the manuscript, and RAV contributed to the development of the ideas and helped editing the manuscript.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

References

  1. Addis EA, Clark AD, Wingfield JC (2011) Modulation of androgens in southern hemisphere temperate breeding sparrows (Zonotrichia capensis): an altitudinal comparison. Horm Behav 60:195–201.  https://doi.org/10.1016/j.yhbeh.2011.05.002 CrossRefPubMedGoogle Scholar
  2. Beauchamp G (1999) Individual differences in activity and exploration influence leadership in pairs of foraging zebra finches. Behav 137:301–314.  https://doi.org/10.1163/156853900502097 CrossRefGoogle Scholar
  3. Bell AM (2007) Future directions in behavioural syndromes research. Proc R Soc B 274:755–761.  https://doi.org/10.1098/rspb.2006.0199 CrossRefPubMedGoogle Scholar
  4. Bowen GJ, Wassenaar LI, Hobson KA (2005) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337–348.  https://doi.org/10.1007/s00442-004-1813-y CrossRefPubMedGoogle Scholar
  5. Broggi J, Orell M, Hohtola E, Nilsson JÅ (2004) Metabolic response to temperature variation in the great tit: an interpopulation comparison. J Anim Ecol 73:967–972.  https://doi.org/10.1111/j.0021-8790.2004.00872.x CrossRefGoogle Scholar
  6. Brown M (2006) Annual and seasonal trends in avifaunal species richness in a coastal lowlands forest reserve in South Africa. Ostrich 77:58–66.  https://doi.org/10.2989/00306520609485509 CrossRefGoogle Scholar
  7. Burgess ND, Mlingwa COF (2000) Evidence for altitudinal migration of Forest birds between montane Eastern Arc and lowland forests in East Africa. Ostrich.  https://doi.org/10.1080/00306525.2000.9639908 CrossRefGoogle Scholar
  8. Careau V, Bininda-Emonds ORP, Thomas DW, Reale D, Humphries MM (2009) Exploration strategies map along fast-slow metabolic and life-history continua in muroid rodents. Funct Ecol 23:150–156.  https://doi.org/10.1111/j.1365-2435.2008.01468.x CrossRefGoogle Scholar
  9. Cavieres G, Sabat P (2008) Geographic variation in the response to thermal acclimation in rufous-collared sparrows: are physiological flexibility and environmental heterogeneity correlated? Funct Ecol 22:509–515.  https://doi.org/10.1111/j.1365-2435.2008.01382.x CrossRefGoogle Scholar
  10. Chapman FM (1926) The distribution of birdlife in Ecuador A contribution to a study of the origin of Andean bird-life. B Am Mus Nat Hist 55:1–784Google Scholar
  11. Chapman FM (1940) The post-glacial history of Zonotrichia capensis. B Am Mus Nat Hist 77:381–438. https://www.hdlhandlenet/2246/876
  12. Chapman CA, Rothman J (2009) Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates 50:12–22.  https://doi.org/10.1007/s10329-008-0123-0 CrossRefPubMedGoogle Scholar
  13. Chernetsov N (2012) Passerine migration: stopovers and flight. Springer, Berlin.  https://doi.org/10.1007/978-3-642-29020-6
  14. Cheviron ZA, Brumfield RT (2009) Migration-selection balance and local adaptation of mitochondrial haplotypes in rufous-collared sparrows (Zonotrichia capensis) along an elevational gradient. Evolution 63:1593–1605.  https://doi.org/10.1111/j.1558-5646.2009.00644.x CrossRefPubMedGoogle Scholar
  15. Dalerum F, Angerbjörn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658.  https://doi.org/10.1007/s00442-005-0118-0 CrossRefPubMedGoogle Scholar
  16. di Castri F, Hajek E (1976) Bioclimatología de Chile. Editorial Universidad Católica, Santiago. https://grn.cl/bioclimatologia_de_chile.pdf. Accessed 27 Jan 2018
  17. Dingemanse NJ, Both C, Drent PJ, Van Oers K, van Noordwijk AJ (2002) Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim Behav 64:929–938.  https://doi.org/10.1006/anbe.2002.2006 CrossRefGoogle Scholar
  18. Dingemanse NJ, Kazem AJ, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89.  https://doi.org/10.1016/j.tree.2009.07.013 CrossRefPubMedGoogle Scholar
  19. Dirección meteorológica de Chile (2016) Guía climatológica práctica. http://www.meteochile.cl/PortalDMC-web/index.xhtml. Accessed 27 Dec 2017
  20. Drent PJ, van Oers K, van Noordwijk AJ (2003) Realized heritability of personalities in the great tit. Proc R Soc Lond B 27045–27051. https://doi.org/10.1098/rspb.2002.2168
  21. Fiedler W (2005) Ecomorphology of the External Flight Apparatus of Blackcaps (Sylvia atricapilla) with Different Migration Behavior. Ann NY Acad Sci.  https://doi.org/10.1196/annals.1343.022 CrossRefPubMedGoogle Scholar
  22. Garamszegi L, Eens M, Toro K (2008) Bird reveal their personality when singing. PLoS One 3:e2647.  https://doi.org/10.1371/journal.pone.0002647 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Griffiths R, Double MC, Orr K, Dawson JG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075.  https://doi.org/10.1046/j.1365-294x.1998.00389.x CrossRefPubMedGoogle Scholar
  24. Handford P (1983) Continental patterns of morphological variation in a South American sparrow. Evolution 37:920–930.  https://doi.org/10.1111/j.1558-5646.1983.tb05621.x CrossRefPubMedGoogle Scholar
  25. Handford P (1985) Morphological relationships among subspecies of the rufous-collared sparrow Zonotrichia capensis. Can J Zool 63:2383–2388.  https://doi.org/10.1139/z85-352 CrossRefGoogle Scholar
  26. Hardesty JL, Fraser KC (2010) Using deuterium to examine altitudinal migration by Andean birds. J Field Ornithol 83:183–191.  https://doi.org/10.1111/j.1557-9263.2009.00264.x Google Scholar
  27. Hobson KA (2005) Stable isotopes and the determination of avian migratory connectivity and seasonal interactions. Auk 122:1037–1048.  https://doi.org/10.1642/0004-8038 CrossRefGoogle Scholar
  28. Hobson KA (2011) Isotopic ornithology: a perspective. J Ornithol 152:49–66.  https://doi.org/10.1007/s10336-011-0653-x CrossRefGoogle Scholar
  29. Hobson KA, Wassenaar LI, Milá B, Lovette I, Dingle C, Smith TB (2003) Stable isotopes as indicators of altitudinal distributions and movements in an Ecuadorean hummingbird community. Oecologia, 136(2):302–308.  https://doi.org/10.1007/s00442-003-1271-y CrossRefPubMedGoogle Scholar
  30. Hudson JW, Kimzey SL (1966) Temperature regulation and metabolic rhythms in populations of the House sparrow Passer domesticus. Comp Biochem Physiol 17:203–217.  https://doi.org/10.1016/0010-406X(66)90021-1 CrossRefPubMedGoogle Scholar
  31. International Atomic Energy Agency [IAEA]/World Meteorological Organization [WMO] (2011) Global Network of Isotopes in Precipitation (GNIP) database. https://www.nawebiaeaorg/napc/ih/IHS_resources_gnip.html. Accessed 03 Nov 2016
  32. Johnson DN, Maclean GL (1994) Altitudinal migration in Natal. Ostrich. 65:86–94.  https://doi.org/10.1080/00306525.1994.9639670 CrossRefGoogle Scholar
  33. Kolluru GR, Grether GF, Contreras H (2007) Environmental and genetic influences on mating strategies along a replicated food availability gradient in guppies (Poecilia reticulata). Behav Ecol Sociobiol 61:689–701.  https://doi.org/10.1007/s00265-006-0299-5 CrossRefGoogle Scholar
  34. Körner C (2007) The use of ‘altitude’in ecological research. Trends Ecol Evol 22:569–574.  https://doi.org/10.1016/j.tree.2007.09.006 CrossRefPubMedGoogle Scholar
  35. Laland KN, Janik VM (2006) The animal cultures debate. Trends Ecol Evol 21:542–547.  https://doi.org/10.1016/j.tree.2006.06.005 CrossRefPubMedGoogle Scholar
  36. Leisler B, Winkler H (2003) Morphological consequences of migration in passerines. In: Sonnenschein E, Bertold P, Gwinner E (eds) Avian migration. Springer, Heidelberg, pp 175–186CrossRefGoogle Scholar
  37. Lijtmaer DA, Tubaro PL (2007) A reversed pattern of association between song dialects and habitat in the rufous-collared sparrow. Condor 109:658–667.  https://doi.org/10.1650/8176.1 CrossRefGoogle Scholar
  38. Loiselle BA, Blake JG (1991) Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology 72:180–193.  https://doi.org/10.2307/1938913 CrossRefGoogle Scholar
  39. Lougheed SC, Handford P (1992) Vocal dialects and the structure of geographic variation in morphological and allozymic frequency characters in the rufous-collared sparrow Zonotrichia capensis. Evolution 46:1443–1456.  https://doi.org/10.1111/j.1558-5646.1992.tb01135.x CrossRefPubMedGoogle Scholar
  40. Lougheed SC, Campagna L, Dávila JA, Tubaro PL, Lijtmaer DA, Handford P (2013) Continental phylogeography of an ecologically and morphologically diverse Neotropical songbird Zonotrichia capensis. BMC Evol Biol 131.  https://doi.org/10.1186/1471-2148-13-58
  41. Maldonado K, van Dongen WFD, Vásquez RA, Sabat P (2012) Geographic variation in the association between exploratory behavior and physiology in Rufous-Collared sparrows. Physiol Biochem Zool 85:618–624.  https://doi.org/10.1086/667406 CrossRefPubMedGoogle Scholar
  42. Martínez Del Rio C, Sabat P, Andreson-Sprecher R, Gonzalez SP (2009) Dietary and isotopic specialization: the isotopic niche of three Cinclodes ovenbirds. Oecologia 161:149–159.  https://doi.org/10.1007/s00442-009-1357-2 CrossRefGoogle Scholar
  43. Mazerolle DF, Hobson KA (2005) Estimating origins of short-distance migrant songbirds in North America: contrasting inferences from hydrogen isotope measurements of feathers claws and blood. Condor 107:280–288.  https://doi.org/10.1650/7681 CrossRefGoogle Scholar
  44. Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. J Biogeogr 30:331–351.  https://doi.org/10.1046/j.1365-2699.2003.00837.x CrossRefGoogle Scholar
  45. Mettke-Hofmann C (2006) Object exploration of garden and sardinian warblers peaks in spring. Ethology 113:174–182.  https://doi.org/10.1111/j.1439-0310.2006.01307.x CrossRefGoogle Scholar
  46. Mettke-Hofmann C, Winkler H, Leisler B (2002) The significance of ecological factors for exploration and neophobia in parrots. Ethology 108:249–272.  https://doi.org/10.1046/j.1439-0310.2002.00773.x CrossRefGoogle Scholar
  47. Minderman J, Reid JM, Evans PGH, Whittingham MJ (2009) Personality traits in wild starlings: exploration behaviour and environmental sensitivity. Behav Ecol 20:830–837.  https://doi.org/10.1093/beheco/arp067 CrossRefGoogle Scholar
  48. Narosky T, Di Giacomo AG (1993) Las aves de la provincia de Buenos Aires: distribución y estatus. In: Vázquez AOP, Mazzini LOLA (eds) Asociación Ornitológica del Plata. Buenos Aires, Argentina p 127Google Scholar
  49. Newsome SD, Sabat P, Wolf N, Rader JA, del Rio CM (2015) Multi-tissue δ2H analysis reveals altitudinal migration and tissue-specific discrimination patterns in Cinclodes. Ecosphere 6:1–18.  https://doi.org/10.1890/ES15-00086.1 CrossRefGoogle Scholar
  50. Newton I, Dale L (1996) Relationship between migration and latitude among west European birds. J Anim Ecol 65:137–146.  https://doi.org/10.2307/5716 CrossRefGoogle Scholar
  51. Olrog CC (1979) Nueva lista de la avifauna Argentina. Opera Lilloana 27:1–324Google Scholar
  52. Ortiz D, Capllonch P (2011) The migration of the Rufous-Collared Sparrow (Zonotrichia capensis) in Argentina. Hist Nat 1:105–109Google Scholar
  53. Pennycuick CJ (1975) Mechanics of flight. In: Farner DS, King JR (eds) Avian biology. Academic Press, London, pp 1–75Google Scholar
  54. Poage MA, Chamberlain CP (2001) Empirical relationships between elevation and the stable isotope composition of precipitation and surface waters: considerations for studies of paleoelevation change. Am J Sci 301:1–15CrossRefGoogle Scholar
  55. Quispe R, Villavicencio CP, Cortes A, Vásquez RA (2009) Inter-population variation in hoarding behaviour in degus Octodon degus. Ethology 115:465–474.  https://doi.org/10.1111/j.1439-0310.2009.01621.x CrossRefGoogle Scholar
  56. Ralph C, John GR, Geupel P, Pyle TE, Martin DF, DeSante F (1996) Manual de métodos de campo para elmonitoreo de aves terrestres. General Technical Report, Albany, CA: Pacific Southwest Station, Forest Service, U.S. Departament of Agriculture Google Scholar
  57. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318.  https://doi.org/10.1111/j.1469-185X.2007.00010.x CrossRefPubMedGoogle Scholar
  58. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19372–378.  https://doi.org/10.1016/j.tree.2004.04.009
  59. Stiles FG (1985) Conservation of forest birds in Costa Rica: problems and perspectives. In: Lovejoy TE, Diamond AW (eds) Conservation of tropical forest birds. International Council for Bird Preservation, Cambridge, pp 141–168Google Scholar
  60. Thrower NJW, Bradbury DE (1977) Chile-California mediterranean scrub atlas: a comparative analysis v 2 US/IBP Synthesis Series USAGoogle Scholar
  61. van Dongen WFD, Maldonado K, Sabat P, Vásquez RA (2010) Geographic variation in the repeatability of a personality trait. Behav Ecol 11243–1250.  https://doi.org/10.1093/beheco/arq145
  62. van Oers K, Naguib M (2013) Avian personality. In: Carere C, Maestripiere D (eds) Animal personalities: behavior physiology and evolution. The University of Chicago Press, Chicago, pp 66–85CrossRefGoogle Scholar
  63. van Oers K, Drent PJ, de Goede P, van Noordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc B 271:65–73.  https://doi.org/10.1098/rspb.2003.2518 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Villegas M, Newsome SD, Blake JG (2016) Seasonal patterns in δ2H values of multiple tissues from Andean birds provide insights into elevational migration. Ecol Appl 8:2383–2389.  https://doi.org/10.1002/eap.1456 CrossRefGoogle Scholar
  65. Whiten A, van Schaik CP (2007) The evolution of animal ‘cultures’ and social intelligence. Philos Trans R Soc Lond B 362:603–620.  https://doi.org/10.1098/rstb.2006.1998 CrossRefGoogle Scholar
  66. Winker K, Escalante P, Rappole JH, Ramos MA, Oehlenschlager RJ, Warner DW (1997) Periodic migration and lowland forest refugia in a “sedentary” Neotropical bird Wetmore’s Bush- Tanager. Conserv Biol 11:692–697.  https://doi.org/10.1046/j.1523-1739.1997.95450.x CrossRefGoogle Scholar
  67. Wright D (2005) Diet keystone resources and altitudinal movement of dwarf cassowaries in relation to fruiting phenology in a Papua New Guinean rainforest. In: Lawrence D, Boubli JP (eds) Tropical fruits and frugivores. Springer, Dordrecht, pp 205–236CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Yanina Poblete
    • 1
    • 4
  • Víctor Gutiérrez
    • 1
  • Valeska Cid
    • 1
  • Seth D. Newsome
    • 2
  • Pablo Sabat
    • 3
    • 5
  • Rodrigo A. Vasquez
    • 1
    • 3
  1. 1.Instituto de Ecología y Biodiversidad, Facultad de CienciasUniversidad de ChileÑuñoaChile
  2. 2.Department of BiologyUniversity of New MexicoAlbuquerqueUSA
  3. 3.Departamento de Ciencias EcológicasUniversidad de ChileÑuñoaChile
  4. 4.Instituto de Ciencias Naturales, Universidad de las AméricasProvidenciaChile
  5. 5.Center of Applied Ecology and Sustainability (CAPES)Pontificia Universidad Católica de ChileSantiagoChile

Personalised recommendations