Advertisement

Urban Ecosystems

, Volume 22, Issue 5, pp 893–906 | Cite as

Disentangling an avian assemblages’ evolutionary and functional history in a Chihuahuan desert city

  • Israel Moreno-ContrerasEmail author
  • Héctor Gómez de Silva
  • Violeta Andrade-González
  • Cuauhcihuatl Vital-García
  • Marco F. Ortiz-Ramírez
Article
  • 190 Downloads

Abstract

Urban green spaces have been shown to be important hotspots of biodiversity in cities of temperate and humid/semihumid tropical ecoregions. Nonetheless, whether this pattern applies to urban ecosystems of desert environments has been rarely studied. Temperature, precipitation, vegetation complexity, human density, and presence of invasive species could act as urban filters limiting the incidence of desert-adapted species into cities. Such effects could be reshaping biotic communities, favoring habitat generalist species in human-dominated environments. In this study, we examined the phylogenetic and functional structure of avian assemblages in a Chihuahuan desert city and its surroundings to infer the processes underlying community assembly. We used phylogenetic comparative methods to test the hypothesis whether there is an underlying pattern determining which desert-adapted species penetrate or tolerate a novel urban ecosystem. We also performed a regression approach to determine which environmental and anthropogenic variables may be associated with these metrics. We found that urban green spaces present more evolutionary and functional diversity (based on the proportion of total tree branch length) than agricultural fields and desert scrub, although not statistically significant. On the other hand, based on the mean branch length distance among sample taxa, we observed clustered communities suggesting environmental filtering. Most continuous functional traits presented a low and significant phylogenetic signal, but nearly all binary traits were conserved across phylogeny. Phylogenetic predisposition to be a habitat generalist is present in the surveyed avian assemblages. Our regression analysis indicates that invasive bird species richness was negatively correlated with net relatedness index (NRI) and functional net relatedness index (FNRI), while functional diversity metrics were influenced by temperature and precipitation.

Keywords

Desert Functional diversity Mexico Niche conservationism Phylogenetic diversity Urban ecology 

Notes

Acknowledgements

IMC received a Master scholarship grant provided by CONACyT and Posgrado en Ciencias Biológicas of the Universidad Nacional Autónoma de México (UNAM) (grant number: 451119). We thank to Miguel Angel Viveros for providing access to Club Campestre. Thanks to Macaulay library (Cornell University) and xeno-canto.org for providing us their recordings for this study. Thanks to editor and two anonymous reviewers for their comments on the early version of this manuscript.

Supplementary material

11252_2019_864_MOESM1_ESM.docx (58 kb)
ESM 1 (DOCX 58 kb)
11252_2019_864_MOESM2_ESM.docx (36 kb)
ESM 2 (DOCX 35 kb)
11252_2019_864_MOESM3_ESM.docx (48 kb)
ESM 3 (DOCX 48 kb)
11252_2019_864_MOESM4_ESM.docx (19 kb)
ESM 4 (DOCX 19 kb)

References

  1. Araya-Salas M, Smith-Vidaurre G (2017) warbleR: an r package to streamline analysis of animal acoustic signals. Methods Ecol Evol 8(2):184–191.  https://doi.org/10.1111/2041-210X.12624 CrossRefGoogle Scholar
  2. Aronson MFJ, Nilon CH, Lepczyk CA, Parker TS, Warren PS, Cilliers SS, Goddard MA, Hahs AK, Herzog C, Katti M, La Sorte FA, Williams NSG, Zipperer W (2016) Hierarchical filters determine community assembly of urban species pools. Ecology 97(11):2952–2963.  https://doi.org/10.1002/ecy.1535 CrossRefPubMedGoogle Scholar
  3. Barton K (2018). MuMIn: Multi-Model Inference. R package version 1.40.4. https://CRAN.R-project.org/package=MuMIn. Accessed 21 June 2018
  4. Bermudez-Cuamatzin E, Rios-Chelen AA, Gil D, Garcia CM (2011) Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird. Biol Lett 7(1):36–38.  https://doi.org/10.1098/rsbl.2010.0437
  5. Bivand R, Piras G (2015) Comparing implementations of estimation methods for spatial econometrics. J Stat Softw 63(18):1–36.  https://doi.org/10.18637/jss.v063.i18 CrossRefGoogle Scholar
  6. Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57(4):717–745. https://doi.org/10.1554/0014-3820(2003)057[0717:TFPSIC]2.0.CO;2Google Scholar
  7. Bonier F, Martin PR, Wingfield JC (2007) Urban birds have broader environmental tolerance. Biol Lett 3(6):670–673.  https://doi.org/10.1098/rsbl.2007.0349 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brown DE (1994) Chihuahuan desert scrub. In: Brown DE (ed) Biotic communities: southwestern United States and northwestern Mexico. Utah University Press, Salt Lake City, pp 169–179Google Scholar
  9. Brown JL (2014) SDMtoolbox: a python–based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Methods Ecol Evol 5(7):694–700.  https://doi.org/10.1111/2041-210X.12200 CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  11. Cadotte MW, Tucker CM (2017) Should environmental filtering be abandoned? Trends Ecol Evol 32(6):429–437.  https://doi.org/10.1016/j.tree.2017.03.004 CrossRefPubMedGoogle Scholar
  12. Chace JF, Walsh JJ (2006) Urban effects on native avifauna: a review. Landsc Urban Plan 74(1):46–49.  https://doi.org/10.1016/j.landurbplan.2004.08.007 CrossRefGoogle Scholar
  13. Chesser RT, Burns KJ, Cicero C, Dunn JL, Kratter AW, Lovette IJ, Rasmussen PC, Remsen JV, Rising JD, Stotz DF, Winker K (2017) Fifty-eighth supplement to the American ornithological Society’s check-list of north American birds. Auk 134(3):751–773.  https://doi.org/10.1642/AUK-17-72.1 CrossRefGoogle Scholar
  14. del Hoyo J, Elliott A, Sargatal J, Christie DA, and de Juana E (eds) (2017) Handbook of the birds of the world alive. Lynx Edicions, Barcelona. http://www.hbw.com/. Accessed 21 April 2017Google Scholar
  15. Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, García Marquéz JR, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AD, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36(1):27–46.  https://doi.org/10.1111/j.1600-0587.2012.07348.x CrossRefGoogle Scholar
  16. Dunning JB Jr (2008) CRC handbook of avian body masses, 2nd edn. CRC Press, FloridaGoogle Scholar
  17. Ehrlich PR, Dobkin DS, Wheye D (1988) The birder’s handbook: a field guide to the natural history of north American birds. Simon and Schuster, New YorkGoogle Scholar
  18. Emerson BC, Gillespie RG (2008) Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol Evol 23(11):619–630.  https://doi.org/10.1016/j.tree.2008.07.005 CrossRefPubMedGoogle Scholar
  19. Evans KL, Chamberlain DE, Hatchwell BJ, Gregory RD, Gaston KJ (2011) What makes an urban bird? Glob Chang Biol 17(1):32–44.  https://doi.org/10.1111/j.1365-2486.2010.02247.x CrossRefGoogle Scholar
  20. Fritz SA, Purvis A (2010) Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conserv Biol 24(4):1042–1051.  https://doi.org/10.1111/j.1523-1739.2010.01455.x CrossRefGoogle Scholar
  21. García E (2004) Modificaciones al sistema de clasificación climática de Koppen, 5th edn. Instituto de Geografía, UNAM, Mexico CityGoogle Scholar
  22. Gómez-Baggethun E, Barton DN (2013) Classifying and valuing ecosystem services for urban planning. Ecol Econom 86:235–245.  https://doi.org/10.1016/j.ecolecon.2012.08.019 CrossRefGoogle Scholar
  23. Green DM, Baker MG (2003) Urbanization impacts on habitat and bird communities in a Sonoran desert ecosystem. Landsc Urban Plan 63(4):225–239.  https://doi.org/10.1016/S0169-2046(02)00195-0 CrossRefGoogle Scholar
  24. Hagen EO, Hagen O, Ibáñez-Álamo JD, Petchey OL, Evans KL (2017) Impacts of urban areas and their characteristics on avian functional diversity. Front Ecol Evol 5:84.  https://doi.org/10.3389/fevo.2017.00084 CrossRefGoogle Scholar
  25. Howell SNG, Webb S (1995) A guide to the birds of Mexico and northern Central America. Oxford University Press, OxfordGoogle Scholar
  26. Hubbard JP (1974) Avian evolution in the aridlands of North America. Living Bird 12:155–196Google Scholar
  27. Ibáñez-Álamo JD, Rubio E, Benedetti Y, Morelli F (2017) Global loss of avian evolutionary uniqueness in urban areas. Glob Chang Biol 23(8):2990–2998.  https://doi.org/10.1111/gcb.13567 CrossRefPubMedGoogle Scholar
  28. Inger R, Cox DTC, Per E, Norton BA, Gaston KJ (2016) Ecological role of vertebrate scavengers in urban ecosystems in the UK. Ecol Evol 6(19):7015–7023.  https://doi.org/10.1002/ece3.2414 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Instituto Municipal de Investigación y Planeación (IMIP) (2016) Radiografía socioeconómica del Municipio de Juárez 2015. Instituto Municipal de Investigación y Planeación, Ciudad JuárezGoogle Scholar
  30. Instituto Nacional de Estadística y Geografía (INEGI). (2016) Panorama sociodemográfico de Chihuahua 2015. Instituto Nacional de Estadística y Geografía, AguascalientesGoogle Scholar
  31. Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO (2012) The global diversity of birds in space and time. Nature 491(7424):444–448.  https://doi.org/10.1038/nature11631 CrossRefGoogle Scholar
  32. Job JR, Kohler SL, Gill SA (2016) Song adjustments by an open habitat bird to anthropogenic noise, urban structure, and vegetation. Behav Ecol 27(6):1734–1744.  https://doi.org/10.1093/beheco/arw105 CrossRefGoogle Scholar
  33. Karger DN, Conrad O, Böhner J, Kawohl T, Kreft H, Soria-Auza RW, Zimmermann NE, Linder HP, Kessler M (2017) Climatologies at high resolution for the earth land surface areas. Sci Data 4:170122.  https://doi.org/10.1038/sdata.2017.122 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26(11):1463–1464.  https://doi.org/10.1093/bioinformatics/btq166 CrossRefGoogle Scholar
  35. Kissling WD, Carl G (2008) Spatial autocorrelation and the selection of simultaneous autoregressive models. Glob Ecol Biogeogr 17(1):59–71.  https://doi.org/10.1111/j.1466-8238.2007.00334.x CrossRefGoogle Scholar
  36. Kowarik I (2011) Novel urban ecosystems, biodiversity, and conservation. Environ Pollut 159(8):1974–1983.  https://doi.org/10.1016/j.envpol.2011.02.022 CrossRefPubMedGoogle Scholar
  37. Kraft NJB, Cornwell WK, Webb CO, Ackerly DD (2007) Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat 170(2):271–283.  https://doi.org/10.1086/519400 CrossRefPubMedGoogle Scholar
  38. La Sorte FA, Lepczyk CA, Aronson MFJ, Goddard MA, Hedblom M, Katti M, MacGregor-Fors I, Mörtberg U, Nilon CH, Warren PS, Williams NSG, Yang J (2018) The phylogenetic and functional diversity of regional breeding bird assemblages is reduced and constricted through urbanization. Divers Distrib 24(2):928–938.  https://doi.org/10.1111/ddi.12738 CrossRefGoogle Scholar
  39. Laliberté E, Legendre P, Shipley B (2014) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0–12. https://CRAN.R-project.org/package=FD. Accessed 27 June 2018
  40. Lepczyk CA, Flather CH, Radeloff VC, Pidgeon AM, Hammer RB, Liu K (2008) Human impacts on regional avian diversity and abundance. Conserv Biol 22(2):405–416.  https://doi.org/10.1111/j.1523-1739.2008.00881.x CrossRefPubMedGoogle Scholar
  41. Lepczyk CA, Aronson MFJ, Evans KL, Goddard MA, Lerman SB, Macivor JS (2017) Biodiversity in the city: fundamental questions for understanding the ecology of urban green spaces for biodiversity conservation. BioScience 67(9):799–807.  https://doi.org/10.1093/biosci/bix079 CrossRefGoogle Scholar
  42. Lockwood MW, Freeman B (2014) The Texas Ornithological Society Handbook of Texas Birds, 2nd edn. Texas A&M University Press, College StationGoogle Scholar
  43. Lopes EL, Fernandes AM, Medeiros MCI, Marini MA (2016) A classification scheme for avian diet types. J Field Ornithol 87(3):309–322.  https://doi.org/10.1111/jofo.12158 CrossRefGoogle Scholar
  44. Luther D, Baptista L (2010) Urban noise and the cultural evolution of bird songs. Proc Biol Sci 277(1680):469–473.  https://doi.org/10.1098/rspb.2009.1571
  45. MacGregor-Fors I, Escobar-Ibáñez J, Rueda-Hernández R (2017) Concluding remarks: current knowledge and future directions. In: MacGregor-Fors I, Escobar-Ibáñez JF (eds) Avian ecology in Latin American cityscapes. Springer, Cham, pp 159–168CrossRefGoogle Scholar
  46. Maddison WP, Slatkin M (1991) Null models for the number of evolutionary steps in a character on a phylogenetic tree. Evolution 45(5):1184–1197.  https://doi.org/10.1111/j.1558-5646.1991.tb04385.x CrossRefPubMedGoogle Scholar
  47. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127(3):247–260.  https://doi.org/10.1016/j.biocon.2005.09.005 CrossRefGoogle Scholar
  48. McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11(2):161–176.  https://doi.org/10.1007/s11252-007-0045-4 CrossRefGoogle Scholar
  49. Moiron M, González-Lagos C, Slabbekoorn H, Sol D (2015) Singing in the city: high song frequencies are no guarantee for urban success in birds. Behav Ecol 26(3):843–850.  https://doi.org/10.1093/beheco/arv026 CrossRefGoogle Scholar
  50. Ndiribe C, Salamin N, Guisan A (2013) Understanding the concepts of community phylogenetics. Evol Ecol Res 15(8):1–16 http://www.evolutionary-ecology.com/abstracts/v15/2856.html. Accessed 15 July 2018
  51. Nielsen AB, van den Bosch M, Maruthaveeran S, van den Bosch CK (2014) Species richness in urban parks and its drivers: a review of empirical evidence. Urban Ecosyst 17(1):305–327.  https://doi.org/10.1007/s11252-013-0316-1 CrossRefGoogle Scholar
  52. Olden JD, Lockwood JL, Parr CL (2011) Biological invasions and the homogenization of faunas and floras. In: Ladle RJ, Whittaker RJ (eds) Conservation biogeography. Wiley-Blackwell, West Sussex, pp 224–243CrossRefGoogle Scholar
  53. Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2013) Caper: comparative analyses of phylogenetics and evolution in R. R package version 0.5.2. https://CRAN.R-project.org/package=caper. Accessed 10 November 2017
  54. Osorio F, Vallejos R (2014) SpatialPack: package for analysis of spatial data. R package version 0.2-3. https://CRAN.R-project.org/package=SpatialPack. Accessed 18 March 2017
  55. Pautasso M (2007) Scale-dependence of the correlation between human population presence and vertebrate and plant species richness. Ecol Lett 10(1):16–24.  https://doi.org/10.1111/j.1461-0248.2006.00993.x CrossRefPubMedGoogle Scholar
  56. Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9(6):741–758.  https://doi.org/10.1111/j.1461-0248.2006.00924.x CrossRefGoogle Scholar
  57. Podani J, Schmera D (2006) On dendrogram-based measures of functional diversity. Oikos 115(1):179–185.  https://doi.org/10.1111/j.2006.0030-1299.15048.x CrossRefGoogle Scholar
  58. Popescu AA, Huber KT, Paradis E (2012) Ape 3.0: new tools for distance based phylogenetics and evolutionary analysis in R. Bioinformatics 28(11):1536–1537.  https://doi.org/10.1093/bioinformatics/bts184 CrossRefPubMedGoogle Scholar
  59. Portnov BA, Paz S (2008) Climate change and urbanization in arid regions. Ann Arid Zone 47(3–4):1–15Google Scholar
  60. R Development Core Team (2017) R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. http://www.R-project.org. Accessed 10 March 2017
  61. Ralph CJ, Geupel GR, Pyle P, Martin TE, Desante DF (1993) Handbook of field methods for monitoring landbirds. General technical report PSW-GTR-144. U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station, AlbanyGoogle Scholar
  62. Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3(2):217–223.  https://doi.org/10.1111/j.2041-210X.2011.00169.x CrossRefGoogle Scholar
  63. Revell LJ (2014) Ancestral character estimation under the threshold model from quantitative genetics. Evolution 68(3):743–759.  https://doi.org/10.1111/evo.12300 CrossRefPubMedGoogle Scholar
  64. Rodewald P (ed) (2017) The birds of North America. Cornell Lab of Ornithology, Ithaca https://birdsna.org. Accessed 25 March 2017
  65. Schwarz N, Moretti N, Bugalho MN, Davies ZG, Haase D, Hack J, Hof A, Melero Y, Pett TJ, Knapp S (2017) Understanding biodiversity-ecosystem service relationships in urban areas: a comprehensive literature review. Ecosyst Serv 27:161–171.  https://doi.org/10.1016/j.ecoser.2017.08.014 CrossRefGoogle Scholar
  66. Silva PC, Sepúlveda RD, Barbosa O (2016) Nonrandom filtering effect on birds: species and guilds response to urbanization. Ecol Evol 6(11):3711–3720.  https://doi.org/10.1002/ece3.2144 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Sims V, Evans KL, Newson SE, Tratalos JA, Gaston KJ (2008) Avian assemblage structure and domestic cat densities in urban environments. Divers Distrib 14(2):387–399.  https://doi.org/10.1111/j.1472-4642.2007.00444.x CrossRefGoogle Scholar
  68. Sol D, González-Lagos C, Moreira D, Maspons J, Lapiedra O (2014) Urbanization tolerance and the loss of avian diversity. Ecol Lett 17(8):942–950.  https://doi.org/10.1111/ele.12297 CrossRefPubMedGoogle Scholar
  69. Sol D, Bartomeus I, González-Lagos C, Pavoine S (2017) Urbanisation and the loss of phylogenetic diversity in birds. Ecol Lett 20(6):721–729.  https://doi.org/10.1111/ele.12769 CrossRefPubMedGoogle Scholar
  70. Swenson NG (2011) The role of evolutionary processes in producing biodiversity patterns, and the interrelationships between taxonomic, functional and phylogenetic biodiversity. Am J Bot 98(3):472–480.  https://doi.org/10.3732/ajb.1000289 CrossRefPubMedGoogle Scholar
  71. Tuanmu MN, Jetz W (2014) A global 1-km consensus land-cover product for biodiversity and ecosystem modeling. Glob Ecol Biogeogr 23(9):1031–1045.  https://doi.org/10.1111/geb.12182 CrossRefGoogle Scholar
  72. Walker JS, Shochat E (2009) Scalar effects of vegetation on bird communities in an urbanizing desert ecosystem. Urban Ecosyst 13(2):155–167.  https://doi.org/10.1007/s11252-009-0112-0 CrossRefGoogle Scholar
  73. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33(1):475–505.  https://doi.org/10.1146/annurev.ecolsys.33.010802.150448 CrossRefGoogle Scholar
  74. Wiens JA (1989) The ecology of bird assemblages. In: Foundations and patterns, vol 1. Cambridge University Press, CambridgeGoogle Scholar
  75. Wilkins MR, Seddon N, Safran RJ (2013) Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol Evol 28(3):156–166.  https://doi.org/10.1016/j.tree.2012.10.002 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Posgrado en Ciencias BiológicasUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMéxico
  2. 2.Museo de Zoología, Departamento de Biología Evolutiva, Facultad de CienciasUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMéxico
  3. 3.Ciudad de MéxicoMéxico
  4. 4.Departamento de Ciencias Veterinarias, Instituto de Ciencias BiomédicasUniversidad Autónoma de Ciudad JuárezCiudad JuárezMéxico

Personalised recommendations