, Volume 189, Issue 4, pp 863–873 | Cite as

Different responses of taxonomic and functional bird diversity to forest fragmentation across an elevational gradient

  • Vinicio SantillánEmail author
  • Marta Quitián
  • Boris A. Tinoco
  • Edwin Zárate
  • Matthias Schleuning
  • Katrin Böhning-Gaese
  • Eike Lena Neuschulz
Highlighted Student Research


Many studies have investigated how habitat fragmentation affects the taxonomic and functional diversity of species assemblages. However, the joint effects of habitat fragmentation and environmental conditions on taxonomic and functional diversity, for instance across elevational gradients, have largely been neglected so far. In this study, we compare whether taxonomic and functional indicators show similar or distinct responses to forest fragmentation across an elevational gradient. We based our analysis on a comprehensive data set of species-rich bird assemblages from tropical montane forest in the Southern Andes of Ecuador. We monitored birds over 2 years in two habitat types (continuous and fragmented forest) at three elevations (i.e., 1000, 2000, and 3000 m a.s.l) and measured nine morphological traits for each bird species on museum specimens. Bird species richness and abundance were significantly higher in fragmented compared to continuous forests and decreased towards high elevations. In contrast, functional diversity was significantly reduced in fragmented compared to continuous forests at low elevations, but fragmentation effects on functional diversity tended to be reversed at high elevations. Our results demonstrate that taxonomic and functional indicators can show decoupled responses to forest fragmentation and that these effects are highly variable across elevations. Our findings reveal that functional homogenization in bird communities in response to fragmentation can be masked by apparent increases in taxonomic diversity, particularly in diverse communities at low elevations.


Ecuador Monitoring Traits Richness Abundance Functional diversity 



We thank the German Research Foundation (DFG) for funding our projects in the framework of the Research Bundle 823–825 “Platform for Biodiversity and Ecosystem Monitoring and Research in South Ecuador” (PAK 825/1) and the Research Unit FOR2730 “Environmental changes in biodiversity hotspot ecosystems of South Ecuador: RESPonse and feedback effECTs”. The Ecuadorian Ministry of the Environment (MAE) kindly provided permission to conduct research. We are grateful to Agustín Carrasco and Patricio Estrella, for their help in fieldwork. We thank Nature and Culture International (NCI), Felix Matt, Jörg Zeilinger, Mathias Templin, and Catherine Vits for logistic support. Two anonymous reviewers provided the helpful comments on an earlier version of this manuscript.

Author contribution statement

VS, MQ, KBG, MS and ELN conceived and designed this study. VS and MQ conducted fieldwork. VS analysed the data. VS, ELN, and MS wrote the manuscript. KBG, BT, and EZ provided editorial advice.

Supplementary material

442_2018_4309_MOESM1_ESM.docx (185 kb)
Supplementary material 1 (DOCX 184 kb)


  1. Bässler C, Cadotte MW, Beudert B et al (2016) Contrasting patterns of lichen functional diversity and species richness across an elevation gradient. Ecography 39:689–698CrossRefGoogle Scholar
  2. Bates D, Maechler M, Bolker B, Walker S (2017) Linear mixed-effects models using ‘Eigen’ and S4 Contact. R package version 1.1–17. Available at: Accessed Apr 2018
  3. Bibby CJ, Burgess ND, Hill DA, Mustoe S (2000) Bird census techniques, 2nd edn. Academic Press, CambridgeGoogle Scholar
  4. Blake JG, Loiselle BA (2001) Bird assemblages in second-growth and old-growth forests, Costa Rica: perspectives from mist nets and point counts. Auk 118:304–326CrossRefGoogle Scholar
  5. Bregman TP, Sekercioglu CH, Tobias JA (2014) Global patterns and predictors of bird species responses to forest fragmentation: implications for ecosystem function and conservation. Biol Conserv 169:372–383CrossRefGoogle Scholar
  6. Bregman TP, Lees AC, MacGregor HEA et al (2016) Using avian functional traits to assess the impact of land-cover change on ecosystem processes linked to resilience in tropical forests. Proc R Soc B Biol Sci 283:20161289CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: A practical information-theoretic approach, 2nd edn. Springer-Verlag, New YorkGoogle Scholar
  8. Calba S, Maris V, Devictor V (2014) Measuring and explaining large-scale distribution of functional and phylogenetic diversity in birds: separating ecological drivers from methodological choices. Glob Ecol Biogeogr 23:669–678CrossRefGoogle Scholar
  9. Chamberlain D, Arlettaz RL, Caprio E, Maggini R, Pedrini P, Rolando A, Zbinden N (2012) The altitudinal frontier in avian climate impact research. Ibis 154:205–209CrossRefGoogle Scholar
  10. Chamberlain D, Negro M, Caprio E, Rolando A (2013) Assessing the sensitivity of alpine birds to potential future changes in habitat and climate to inform management strategies. Biol Conserv 167:127–135CrossRefGoogle Scholar
  11. Chamberlain D, Brambilla M, Caprio E, Pedrini P, Rolando A (2016) Alpine bird distributions along elevation gradients: the consistency of climate and habitat effects across geographic regions. Oecologia 181:1139–1150. CrossRefGoogle Scholar
  12. Chapin FS, Zavaleta ES, Eviner VT et al (2000) Consequences of changing biodiversity. Nature 405:234–242CrossRefGoogle Scholar
  13. Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package—I: one-table methods. R News 4:5–10Google Scholar
  14. Cracraft J (1981) Toward a phylogenetic classification of the recent birds of the world (Class Aves). Auk 98:681–714Google Scholar
  15. Dawideit BA, Phillimore AB, Laube I et al (2009) Ecomorphological predictors of natal dispersal distances in birds. J Anim Ecol 78:388–395CrossRefGoogle Scholar
  16. Dehling DM, Fritz SA, Töpfer T et al (2014) Functional and phylogenetic diversity and assemblage structure of frugivorous birds along an elevational gradient in the tropical Andes. Ecography 37:1047–1055Google Scholar
  17. Devictor V, Mouillot D, Meynard C et al (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 13:1030–1040Google Scholar
  18. Díaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655CrossRefGoogle Scholar
  19. Dolédec S, Chessel D, Ter Braak CJF, Champely S (1996) Matching species traits to environmental variables: a new three-table ordination method. Environ Ecol Stat 3:143–166CrossRefGoogle Scholar
  20. Dunning JB (2007) CRC handbook of avian body masses. Taylor and Francis, Boca RatonCrossRefGoogle Scholar
  21. Edwards FA, Edwards DP, Hamer KC, Davies RG (2013) Impacts of logging and conversion of rainforest to oil palm on the functional diversity of birds in Sundaland. Ibis 155:313–326CrossRefGoogle Scholar
  22. Emck P (2007) A climatology of south Ecuador. PhD disertation. Universität Erlangen-NürnbergGoogle Scholar
  23. Ferger SW, Schleuning M, Hemp A et al (2014) Food resources and vegetation structure mediate climatic effects on species richness of birds. Glob Ecol Biogeogr 23:541–549CrossRefGoogle Scholar
  24. Fleming TH (1979) Do tropical frugivores compete for food? Integr Comp Biol 19:1157–1172Google Scholar
  25. Flynn DFB, Gogol-Prokurat M, Nogeire T et al (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12:22–33CrossRefGoogle Scholar
  26. Forrest JRK, Thorp RW, Kremen C, Williams NM (2015) Contrasting patterns in species and functional-trait diversity of bees in an agricultural landscape. J Appl Ecol 52:706–715CrossRefGoogle Scholar
  27. Gagic V, Bartomeus I, Jonsson T et al (2015) Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proc R Soc B Biol Sci 282:20142620CrossRefGoogle Scholar
  28. Graham CH, Parra JL, Rahbek C, Mcguire JA (2009) Phylogenetic structure in tropical hummingbird communities. Proc Natl Acad Sci 107:513Google Scholar
  29. Harris JBC, Dwi Putra D, Gregory SD et al (2014) Rapid deforestation threatens mid-elevational endemic birds but climate change is most important at higher elevations. Divers Distrib 20:773–785CrossRefGoogle Scholar
  30. Herrel A, Podos J, Huber SK, Hendry AP (2005) Bite performance and morphology in a population of Darwin’s finches: implications for the evolution of beak shape. Funct Ecol 19:43–48CrossRefGoogle Scholar
  31. Homeier J, Werner FA, Gradstein SR et al (2008) Potential vegetation and floristic composition of Andean forests in south Ecuador, with a focus on the RBSF. In: Beck E, Bendix J, Kottke I et al (eds) Gradients in a tropical mountain ecosystem of Ecuador. Ecological studies, vol 198. Springer, Berlin, pp 87–100CrossRefGoogle Scholar
  32. Jarzyna MA, Jetz W (2017) A near half-century of temporal change in different facets of avian diversity. Glob Chang Biol 23:2999–3011CrossRefGoogle Scholar
  33. Kottek M, Grieser J, Beck C et al (2006) World map of the Köppen–Geiger climate classification updated. Meteorol Z 15:259–263CrossRefGoogle Scholar
  34. Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305CrossRefGoogle Scholar
  35. Laliberté E, Legendre P, Bill Shipley (2015) Measuring functional diversity (FD) from multiple traits, and other tools for functional ecology. R package version 1.0–12. Available at: Accessed Jan 2017
  36. Lawton JH, Bignell DE, Bolton B et al (1998) Biodiversity inventories, indicator taxa and effects of habitat modification in tropical forest. Nature 391:72–76CrossRefGoogle Scholar
  37. Lehouck V, Spanhove T, Vangestel C et al (2009) Does landscape structure affect resource tracking by avian frugivores in a fragmented Afrotropical forest? Ecography 32:789–799CrossRefGoogle Scholar
  38. Lockwood R, Swaddle JP, Rayner JMV (1998) Avian wingtip shape reconsidered: wingtip shape indices and morphological adaptations to migration. J Avian Biol 29:273–292CrossRefGoogle Scholar
  39. McCain CM (2009) Global analysis of bird elevational diversity. Glob Ecol Biogeogr 18:346–360CrossRefGoogle Scholar
  40. Meynard CN, Devictor V, Mouillot D et al (2011) Beyond taxonomic diversity patterns: how do α, β and γ components of bird functional and phylogenetic diversity respond to environmental gradients across France? Glob Ecol Biogeogr 20:893–903CrossRefGoogle Scholar
  41. Moermond TC, Denslow JS (1985) Neotropical avian frugivores : patterns of behavior, morphology, and nutrition, with consequences for fruit selection. Ornithol Monogr 36:865–897CrossRefGoogle Scholar
  42. Montaño-Centellas FA, Garitano-Zavala Á (2015) Andean bird responses to human disturbances along an elevational gradient. Acta Oecologica 65–66:51–60CrossRefGoogle Scholar
  43. Morueta-Holme N, Engemann K, Sandoval-Acuña P, Jonas JD, Segnitz M, Svenning JC (2015) Strong upslope shifts in Chimborazo’s vegetation over two centuries since Humboldt. Proc Natl Acad Sci 112:12741–12745CrossRefGoogle Scholar
  44. Mulwa RK, Böhning-Gaese K, Schleuning M (2012) High bird species diversity in structurally heterogeneous farmland in western Kenya. Biotropica 44:801–809CrossRefGoogle Scholar
  45. Mulwa RK, Neuschulz EL, Böhning-Gaese K, Schleuning M (2013) Seasonal fluctuations of resource abundance and avian feeding guilds across forest-farmland boundaries in tropical Africa. Oikos 122:524–532CrossRefGoogle Scholar
  46. Neuschulz EL, Botzat A, Farwig N (2011) Effects of forest modification on bird community composition and seed removal in a heterogeneous landscape in South Africa. Oikos 120:1371–1379CrossRefGoogle Scholar
  47. Niu K, Choler P, de Bello F et al (2014) Fertilization decreases species diversity but increases functional diversity: a three-year experiment in a Tibetan alpine meadow. Agric Ecosyst Environ 182:106–112CrossRefGoogle Scholar
  48. Nogués-Bravo D, Araujo MB, Romdal T, Rahbek C (2008) Scale effects and human impact on the elevational species richness gradients. Nature 453:216–219CrossRefGoogle Scholar
  49. Norberg UM (1995) How a long tail and changes in mass and wing shape affect the cost for flight in animals. Funct Ecol 9:48–54CrossRefGoogle Scholar
  50. Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758CrossRefGoogle Scholar
  51. Pigot AL, Trisos CH, Tobias JA (2016) Functional traits reveal the expansion and packing of ecological niche space underlying an elevational diversity gradient in passerine birds. Proc R Soc B Biol Sci 283:20152013CrossRefGoogle Scholar
  52. R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. Available at:
  53. Ricklefs RE (2012) Species richness and morphological diversity of passerine birds. Proc Natl Acad Sci 109:14482–14487CrossRefGoogle Scholar
  54. Ridgely RS, Greenfield PJ (2001) The birds of Ecuador, vol II. Christopher Helm, LondonGoogle Scholar
  55. Sabatini FM, Burton JI, Scheller RM et al (2014) Functional diversity of ground-layer plant communities in old-growth and managed northern hardwood forests. Appl Veg Sci 17:398–407CrossRefGoogle Scholar
  56. Schipper AM, Belmaker J, de Miranda MD et al (2016) Contrasting changes in the abundance and diversity of North American bird assemblages from 1971 to 2010. Glob Chang Biol 22:3948–3959CrossRefGoogle Scholar
  57. Sekercioglu CH (2006) Increasing awareness of avian ecological function. Trends Ecol Evol 21:464–471CrossRefGoogle Scholar
  58. Seymour CL, Simmons RE, Joseph GS, Slingsby JA (2015) On bird functional diversity: species richness and functional differentiation show contrasting responses to rainfall and vegetation structure in an arid landscape. Ecosystems 18:971–984CrossRefGoogle Scholar
  59. Sitters H, Di Stefano U, Christie F et al (2016) Bird functional diversity decreases with time since disturbance: does patchy prescribed fire enhance ecosystem function? Ecol Appl 26:115–127CrossRefGoogle Scholar
  60. Smith B, Wilson JB (1996) A consumer’s guide to evenness indices. Oikos 76:70–82CrossRefGoogle Scholar
  61. Soh MCK, Sodhi NS, Lim SLH (2006) High sensitivity of montane bird communities to habitat disturbance in Peninsular Malaysia. Biol Conserv 129:149–166CrossRefGoogle Scholar
  62. Stotz DF, Fitzpatrick JW, Parker TAI, Moskovits DK (1996) Neotropical birds: ecology and conservation. University of Chicago Press, ChicagoGoogle Scholar
  63. Suding KN, Lavorel S, Chapin FS et al (2008) Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Glob Chang Biol 14:1125–1140CrossRefGoogle Scholar
  64. Tapia-Armijos MF, Homeier J, Espinosa CI et al (2015) Deforestation and forest fragmentation in south Ecuador since the 1970s—losing a hotspot of biodiversity. PLoS One 10:1–18Google Scholar
  65. Tscharntke T, Sekercioglu CH, Dietsch TV et al (2008) Landscape constraints on functional diversity of birds and insects in tropical agroecosystems. Ecology 89:944–951CrossRefGoogle Scholar
  66. Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301CrossRefGoogle Scholar
  67. Villéger S, Miranda JR, Hernández DF, Mouillot D (2010) Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecol Appl 20:1512–1522CrossRefGoogle Scholar
  68. Vollstädt MGR, Ferger SW, Hemp A et al (2017) Direct and indirect effects of climate, human disturbance and plant traits on avian functional diversity. Glob Ecol Biogeogr 26:1–10CrossRefGoogle Scholar
  69. Webb CO, Ackerly DD, McPeek MA et al (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505CrossRefGoogle Scholar
  70. Wilman H, Belmaker J, Jennifer S et al (2014) EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95:2027CrossRefGoogle Scholar
  71. Zeffer A, Johansson LC, Marmebro Å (2003) Functional correlation between habitat use and leg morphology in birds (Aves). Biol J Linn Soc 79:461–484CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Senckenberg Biodiversity and Climate Research CentreFrankfurt Am MainGermany
  2. 2.Department of Biological SciencesGoethe-Universität FrankfurtFrankfurt Am MainGermany
  3. 3.Escuela de Biología, Ecología Y GestiónUniversidad Del AzuayCuencaEcuador

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