FUNCTIONAL DIVERSITY OF AVIAN MIXED-SPECIES FORAGING FLOCKS ON THE TILARÁN CORDILLERA, COSTA RICA

Authors

DOI:

https://doi.org/10.58843/ornneo.v36i1.1283

Keywords:

altitudinal gradient, functional outliers, Monteverde, Neotropics, tropical montane forest

Abstract

Avian mixed-species foraging flocks are a common phenomenon in neotropical forests. In order to characterize the variation in such flocks at different elevations, we studied the species composition of avian flocks over a 624 meter elevational gradient on both sides of the continental divide that crosses the Tilarán Cordillera in northwest Costa Rica. We characterized the change in diversity of these flocks across the elevational gradient using several diversity metrics: species richness, functional richness, functional evenness and functional divergence. While the lower elevations of the Atlantic side featured higher species richness, the lower elevations of the Pacific side featured the greatest functional richness and greatest functional divergence. Upper Elevations showed the lowest species richness and lowest functional evenness. A strong understanding of how functional diversity changes with elevation is important in the context of anticipated species altitudinal range shifts with climate change. 

Author Biography

Natalia Ocampo-Peñuela, University of California, Santa Cruz

Environmental Studies Department, Assistant Professor

References

Arbeláez-Cortés E, OH Marín-Gomez (2012) The Composition of Mixed-Species Bird Flocks in Alto Quindío, Colombia. The Wilson Journal of Ornithology 124: 572–580. https://doi.org/10.1676/11-132.1

Arciniega-Esparza S, C Birkel, A Chavarría-Palma, B Arheimer, JA Breña-Naranjo (2022) Remote sensing-aided rainfall–runoff modeling in the tropics of Costa Rica. Hydrology and Earth System Sciences 26: 975–999. https://doi.org/10.5194/hess-26-975-2022

Beauchamp G (2021) Flocking in birds increases annual adult survival in a global analysis. Oecologia 197: 387–394. https://doi.org/10.1007/s00442-021-05023-5

BirdLife International (2020) Campylorhamphus pusillus. In: IUCN Red list of threatened species. Version 2020. Available at http://www.iucnredlist.org [Accessed 16 April 2024]

BirdLife International (2020) Pheucticus tibialis. In: IUCN Red list of threatened species. Version 2020. Available at http://www.iucnredlist.org [Accessed 16 April 2024]

BirdLife International (2022) Trogon collaris. In: IUCN Red list of threatened species. Version 2022. Available at http://www.iucnredlist.org [Accessed 16 April 2024]

Bregman TP, CH Sekercioglu, JA Tobias (2014) Global patterns and predictors of bird species responses to forest fragmentation: Implications for ecosystem function and conservation. Biological Conservation 169: 372–383. https://doi.org/10.1016/j.biocon.2013.11.024

Bregman TP, AC Lees, HEA MacGregor, B Darski, NG de Moura, A Aleixo, J Barlow, JA Tobias (2016) Using avian functional traits to assess the impact of land cover change on ecosystem processes linked to resilience in tropical forests. Proceedings of the Royal Society B: Biological Sciences 283(1844). https://doi.org/10.1098/rspb.2016.1289

Cadotte MW, K Carscadden, N Mirotchnick (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. Journal of Applied Ecology 48: 1079–1087. https://doi.org/10.1111/j.1365-2664.2011.02048.x

Chesser RT, SM Billerman, KJ Burns, C Cicero, JL Dunn, BE Hernández-Baños, RA Jiménez, AW Kratter, NA Mason, PC Rasmussen, JV Remsen Jr., K Winker (2023) Sixty-fourth Supplement to the American Ornithological Society’s Check-list of North American Birds. Ornithology 140: Issue 3. https://doi.org/10.1093/ornithology/ukad023

Claramunt S, M Hong, A Bravo (2022) The effect of flight efficiency on gap‐crossing ability in Amazonian forest birds. Biotropica 54: 860–868. https://doi.org/10.1111/btp.13109

Coates-Estrada R, A Estrada (1988) Frugivory and seed dispersal in Cymbopetalum baillonii (Annonaceae) at Los Tuxtlas, Mexico. Journal of Tropical Ecology 4: 157–172. https://doi.org/10.1017/S0266467400002650

Coddington CPJ, WJ Cooper, CL Rutt, K Mokross, BR Amaral, PC Stouffer, DA Luther (2023) Amazonian mixed‐species flocks demonstrate flexible preferences for vertical forest structure. Ecosphere 14: e4720. https://doi.org/10.1002/ecs2.4720

Colorado GJ, AD Rodewald (2014) Assembly patterns of mixed-species flocks in the Andes. Journal of Animal Ecology 84: 386–395. https://doi.org/10.1111/1365-2656.12300

Colorado Zuluaga GJ, AD Rodewald (2015) Response of mixed-species flocks to habitat alteration and deforestation in the Andes. Biological Conservation 188: 72–81. https://doi.org/10.1016/j.biocon.2015.02.008

Cornwell WK, DW Schwilk, DD Ackerly (2006) A trait-based test for habitat filtering: convex hull volume. Ecology 87: 1465–1471. https://doi.org/10.1890/0012-9658(2006)87[1465:ATTFHF]2.0.CO;2

Develey PF, CA Peres (2000) Resource seasonality and the structure of mixed species bird flocks in a coastal Atlantic forest of southeastern Brazil. Journal of Tropical Ecology 16: 33–53. https://doi.org/10.1017/S0266467400001255

Fanjul ME, AL Echevarria, MV Martínez (2021) Estructura y composición de las bandadas mixtas de aves invernales a lo largo del gradiente latitudinal en las selvas montanas de las Yungas, Argentina. Acta Zoológica Lilloana: 268–286. https://doi.org/10.30550/j.azl/2021.65.2/2021-11-04

Fanjul ME, AL Echevarria, MV Martínez (2023) Relationship among vegetation structure and mixed-species flocks composition along the latitudinal gradient of the subtropical montane forest of the Yungas, Argentina. Philosophical Transactions of the Royal Society B: Biological Sciences 378: 20220107. https://doi.org/10.1098/rstb.2022.0107

Ferro I, JJ Morrone (2014) Biogeographical transition zones: a search for conceptual synthesis: Biogeographical Transition Zones. Biological Journal of the Linnean Society 113: 1–12. https://doi.org/10.1111/bij.12333

Freeman BG, MN Scholer, V Ruiz-Gutierrez, JW Fitzpatrick (2018) Climate change causes upslope shifts and mountaintop extirpations in a tropical bird community. Proceedings of the National Academy of Sciences 115: 11982–11987. https://doi.org/10.1073/pnas.1804224115

Gaston KJ, RG Davies, CDL Orme, VA Olson, GH Thomas, TS Ding, PC Rasmussen, et al. (2007) Spatial turnover in the global avifauna. Proceedings of the Royal Society B: Biological Sciences 274: 1567–1574. https://doi.org/10.1098/rspb.2007.0236

Gentry AH (1988) Changes in Plant Community Diversity and Floristic Composition on Environmental and Geographical Gradients. Annals of the Missouri Botanical Garden 75: 1. https://doi.org/10.2307/2399464

González-Varo JP, J Albrecht, JM Arroyo, RS Bueno, T Burgos, G Escribano-Ávila, N Farwig, et al. (2023) Frugivore-mediated seed dispersal in fragmented landscapes: Compositional and functional turnover from forest to matrix. Proceedings of the National Academy of Sciences 120: 4–23. https://doi.org/10.1073/pnas.2302440120

Grant PR (1981) The feeding of darwin’s finches on Tribulus cistoides (L.) seeds. Animal Behaviour 29: 785–793. https://doi.org/10.1016/S0003-3472(81)80012-7

Graves GR, NJ Gotelli (1993) Assembly of avian mixed-species flocks in Amazonia. Proceedings of the National Academy of Sciences 90: 1388–1391. https://doi.org/10.1073/pnas.90.4.1388

Grenié M, H Gruson (2023) fundiversity: Easy computation of functional diversity indices. doi:10.5281/zenodo.4761754, R package version 1.1.1, https://CRAN.R-project.org/package=fundiversity

Griffin JN, V Méndez, AF Johnson, SR Jenkins, A Foggo (2009) Functional diversity predicts overyielding effect of species combination on primary productivity. Oikos 118: 37–44. https://doi.org/10.1111/j.1600-0706.2008.16960.x

Hazzi NA, JS Moreno, C Ortiz-Movliav, RD Palacio (2018) Biogeographic regions and events of isolation and diversification of the endemic biota of the tropical Andes. Proceedings of the National Academy of Sciences 115: 7985–7990. https://doi.org/10.1073/pnas.1803908115

Jankowski JE, AL Ciecka, NY Meyer, KN Rabenold (2009) Beta diversity along environmental gradients: implications of habitat specialization in tropical montane landscapes. Journal of Animal Ecology 78: 315–327. https://doi.org/10.1111/j.1365-2656.2008.01487.x

Janzen DH (1967) Why Mountain Passes are higher in the Tropics. The American Naturalist 101: 233–249. doi:10.1086/282487

Kattan GH, H Alvarez‐López, M Giraldo (1994) Forest Fragmentation and Bird Extinctions: San Antonio Eighty Years Later. Conservation Biology 8: 138–146. https://doi.org/10.1046/j.1523-1739.1994.08010138.x

Lederer RJ (1975) Bill Size, Food Size, and Jaw Forces of Insectivorous Birds. The Auk 92: 385–387. https://doi.org/10.2307/4084573

Lomolino MV (2001) Elevation gradients of species‐density: historical and prospective views. Global Ecology and Biogeography 10: 3–13. https://doi.org/10.1046/j.1466-822x.2001.00229.x

Mammola S, CP Carmona, T Guillerme, P Cardoso (2021) Concepts and applications in functional diversity. Functional Ecology 35: 1869–1885. https://doi.org/10.1111/1365-2435.13882

Mangini G, K Mokross, F Gandoy, JI Areta (2022) Mixed-species flocking is associated with low arthropod detectability and increased foraging efficiency by Yungas forest birds in Argentina. Ornithology 139: 1–18. 10.1093/ornithology/ukab087

Marantz CA, J Del Hoyo, N Collar, A Aleixo, LR Bevier, GM Kirwan, MA Patten (2020) Northern Barred-Woodcreeper (Dendrocolaptes sanctithomae). Version 1.0 in Billerman SM, BK Keeney, PG Rodewald, TS Schulenberg (eds). Birds of the World. Cornell Lab of Ornithology, USA. https://doi.org/10.2173/bow.nobwoo1.01

Mason NWH, D Mouillot, WG Lee, JB Wilson (2005) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111: 112–118. https://doi.org/10.1111/j.0030-1299.2005.13886.x

McCain CM, J Grytnes (2010) Elevational Gradients in Species Richness. Encyclopedia of Life Sciences. Wiley. https://doi.org/10.1002/9780470015902.a0022548

Mcgill B, B Enquist, E Weiher, M Westoby (2006) Rebuilding community ecology from functional traits. Trends in Ecology and Evolution 21: 178–185. https://doi.org/10.1016/j.tree.2006.02.002

Moermond TC, JS Denslow, DJ Levey, EC Santana (1986) The influence of morphology on fruit choice in neotropical birds. Pp. 137–146 in Estrada A, TH Fleming (eds). Frugivores and seed dispersal. Tasks for vegetation science. Springer Netherlands, Dordrecht, 137–146. https://doi.org/10.1007/978-94-009-4812-9_13

Mokross K, TB Ryder, MC Côrtes, JD Wolfe, PC Stouffer (2014) Decay of interspecific avian flock networks along a disturbance gradient in Amazonia. Proceedings of the Royal Society B: Biological Sciences 281: 20132599. https://doi.org/10.1098/rspb.2013.2599

Montaño‐Centellas FA (2020) Interaction networks of avian mixed‐species flocks along elevation in the tropical Andes. Ecography 43: 930–942. https://doi.org/10.1111/ecog.05135

Montaño‐Centellas FA (2023) Network structure of avian mixed-species flocks decays with elevation and latitude across the Andes. Philosophical Transactions of the Royal Society B: Biological Sciences 378: 1878. https://doi.org/10.1098/rstb.2022.0099

Montaño‐Centellas FA, HH Jones (2021) Temperature and vegetation complexity structure mixed-species flocks along a gradient of elevation in the tropical Andes. Ornithology 138: 3. 10.1093/ornithology/ukab027

Muñoz J (2016) The role of facilitation in the structure of tropical bird communities: a case study of mixed-species flocks. Master’s Thesis, University of British Columbia, British Columbia, Canada.

Muñoz J, JE Jankowski (2023) Neotropical mixed-species bird flocks in a community context. Philosophical Transactions of the Royal Society B: Biological Sciences 378: 20220104. https://doi.org/10.1098/rstb.2022.0104

Nadkarni NM, TJ Matelson, WA Haber (1995) Structural characteristics and floristic composition of a Neotropical cloud forest, Monteverde, Costa Rica. Journal of Tropical Ecology 11: 481–495. https://doi.org/10.1017/S0266467400009020

Neate-Clegg MHC, SN Stuart, D Mtui, ÇH Şekercioğlu, WD Newmark (2021) Afrotropical montane birds experience upslope shifts and range contractions along a fragmented elevational gradient in response to global warming. PLOS ONE 16: e0248712. https://doi.org/10.1371/journal.pone.0248712

Newbold T, JPW Scharlemann, SHM Butchart, ÇH Şekercioğlu, L Joppa, R Alkemade, DW Purves (2014) Functional traits, land-use change and the structure of present and future bird communities in tropical forests. Global Ecology and Biogeography 23: 1073–1084. https://doi.org/10.1111/geb.12186

Nguyen DT, J Gómez-Zurita (2016) Subtle Ecological Gradient in the Tropics Triggers High Species-Turnover in a Local Geographical Scale. PLOS ONE 11: e0156840. https://doi.org/10.1371/journal.pone.0156840

Norberg J, DP Swaney, J Dushoff, J Lin, R Casagrandi, SA Levin (2001) Phenotypic diversity and ecosystem functioning in changing environments: A theoretical framework. Proceedings of the National Academy of Sciences 98: 11376–11381. https://doi.org/10.1073/pnas.171315998

O’Donnell S (2017) Evidence for facilitation among avian army‐ant attendants: specialization and species associations across elevations. Biotropica 49: 665–674. https://doi.org/10.1111/btp.12452

Ocampo-Peñuela N, CN Jenkins, V Vijay, BV Li, SL Pimm (2016) Incorporating explicit geospatial data shows more species at risk of extinction than the current Red List. Science Advances 2: e1601367. https://doi.org/10.1126/sciadv.1601367

Oksanen J, G Simpson, F Blanchet, R Kindt, P Legendre, P Minchin, R O'Hara, P Solymos, M Stevens, E Szoecs, H Wagner, M Barbour, M Bedward, B Bolker, D Borcard, T Borman, G Carvalho, M Chirico, M De Caceres, S Durand, H Evangelista, R FitzJohn, M Friendly, B Furneaux, G Hannigan, M Hill, L Lahti, C Martino, D McGlinn, M Ouellette, E Ribeiro Cunha, T Smith, A Stier, C Ter Braak, J Weedon (2025). vegan: Community Ecology Package. R package version 2.8-0, 10.32614/CRAN.package.vegan

Petchey OL, KJ Gaston (2006) Functional diversity: back to basics and looking forward. Ecology Letters 9: 741–758. https://doi.org/10.1111/j.1461-0248.2006.00924.x

Powell GVN (1979) Structure and dynamics of interspecific flocks in a neotropical mid-elevation forest. The Auk 96: 375–390. https://doi.org/10.1093/auk/96.2.375

R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/.

Rahbek C (1997) The Relationship among Area, Elevation, and Regional Species Richness in Neotropical Birds. The American Naturalist 149: 875–902. https://doi.org/10.1086/286028

Rojas TN, OA Bruzzone, IC Zampini, MI Isla, PG Blendinger (2021) A combination of rules govern fruit trait preference by frugivorous bat and bird species: nutrients, defence and size. Animal Behaviour 176: 111–123. https://doi.org/10.1016/j.anbehav.2021.04.001

Rompré G, W Douglas Robinson, A Desrochers, G Angehr (2007) Environmental correlates of avian diversity in lowland Panama rain forests. Journal of Biogeography 34: 802–815. https://doi.org/10.1111/j.1365-2699.2006.01657.x

Santillán V, M Quitián, BA Tinoco (2019) Different responses of taxonomic and functional bird diversity to forest fragmentation across an elevational gradient. Oecologia 189: 863–873. https://doi.org/10.1007/s00442-018-4309-x

Sekercioglu CH, SH Schneider, JP Fay, SR Loarie (2008) Climate change, elevational range shifts, and bird extinctions. Conservation Biology 22: 140–150. https://doi.org/10.1111/j.1523-1739.2007.00852.x

Sheard C, MHC Neate-Clegg, N Alioravainen, SEI Jones, C Vincent, HEA MacGregor, TP Bregman, et al. (2020) Ecological drivers of global gradients in avian dispersal inferred from wing morphology. Nature Communications 11: 2463. https://doi.org/10.1038/s41467-020-16313-6

Sigel BJ, TW Sherry, BE Young (2006) Avian Community Response to Lowland Tropical Rainforest Isolation: 40 Years of Change at La Selva Biological Station, Costa Rica. Conservation Biology 20: 111–121. https://doi.org/10.1111/j.1523-1739.2005.00293.x

Slifkin J (2019) Surveys of Mixed Species Feeding Flocks in Cloudbridge Nature Reserve Costa Rica: A Progress Report. Cloudbridge Nature Reserve 2019.

Snow SS, L Sandoval, HF Greeney (2017) The Nest and Eggs of the Rufous Mourner (Rhytipterna h. holerythra). The Wilson Journal of Ornithology 129: 626–630. https://doi.org/10.1676/16-147.1

Sridhar H, K Shanker (2014) Using intra-flock association patterns to understand why birds participate in mixed-species foraging flocks in terrestrial habitats. Behavioral Ecology and Sociobiology 68: 185-196. https://doi.org/10.1007/s00265-013-1633-3

Sridhar H, G Beauchamp, K Shanker (2009) Why do birds participate in mixed-species foraging flocks? A large-scale synthesis. Animal Behaviour 78: 337–347. https://doi.org/10.1016/j.anbehav.2009.05.008

Srinivasan U, RH Raza, S Quader (2012) Patterns of species participation across multiple mixed-species flock types in a tropical forest in northeastern India. Journal of Natural History 46: 2749–2762. https://doi.org/10.1080/00222933.2012.717644

Stotz DF (1993) Geographic variation in species composition of mixed species flocks in lowland humid forests in Brazil. Papéis Avulsos de Zoologia 34: 61–75.

Thiollay JM (1999) Frequency of Mixed Species Flocking in Tropical Forest Birds and Correlates of Predation Risk: An Intertropical Comparison. Journal of Avian Biology 30: 282. https://doi.org/10.2307/3677354

Tobias JA, C Sheard, AL Pigot, AJ Devenish, J Yang, F Sayol, MHC Neate-Clegg, et al. (2022) AVONET: morphological, ecological and geographical data for all birds. Ecology Letters 25: 581–597. https://doi.org/10.1111/ele.13898

Valburg LK (1992) Flocking and Frugivory: The Effect of Social Groupings on Resource Use in the Common Bush-Tanager. The Condor 94: 358–363. https://doi.org/10.2307/1369208

Van Der Hoek Y, GV Gaona, K Martin (2017) The diversity, distribution and conservation status of the tree‐cavity‐nesting birds of the world. Diversity and Distributions 23: 1120–1131. https://doi.org/10.1111/ddi.12601

Vásquez‐Ávila B, JL Knowlton, CL Espinosa, BA Tinoco (2021) Habitat alteration modifies the structure and function of mixed‐species flocks in an Andean landscape. Biotropica 53: 1153–1162. https://doi.org/10.1111/btp.12957

Velho N, J Ratnam, U Srinivasan, M Sankaran (2012) Shifts in community structure of tropical trees and avian frugivores in forests recovering from past logging. Biological Conservation 153: 32–40. https://doi.org/10.1016/j.biocon.2012.04.028

Villéger S, NWH Mason, D Mouillot (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89: 2290–2301. https://doi.org/10.1890/07-1206.1

Waylen P, C Caviedes, G Poveda, O Mesa, M Quesada (1998) Rainfall Distribution and Regime in Costa Rica and its Response to the El Niño-Southern Oscillation. Yearbook (Conference of Latin American Geographers) 24: 75–84.

Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York.

Zou F, H Jones, ZGJ Colorado, D Jiang, T-M Lee, A Martínez, K Sieving, et al. (2018) The conservation implications of mixed-species flocking in terrestrial birds, a globally-distributed species interaction network. Biological Conservation 224: 267–276. https://doi.org/10.1016/j.biocon.2018.06.004

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30-10-2025

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