No CrossRef data available.
Article contents
Forest cover and environment type shape functional diversity of insectivorous birds within the Brazilian Atlantic Forest
Published online by Cambridge University Press: 26 March 2024
Summary
Tropical insectivorous birds comprise a diverse group that has a distinct response to habitat degradation. However, knowledge on birds’ ecological functions and their large-scale functional responses to human impacts across various habitats is scarce. We sampled 22 1-km-radius buffer landscapes within the Cantareira-Mantiqueira region (south-east Brazil), including native forests, pastures and marshes, to assess how landscape and habitat characteristics might affect insectivorous birds within the Brazilian Atlantic Forest. We studied whether bird species and functional diversity might respond to habitat turnover and nestedness and to native forest cover using generalized linear mixed models. We found negative effects of increased native forest cover on functional diversity indices. Bird communities in pastures show more nestedness, whereas marsh areas exhibit higher turnover. Forest areas receive a balanced contribution from both nestedness and turnover. These results are attributable to the predominantly secondary growth and early successional stages of the native forest fragments in the region, emphasizing the connection between landscape characteristics, habitat types and bird functional diversity in the Brazilian Atlantic Forest.
Keywords
- Type
- Research Paper
- Information
- Copyright
- © The Author(s), 2024. Published by Cambridge University Press on behalf of Foundation for Environmental Conservation
References
Acevedo-Charry, O, Aide, TM (2019) Recovery of amphibian, reptile, bird and mammal diversity during secondary forest succession in the tropics. Oikos 128: 1065–1078.CrossRefGoogle Scholar
Adorno, BFCB, Barros, FM, Cezar Ribeiro, M, da Silva, VX, Hasui, É (2021) Landscape heterogeneity shapes bird phylogenetic responses at forest–matrix interfaces in Atlantic Forest, Brazil. Biotropica 53: 409–421.CrossRefGoogle Scholar
Alcarde Alvares, C, Stape, J, Sentelhas, P, Gonçalves, J, Sparovek, G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711–728.CrossRefGoogle Scholar
Alexander, J, Ehlers Smith, DA, Ehlers Smith, YC, Downs, CT (2019) Drivers of fine-scale avian functional diversity with changing land use: an assessment of the effects of eco-estate housing development and management. Landscape Ecology 34: 537–549.10.1007/s10980-019-00786-yCrossRefGoogle Scholar
Almeida-Gomes, M, Vieira, MV, Rocha, CFD, Melo, AS (2019) Habitat amount drives the functional diversity and nestedness of anuran communities in an Atlantic Forest fragmented landscape. Biotropica 51: 874–884.CrossRefGoogle Scholar
Arroyo-Rodríguez, V, Rös, M, Escobar, F, Melo, FPL, Santos, BA, Tabarelli, M et al. (2013) Plant β-diversity in fragmented rain forests: testing floristic homogenization and differentiation hypotheses. Journal of Ecology 101: 1449–1458.CrossRefGoogle Scholar
Barbaro, L, Giffard, B, Charbonnier, Y, van Halder, I, Brockerhoff, EG (2014) Bird functional diversity enhances insectivory at forest edges: a transcontinental experiment. Diversity and Distributions 20: 149–159.10.1111/ddi.12132CrossRefGoogle Scholar
Barbaro, L, Rusch, A, Muiruri, EW, Gravellier, B, Thiery, D, Castagneyrol, B (2017) Avian pest control in vineyards is driven by interactions between bird functional diversity and landscape heterogeneity. Journal of Applied Ecology 54: 500–508.CrossRefGoogle Scholar
Barbosa, KV de C, Knogge, C, Develey, PF, Jenkins, CN, Uezu, A (2017) Use of small Atlantic Forest fragments by birds in southeast Brazil. Perspectives in Ecology and Conservation 15: 42–46.CrossRefGoogle Scholar
Barbosa, KVdC, Rodewald, AD, Ribeiro, MC, Jahn, AE (2020) Noise level and water distance drive resident and migratory bird species richness within a Neotropical megacity. Landscape and Urban Planning 197: 103769.
CrossRefGoogle Scholar
Barros, FM, Martello, F, Peres, CA, Pizo, MA, Ribeiro, MC (2019a) Matrix type and landscape attributes modulate avian taxonomic and functional spillover across habitat boundaries in the Brazilian Atlantic Forest. Oikos 128: 1600–1612.10.1111/oik.05910CrossRefGoogle Scholar
Barros, FM, Peres, C, Pizo, M, Ribeiro, M (2019b) Divergent flows of avian-mediated ecosystem services across forest-matrix interfaces in human-modified landscapes. Landscape Ecology 34: 879–894.10.1007/s10980-019-00812-zCrossRefGoogle Scholar
Baselga, A (2010) Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography 19: 134–143.10.1111/j.1466-8238.2009.00490.xCrossRefGoogle Scholar
Baselga, A, Orme, CDL (2012)
betapart: an R package for the study of beta diversity. Methods in Ecology and Evolution 3: 808–812.CrossRefGoogle Scholar
Bello, FP, Carmona, C, Dias, A, Götzenberger, L, Moretti, M, Berg, M (2021) Handbook of Trait-Based Ecology: From Theory to R Tools. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Blake, JG, Loiselle, BA (2001) Bird assemblages in second-growth and old-growth forests, Costa Rica: perspectives from mist nets and point counts. The Auk 118: 304–326.CrossRefGoogle Scholar
Boscolo, D, Tokumoto, PM, Ferreira, PA, Ribeiro, JW, dos Santos, JS (2017) Positive responses of flower visiting bees to landscape heterogeneity depend on functional connectivity levels. Perspectives in Ecology and Conservation 15: 18–24.CrossRefGoogle Scholar
Bregman, TP, Lees, AC, MacGregor, HEA, Darski, B, de Moura, NG, Aleixo, A et al. (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: 20161289.CrossRefGoogle ScholarPubMed
Brooks, M, Kristensen, K, van Benthem, K, Magnusson, A, Berg, CW, Nielsen, A et al. (2017)
glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R Journal 9: 378–400.CrossRefGoogle Scholar
Burnham, KP, Anderson, DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods & Research 33: 261–304.CrossRefGoogle Scholar
Carmona, CP, Guerrero, I, Morales, MB, Oñate, JJ, Peco, B (2017) Assessing vulnerability of functional diversity to species loss: a case study in Mediterranean agricultural systems. Functional Ecology 31: 427–435.10.1111/1365-2435.12709CrossRefGoogle Scholar
Clavel, J, Julliard, R, Devictor, V (2011) Worldwide decline of specialist species: toward a global functional homogenization? Frontiers in Ecology and the Environment 9: 222–228.10.1890/080216CrossRefGoogle Scholar
De Coster, G, Banks-Leite, C, Metzger, JP (2015) Atlantic forest bird communities provide different but not fewer functions after habitat loss. Proceedings of the Royal Society B: Biological Sciences 282: 20142844.CrossRefGoogle Scholar
Desrochers A (2010) Morphological response of songbirds to 100 years of landscape change in North America. Ecology 91: 1577–1582.CrossRefGoogle Scholar
Develey, PF, Peres, CA (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.CrossRefGoogle Scholar
Dias, RA, Gianuca, AT, Vizentin-Bugoni, J, Gonçalves, MSS, Bencke, GA, Bastazini, VAG (2017) Livestock disturbance in Brazilian grasslands influences avian species diversity via turnover. Biodiversity and Conservation 26: 2473–2490.CrossRefGoogle Scholar
Diniz, MF, Coelho, MTP, Sánchez-Cuervo, AM, Loyola, R (2022) How 30 years of land-use changes have affected habitat suitability and connectivity for Atlantic Forest species. Biological Conservation 274: 109737.CrossRefGoogle Scholar
Dobrovolski, R, Melo, AS, Cassemiro, FAS, Diniz-Filho, JAF (2012) Climatic history and dispersal ability explain the relative importance of turnover and nestedness components of beta diversity. Global Ecology and Biogeography 21: 191–197.10.1111/j.1466-8238.2011.00671.xCrossRefGoogle Scholar
dos Anjos L, Bochio, GM, Medeiros, HR, Almeida, B de A, Lindsey, BRA, Calsavara, LC et al. (2019) Insights on the functional composition of specialist and generalist birds throughout continuous and fragmented forests. Ecology and Evolution 9: 6318–6328.Google Scholar
Duarte, GT, Santos, PM, Cornelissen, TG, Ribeiro, MC, Paglia, AP (2018) The effects of landscape patterns on ecosystem services: meta-analyses of landscape services. Landscape Ecology 33: 1247–1257.CrossRefGoogle Scholar
Fortin, M-J, Dale, MRT (2005) Spatial Analysis: A Guide for Ecologists. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Gardner, TA, Barlow, J, Chazdon, R, Ewers, RM, Harvey, CA, Peres, CA et al. (2009) Prospects for tropical forest biodiversity in a human-modified world. Ecology Letters 12: 561–582.CrossRefGoogle Scholar
Gaspar, LP, Scarpelli, MDA, Oliveira, EG, Alves, RS-C, Gomes, AM, Wolf, R et al. (2023) Predicting bird diversity through acoustic indices within the Atlantic Forest biodiversity hotspot. Frontiers in Remote Sensing 4: 1283719.CrossRefGoogle Scholar
Gower, JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53: 325–338.10.1093/biomet/53.3-4.325CrossRefGoogle Scholar
IUCN (2022) The IUCN Red List of Threatened Species [www document]. URL https://www.iucnredlist.org
Google Scholar
Johnstone, JF, Allen, CD, Franklin, JF, Frelich, LE, Harvey, BJ, Higuera, PE et al. (2016) Changing disturbance regimes, ecological memory, and forest resilience. Frontiers in Ecology and the Environment 14: 369–378.CrossRefGoogle Scholar
Karp, DS, Rominger, AJ, Zook, J, Ranganathan, J, Ehrlich, PR, Daily, GC (2012) Intensive agriculture erodes β-diversity at large scales. Ecology Letters 15: 963–970.CrossRefGoogle ScholarPubMed
Laliberté, E, Legendre, P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91: 299–305.CrossRefGoogle ScholarPubMed
Legendre, P, Birks, HJB (2012) From classical to canonical ordination. In: Birks, HJB, Lotter, AF, Juggins, S, Smol, JP (eds), Tracking Environmental Change Using Lake Sediments: Data Handling and Numerical Techniques (pp. 201–248). Dordrecht, The Netherlands: Springer Netherlands.10.1007/978-94-007-2745-8_8CrossRefGoogle Scholar
Legendre, P, Legendre, LFJ (1998) Numerical Ecology, 2nd English edition. Amsterdam, The Netherlands: Elsevier.Google Scholar
Logez, M, Pont, D, Ferreira, MT (2010) Do Iberian and European fish faunas exhibit convergent functional structure along environmental gradients? Journal of the North American Benthological Society 29: 1310–1323.CrossRefGoogle Scholar
Mariano-Neto, E, Santos, RAS (2023) Changes in the functional diversity of birds due to habitat loss in the Brazil Atlantic Forest. Frontiers in Forests and Global Change 6: 1041268.10.3389/ffgc.2023.1041268CrossRefGoogle Scholar
Mason, N, Mouillot, D, Lee, W, Wilson, J (2005) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111: 112–118.10.1111/j.0030-1299.2005.13886.xCrossRefGoogle Scholar
Matuoka, MA, Benchimol, M, Morante-Filho, JC (2020) Tropical forest loss drives divergent patterns in functional diversity of forest and non-forest birds. Biotropica 52: 738–748.CrossRefGoogle Scholar
Mazel, F, Pennell, MW, Cadotte, MW, Diaz, S, Dalla Riva, GV, Grenyer, R et al. (2018) Prioritizing phylogenetic diversity captures functional diversity unreliably. Nature Communications 9: 2888.10.1038/s41467-018-05126-3CrossRefGoogle ScholarPubMed
Melo, MA, Sanches, PM, Silva Filho, DF, Piratelli, AJ (2022) Influence of habitat type and distance from source area on bird taxonomic and functional diversity in a Neotropical megacity. Urban Ecosystems 25: 545–560.CrossRefGoogle Scholar
Melo, MA, Silva, MAGDA, Piratelli, AJ (2020) Improvement of vegetation structure enhances bird functional traits and habitat resilience in an area of ongoing restoration in the Atlantic Forest. Anais da Academia Brasileira de Ciências 92: e20191241.10.1590/0001-3765202020191241CrossRefGoogle Scholar
Metzger, J, Martensen, A, Dixo, M, Bernacci, L, Ribeiro, M, Teixeira, A et al. (2009) Time-lag in biological responses to landscape changes in a highly dynamic Atlantic Forest region. Biological Conservation 142: 1166–1177.CrossRefGoogle Scholar
Morante-Filho, JC, Arroyo-Rodríguez, V, Faria, D (2016) Patterns and predictors of β-diversity in the fragmented Brazilian Atlantic forest: a multiscale analysis of forest specialist and generalist birds. Journal of Animal Ecology 85: 240–250.CrossRefGoogle Scholar
Morante-Filho, JC, Faria, D, Mariano-Neto, E, Rhodes, J (2015) Birds in anthropogenic landscapes: the responses of ecological groups to forest loss in the Brazilian Atlantic Forest. PLoS ONE 10: e0128923.10.1371/journal.pone.0128923CrossRefGoogle ScholarPubMed
Morelli, F, Benedetti, Y, Perna, P, Santolini, R (2018) Associations among taxonomic diversity, functional diversity and evolutionary distinctiveness vary among environments. Ecological Indicators 88: 8–16.10.1016/j.ecolind.2018.01.022CrossRefGoogle Scholar
Moritz, C, Agudo, R (2013) The future of species under climate change: resilience or decline? Science 341: 504–508.CrossRefGoogle ScholarPubMed
Mouillot, D, Graham, NAJ, Villéger, S, Mason, NWH, Bellwood, DR (2013) A functional approach reveals community responses to disturbances. Trends in Ecology & Evolution 28: 167–177.CrossRefGoogle ScholarPubMed
Odum, EP, Barret, GW (1971) Fundamentals of Ecology, 3rd edition. Philadephia, PA, USA: W.B. Saunders Co.Google Scholar
Paradis, E, Schliep, K (2019)
ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R
. Bioinformatics 35: 526–528.CrossRefGoogle ScholarPubMed
Pavoine, S, Vallet, J, Dufour, A-B, Gachet, S, Daniel, H (2009) On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118: 391–402.CrossRefGoogle Scholar
Petchey, OL, Gaston, KJ (2006) Functional diversity: back to basics and looking forward. Ecology Letters 9: 741–758.CrossRefGoogle ScholarPubMed
Pollock, HS, Jones, TM, Tarwater, CE, Nishikawa, ET, Brawn, JD (2020) Rapid colonization and turnover of birds in a tropical forest treefall gap. Journal of Field Ornithology 91: 107–117.10.1111/jofo.12328CrossRefGoogle Scholar
Prescott, GW, Gilroy, JJ, Haugaasen, T, Medina Uribe, CA, Foster, WA, Edwards, DP (2016) Reducing the impacts of Neotropical oil palm development on functional diversity. Biological Conservation 197: 139–145.CrossRefGoogle Scholar
R Core Team (2022) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Core Development Team.Google Scholar
Rezende, CL, Scarano, FR, Assad, ED, Joly, CA, Metzger, JP, Strassburg, BBN et al. (2018) From hotspot to hopespot: an opportunity for the Brazilian Atlantic Forest. Perspectives in Ecology and Conservation 16: 208–214.CrossRefGoogle Scholar
Ribeiro, MC, Metzger, JP, Martensen, AC, Ponzoni, FJ, Hirota, MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142: 1141–1153.CrossRefGoogle Scholar
Riemann, JC, Ndriantsoa, SH, Rödel, M-O, Glos, J (2017) Functional diversity in a fragmented landscape – habitat alterations affect functional trait composition of frog assemblages in Madagascar. Global Ecology and Conservation 10: 173–183.CrossRefGoogle Scholar
Rodrigues, RC, Hasui, É, Assis, JC, Pena, JCC, Muylaert, RL, Tonetti, VR et al. (2019) ATLANTIC BIRD TRAITS: a data set of bird morphological traits from the Atlantic forests of South America. Ecology 100: e02647.CrossRefGoogle ScholarPubMed
Santos Junior, PCA, Marques, FC, Lima, MR, dos Anjos, L (2016) The importance of restoration areas to conserve bird species in a highly fragmented Atlantic Forest landscape. Perspectives in Ecology and Conservation 14: 1–7.Google Scholar
Scarpelli, MDA, Ribeiro, MC, Teixeira, CP (2021) What does Atlantic Forest soundscapes can tell us about landscape? Ecological Indicators 121: 107050.CrossRefGoogle Scholar
Sekercioglu, CH (2006) Ecological Significance of Bird Populations. Cerdanyola del Vallès, Spain: Lynx Edicions.Google Scholar
Sekercioglu, CH (2012) Bird functional diversity and ecosystem services in tropical forests, agroforests and agricultural areas. Journal of Ornithology 153: 153–161.CrossRefGoogle Scholar
Sick, H, Barruel, P (1984) Ornitologia brasileira. Brasília, Brazil: Editora Universidade de Brasília.Google Scholar
Somenzari, M, do Amaral, PP, Cueto, VR, Guaraldo, AdC, Jahn, AE, Lima, DM et al. (2018) An overview of migratory birds in Brazil. Papéis Avulsos de Zoologia 58: e20185803.CrossRefGoogle Scholar
Thorn, S, Chao, A, Bernhardt-Römermann, M, Chen, Y-H, Georgiev, KB, Heibl, C et al. (2020) Rare species, functional groups, and evolutionary lineages drive successional trajectories in disturbed forests. Ecology 101: e02949.10.1002/ecy.2949CrossRefGoogle ScholarPubMed
Tilman, D (1996) Biodiversity: population versus ecosystem stability. Ecology 77: 350–363.CrossRefGoogle Scholar
Tobias, JA, Sheard, C, Pigot, AL, Devenish, AJM, Yang, J, Sayol, F et al. (2022) AVONET: morphological, ecological and geographical data for all birds. Ecology Letters 25: 581–597.10.1111/ele.13898CrossRefGoogle ScholarPubMed
Tonetti, VR, Rego, MA, De Luca, AC, Develey, PF, Schunck, F, Silveira, LF (2017) Historical knowledge, richness and relative representativeness of the avifauna of the largest native urban rainforest in the world. Zoologia 34: 1–18.CrossRefGoogle Scholar
Villéger, S, Mason, NWH, Mouillot, D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89: 2290–2301.10.1890/07-1206.1CrossRefGoogle ScholarPubMed
Violle, C, Navas, M-L, Vile, D, Kazakou, E, Fortunel, C, Hummel, I et al. (2007) Let the concept of trait be functional! Oikos 116: 882–892.10.1111/j.0030-1299.2007.15559.xCrossRefGoogle Scholar
Wilman, H, Belmaker, J, Simpson, J, de la Rosa, C, Rivadeneira, MM, Jetz, W (2014)
EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95: 2027.10.1890/13-1917.1CrossRefGoogle Scholar
Zuur, AF, Ieno, EN, Walker, NJ, Saveliev, AA, Smith, GM (2009) Mixed Effects Models and Extensions in Ecology with R. Berlin, Germany: Springer.CrossRefGoogle Scholar
Manzoli et al. supplementary material 1
Manzoli et al. supplementary material
File
2.8 KB
Manzoli et al. supplementary material 2
Manzoli et al. supplementary material
File
5.8 KB
Manzoli et al. supplementary material 3
Manzoli et al. supplementary material
File
5.7 KB
Manzoli et al. supplementary material 4
Manzoli et al. supplementary material
File
8.1 KB
Manzoli et al. supplementary material 5
Manzoli et al. supplementary material
File
3.9 MB
Manzoli et al. supplementary material 6
Manzoli et al. supplementary material
File
65.7 KB