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The effects of oil palm plantations on the functional diversity of Amazonian birds

Published online by Cambridge University Press:  05 August 2016

Sara M. Almeida ,
Larissa C. Silva ,
Maíra R. Cardoso ,
Pablo V. Cerqueira ,
Leandro Juen  and
Marcos P. D. Santos
Sara M. Almeida*
Affiliation:
Graduate Program in Zoology, Universidade Federal do Pará/Museu Paraense Emílio Goeldi, Caixa Postal 479, CEP 66075-110, Belém, Pará, Brazil
Larissa C. Silva
Affiliation:
Graduate Program in Zoology, Universidade Federal do Pará/Museu Paraense Emílio Goeldi, Caixa Postal 479, CEP 66075-110, Belém, Pará, Brazil
Maíra R. Cardoso
Affiliation:
Graduate Program in Zoology, Universidade Federal do Pará/Museu Paraense Emílio Goeldi, Caixa Postal 479, CEP 66075-110, Belém, Pará, Brazil
Pablo V. Cerqueira
Affiliation:
Graduate Program in Zoology, Universidade Federal do Pará/Museu Paraense Emílio Goeldi, Caixa Postal 479, CEP 66075-110, Belém, Pará, Brazil
Leandro Juen
Affiliation:
Graduate Program in Zoology, Universidade Federal do Pará/Museu Paraense Emílio Goeldi, Caixa Postal 479, CEP 66075-110, Belém, Pará, Brazil Institute of Biological Sciences, Universidade Federal do Pará (UFPA), Belém, Pará, Brazil
Marcos P. D. Santos
Affiliation:
Graduate Program in Zoology, Universidade Federal do Pará/Museu Paraense Emílio Goeldi, Caixa Postal 479, CEP 66075-110, Belém, Pará, Brazil Institute of Biological Sciences, Universidade Federal do Pará (UFPA), Belém, Pará, Brazil
*
1Corresponding author. Email: salmeida.eco@gmail.com
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Abstract:

Oil palm plantations are rapidly expanding in tropical areas, although the nature of the impacts on the functional roles of the different species in the ecosystem is poorly understood. The present study is the first assessment of how oil palm affects the functional diversity of birds in the Brazilian Amazon and tests the hypothesis that converting forest to oil palm decreases functional diversity of bird communities, selecting species more tolerant to environmental disturbances. We conducted point counts to survey bird communities in 16 plots in the eastern Amazon. We sampled 32 points in riparian forest, 128 in oil palm and 160 in forested habitats. To test whether the conversion of forest into oil palm plantations affects functional diversity of birds we calculated the FD (Functional Diversity) and FRic (Functional Richness) indices. To examine whether oil palm plantations select species functionally more similar than expected by chance we used a null model (SES.FD). FD was significantly higher in the forest plots in comparison with riparian forests and oil palm, and lower in oil palm when compared with riparian forests. FRic, in turn, was greater in forest plots than in oil palm and in riparian forest. These results show that the conversion of forested areas to oil palm represents a great loss of functional strategies. The SES values indicate that in forested habitats bird communities tend to be functionally clustered while in the oil palm they are functionally overdispersed. The functional traits most affected by oil palm were those associated with diet and foraging stratum. In short, oil palm plantations reduced functional diversity of birds, although the presence of riparian forests within the plantations and the fragments of forest adjacent are extremely important for the maintenance of ecosystem services.

Keywords

classification treeecological corridorsElaeis guineensisfunctional overdispersiontraits
Type
Research Article
Information
Journal of Tropical Ecology , Volume 32 , Issue 6 , November 2016 , pp. 510 - 525
Copyright
Copyright © Cambridge University Press 2016 

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References

LITERATURE CITED

ARATRAKORN, S., THUNHIKORN, S. & DONALD, P. F. 2006. Changes in bird communities following conversion of lowland forest to oil palm and rubber plantations in southern Thailand. Bird Conservation International 16:71–82.Google Scholar
AZHAR, B., LINDENMAYER, D. B., WOOD, J., FISCHER, J., MANNING, A., MCELHINNY, C. & ZAKARIA, M. 2013. The influence of agricultural system, stand structural complexity and landscape context on foraging birds in oil palm landscapes. Ibis 155: 297–312.Google Scholar
BASTOS, T. X., MULLER, A. A., PACHECO, N. A., SAMPAIO, S. M. N., ASSAD, E. D. & MARQUES, A. F. S. 2001. Zoneamento de riscos climáticos para a cultura do dendezeiro no estado do Pará. Revista Brasileira de Agrometeorologia 9:564–570.Google Scholar
BAWA, K. S. 1990. Plant–pollinator interactions in a tropical rain forest. Annual Review of Ecology and Systematics 21:339–422.CrossRefGoogle Scholar
BLITZER, E. J., DORMANN, C. F., HOLZSCHUH, A., KLEIN, A. M., RAND, T. A. & TSCHARNTKE, T. 2012. Spillover of functionally important organisms between managed and natural habitats. Agriculture Ecosystems and Environment 146:34–43.CrossRefGoogle Scholar
BLONDEL, J., FERRY, C. & FROCHOT, B. 1970. La méthode des indices ponctuels d'abundance (IPA) ou des relevés d'avifaune par “stations d’écoute”. Alauda 38:55–71.Google Scholar
BOLFE, E. L & BATISTELLA, M. 2011. Análise florística e estrutural de sistemas silviagrícolas em Tomé-Açú, Pará. Pesquisa Agropecuária Brasileira 46:1139–1147.CrossRefGoogle Scholar
BREIMAN, L., FRIEDMAN, J. H., OLSHEN, R. A. & STONE, C. J. 1984. Classification and regression trees. Wadsworth & Brooks/Cole Advanced Books & Software, Monterey. 358 pp.Google Scholar
CORNWELL, W. K., SCHWILK, D. W. & ACKERLY, D. D. 2006. A trait-based test for habitat filtering: convex hull volume. Ecology 87:1465–1471.Google Scholar
CORREA, F. S., JUEN, L., RODRIGUES, L. C., SILVA-FILHO, H. F. & SANTOS-COSTA, M. C. 2015. Effects of oil palm plantations on anuran diversity in the eastern Amazon. Animal Biology 65:321–335.Google Scholar
CUNHA, E. J., MONTAG, L. F. & JUEN, L. 2015. Oil palm crops effects on environmental integrity of Amazonian streams and heteropteran (Hemiptera) species diversity. Ecological Indicators 52:422–429.Google Scholar
DEVELEY, P. F. & PONGILUPPI, T. 2010. Impactos potenciais na avifauna decorrentes das alterações propostas para o Código Florestal Brasileiro. Biota Neotropica 10:43–45.CrossRefGoogle Scholar
DEVICTOR, V., MOUILLOT, D., MEYNARD, C., JIGUET, F., THUILLER, W. & MOUQUET, N. 2010. Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecology Letters 13:1030–1040.CrossRefGoogle Scholar
DÍAZ, S. & CABIDO, M. 2001. Vive la difference: plant functional diversity matters to ecosystem processes. Trends in Ecology and Evolution 16:646–655.CrossRefGoogle Scholar
DRAY, S. & DUFOUR, A. B. 2007. The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22:1–20.Google Scholar
EDWARDS, D. P., HODGSON, J. A., HAMER, K. C., MITCHELL, S. L., AHMAD, A. H., CORNELL, S. J. & WILCOVE, D. S. 2010. Wildlife-friendly oil palm plantations fail to protect biodiversity effectively. Conservation Letters 3:236–242.CrossRefGoogle Scholar
EDWARDS, F. A., EDWARDS, D. P., HAMER, K. C. & DAVIES, R. G. 2013. Impacts of logging and conversion of rainforest to oil palm on the functional diversity of birds in Sundaland. Ibis 155:313–326.CrossRefGoogle Scholar
EDWARDS, F. A., EDWARDS, D. P., LARSEN, T. H., HSU, W. W., BENEDICK, S., CHUNG, A., VUN KHEN, C., WILCOVE, D. S. & HAMER, K. C. 2014. Does logging and forest conversion to oil palm agriculture alter functional diversity in a biodiversity hotspot? Animal Conservation 17:163–173.CrossRefGoogle Scholar
ELMQVIST, T., FOLKE, C., NYSTROM, M., PETERSON, G., BENGSTON, J., WALKER, B. & NORBERG, J. 2003. Response diversity and ecosystem resilience. Frontiers in Ecology and the Environment 1:488–494.CrossRefGoogle Scholar
FAGAN, W. 1997. Omnivory as a stabilizing feature of natural communities. American Naturalist 150:554–567.CrossRefGoogle ScholarPubMed
FITZHERBERT, E. B., STRUEBIG, M. J., MOREL, A., DANIELSEN, F., BRÜHL, C. A., DONALD, P. F. & PHALAN, B. 2008. How will oil palm expansion affect biodiversity? Trends in Ecology and Evolution 23:538–545.CrossRefGoogle ScholarPubMed
FLYNN, D. F. B., GOGOL-PROKURAT, M., NOGEIRE, T., MOLINARI, N., RICHERS, B. T., LIN, B. B., SIMPSON, N., MAYFIELD, M. M. & DECLERCK, F. 2009. Loss of functional diversity under land use intensification across multiple taxa. Ecology Letters 12:22–33.CrossRefGoogle ScholarPubMed
GALETTI, M. & ALEIXO, A. 1998. Effects of palm heart harvesting on avian frugivores in the Atlantic rain forest of Brazil. Journal of Applied Ecology 35:286–293.CrossRefGoogle Scholar
HAWES, J., BARLOW, J., GARDNER, T. A. & PERES, C. A. 2008. The value of forest strips for understorey birds in an Amazonian plantation landscape. Biological Conservation 141:2262–2278.CrossRefGoogle Scholar
HIDASI-NETO, J., BARLOW, J. & CIANCIARUSO, M. V. 2012. Bird functional diversity and wildfires in the Amazon: the role of forest structure. Animal Conservation 15:407–415.Google Scholar
HUTCHINSON, G. E. 1957. Concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology 22:415–427.CrossRefGoogle Scholar
KEMBEL, S. W., COWAN, P. D., HELMUS, M. R., CORNWELL, W. K., MORLON, H., ACKERLY, D. D., BLOMBERG, S. P. & WEBB, C. O. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464.Google Scholar
KOH, L. P. 2008. Can oil palm plantations be made more hospitable for forest butterflies and birds? Journal of Applied Ecology 45:1002–1009.CrossRefGoogle Scholar
KOH, L. P., LEVANG, P. & GHAZOUL, J. 2009. Designer landscapes for sustainable biofuels. Trends in Ecology and Evolution 24:431–438.CrossRefGoogle ScholarPubMed
LALIBERTÉ, E. & LEGENDRE, P. 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305.Google Scholar
LEES, A. C. & PERES, C. A. 2008. Conservation value of remnant riparian forest corridors of varying quality for Amazonian birds and mammals. Conservation Biology 22:439–449.Google Scholar
LEES, A. C., MOURA, N. G., ALMEIDA, A. S. & VIEIRA, I. C. G. 2015. Poor prospects for avian biodiversity in Amazonian oil palm. PLoS ONE 10:e0122432.Google Scholar
LOVEJOY, T. E. 1974. Bird diversity and abundance in Amazon forest communities. Living Bird 13:127–191.Google Scholar
LUCK, G. W., CARTER, A. & SMALLBONE, L. 2013. Changes in bird functional diversity across multiple land uses: interpretations of functional redundancy depend on functional group identity. PLoS ONE 8:e63671–e63671.Google Scholar
MALHI, Y., GARDNER, T. A., GOLDSMITH, G. R., SILMAN, M. R. & ZELAZOWSKI, P. 2014. Tropical forests in the Anthropocene. Annual Review of Environment and Resources 39: 125–159.Google Scholar
MOUCHET, M. A., VILLÉGER, S., MASON, N. W. H. & MOUILLOT, D. 2010. Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Functional Ecology 24:867–876.CrossRefGoogle Scholar
NAMBA, T., TANABE, K. & MAEDA, N. 2008. Omnivory and stability of food webs. Ecological Complexity 5:73–85.CrossRefGoogle Scholar
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
PERFECTO, I., VANDREMEER, J. H., BAUTISTA, G. L., NUÑEZ, G. I., GREENBERG, R., BICHIER, P. & LANGRIDGE, S. 2004. Greater predation in shaded coffee farms: the role of resident neotropical birds. Ecology 85:2677–2681.CrossRefGoogle Scholar
PETCHEY, O. L. & GASTON, K. 2006. Functional diversity: back to basics and looking forward. Ecology Letters 9:741–758.CrossRefGoogle ScholarPubMed
PETCHEY, O. L., EVANS, K. L., FISHBURN, I. S. & GASTON, K. J. 2007. Low functional diversity and no redundancy in British avian assemblages. Journal of Animal Ecology 76: 977–985.Google Scholar
PIACENTINI, V. Q., ALEIXO, A., AGNE, C. E., MAURÍCIO, G. N., PACHECO, J. F., BRAVO, G. A., BRITO, G. R. R., NAKA, L. N., OLMOS, F., POSSO, S., SILVEIRA, L. F., BETINI, G. S., CARRANO, E., FRANZ, I., LEES, A. C., LIMA, L. M., PIOLI, D., SCHUNCK, F., AMARAL, F. R., BENCKE, G. A., COHN-HAFT, M., FIGUEIREDO, L. F. A., STRAUBE, F. C. & CESARI, E. 2015. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. Revista Brasileira de Ornitologia 23:91–298.CrossRefGoogle Scholar
PIZO, M. A. & GALETTI, M. 2010. Métodos e perspectivas do estudo da frugivoria e dispersão de sementes por aves. pp. 493–503 in Von Matter, S., Straube, F. C., Accordi, I. A., Piacentini, V. & Cândido, J. F. Jr (eds.). Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Ed. Technical Books, Rio de Janeiro.Google Scholar
PORTES, C. E. B., CARNEIRO, L. S., SCHUNCK, F., SILVA, M. S., ZIMMER, K. J., WHITTAKER, A., POLETTO, F., SILVEIRA, L. F. & ALEIXO, A. 2011. Annotated checklist of birds recorded between 1998 and 2009 at nine areas in the Belém area of endemism, with notes on some range extensions and the conservation status of endangered species. Revista Brasileira Ornitologia 19:167– 184.Google Scholar
PRESCOTT, G. W., GILROY, J. J., HAUGAASEN, T., URIBE, C. A. M., FOSTER, W. A. & EDWARDS, D. P. 2016. Reducing the impacts of Neotropical oil palm development on functional diversity. Biological Conservation 197:139–145.CrossRefGoogle Scholar
ROSENBERG, G. H. 1990. Habitat specialization and foraging behavior by birds of Amazonian river islands in northeastern Peru. Condor 92:427–443.CrossRefGoogle Scholar
SAVILAAKSO, S., GARCIA, C., GARCIA-ULLOA, J., GHAZOUL, J., GROOM, M., GUARIGUATA, M. R., LAUMONIER, Y., NASI, R., PETROKOFSKY, G., SNADDON, J. & ZRUST, M. 2014. Systematic review of effects on biodiversity from oil palm production. Environmental Evidence 3:4.Google Scholar
SCHROEDER, M. S., CULHANE, A. C., QUACKENBUSH, J. & HAIBE-KAINS, B. 2011. survcomp: an R/Bioconductor package for performance assessment and comparison of survival models. Bioinformatics 27:3206–3208.Google Scholar
ŞEKERCIOĞLU, Ç. H. 2006. Increasing awareness of avian ecological function. Trends in Ecology and Evolution 21:464–471.CrossRefGoogle ScholarPubMed
ŞEKERCIOĞLU, Ç. H. 2012. Bird functional diversity and ecosystem services in tropical forests, agroforests and agricultural areas. Journal of Ornithology 153:S153–S161.CrossRefGoogle Scholar
ŞEKERCIOĞLU, Ç. H., DAILY, G. C. & EHRLICH, P. R. 2004. Ecosystem consequences of bird declines. Proceedings of the National Academy of Sciences USA 101:18042–18047.Google Scholar
SOBRAL, F. L. & CIANCIARUSO, M. V. 2015. Functional and phylogenetic structure of forest and savanna bird assemblages across spatial scales. Ecography 38:1–9.Google Scholar
TEWS, J., BROSE, U., GRIMM, V., TIELBÖRRGER, K., WICHMANN, M. C., SCHWAGER, M. & JELTSCH, F. 2004. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography 31:79–92.Google Scholar
TILMAN, D. 2001. Functional diversity. pp. 109–120 in Levin, S. A. (ed.). Encyclopedia of biodiversity. Academic Press, San Diego.CrossRefGoogle Scholar
TILMAN, D., FARGIONE, J., WOLFF, B., ANTONIO, C. D., DOBSON, A., HOWARTH, R., SCHINDLER, D., SCHLESINGER, W. H., SIMBERLOFF, D. & SWACKHAMER, D. 2001. Forecasting agriculturally driven global environmental change. Science 292:281–284.Google Scholar
VIEIRA, I. C. G., TOLEDO, P. M., SILVA, J. M. C. & HIGUCHI, H. 2008. Deforestation and threats to the biodiversity of Amazonia. Brazilian Journal of Biology 68:949–956.CrossRefGoogle Scholar
VIELLIARD, J. M. E., ALMEIDA, M.E.C., ANJOS, L. & SILVA, W. R. 2010. Levantamento quantitativo por pontos de escuta e o Índico Pontual de Abundância (IPA). Pp. 47–60 in Von Matter, S., Straube, F. C., Accordi, I. A, Piacentini, V. & Cândido, J. F. Jr (eds.). Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Ed. Technical Books, Rio de Janeiro.Google Scholar
VILLÉGER, S., MASON, N. W. H. & MOUILLOT, D. 2008. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301.Google Scholar
VILLELA, A. A., JACCOUD, D., ROSA, L. P. & FREITAS, M. V. 2014. Status and prospects of oil palm in the Brazilian Amazon. Biomass Bioenergy 67:270–278.Google Scholar
WHITLOCK, M. C. 2005. Combining probability from independent tests: the weighted Z-method is superior to Fisher's approach. Journal of Evolutionary Biology 18:1368–1373.Google Scholar
WIENS, J. A. & JOHNSTON, R. F. 1977. Adaptative correlates of granivory in birds. pp. 301–340 in Pinowski, J. & Kendeigh, S. C. (eds.). Granivorous birds in ecosystems. Cambridge University Press, Cambridge.Google Scholar
WILMAN, H., BELMAKER, J., SIMPSON, J., DE LA ROSA, C., RIVADENEIRA, M. M. & JETZ, W. 2014. EltonTraits 1.0: Species-level foraging attributes of the world's birds and mammals. Ecology 95:2027.Google Scholar
ZANETTE, L., DOYLE, P. & TRÉMONT, S. 2000. Food shortage in small fragments: evidence from an area-sensitive passerine. Ecology 81:1654–1666.Google Scholar