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Impacts of oil palm agriculture on phyllostomid bat assemblages

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Abstract

Rising global demand for palm oil comes mainly at the expense of tropical forests, and palm plantations are increasing steadily in Latin America. Conversion of forest to oil palm agriculture accelerates biodiversity loss by dramatically altering availability and abundance of resources. Assessing the impact of these monocultures on highly diverse keystone groups such as bats is of particular ecological and economic importance. We compared phyllostomid bat assemblages in mature lowland forest interior, at forest margins and within oil palm plantations in southwestern Costa Rica. A total of 45 mist-netting nights in the late dry season yielded 1235 individual captures from 31 species. Bat assemblages in oil palm plantations were clearly distinct from those at forest sites and exhibited lower species richness, similar to results reported for Southeast Asia. Assemblage structure within oil palm plantations was characterized by increased relative abundance of common frugivorous Stenodermatinae and the loss of rare species, mainly disturbance-sensitive animalivorous Phyllostominae. Although plantations may serve as flyways for highly mobile matrix-tolerant species, even small oil palm plantations seem to act as effective barriers for many others, particularly understory gleaning animalivores. By decreasing landscape permeability even for highly mobile animals such as bats, oil palm agriculture may consequently reduce population connectivity and foster faunal impoverishment, which in turn can diminish crucial ecosystem services provided by bats. The advancing expansion of these monocultures in Latin America calls for appropriate precautionary conservation measures to protect and preserve biodiversity in oil palm growing countries.

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References

  • Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11(7):36–42

    Google Scholar 

  • Aide TM, Clark ML, Grau HR, López-Carr D, Levy M et al (2013) Deforestation and reforestation of Latin America and the Caribbean (2001–2010). Biotropica 45:262–271

    Article  Google Scholar 

  • Baker RJ, Hoofer SR, Porter CA, Van Den Bussche RA (2003) Diversification among new world leaf-nosed bats: an evolutionary hypothesis and classification inferred from digenomic congruence of DNA sequence. Occas Papers Mus, Texas Tech Univ 230:1–32

    Google Scholar 

  • Barlow J, Gardner TA, Araujo IS, Avila-Pires TCS, Bonaldo AB et al (2007) Quantifying the biodiversity value of tropical primary, secondary and plantation forests. Proc Natl Acad Sci USA 104:18555–18560

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bhagwat SA, Willis KJ (2008) Agroforestry as a solution to the oil-palm debate. Conserv Biol 22(6):1368–1369

    Article  PubMed  Google Scholar 

  • Boyles JG, Cryan PM, McCracken GF, Kunz TH (2011) Economic importance of bats in agriculture. Science 332(6025):41–42

    Article  PubMed  Google Scholar 

  • Castro-Luna AA, Galindo-González J (2012) Enriching agroecosystems with fruit-producing tree species favors the abundance and richness of frugivorous and nectarivorous bats in Veracruz, Mexico. Mamm Biol 77(1):32–40

    Google Scholar 

  • Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93(12):2533–2547

    Article  PubMed  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Clarke FM, Pio DV, Racey PA (2005) A comparison of logging systems and bat diversity in the Neotropics. Conserv Biol 19(4):1194–1204

    Google Scholar 

  • Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX et al (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5(1):3–21

    Article  Google Scholar 

  • Corley RHV (2009) How much palm oil do we need? Environ Sci Policy 2712(2):134–139

    Article  Google Scholar 

  • Danielsen F, Heegaard M (1995) Impact of logging and plantation development on species diversity: a case study from Sumatra. In: Sandbukt Ø (ed) Management of tropical forests: towards an integrated perspective. University of Oslo, Oslo, pp 73–92

    Google Scholar 

  • Danielsen F, Beukema H, Burgess ND, Parish F, Brühl CA et al (2009) Biofuel plantations on forested lands: double jeopardy for biodiversity and climate. Conserv Biol 23(2):348–358

    Article  PubMed  Google Scholar 

  • Datzmann T, von Helversen O, Mayer F (2010) Evolution of nectarivory in phyllostomid bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia). BMC Evol Biol 10:165

    Article  PubMed Central  PubMed  Google Scholar 

  • de la Peña-Cuéllar E, Benítez-Malvido J, Avila-Cabadilla LD, Martínez-Ramos M, Estrada A (2015) Structure and diversity of phyllostomid bat assemblages on riparian corridors in a human-dominated tropical landscape. Ecol Evol 5(4):903–913

    Article  PubMed Central  PubMed  Google Scholar 

  • Donald PF (2004) Biodiversity impacts of some agricultural commodity production systems. Conserv Biol 18(1):17–38

    Article  Google Scholar 

  • Estrada A, Coates-Estrada R (2001) Bat species richness in live fences and in corridors of residual rain forest vegetation at Los Tuxtlas, Mexico. Ecography 24(1):94–102

    Article  Google Scholar 

  • Estrada A, Coates-Estrada R, Meritt D (1993) Bat species richness and abundance in tropical rain forest fragments and in agricultural habitats at Los Tuxtlas, Mexico. Ecography 16(4):309–318

    Article  Google Scholar 

  • Eycott AE, Stewart GB, Buyung-Ali LM, Bowler DE, Watts K, Pullin AS (2012) A meta-analysis on the impact of different matrix structures on species movement rates. Landsc Ecol 27(9):1263–1278

    Article  Google Scholar 

  • Farneda FZ, Rocha R, López-Baucells A, Groenenberg M, Silva I et al (2015) Trait-related responses to habitat fragmentation in Amazonian bats. J Appl Ecol. doi:10.1111/1365-2664.12490

    Google Scholar 

  • Fitzherbert EB, Struebig MJ, Morel A, Danielsen F, Brühl CA, Donald PF, Phalan B (2008) How will oil palm expansion affect biodiversity? Trends Ecol Evol 23:538–545

    Article  PubMed  Google Scholar 

  • Foster WA, Snaddon JL, Turner EC, Fayle TM, Cockerill TD et al (2011) Establishing the evidence base for maintaining biodiversity and ecosystem function in the oil palm landscapes of South East Asia. Phil Trans R Soc B: Biol Sci 366(1582):3277–3291

    Article  Google Scholar 

  • Fukuda D, Tisen OB, Momose K, Sakai S (2009) Bat diversity in the vegetation mosaic around a lowland dipterocarp forest of Borneo. Raffles Bull Zool 57(1):213–221

    Google Scholar 

  • Galindo-González J, Sosa VJ (2003) Frugivorous bats in isolated trees and riparian vegetation associated with human-made pastures in a fragmented tropical landscape. Southwest Nat 48(4):579–589

    Article  Google Scholar 

  • Gilroy JJ, Prescott GW, Cardenas JS, Castañeda PGDP, Sánchez A, Rojas-Murcia LE et al (2014) Minimizing the biodiversity impact of Neotropical oil palm development. Glob Change Biol 21(4):1531–1540

    Article  Google Scholar 

  • Gutiérrez-Vélez VH, DeFries R (2013) Annual multi-resolution detection of land cover conversion to oil palm in the Peruvian Amazon. Remote Sens Environ 129:154–167

    Article  Google Scholar 

  • Gutiérrez-Vélez VH, DeFries R, Pinedo-Vásquez M, Uriarte M, Padoch C et al (2011) High-yield oil palm expansion spares land at the expense of forests in the Peruvian Amazon. Environ Res Lett 6(4):044029

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9

    Google Scholar 

  • Harvey CA, Villalobos JAG (2007) Agroforestry systems conserve species-rich but modified assemblages of tropical birds and bats. Biodivers Conserv 16(8):2257–2292

    Article  Google Scholar 

  • Harvey CA, Villanueva C, Villacís J, Chacón M, Muñoz D et al (2005) Contribution of live fences to the ecological integrity of agricultural landscapes. Agric Ecosyst Environ 111(1):200–230

    Article  Google Scholar 

  • Heer K, Helbig-Bonitz M, Fernandes RG, Mello MA, Kalko EKV (2015) Effects of land use on bat diversity in a complex plantation-forest landscape in northeastern Brazil. J Mammal. doi:10.1093/jmammal/gyv068

    Google Scholar 

  • Henry M, Pons J, Cosson JF (2007) Foraging behaviour of a frugivorous bat helps bridge landscape connectivity and ecological processes in a fragmented rainforest. J Anim Ecol 76(4):801–813

    Article  PubMed  Google Scholar 

  • Höbinger T, Schindler S, Seaman BS, Wrbka T, Weissenhofer A (2012) Impact of oil palm plantations on the structure of the agroforestry mosaic of La Gamba, southern Costa Rica: potential implications for biodiversity. Agrofor Syst 85(3):367–381

    Article  Google Scholar 

  • Hoofer SR, Solari S, Larsen PA, Bradley RD, Baker RJ (2008) Phylogenetics of the fruit-eating bats (Phyllostomidae: Artibeina) inferred from mitochondrial DNA sequences. Occas Papers Mus, Texas Tech Univ 277:1–15

    Google Scholar 

  • Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Evol Syst 13:201–228

    Article  Google Scholar 

  • Hsieh TC, Ma KH, Chao A (2013) iNEXT online: interpolation and extrapolation (Version 10). [Software] Available from https://chao.shinyapps.io/iNEXT/

  • Jose S (2012) Agroforestry for conserving and enhancing biodiversity. Agrofor Syst 85(1):1–8

    Article  Google Scholar 

  • Kalko EKV, Friemel D, Handley CO, Schnitzler HU (1999) Roosting and foraging behavior of two Neotropical gleaning bats, Tonatia silvicola and Trachops cirrhosus (Phyllostomidae). Biotropica 31(2):344–353

    Article  Google Scholar 

  • Kunz TH, Braun de Torrez E, Bauer D, Lobova T, Fleming TH (2011) Ecosystem services provided by bats. Ann NY Acad Sci 1223(1):1–38

    Article  PubMed  Google Scholar 

  • Laube I, Breitbach N, Böhning-Gaese K (2008) Avian diversity in a Kenyan agroecosystem: effects of habitat structure and proximity to forest. J Ornithol 149(2):181–191

    Article  Google Scholar 

  • Laurance WF, Useche DC, Rendeiro J, Kalka M, Bradshaw CJ et al (2012) Averting biodiversity collapse in tropical forest protected areas. Nature 489(7415):290–294

    Article  CAS  PubMed  Google Scholar 

  • Lees AC, Moura NG, de Almeida AS, Vieira ICG (2015) Poor prospects for Avian biodiversity in Amazonian oil palm. PLoS One 10(5):e0122432

    Article  PubMed Central  PubMed  Google Scholar 

  • Livingston G, Jha S, Vega A, Gilbert L (2013) Conservation value and permeability of neotropical oil palm landscapes for orchid bees. PLoS One 8(10):e78523

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lucey JM, Tawatao N, Senior MJ, Chey VK, Benedick S et al (2014) Tropical forest fragments contribute to species richness in adjacent oil palm plantations. Biol Conserv 169:268–276

    Article  Google Scholar 

  • Maas B, Karp DS, Bumrungsri S, Darras K, Gonthier D et al (2015) Bird and bat predation services in tropical forests and agroforestry landscapes. Biol Rev. doi:10.1111/brv12211

    PubMed  Google Scholar 

  • Medellín RA, Equihua M, Amin MA (2000) Bat diversity and abundance as indicators of disturbance in Neotropical rainforests. Conserv Biol 14:1666–1675

    Article  Google Scholar 

  • Melo FP, Rodriguez-Herrera B, Chazdon RL, Medellín RA, Ceballos GG (2009) Small tent-roosting bats promote dispersal of large-seeded plants in a Neotropical forest. Biotropica 41(6):737–743

    Article  Google Scholar 

  • Meyer CF, Kalko EKV (2008) Assemblage-level responses of phyllostomid bats to tropical forest fragmentation: land-bridge islands as a model system. J Biogeogr 35(9):1711–1726

    Article  Google Scholar 

  • Meyer CF, Fründ J, Lizano WP, Kalko EKV (2008) Ecological correlates of vulnerability to fragmentation in Neotropical bats. J Appl Ecol 45(1):381–391

    Article  Google Scholar 

  • Meyer CF, Kalko EKV, Kerth G (2009) Small-scale fragmentation effects on local genetic diversity in two Phyllostomid bats with different dispersal abilities in Panama. Biotropica 41(1):95–102

    Article  Google Scholar 

  • Nájera A, Simonetti JA (2010) Can oil palm plantations become bird friendly? Agrofor Syst 80(2):203–209

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR et al (2015) R Package ‘vegan’. Community ecology package, Version 2.2-1, http://www.cran.r-project.org/package=vegan

  • Pike N (2011) Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol Evol 2(3):278–282

    Article  Google Scholar 

  • Pinto N, Keitt TH (2008) Scale-dependent responses to forest cover displayed by frugivore bats. Oikos 117(11):1725–1731

    Article  Google Scholar 

  • Presley SJ, Willig MR, Castro-Arellano I, Weaver SC (2009) Effects of habitat conversion on temporal activity patterns of phyllostomid bats in lowland Amazonian rain forest. J Mammal 90(1):210–221

    Article  Google Scholar 

  • Quesada M, Stoner KE, Lobo JA, Herrerías-Diego Y, Palacios-Guevara C et al (2004) Effects of forest fragmentation on pollinator activity and consequences for plant reproductive success and mating patterns in bat-pollinated Bombacaceous trees. Biotropica 36(2):131–138

    Article  Google Scholar 

  • Reid FA (2009) A field guide to the mammals of central America & Southeast Mexico, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Rex K, Kelm DH, Wiesner K, Kunz TH, Voigt CC (2008) Species richness and structure of three Neotropical bat assemblages. Biol J Linnean Soc 94(3):617–629

    Article  Google Scholar 

  • Rex K, Michener R, Kunz TH, Voigt CC (2011) Vertical stratification of Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae) revealed by stable carbon isotopes. J Trop Ecol 27(3):211–222

    Article  Google Scholar 

  • Ripperger SP, Tschapka M, Kalko EKV, Rodriguez-Herrera B, Mayer F (2013) Life in a mosaic landscape: anthropogenic habitat fragmentation affects genetic population structure in a frugivorous bat species. Conserv Genet 14(5):925–934

    Article  Google Scholar 

  • Ripperger SP, Kalko EKV, Rodríguez-Herrera B, Mayer F, Tschapka M (2015) Frugivorous bats maintain functional habitat connectivity in agricultural landscapes but rely strongly on natural forest fragments. PLoS One 10(4):e0120535

    Article  PubMed Central  PubMed  Google Scholar 

  • Savilaakso S, Garcia C, Garcia-Ulloa J, Ghazoul J, Groom M et al (2014) Systematic review of effects on biodiversity from oil palm production. Environ Evid 3(1):1–21

    Article  Google Scholar 

  • Scales BR, Marsden SJ (2008) Biodiversity in small-scale tropical agroforests: a review of species richness and abundance shifts and the factors influencing them. Environ Conserv 35(02):160–172

    Article  Google Scholar 

  • Schulze MD, Seavy NE, Whitacre DF (2000) A comparison of the phyllostomid bat assemblages in undisturbed Neotropical forest and in forest fragments of a slash-and-burn farming mosaic in Petén, Guatemala. Biotropica 32(1):174–184

    Google Scholar 

  • Stewart AM, Edmisten KL, Wells R, Collins GD (2007) Measuring canopy coverage with digital imaging. Commun Soil Sci Plant Anal 38(7–8):895–902

    Article  CAS  Google Scholar 

  • Stickler C, Coe M, Nepstad D, Fiske G & Lefebvre P (2007) Readiness for REDD? A preliminary assessment of global forested land suitability for agriculture. Woods Hole Massachusetts: Woods Hole Research Center. http://www.whrc.org/resources/publications/pdf/WHRC_REDD_crop_suitability.pdf Accessed July 02 2015

  • Timm RM, LaVal RK (1998) A field key to the bats of Costa Rica. Center of Latin American studies. Univ Kansas Occ Pub Ser 22:1–30

    Google Scholar 

  • Trevelin LC, Silveira M, Port-Carvalho M, Homem DH, Cruz-Neto AP (2013) Use of space by frugivorous bats (Chiroptera: Phyllostomidae) in a restored Atlantic forest fragment in Brazil. Forest Ecol Manag 291:136–143

    Article  Google Scholar 

  • Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity-ecosystem service management. Ecol Lett 8(8):857–874

    Article  Google Scholar 

  • Weissenhofer A, Huber W, Mayer V, Pamperl S, Weber A & Aubrecht G (2008) Natural and Cultural History of the Golfo Dulce Region, Costa Rica. Stapfia 88, Biologiezentrum des Oberösterreichischen Landesmuseums Linz

  • Williams-Guillén K, Perfecto I (2010) Effects of agricultural intensification on the assemblage of Leaf-Nosed bats (Phyllostomidae) in a coffee landscape in Chiapas, Mexico. Biotropica 42(5):605–613

    Article  Google Scholar 

  • Yue S, Brodie JF, Zipkin EF, Bernard H (2015) Oil palm plantations fail to support mammal diversity. Ecol Appl doi: http://dx.doi.org/10.1890/14-1928.1

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Acknowledgments

Our thanks go to the plantation owners who kindly provided permission to work on their land, the La Gamba field station staff for administrative and logistic support and Ralph Hertlein for assistance in the field. Thanks to Konrad Fiedler and Marc-Oliver Adams for feedback and statistical advice, as well as three anonymous reviewers for providing helpful comments on an earlier version of the manuscript.

Funding

AF received partial funding by the University of Vienna (KWA and research scholarship) and the Austrian Federal Ministry of Science, Research and Economy.

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Authors and Affiliations

  1. Department of Botany & Biodiversity Research, University of Vienna, Rennweg 14, 1030, Vienna, Austria

    Anita Freudmann, Philipp Mollik & Christian H. Schulze

  2. Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany

    Marco Tschapka

  3. Smithsonian Tropical Research Institute, Balboa, Panama

    Marco Tschapka

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  1. Anita Freudmann
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  2. Philipp Mollik
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  3. Marco Tschapka
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  4. Christian H. Schulze
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Correspondence to Anita Freudmann.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Communicated by Kirsty Park.

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Freudmann, A., Mollik, P., Tschapka, M. et al. Impacts of oil palm agriculture on phyllostomid bat assemblages. Biodivers Conserv 24, 3583–3599 (2015). https://doi.org/10.1007/s10531-015-1021-6

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