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Consequences of a large-scale fragmentation experiment for Neotropical bats: disentangling the relative importance of local and landscape-scale effects

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Abstract

Context

Habitat loss, fragmentation and degradation are widespread drivers of biodiversity decline. Understanding how habitat quality interacts with landscape context, and how they jointly affect species in human-modified landscapes, is of great importance for informing conservation and management.

Objectives

We used a whole-ecosystem manipulation experiment in the Brazilian Amazon to investigate the relative roles of local and landscape attributes in affecting bat assemblages at an interior-edge-matrix disturbance gradient.

Methods

We surveyed bats in 39 sites, comprising continuous forest (CF), fragments, forest edges and intervening secondary regrowth. For each site, we assessed vegetation structure (local-scale variable) and, for five focal scales, quantified habitat amount and four landscape configuration metrics.

Results

Smaller fragments, edges and regrowth sites had fewer species and higher levels of dominance than CF. Regardless of the landscape scale analysed, species richness and evenness were mostly related to the amount of forest cover. Vegetation structure and configurational metrics were important predictors of abundance, whereby the magnitude and direction of response to configurational metrics were scale-dependent. Responses were ensemble-specific with local-scale vegetation structure being more important for frugivorous than for gleaning animalivorous bats.

Conclusions

Our study indicates that scale-sensitive measures of landscape structure are needed for a more comprehensive understanding of the effects of fragmentation on tropical biota. Although forest fragments and regrowth habitats can be of conservation significance for tropical bats our results further emphasize that primary forest is of irreplaceable value, underlining that their conservation can only be achieved by the preservation of large expanses of pristine habitat.

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References

  • Antongiovanni M, Metzger JP (2005) Influence of matrix habitats on the occurrence of insectivorous bird species in Amazonian forest fragments. Biol Conserv 122:441–451

    Article  Google Scholar 

  • Arroyo-Rodríguez V, Rojas C, Saldaña-Vázquez RA, Stoner KE (2016) Landscape composition is more important than landscape configuration for phyllostomid bat assemblages in a fragmented biodiversity hotspot. Biol Conserv 198:84–92

    Article  Google Scholar 

  • Avila-Cabadilla LD, Sanchez-Azofeifa GA, Stoner KE, Alvarez-Anorve MY, Quesada M, Portillo-Quintero CA (2012) Local and landscape factors determining occurrence of phyllostomid bats in tropical secondary forests. PLoS ONE 7:e35228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avila-Cabadilla LD, Stoner KE, Henry M, Añorve MYA (2009) Composition, structure and diversity of phyllostomid bat assemblages in different successional stages of a tropical dry forest. For Ecol Manag 258:986–996

    Article  Google Scholar 

  • Avila-Cabadilla LD, Stoner KE, Nassar JM, Espírito-Santo MM, Alvarez-Añorve MY, Aranguren CI, Henry M, González-Carcacía JA, Falcão LAD, Sanchez-Azofeifa GA (2014) Phyllostomid bat occurrence in successional stages of Neotropical dry forests. PLoS ONE 9:e84572

    Article  PubMed  PubMed Central  Google Scholar 

  • Banks-Leite C, Ewers RM, Metzger JP (2010) Edge effects as the principal cause of area effects on birds in fragmented secondary forest. Oikos 119:918–926

    Article  Google Scholar 

  • Barlow J, Gardner TA, Araujo IS, Ávila-Pires TC, Bonaldo AB, Costa JE, Esposito MC, Ferreira LV, Hawes J, Hernandez MIM, Hoogmoed MS, Leite RN, Lo-Man-Hung NF, Malcolm JR, Martins MB, Mestre LAM, Miranda-Santos R, Nunes-Gutjahr AL, Overal WL, Parry L, Peters SL, Ribeiro-Junior MA, da Silva MNF, da Silva Motta C, Peres CA (2007) Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Proc Natl Acad Sci USA 104:18555–18560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates DM (2010) lme4: mixed-effects modeling with R. Springer, New York. http://lme4.r-forge.r-project.org/book/

  • Benchimol M, Peres CA (2015) Edge-mediated compositional and functional decay of tree assemblages in Amazonian forest islands after 26 years of isolation. J Ecol 103:408–420

    Article  Google Scholar 

  • Benchimol M, Venticinque EM (2014) Responses of primates to landscape change in Amazonian land-bridge islands—a multi-scale analysis. Biotropica 46:470–478

    Article  Google Scholar 

  • Bernard E (2001) Vertical stratification of bat communities in primary forests of Central Amazon, Brazil. J Trop Ecol 17:115–126

    Article  Google Scholar 

  • Bernard E (2002) Diet, activity and reproduction of bat species (Mammalia, Chiroptera) in Central Amazonia, Brazil. Rev Bras Zool 19:173–188

    Article  Google Scholar 

  • Bobrowiec P, Gribel R (2010) Effects of different secondary vegetation types on bat community composition in Central Amazonia, Brazil. Anim Conserv 13:204–216

    Article  Google Scholar 

  • Bolívar-Cimé B, Laborde J, MacSwiney GMC, Muñoz-Robles C, Tun-Garrido J (2013) Response of phytophagous bats to patch quality and landscape attributes in fragmented tropical semi-deciduous forest. Acta Chirop 15:399–409

    Article  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Boyle SA, Smith AT (2010) Can landscape and species characteristics predict primate presence in forest fragments in the Brazilian Amazon? Biol Conserv 143:1134–1143

    Article  Google Scholar 

  • Bradshaw CJA, Sodhi NS, Brook BW (2008) Tropical turmoil: a biodiversity tragedy in progress. Front Ecol Environ 7:79–87

    Article  Google Scholar 

  • 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 169:372–383

    Article  Google Scholar 

  • Broadbent EN, Asner GP, Keller M, Knapp DE, Oliveira PJC, Silva JN (2008) Forest fragmentation and edge effects from deforestation and selective logging in the Brazilian Amazon. Biol Conserv 141:1745–1757

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Carreiras JMB, Pereira JMC, Campagnolo ML, Shimabukuro YE (2006) Assessing the extent of agriculture/pasture and secondary succession forest in the Brazilian Legal Amazon using SPOT VEGETATION data. Remote Sens Environ 101:283–298

    Article  Google Scholar 

  • Chambers CL, Cushman SA, Medina-Fitoria A, Martínez-Fonseca J, Chávez-Velásquez M (2016) Influences of scale on bat habitat relationships in a forested landscape in Nicaragua. Landscape Ecol 31(6):1299–1318

    Article  Google Scholar 

  • Charbonnier Y, Gaüzère P, van Halder I, Nezan J, Barnagaud JY, Jactel H, Barbaro L (2016) Deciduous trees increase bat diversity at stand and landscape scales in mosaic pine plantations. Landscape Ecol 31:291–300

    Article  Google Scholar 

  • Chazdon RL (2014) Second growth: The promise of tropical forest regeneration in an age of deforestation. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Cisneros LM, Fagan ME, Willig MR (2015) Effects of human-modified landscapes on taxonomic, functional and phylogenetic dimensions of bat biodiversity. Divers Distrib 5:523–533

    Article  Google Scholar 

  • Cosson J-F, Pons J-M, Masson D (1999) Effects of forest fragmentation on frugivorous and nectarivorous bats in French Guiana. J Trop Ecol 15:515–534

    Article  Google Scholar 

  • Delaval M, Charles-Dominique P (2006) Edge effects on frugivorous and nectarivorous bat communities in a neotropical primary forest in French Guiana. Rev Ecol Terre Vie 61:343–352

    Google Scholar 

  • Didham RK, Lawton JH (1999) Edge structure determines the magnitude of changes in microclimate and vegetation structure in tropical forest fragments. Biotropica 31:17–30

    Google Scholar 

  • Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJ, Collen B (2014) Defaunation in the Anthropocene. Science 345:401–406

    Article  CAS  PubMed  Google Scholar 

  • Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:027–046

    Article  Google Scholar 

  • Erickson JL, West SD (2003) Associations of bats with local structure and landscape features of forested stands in western Oregon and Washington. Biol Conserv 109:95–102

    Article  Google Scholar 

  • Estrada-Villegas S, Meyer CF, Kalko EK (2010) Effects of tropical forest fragmentation on aerial insectivorous bats in a land-bridge island system. Biol Conserv 143:597–608

    Article  Google Scholar 

  • Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142

    Article  PubMed  Google Scholar 

  • Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40:1649–1663

    Article  Google Scholar 

  • Faria D (2006) Phyllostomid bats of a fragmented landscape in the north-eastern Atlantic forest, Brazil. J Trop Ecol 22:531–542

    Article  Google Scholar 

  • Faria D, Mariano-Neto E, Martini AMZ, Ortiz JV, Montingelli R, Rosso S, Paciencia MLB, Baumgarten J (2009) Forest structure in a mosaic of rainforest sites: the effect of fragmentation and recovery after clear cut. For Ecol Manag 257:2226–2234

    Article  Google Scholar 

  • Farneda FZ, Rocha R, López-Baucells A, Groenenberg M, Silva I, Palmeirim JM, Bobrowiec PED, Meyer CFJ (2015) Trait-related responses to habitat fragmentation in Amazonian bats. J Appl Ecol 52:1381–1391

    Article  Google Scholar 

  • Ferraz G, Nichols JD, Hines JE, Stouffer PC, Bierregaard RO, Lovejoy TE (2007) A large-scale deforestation experiment: effects of patch area and isolation on amazon birds. Science 315:238–241

    Article  CAS  PubMed  Google Scholar 

  • Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280

    Article  Google Scholar 

  • Galitsky C, Lawler JJ (2015) Relative influence of local and landscape factors on bird communities vary by species and functional group. Landscape Ecol 30:287–299

    Article  Google Scholar 

  • García-Morales R, Badano EI, Moreno CE (2013) Response of Neotropical bat assemblages to human land use. Conserv Biol 27:1096–1106

    Article  PubMed  Google Scholar 

  • Gardner A (2007) Mammals of South America, vol. 1: Marsupials, xenarthrans, shrews, and bats. The University of Chicago Press, Chicago

  • Gascon C, Lovejoy TE, Bierregaard RO Jr, Malcolm JR, Stouffer PC, Vasconcelos HL, Laurance WF, Zimmerman B, Tocher M, Borges S (1999) Matrix habitat and species richness in tropical forest remnants. Biol Conserv 91:223–229

    Article  Google Scholar 

  • Giannini NP, Kalko EKV (2004) Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 105:209–220

    Article  Google Scholar 

  • Gibson L, Lee TM, Koh LP, Brook BW, Gardner TA, Barlow J, Peres CA, Bradshaw CJ, Laurance WF, Lovejoy TE (2011) Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478:378–381

    Article  CAS  PubMed  Google Scholar 

  • Gorresen PM, Willig MR (2004) Landscape responses of bats to habitat fragmentation in Atlantic forest of Paraguay. J Mammal 85:688–697

    Article  Google Scholar 

  • Gotelli NJ, Entsminger GL (2004) EcoSim: null models software for ecology, version 7. Acquired Intelligence Inc. & Kesey-Bear, Jericho. http://garyentsminger.com/ecosim/index.htm

  • Henry M, Cosson JF, Pons JM (2010) Modelling multi-scale spatial variation in species richness from abundance data in a complex neotropical bat assemblage. Ecol Model 221:2018–2027

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P, Heiberger RM, Schuetzenmeister A, Scheibe S (2014) multcomp: simultaneous inference in general parametric models. R package version 1.3-2. http://cran.r-project.org/web/packages/multcomp/

  • Jeppsson T, Lindhe A, Gärdenfors U, Forslund P (2010) The use of historical collections to estimate population trends: a case study using Swedish longhorn beetles (Coleoptera: Cerambycidae). Biol Conserv 143:1940–1950

    Article  Google Scholar 

  • Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA (2009) Carpe noctem: the importance of bats as bioindicators. Endanger Species Res 8:93–115

    Article  Google Scholar 

  • Kalda R, Kalda O, Lõhmus K, Liira J (2015) Multi-scale ecology of woodland bat the role of species pool, landscape complexity and stand structure. Biodivers Conserv 24:337–353

    Article  Google Scholar 

  • Kalko EKV (1998) Organisation and diversity of tropical bat communities through space and time. Zoology 101:281–297

    Google Scholar 

  • Klingbeil BT, Willig MR (2009) Guild-specific responses of bats to landscape composition and configuration in fragmented Amazonian rainforest. J Appl Ecol 46:203–213

    Article  Google Scholar 

  • Klingbeil BT, Willig MR (2010) Seasonal differences in population-, ensemble- and community-level responses of bats to landscape structure in Amazonia. Oikos 119:1654–1664

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Laurance WF, Camargo JL, Luizão RC, Laurance SG, Pimm SL, Bruna EM, Stouffer PC, Williamson GB, Benítez-Malvido J, Vasconcelos HL (2011) The fate of Amazonian forest fragments: a 32-year investigation. Biol Conserv 144:56–67

    Article  Google Scholar 

  • Laurance WF, Lovejoy TE, Vasconcelos HL, Bruna EM, Didham RK, Stouffer PC, Gascon C, Bierregaard RO, Laurance SG, Sampaio E (2002) Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conserv Biol 16:605–618

    Article  Google Scholar 

  • Laurance WF, Nascimento HE, Laurance SG, Andrade AC, Fearnside PM, Ribeiro JE, Capretz RL (2006a) Rain forest fragmentation and the proliferation of successional trees. Ecology 87:469–482

    Article  PubMed  Google Scholar 

  • Laurance WF, Nascimento HE, Laurance SG, Andrade AC, Ribeiro JE, Giraldo JP, Lovejoy TE, Condit R, Chave J, Harms KE (2006b) Rapid decay of tree-community composition in Amazonian forest fragments. Proc Natl Acad Sci USA 103:19010–19014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laurance WF, Sayer J, Cassman KG (2014) Agricultural expansion and its impacts on tropical nature. Trends Ecol Evol 29:107–116

    Article  PubMed  Google Scholar 

  • Lenz BB, Jack KM, Spironello WR (2014) Edge effects in the primate community of the biological dynamics of forest fragments project, Amazonas, Brazil. Am J Phys Anthropol 155:436–446

    Article  PubMed  Google Scholar 

  • Lim BK, Engstrom MD (2010) Species diversity of bats (Mammalia: Chiroptera) in Iwokrama Forest, Guyana, and the Guianan subregion: implications for conservation. Biodivers Conserv 10:613–657

    Article  Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  • Marciente R, Bobrowiec PED, Magnusson WE (2015) Ground-vegetation clutter affects phyllostomid bat assemblage structure in lowland Amazonian forest. PLoS ONE 10:e0129560

    Article  PubMed  PubMed Central  Google Scholar 

  • Marques JT, Ramos Pereira MJ, Marques TA, Santos CD, Santana J, Beja P, Palmeirim JM (2013) Optimizing sampling design to deal with mist-net avoidance in Amazonian birds and bats. PLoS ONE 8:e74505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps. University of Massachusetts, Amherst. http://www.umass.edu/landeco/research/fragstats/fragstats.html

  • McGill BJ (2010) Matters of scale. Science 328:575–576

    Article  CAS  PubMed  Google Scholar 

  • Mendenhall CD, Karp DS, Meyer CF, Hadly EA, Daily GC (2014) Predicting biodiversity change and averting collapse in agricultural landscapes. Nature 509:213–217

    Article  CAS  PubMed  Google Scholar 

  • Mesquita RCG, Ickes K, Ganade G, Williamson GB (2001) Alternative successional pathways in the Amazon Basin. J Ecol 89:528–537

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Meyer CFJ, Struebig M, Willig MR (2016) Responses of tropical bats to habitat fragmentation, logging, and deforestation. In: Voigt CC, Kingston T (eds) Bats in the Anthropocene: conservation of bats in a changing world. Springer, New York, pp 63–103

    Chapter  Google Scholar 

  • Mokross K, Ryder TB, Côrtes MC, Wolfe JD, Stouffer PC (2014) Decay of interspecific avian flock networks along a disturbance gradient in Amazonia. Proc R Soc Lond Ser B Biol Sci 281:20132599

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models. Irwin, Homewood

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: community ecology. R package version 2.2-1. http://cran.r-project.org/web/packages/vegan/

  • Palmeirim JM, Etheridge K (1985) The influence of man-made trails on foraging by tropical frugivorous bats. Biotropica 17:82–83

    Article  Google Scholar 

  • Pereira MJR, Marques JT, Palmeirim JM (2010) Vertical stratification of bat assemblages in flooded and unflooded Amazonian forests. Curr Zool 56:469–478

    Google Scholar 

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

    Article  Google Scholar 

  • Powell LL, Stouffer PC, Johnson EI (2013) Recovery of understory bird movement across the interface of primary and secondary Amazon rainforest. Auk 130:459–468

    Article  Google Scholar 

  • Powell LL, Zurita G, Wolfe JD, Johnson EI, Stouffer PC (2015) Changes in habitat use at rain forest edges through succession: a case study of understory birds in the Brazilian Amazon. Biotropica 47:723–732

    Article  Google Scholar 

  • R Development Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Rocha R, Tarmo V, Cabeza M (2015) Bird assemblages in a Malagasy forest-agricultural frontier: effects of habitat structure and landscape-scale forest cover. Trop Conserv Sci 8:681–710

    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 32:174–184

    Google Scholar 

  • Smart SM, Thompson K, Marrs RH, Le Duc MG, Maskell LC, Firbank LG (2006) Biotic homogenization and changes in species diversity across human-modified ecosystems. Proc R Soc Lond Ser B Biol Sci 273:2659–2665

    Article  Google Scholar 

  • Stouffer PC, Bierregaard RO, Strong C, Lovejoy TE (2006) Long-term landscape change and bird abundance in Amazonian rainforest fragments. Conserv Biol 20:1212–1223

    Article  PubMed  Google Scholar 

  • Stratford JA, Stouffer PC (2013) Microhabitat associations of terrestrial insectivorous birds in Amazonian rainforest and second-growth forests. J Field Ornithol 84:1–12

    Article  Google Scholar 

  • Struebig MJ, Kingston T, Zubaid A, Mohd-Adnan A, Rossiter SJ (2008) Conservation value of forest fragments to Palaeotropical bats. Biol Conserv 141:2112–2126

    Article  Google Scholar 

  • Walsh C, Mac Nally R (2013) Hier.part: variance partition of a multivariate data set. R package version 1.0-4. http://cran.r-project.org/web/packages/hier.part/

  • Williamson GB, Bentos TV, Longworth JB, Mesquita RCG (2014) Convergence and divergence in alternative successional pathways in Central Amazonia. Plant Ecol Divers 7:341

    Article  Google Scholar 

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Acknowledgments

We would like to thank the many volunteers and field assistants that helped during fieldwork, Tobias Jeppsson for providing a modified version of the hier.part function for the hierarchical partitioning analysis, and the BDFFP management team for logistic support. Funding was provided by a Portuguese Foundation for Science and Technology (FCT) project grant (PTDC/BIA-BIC/111184/2009) to C.F.J.M. R.R. was supported by FCT (SFRH/BD/80488/2011), A.L.-B. by (FCT PD/BD/52597/2014) and CNPq (160049/2013-0), P.E.D.B. by CAPES and M.C. by Academy of Finland (grant #257686). Research was conducted under ICMBio permit (26877-2) and is publication 698 in the BDFFP technical series.

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Correspondence to Ricardo Rocha.

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Rocha, R., López-Baucells, A., Farneda, F.Z. et al. Consequences of a large-scale fragmentation experiment for Neotropical bats: disentangling the relative importance of local and landscape-scale effects. Landscape Ecol 32, 31–45 (2017). https://doi.org/10.1007/s10980-016-0425-3

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