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Small mammal responses to Amazonian forest islands are modulated by their forest dependence

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Abstract

Hydroelectric dams have induced widespread loss, fragmentation and degradation of terrestrial habitats in lowland tropical forests. Yet their ecological impacts have been widely neglected, particularly in developing countries, which are currently earmarked for exponential hydropower development. Here we assess small mammal assemblage responses to Amazonian forest habitat insularization induced by the 28-year-old Balbina Hydroelectric Dam. We sampled small mammals on 25 forest islands (0.83–1466 ha) and four continuous forest sites in the mainland to assess the overall community structure and species-specific responses to forest insularization. We classified all species according to their degree of forest-dependency using a multi-scale approach, considering landscape, patch and local habitat characteristics. Based on 65,520 trap-nights, we recorded 884 individuals of at least 22 small mammal species. Species richness was best predicted by island area and isolation, with small islands (< 15 ha) harbouring an impoverished nested subset of species (mean ± SD: 2.6 ± 1.3 species), whereas large islands (> 200 ha; 10.8 ± 1.3 species) and continuous forest sites (∞ ha; 12.5 ± 2.5 species) exhibited similarly high species richness. Forest-dependent species showed higher local extinction rates and were often either absent or persisted at low abundances on small islands, where non-forest-dependent species became hyper-abundant. Species capacity to use non-forest habitat matrices appears to dictate small mammal success in small isolated islands. We suggest that ecosystem functioning may be highly disrupted on small islands, which account for 62.7% of all 3546 islands in the Balbina Reservoir.

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References

  • Adler GH, Seamon JO (1996) Distribution of four-eyed opossum, Philander opossum (Marsupialia, Didelphidae) on small islands In Panama. Mammalia 60:91–100

    Article  Google Scholar 

  • Adler GH, Wilson ML, Derosa MJ (1986) Influence of island area and isolation on population characteristics of Peromyscus leucopus. J Mammal 67:406–440

    Article  Google Scholar 

  • Almeida-Neto M, Guimarães P, Guimarães PR, Loyola RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239

    Article  Google Scholar 

  • Arroyo-Rodríguez V, Rös M, Escobar F, Melo FP, Santos BA, Tabarelli M, Chazdon R (2013) Plant β-diversity in fragmented rain forests: testing floristic homogenization and differentiation hypotheses. J Ecol 101:1449–1458

    Article  Google Scholar 

  • August PV (1983) The role of habitat complexity and heterogeneity in structuring tropical mammal communities. Ecology 64:1495–1507

    Article  Google Scholar 

  • Aurélio-Silva M, Anciães M, Henriques LMP, Benchimol M, Peres CA (2016) Patterns of local extinction in an Amazonian archipelagic avifauna following 25 years of insularization. Biol Cons 199:101–109

    Article  Google Scholar 

  • Bartoń K (2016) MuMIn: multi-model inference. R package version 1(15):6

    Google Scholar 

  • Benchimol M, Peres CA (2015a) Widespread forest vertebrate extinctions induced by a mega hydroelectric dam in lowland Amazonia. PLoS One 10:e0129818

    Article  PubMed  PubMed Central  Google Scholar 

  • Benchimol M, Peres CA (2015b) Predicting local extinctions of Amazonian vertebrates in forest islands created by a mega dam. Biol Cons 187:61–72

    Article  Google Scholar 

  • Benchimol M, Peres CA (2015c) 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 

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

    Google Scholar 

  • Carvalho FMV, Fernandez FAS, Nessimian JL (2005) Food habits of sympatric opossums coexisting in small Atlantic Forest fragments in Brazil. Mamm Biol 70:366–375

    Article  Google Scholar 

  • Castello L, McGrath DG, Hess LL, Coe MT, Lefebvre PA, Petry P, Macedo MN, Renó VF, Arantes CC (2013) The vulnerability of Amazon fresh water ecosystems. Conserv Lett 6:217–229

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67

    Article  Google Scholar 

  • Charles-Dominique P, Atramentowicz M, Charles-Dominique M, Gerard H, Hladik A, Hladik CM, Prévost MF (1981) Les mamiferes arboricoles nocturnes d’une foret guyanaise: interrelations plantes-animaux. Rev Ecol-Terre Vie 35:341–435

    Google Scholar 

  • Cosson JF, Ringuet S, Claessens O, De Massary JC, Dalecky A, Villiers JF, Grajon L, Pons JM (1999) Ecological changes in recent land-bridge islands in French Guiana, with emphasis on vertebrate communities. Biol Cons 91:213–222

    Article  Google Scholar 

  • Delciellos AC, Vieira MV, Grelle CE, Cobra P, Cerqueira R (2016) Habitat quality versus spatial variables as determinants of small mammal assemblages in Atlantic Forest fragments. J Mammal 97:253–265

    Article  Google Scholar 

  • Devictor V, Julliard R, Jiguet F (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117:507–514

    Article  Google Scholar 

  • Diamond J (2001) Damned experiments! Science 294:1847–1848

    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 36:27–46

    Article  Google Scholar 

  • ECOA—Ecologia em Ação (2016). International Rivers and Fundacion Proteger, Dams in Amazonia. http://www.dams-info.org/en. Accessed 05 June 2017

  • ESRI (2012) ArcMap 10.1, Environmental Systems Research Institute, Inc. Redlands

  • Estavillo C, Pardini R, da Rocha PLB (2013) Forest loss and the biodiversity threshold: an evaluation considering species habitat requirements and the use of matrix habitats. PLoS One 8:e82369

    Article  PubMed  PubMed Central  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 (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol 34:487–515

    Article  Google Scholar 

  • Fearnside PM (2001) Environmental impacts of Brazil’s Tucuruí Dam: unlearned lessons for hydroelectric development in Amazonia. Environ Manag 27:377–396

    Article  CAS  Google Scholar 

  • Fearnside PM, Pueyo S (2012) Greenhouse-gas emissions from tropical dams. Nat Clim Change 2:382–384

    Article  CAS  Google Scholar 

  • Fonseca GA, Robinson JG (1990) Forest size and structure: competitive and predatory effects on small mammal communities. Biol Cons 53:265–294

    Article  Google Scholar 

  • FUNCATE/INPE/ANEEL (2000) Mapeamento por satélite das áreas inundadas por reservatórios de hidrelétricas brasileiras. Unpublished Report

  • Galetti M, Guevara R, Galbiati LA, Neves CL, Rodarte RR, Mendes CP (2015) Seed predation by rodents and implications for plant recruitment in defaunated Atlantic forests. Biotropica 47:521–525

    Article  Google Scholar 

  • Gibson L, Lynam AJ, Bradshaw CJ, He F, Bickford DP, Woodruff DS, Bumrungsri S, Laurance WF (2013) Near-complete extinction of native small mammal fauna 25 years after forest fragmentation. Science 341:1508–1510

    Article  CAS  PubMed  Google Scholar 

  • Glanz WE (1990) Neotropical mammal densities: how unusual is the community on Barro Colorado Island, Panama. In: Gentry AH (ed) Four neotropical rainforests. Yale University Press, New Haven, pp 287–313

    Google Scholar 

  • Goodman SM, Rakotondravony D (2000) The effects of forest fragmentation and isolation on insectivorous small mammals (Lipotyphla) on the Central High Plateau of Madagascar. J Zool 250:193–200

    Article  Google Scholar 

  • Granjon L, Ringuet S, Cheylan G (2002) Evolution of small terrestrial mammal species richness on newly formed islands in primary tropical forest of French Guiana: a 6 year study. Rev Ecol-Terre Vie 57:131–144

    Google Scholar 

  • Guilhaumon F, Mouillot D, Gimenez O (2010) mmSAR: an R-package for multimodel species–area relationship inference. Ecography 33:420–424

    Google Scholar 

  • Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251

    Article  Google Scholar 

  • Hutchinson GE (1957) Concluding remarks. Cold Spring Harbor Symp Quant Biol 22:415–427

    Article  Google Scholar 

  • IBAMA (1997) Plano de Manejo Fase I: Reserva Biológica do Uatumã. http://www.icmbio.gov.br. Accessed 05 June 2017

  • Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landscape Ecol 27:929–941

    Article  Google Scholar 

  • Jones KE et al (2009) PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90:2648

    Article  Google Scholar 

  • Jones IL, Bunnefeld N, Jump AS, Peres CA, Dent DH (2016) Extinction debt on reservoir land-bridge islands. Biol Cons 199:75–83

    Article  Google Scholar 

  • Junk WJ, Mello JAS (1990) Impactos ecológicos das represas hidrelétricas na bacia amazônica brasileira. Estudos avançados 4:126–143

    Article  Google Scholar 

  • Lambert TD, Adler GH, Riveros CM, Lopez L, Ascanio R, Terborgh J (2003) Rodents on tropical land bridge islands. J Zool 260:179–187

    Article  Google Scholar 

  • Lambert TD, Malcolm JR, Zimmerman BL (2006) Amazonian small mammal abundances in relation to habitat structure and resource abundance. J Mammal 87:766–776

    Article  Google Scholar 

  • Laurance WF (1994) Rainforest fragmentation and the structure of small mammal communities in tropical Queensland. Biol Cons 69:23–32

    Article  Google Scholar 

  • Lees AC, Peres CA, Fearnside PM, Schneider M, Zuanon JA (2016) Hydropower and the future of Amazonian biodiversity. Biodivers Conserv 25:451–466

    Article  Google Scholar 

  • Lynam AJ, Billick I (1999) Differential responses of small mammals to fragmentation in a Thailand tropical forest. Biol Cons 91:191–200

    Article  Google Scholar 

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

    Google Scholar 

  • Malcolm JR (1991) The small mammals of Amazonian forest fragments: pattern and process. PhD dissertation, Department of Zoology, Gainesville, Florida, USA

  • Mangan SA, Adler GH (2000) Consumption of arbuscular mycorrhizal fungi by terrestrial and arboreal small mammals in a Panamanian cloud forest. J Mammal 81:563–570

    Article  Google Scholar 

  • McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: Spatial Pattern Analysis Program for Categorical and Continuous Maps. http://www.umass.edu/landeco/research/fragstats/fragstats.html. Accessed 05 June 2017

  • Muggeo VRM (2017) Segmented: Regression Models with Break-Points/Change-Points Estimation. R package version 0.5-2.1

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH (2007) Vegan: the community ecology package. R package version 2.4-2

  • Pardini R, de Souza SM, Braga-Neto R, Metzger JP (2005) The role of forest structure, fragment size and corridors in maintaining small mammal abundance and diversity in an Atlantic forest landscape. Biol Cons 124:253–266

    Article  Google Scholar 

  • Pardini R, Faria D, Accacio GM, Laps RR, Mariano-Neto E, Paciencia ML, Dixo M, Baumgarten J (2009) The challenge of maintaining Atlantic forest biodiversity: a multi-taxa conservation assessment of specialist and generalist species in an agro-forestry mosaic in southern Bahia. Biol Cons 142:1178–1190

    Article  Google Scholar 

  • Pardini R, de Arruda Bueno A, Gardner TA, Prado PI, Metzger JP (2010) Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. PLoS One 5:e13666

    Article  PubMed  PubMed Central  Google Scholar 

  • Passamani M, Fernandez FAS (2011) Abundance and richness of small mammals in fragmented Atlantic Forest of Southeastern Brazil. J Nat Hist 45:553–565

    Article  Google Scholar 

  • Patton JL, Da Silva MNF, Malcolm JR (2000) Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bull Am Mus Nat Hist 244:1–306

    Article  Google Scholar 

  • Patton JL, Pardiñas UFJ, D’Elía G (2007) Mammals of South America, vol 2, 1st edn. The University of Chicago Press, Chicago

    Google Scholar 

  • Prevedello JA, Vieira MV (2010) Does the type of matrix matter? A quantitative review of the evidence. Biodivers Conserv 19:1205–1223

    Article  Google Scholar 

  • R Development Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org/. Accessed 05 June 2017

  • Rhodes JR, McAlpine CA, Zuur AF, Smith GM, Ieno EN (2009) GLMM applied on the spatial distribution of koalas in a fragmented landscape. In: Zuur AF, Leno EN, Walker NJ, Saveliev AA, Smith GM (eds) Mixed effects models and extensions in ecology with R. Springer, New York, pp 469–492

    Chapter  Google Scholar 

  • Santos-Filho M, Peres CA, Da Silva DJ, Sanaiotti TM (2012) Habitat patch and matrix effects on small-mammal persistence in Amazonian forest fragments. Biodivers Conserv 21:1127–1147

    Article  Google Scholar 

  • Santos-Filho M, Bernardo CS, Silva DJD, Ignácio ARA, Canale GR (2016) The importance of considering both taxonomic and habitat guild approaches in small mammal research. Austral Ecol 41:854–863

    Article  Google Scholar 

  • Sikes RS (2016) 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mammal 97:663–688

    Article  PubMed  PubMed Central  Google Scholar 

  • Strona G, Galli P, Seveso D, Montano S, Fattorini S (2014) Nestedness for Dummies (NeD): a user-friendly web interface for exploratory nestedness analysis. J Stat Softw 59:1–9

    Article  Google Scholar 

  • Terborgh J, Lopez L, Tello S (1997) Bird communities in transition: the Lago Guri islands. Ecology 78:1494–1501

    Article  Google Scholar 

  • Terborgh J, Lopez L, Nuñez P, Rao M, Shahabuddin G, Orihuela G, Riveros M, Ascanio R, Adler GH, Lambert TD, Balbas L (2001) Ecological meltdown in predator-free forest fragments. Science 294:1923–1926

    Article  CAS  PubMed  Google Scholar 

  • Toms JD, Lesperance ML (2003) Piecewise regression: a tool for identifying ecological thresholds. Ecology 84:2034–2041

    Article  Google Scholar 

  • Umetsu F, Pardini R (2007) Small mammals in a mosaic of forest remnants and anthropogenic habitats—evaluating matrix quality in an Atlantic forest landscape. Landscape Ecol 22:517–530

    Article  Google Scholar 

  • Vieira MF, Carvalho-Okano RM, Sazima M (1991) The common opossum (Didelphis marsupialis), as a pollinator of Mabea fistulifera (Euphorbiaceae). Ciência e Cultura 43:390–393

    Google Scholar 

  • Vieira MV, Olifiers N, Delciellos AC, Antunes VZ, Bernardo LR, Grelle CE, Cerqueira R (2009) Land use vs. fragment size and isolation as determinants of small mammal composition and richness in Atlantic Forest remnants. Biol Cons 142:1191–1200

    Article  Google Scholar 

  • Wang Y, Bao Y, Yu M, Xu G, Ding P (2010a) Nestedness for different reasons: the distributions of birds, lizards and small mammals on islands of an inundated lake. Divers Distrib 16:862–873

    Article  Google Scholar 

  • Wang J, Huang J, Wu J, Han X, Lin G (2010b) Ecological consequences of the Three Gorges Dam: insularization affects foraging behavior and dynamics of rodent populations. Front Ecol Environ 8:13–19

    Article  Google Scholar 

  • Watling JI, Donnelly MA (2006) Fragments as islands: a synthesis of faunal responses to habitat patchiness. Conserv Biol 20:1016–1025

    Article  PubMed  Google Scholar 

  • Wright SJ, Gompper ME, DeLeon B (1994) Are large predators keystone species in neotropical forests? The evidence from Barro Colorado Island. Oikos 71:279–294

    Article  Google Scholar 

  • Wright DH, Patterson BD, Mikkelson GM, Cutler A, Atmar W (1998) A comparative analysis of nested subset patterns of species composition. Oecologia 113:1–20

    Article  Google Scholar 

  • Wu J, Huang J, Han X, Gao X, He F, Jiang M, Primack RB, Shen Z (2004) The three gorges dam: an ecological perspective. Front Ecol Environ 2:241–248

    Article  Google Scholar 

  • Zarfl C, Lumsdon AE, Berlekamp J, Tydecks L, Tockner K (2015) A global boom in hydropower dam construction. Aquat Sci 77:161–170

    Article  Google Scholar 

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Acknowledgements

We thank all 15 volunteers/field assistants who assisted in the field; the Reserva Biológica do Uatumã and its staff for logistical support; M.N.F. da Silva for help with species identification and D. Storck-Tonon for assistance with landscape metrics. This study was funded by the Amazon Region Protected Areas Program (ARPA), Amazonas Distribuidora de Energia S.A., and Associação Comunidade Waimiri Atroari; Rufford Foundation (grant number 13,675-1); Idea Wild; and a NERC grant (NE/J01401X/1) awarded to CAP. AFP and MB were funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) scholarship, and MVV was funded by Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

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AFP, MVV and CAP conceived and designed the experiments. AFP performed the experiments, and MB provided additional data. AFP analysed the data and wrote the manuscript under the supervision and advice of MVV and CAP; MB also provided editorial advice.

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Correspondence to Ana Filipa Palmeirim.

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Communicated by Christopher Whelan.

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Palmeirim, A.F., Benchimol, M., Vieira, M.V. et al. Small mammal responses to Amazonian forest islands are modulated by their forest dependence. Oecologia 187, 191–204 (2018). https://doi.org/10.1007/s00442-018-4114-6

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