, Volume 187, Issue 1, pp 191–204 | Cite as

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

  • Ana Filipa Palmeirim
  • Maíra Benchimol
  • Marcus Vinícius Vieira
  • Carlos A. Peres
Community ecology – original research


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.


Habitat fragmentation Hydroelectric dams Island biogeography Land-bridge islands Tropical forests 



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).

Author contribution statement

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.

Supplementary material

442_2018_4114_MOESM1_ESM.docx (970 kb)
Supplementary material 1 (DOCX 969 kb)


  1. Adler GH, Seamon JO (1996) Distribution of four-eyed opossum, Philander opossum (Marsupialia, Didelphidae) on small islands In Panama. Mammalia 60:91–100CrossRefGoogle Scholar
  2. Adler GH, Wilson ML, Derosa MJ (1986) Influence of island area and isolation on population characteristics of Peromyscus leucopus. J Mammal 67:406–440CrossRefGoogle Scholar
  3. 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 117:1227–1239CrossRefGoogle Scholar
  4. 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 101:1449–1458CrossRefGoogle Scholar
  5. August PV (1983) The role of habitat complexity and heterogeneity in structuring tropical mammal communities. Ecology 64:1495–1507CrossRefGoogle Scholar
  6. 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 199:101–109CrossRefGoogle Scholar
  7. Bartoń K (2016) MuMIn: multi-model inference. R package version 1(15):6Google Scholar
  8. Benchimol M, Peres CA (2015a) Widespread forest vertebrate extinctions induced by a mega hydroelectric dam in lowland Amazonia. PLoS One 10:e0129818CrossRefPubMedPubMedCentralGoogle Scholar
  9. Benchimol M, Peres CA (2015b) Predicting local extinctions of Amazonian vertebrates in forest islands created by a mega dam. Biol Cons 187:61–72CrossRefGoogle Scholar
  10. 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 103:408–420CrossRefGoogle Scholar
  11. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer-Verlag, New YorkGoogle Scholar
  12. Carvalho FMV, Fernandez FAS, Nessimian JL (2005) Food habits of sympatric opossums coexisting in small Atlantic Forest fragments in Brazil. Mamm Biol 70:366–375CrossRefGoogle Scholar
  13. 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 6:217–229CrossRefGoogle Scholar
  14. Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547CrossRefPubMedGoogle Scholar
  15. 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 84:45–67CrossRefGoogle Scholar
  16. 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 35:341–435Google Scholar
  17. 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 91:213–222CrossRefGoogle Scholar
  18. 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 97:253–265CrossRefGoogle Scholar
  19. Devictor V, Julliard R, Jiguet F (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117:507–514CrossRefGoogle Scholar
  20. Diamond J (2001) Damned experiments! Science 294:1847–1848CrossRefPubMedGoogle Scholar
  21. 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 36:27–46CrossRefGoogle Scholar
  22. ECOA—Ecologia em Ação (2016). International Rivers and Fundacion Proteger, Dams in Amazonia. Accessed 05 June 2017
  23. ESRI (2012) ArcMap 10.1, Environmental Systems Research Institute, Inc. RedlandsGoogle Scholar
  24. 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:e82369CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142CrossRefPubMedGoogle Scholar
  26. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol 34:487–515CrossRefGoogle Scholar
  27. Fearnside PM (2001) Environmental impacts of Brazil’s Tucuruí Dam: unlearned lessons for hydroelectric development in Amazonia. Environ Manag 27:377–396CrossRefGoogle Scholar
  28. Fearnside PM, Pueyo S (2012) Greenhouse-gas emissions from tropical dams. Nat Clim Change 2:382–384CrossRefGoogle Scholar
  29. Fonseca GA, Robinson JG (1990) Forest size and structure: competitive and predatory effects on small mammal communities. Biol Cons 53:265–294CrossRefGoogle Scholar
  30. FUNCATE/INPE/ANEEL (2000) Mapeamento por satélite das áreas inundadas por reservatórios de hidrelétricas brasileiras. Unpublished ReportGoogle Scholar
  31. 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 47:521–525CrossRefGoogle Scholar
  32. 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 341:1508–1510CrossRefPubMedGoogle Scholar
  33. 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 287–313Google Scholar
  34. 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 250:193–200CrossRefGoogle Scholar
  35. 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 57:131–144Google Scholar
  36. Guilhaumon F, Mouillot D, Gimenez O (2010) mmSAR: an R-package for multimodel species–area relationship inference. Ecography 33:420–424Google Scholar
  37. Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251CrossRefGoogle Scholar
  38. Hutchinson GE (1957) Concluding remarks. Cold Spring Harbor Symp Quant Biol 22:415–427CrossRefGoogle Scholar
  39. IBAMA (1997) Plano de Manejo Fase I: Reserva Biológica do Uatumã. Accessed 05 June 2017
  40. Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landscape Ecol 27:929–941CrossRefGoogle Scholar
  41. Jones KE et al (2009) PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90:2648CrossRefGoogle Scholar
  42. Jones IL, Bunnefeld N, Jump AS, Peres CA, Dent DH (2016) Extinction debt on reservoir land-bridge islands. Biol Cons 199:75–83CrossRefGoogle Scholar
  43. Junk WJ, Mello JAS (1990) Impactos ecológicos das represas hidrelétricas na bacia amazônica brasileira. Estudos avançados 4:126–143CrossRefGoogle Scholar
  44. Lambert TD, Adler GH, Riveros CM, Lopez L, Ascanio R, Terborgh J (2003) Rodents on tropical land bridge islands. J Zool 260:179–187CrossRefGoogle Scholar
  45. Lambert TD, Malcolm JR, Zimmerman BL (2006) Amazonian small mammal abundances in relation to habitat structure and resource abundance. J Mammal 87:766–776CrossRefGoogle Scholar
  46. Laurance WF (1994) Rainforest fragmentation and the structure of small mammal communities in tropical Queensland. Biol Cons 69:23–32CrossRefGoogle Scholar
  47. Lees AC, Peres CA, Fearnside PM, Schneider M, Zuanon JA (2016) Hydropower and the future of Amazonian biodiversity. Biodivers Conserv 25:451–466CrossRefGoogle Scholar
  48. Lynam AJ, Billick I (1999) Differential responses of small mammals to fragmentation in a Thailand tropical forest. Biol Cons 91:191–200CrossRefGoogle Scholar
  49. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Press Princeton, USAGoogle Scholar
  50. Malcolm JR (1991) The small mammals of Amazonian forest fragments: pattern and process. PhD dissertation, Department of Zoology, Gainesville, Florida, USAGoogle Scholar
  51. Mangan SA, Adler GH (2000) Consumption of arbuscular mycorrhizal fungi by terrestrial and arboreal small mammals in a Panamanian cloud forest. J Mammal 81:563–570CrossRefGoogle Scholar
  52. McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: Spatial Pattern Analysis Program for Categorical and Continuous Maps. Accessed 05 June 2017
  53. Muggeo VRM (2017) Segmented: Regression Models with Break-Points/Change-Points Estimation. R package version 0.5-2.1Google Scholar
  54. Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH (2007) Vegan: the community ecology package. R package version 2.4-2Google Scholar
  55. 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 124:253–266CrossRefGoogle Scholar
  56. 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 142:1178–1190CrossRefGoogle Scholar
  57. 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:e13666CrossRefPubMedPubMedCentralGoogle Scholar
  58. Passamani M, Fernandez FAS (2011) Abundance and richness of small mammals in fragmented Atlantic Forest of Southeastern Brazil. J Nat Hist 45:553–565CrossRefGoogle Scholar
  59. 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 244:1–306CrossRefGoogle Scholar
  60. Patton JL, Pardiñas UFJ, D’Elía G (2007) Mammals of South America, vol 2, 1st edn. The University of Chicago Press, ChicagoGoogle Scholar
  61. Prevedello JA, Vieira MV (2010) Does the type of matrix matter? A quantitative review of the evidence. Biodivers Conserv 19:1205–1223CrossRefGoogle Scholar
  62. R Development Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Accessed 05 June 2017
  63. 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 469–492CrossRefGoogle Scholar
  64. 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 21:1127–1147CrossRefGoogle Scholar
  65. 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 41:854–863CrossRefGoogle Scholar
  66. Sikes RS (2016) 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mammal 97:663–688CrossRefPubMedPubMedCentralGoogle Scholar
  67. 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 59:1–9CrossRefGoogle Scholar
  68. Terborgh J, Lopez L, Tello S (1997) Bird communities in transition: the Lago Guri islands. Ecology 78:1494–1501CrossRefGoogle Scholar
  69. 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 294:1923–1926CrossRefPubMedGoogle Scholar
  70. Toms JD, Lesperance ML (2003) Piecewise regression: a tool for identifying ecological thresholds. Ecology 84:2034–2041CrossRefGoogle Scholar
  71. 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 22:517–530CrossRefGoogle Scholar
  72. Vieira MF, Carvalho-Okano RM, Sazima M (1991) The common opossum (Didelphis marsupialis), as a pollinator of Mabea fistulifera (Euphorbiaceae). Ciência e Cultura 43:390–393Google Scholar
  73. 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 142:1191–1200CrossRefGoogle Scholar
  74. 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 16:862–873CrossRefGoogle Scholar
  75. 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 8:13–19CrossRefGoogle Scholar
  76. Watling JI, Donnelly MA (2006) Fragments as islands: a synthesis of faunal responses to habitat patchiness. Conserv Biol 20:1016–1025CrossRefPubMedGoogle Scholar
  77. Wright SJ, Gompper ME, DeLeon B (1994) Are large predators keystone species in neotropical forests? The evidence from Barro Colorado Island. Oikos 71:279–294CrossRefGoogle Scholar
  78. Wright DH, Patterson BD, Mikkelson GM, Cutler A, Atmar W (1998) A comparative analysis of nested subset patterns of species composition. Oecologia 113:1–20CrossRefGoogle Scholar
  79. 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 2:241–248CrossRefGoogle Scholar
  80. Zarfl C, Lumsdon AE, Berlekamp J, Tydecks L, Tockner K (2015) A global boom in hydropower dam construction. Aquat Sci 77:161–170CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratório de Vertebrados, Departamento de EcologiaUniversidade Federal do Rio de JaneiroRio De JaneiroBrazil
  2. 2.School of Environmental SciencesCenter for Ecology, Evolution and Conservation, University of East AngliaNorwichUK
  3. 3.Laboratório de Ecologia Aplicada à ConservaçãoUniversidade Estadual de Santa CruzIlhéusBrazil

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