European Journal of Wildlife Research

, Volume 62, Issue 4, pp 431–446 | Cite as

Connectivity maintain mammal assemblages functional diversity within agricultural and fragmented landscapes

  • Marcelo Magioli
  • Katia Maria Paschoaletto Micchi de Barros Ferraz
  • Eleonore Zulnara Freire Setz
  • Alexandre Reis Percequillo
  • Michelle Viviane de Sá Santos Rondon
  • Vanessa Villanova Kuhnen
  • Mariana Cristina da Silva Canhoto
  • Karen Evelyn Almeida dos Santos
  • Claudia Zukeran Kanda
  • Gabriela de Lima Fregonezi
  • Helena Alves do Prado
  • Mitra Katherina Ferreira
  • Milton Cezar Ribeiro
  • Priscilla Marqui Schmidt Villela
  • Luiz Lehmann Coutinho
  • Márcia Gonçalves Rodrigues
Original Article

Abstract

Despite major advances in mammal research, there are knowledge gaps regarding distribution, composition, and the functional role of mammal species within agricultural and fragmented landscapes. Also, there is a lack of knowledge about which factors influence mammal assemblages within agricultural ecosystems. Therefore, this study aimed to estimate the contribution of forest cover, functional connectivity, drainage, and amount of sugar cane toward explaining the functional diversity of terrestrial mammals. We made an inventory of terrestrial mammals in an agricultural and fragmented landscape in an Atlantic Forest-Cerrado ecotone in southeastern Brazil, assessed the functional diversity of mammal assemblages, and proposed conservation strategies at the landscape level. Data collection occurred from September/2011 to August/2012 through a combination of complementary methods: active search; trapping stations; collection of fecal samples, which were identified by hair cuticle and fecal DNA analysis; and data from the literature. Functional diversity (FD) was calculated using a set of ecological traits including body mass, locomotion form, behavioral and dietary traits, and the environmental sensitivity of species. Akaike information criterion was used to compare generalized linear models between FD values and landscape metrics. Our results reveal a surprising insight about the role exerted by agricultural and fragmented landscapes, which still sustain impressively high biodiversity levels and a meaningful amount of ecological functions, indicating some resistance of species to pressure from the agricultural matrix and advancing urbanization. The amount of ecological functions performed by mammal species within agricultural and fragmented landscapes was similar to pristine areas and more preserved landscapes. Functional connectivity (amount of area assessed for species able to cross 200 m of matrix) was the most plausible model (wAICc = 0.873). Thus, we concluded that improving functional connectivity guarantees high FD values, and we demonstrate the importance of maintaining and restoring structural connections between fragment patches within these landscapes for species conservation and the maintenance of populations over time.

Keyword

Functional diversity Connectivity Tracks Fecal DNA analysis Hair cuticle analysis Live-traps 

Notes

Acknowledgments

We thank the Forest Science Department (“Luiz de Queiroz” College of Agriculture, University of São Paulo), the Forest Resources Graduate Program (PPGRF), the interdisciplinary program in Applied Ecology (PPGI-EA) and the Wildlife Ecology, Management and Conservation Lab (LEMaC). We thank the Project “Pagamento por Serviços Ambientais no Corredor das Onças” (FUNBio 045/2011 – AFCoF II Proteção da Mata Atlântica II) for financial support, including fellowships to M.V.S.S. Rondon and V.V. Kuhnen. We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and São Paulo Research Foundation (FAPESP; grant #2014/10192-7) for the scholarship granted to M. Magioli, and Serviço de Apoio ao Estudante da Universidade Estadual de Campinas (SAE-UNICAMP) for fellowships to M.C.S. Canhoto and K.E.A. Santos. Small mammal sampling has also benefitted from Fundo de Apoio ao Ensino, à Pesquisa e à Extensão da Universidade Estadual de Campinas (FAEPEX-UNICAMP), grant #77910 to E.Z.F. Setz. We are indebted to Conselho Nacional de Pesquisa e Desenvolvimento Científico e Tecnológico (CNPq) for the productivity fellowship and to FAPESP (grant #2009/16009-1) for the grant to A.R. Percequillo. We are indebted to CNPq for the productivity fellowship and FAPESP (grant #2013/50421-2) for the grant to M.C. Ribeiro. We are indebted to CNPq for the productivity fellowship (grant #308503/2014-7) and FAPESP (grant #2014/09300-0) for the grant to K.M.P.M.B. Ferraz. The collection of fecal samples and small mammal sampling was authorized by IBAMA, through SISBIO permissions n. 31729-1 and n. 14705-2, respectively. We thank the anonymous reviewers for comments and suggestions that significantly improved the quality of an earlier version of this manuscript.

Supplementary material

10344_2016_1017_MOESM1_ESM.pdf (39 kb)
Electronic supplementary material (ESM) 1 Table S1Mammal species classification and ecological traits used for the functional diversity (FD) analysis of the assemblages recorded at Campinas Metropolitan Region (CMR), São Paulo State, Brazil (PDF 38 kb)
10344_2016_1017_MOESM2_ESM.pdf (38 kb)
Electronic supplementary material (ESM) 1 Table S2Mammal studies used for comparison between functional diversity (FD) values of the assemblages recorded at Campinas Metropolitan Region (CMR), São Paulo State, Brazil (PDF 37 kb)
10344_2016_1017_MOESM3_ESM.pdf (344 kb)
Electronic supplementary material (ESM) 2 Fig. S1Photographic images of mammals’ tracks at Campinas Metropolitan Region (CMR), São Paulo, Brazil. 1) Didelphis sp.; 2) Lutreolina crassicaudata; 3) Myrmecophaga tridactyla; 4) Dasypus novemcinctus; 5) Dasypus septemcinctus; 6) Euphractus sexcinctus; 7) Cabassous tatouay; 8) Sapajus nigritus; 9) Lepus europaeus; 10) Sylvilagus brasiliensis; 11) Leopardus pardalis; 12) Leopardus guttulus; 13) Leopardus wiedii; 14) Puma concolor; 15) Puma yagouaroundi; 16) Cercdocyon thous; 17) Chrysocyon brachyurus; 18) Lycalopex gymnocercus; 19) Galictis cuja; 20) Lontra longicaudis; 21) Eira barbara; 22) Procyon cancrivorus; 23) Mazama americana; 24) Mazama gouazoubira; 25) Sus scrofa; 26) Hydrochoerus hydrochaeris; 27) Cuniculus paca; 28) Sphiggurus villosus; 29) Myocastor coypus; 30) Nectomys squamipes (PDF 344 kb)
10344_2016_1017_MOESM4_ESM.pdf (257 kb)
Electronic supplementary material (ESM) 2 Fig. S2Small mammals captured at Campinas Metropolitan Region (CMR), São Paulo, Brazil. A) Akodon montensis; B) Olygorizomys nigripes; C) Cerradomys subflavus; D) Didelphis albiventris; E) Didelphis aurita (PDF 256 kb)
10344_2016_1017_MOESM5_ESM.pdf (214 kb)
Electronic supplementary material (ESM) 3 Fig. S3Generalized linear regressions between functional diversity (FD) values of medium- and large-sized mammal assemblages recorded at Campinas Metropolitan Region (CMR), São Paulo, Brazil, and landscape metrics [R2 (coefficient of determination); F and p (significance of the regression coefficients)] (PDF 213 kb)

References

  1. Abra FD (2012) Monitoramento e avaliação das passagens inferiores de fauna presentes na rodovia SP-225 no município de Brotas, São Paulo. Dissertation, Universidade de São Paulo.Google Scholar
  2. AGEMCAMP – Agência Metropolitana de Campinas (2014) Indicadores. http://www.agemcamp.sp.gov.br/produtos/indicadores/pesquisa/index.php?lang=en. Accessed 03 September 2014
  3. Andrén H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71:355–366CrossRefGoogle Scholar
  4. August P (1983) The role of habitat complexity and heterogeneity in structuring tropical mammal communities. Ecology 64:1495–1507CrossRefGoogle Scholar
  5. Ayram CAC, Mendoza ME, Etter A, Salicrup DRP (2015) Habitat connectivity in biodiversity conservation: a review of recent studies and applications. Prog Phys Geog. doi:10.1177/0309133315598713 Google Scholar
  6. Banks-Leite C, Pardini R, Tambosi LR, Pearse WD, Bueno AA, Bruscagin RT, Condez TH, Dixo M, Igari AT, Martensen AC, Metzger JP (2014) Using ecological thresholds to evaluate the costs and benefits of set-asides in a biodiversity hotspot. Science 345:1041–1045CrossRefPubMedGoogle Scholar
  7. Becker M, Dalponte JC (1999) Rastros de mamíferos silvestres brasileiros - um guia de campo. Universidade de Brasília, BrasíliaGoogle Scholar
  8. Beltran JF, Delibes M (1994) Environmental determinants of circadian activity of free-ranging Iberian lynxes. J Mamm 72:382–393CrossRefGoogle Scholar
  9. Bogoni JA, Cherem JJ, Giehl ELH, Oliveira-Santos LG, Castilho PV, Picinatto Filho V, Fantacini FM, Tortato MA, Luiz MR, Rizzaro R, Graipel ME (2016) Landscape features lead to shifts in communities of medium-to large-bodied mammals in subtropical Atlantic Forest. J Mammal. doi:10.1093/jmammal/gyv215 Google Scholar
  10. Bolker B (2008) Ecological models and data in R. Princeton University Press, New YorkGoogle Scholar
  11. Bonecker ST, Portugal LG, Costa-Neto SF, Gentile R (2009) A long term study of small mammal populations in a Brazilian agricultural landscape. Mamm Biol 74:467–477Google Scholar
  12. Borges PAL, Tomás WM (2008) Guia de rastros e outros vestígios de mamíferos do Pantanal. Embrapa Pantanal, CorumbáGoogle Scholar
  13. Bovo AAA, Ferraz KMPMB, Verdade LM, Moreira JM (2016) 11. Capybaras (Hydrochoerus hydrochaeris) in anthropogenic environments: challenges and conflicts. In: Gheler-Costa C, Lyra-Jorge M, Verdade LM (eds). Biodiversity in agricultural landscapes of southeastern Brazil. De Gruyter Open, Berlin. doi:10.1515/9783110480849-013
  14. Braga FG (2004) Tamanduá-bandeira (Myrmecophaga tridactyla), espécie criticamente em perigo: uma preocupação no estado do Paraná. Acta Biol Par 33:193–194Google Scholar
  15. Brocardo CR, Rodarte R, Bueno RS, Culot L, Galetti M (2012) Mamíferos não voadores do Parque Estadual Carlos Botelho, continuum florestal do Paranapiacaba. Biota Neotrop 12:198–208CrossRefGoogle Scholar
  16. Bruna EM, Guimarães JF, Lopes CT, Duarte P, Gomes ACL, Belentani SCS, Pacheco R, Facure KG, Lemos FG, Vasconcelos HL (2010) Mammalia, Estação Ecológica do Panga, a Cerrado protected area in Minas Gerais state, Brazil. Check List 6:668–675Google Scholar
  17. Bueno C, Sousa COM, Freitas SR (2015) Habitat or matrix: which is more relevant to predict road-kill of vertebrates? Braz J Biol 75:228–238CrossRefGoogle Scholar
  18. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  19. Cáceres NC, Hannibal W, Freitas DR, Silva EL, Roman C, Casella J (2010) Mammal occurrence and roadkill in two adjacent ecoregions (Atlantic Forest and Cerrado) in south-western Brazil. Zoologia 27:709–717CrossRefGoogle Scholar
  20. Campos CB, Esteves CF, Ferraz KMPMB, Crawshaw PG Jr, Verdade LM (2007) Diet of free-ranging cats and dogs in a suburban and rural environment, south-eastern Brazil. J Zool 273(1):14–20CrossRefGoogle Scholar
  21. Cantor M, Ferreira LA, Silva WR, Setz EZF (2010) Potential seed dispersal by Didelphis albiventris (Marsupialia, Didelphidae) in highly disturbed environment. Biota Neotrop 10:45–51CrossRefGoogle Scholar
  22. Cantor M, Pires M, Longo G, Guimarães P Jr, Setz EZF (2013) Individual variation in resource use by opossums leading to nested fruit consumption. Oikos 122:1085–1093CrossRefGoogle Scholar
  23. Carmignotto AP (2004) Pequenos mamíferos terrestres do bioma Cerrado: padrões faunísticos locais e regionais. Thesis, Universidade de São PauloGoogle Scholar
  24. Ceballos G, Ehrlich PR (2002) Mammal population losses and the extinction crisis. Science 296:904–907CrossRefPubMedGoogle Scholar
  25. Chame M (2003) Terrestrial mammal feces: a morphometric summary and description. Mem Inst Oswaldo Cruz 98:71–94CrossRefPubMedGoogle Scholar
  26. Chaves PB, Graeff VG, Lion MB, Oliveira LR, Eizirik E (2012) DNA barcoding meets molecular scatology: short mtDNA sequences for standardized species assignment of carnivore noninvasive samples. Mol Ecol Resour 12:18–35CrossRefPubMedGoogle Scholar
  27. Chiarello AG (1999) Effects of fragmentation of the Atlantic forest on mammal communities in south-eastern Brazil. Biol Conserv 89:71–82CrossRefGoogle Scholar
  28. Chiarello AG (2000a) Conservation value of a native forest fragment in a region of extensive agriculture. Rev Bras Biol 60:237–247CrossRefPubMedGoogle Scholar
  29. Chiarello AG (2000b) Density and population size of mammals in remnants of Brazilian Atlantic Forest. Conserv Biol 14:1649–1657CrossRefGoogle Scholar
  30. Cianciaruso MV, Silva IA, Batalha MA (2009) Diversidades filogenética e funcional: novas abordagens para a Ecologia de comunidades. Biota Neotrop 9:93–103CrossRefGoogle Scholar
  31. Coelho IP, Kindel A, Coelho AVP (2008) Roadkills of vertebrate species on two highways through the Atlantic Forest Biosphere Reserve, southern Brazil. Eur J Wildlife Res 54:689–699CrossRefGoogle Scholar
  32. R Core Team (2015) R: A language and environment for statistical computing: R Foundation for Statistical Computing, ViennaGoogle Scholar
  33. Deberdt AJ, Scherer SB (2007) O javali asselvajado: ocorrência e manejo da espécie no Brasil. Nat Conserv 5:31–44Google Scholar
  34. Dixo M, Metzger JP, Morgante JS, Zamudio KR (2009) Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian Atlantic Coastal Forest. Biol Conserv 142:1560–1569CrossRefGoogle Scholar
  35. Dotta G, Verdade LM (2007) Trophic categories in a mammal assemblage: diversity in an agricultural landscape. Biota Neotrop 7:287–292CrossRefGoogle Scholar
  36. Dotta G, Verdade LM (2011) Medium to large-sized mammals in agricultural landscapes of south-eastern Brazil. Mammalia 75:345–352CrossRefGoogle Scholar
  37. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious 5:4, http://www.geneious.com/. Accessed 12 September 2012Google Scholar
  38. Eduardo AA, Passamani M (2009) Mammals of medium and large size in Santa Rita do Sapucai, Minas Gerais, southeastern Brazil. Check List 5:399–404Google Scholar
  39. Emmons LH, Feer F (1997) Neotropical rainforest mammals: a field guide. University of Chicago Press, ChicagoGoogle Scholar
  40. Estrela DC, Souza DC, Souza JM, Castro ALS (2015) Medium and large-sized mammals in a Cerrado area of the state of Goiás, Brazil. Check List 11:1690CrossRefGoogle Scholar
  41. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515CrossRefGoogle Scholar
  42. Fahrig L (2005) When is a landscape perspective important? In: Wiens JA, Moss MR (eds) Issues and perspectives in landscape ecology. Cambridge University Press, New York, pp 3–10CrossRefGoogle Scholar
  43. Faria HH (2006) Plano de manejo do Parque Estadual Morro do Diabo. Instituto Florestal, São Paulo, http://fflorestal.sp.gov.br/files/2012/01/morrododiabo.pdf. Accessed 25 January 2016Google Scholar
  44. Ferraz KMPMB, Siqueira MF, Martin PS, Esteves CF, Couto HTZ (2010) Assessment of Cerdocyon thous distribution in an agricultural mosaic, southeastern Brazil. Mammalia 74:275–280Google Scholar
  45. Ferraz KMPMB, Siqueira MF, Alexandrino ER, Luz DTA, Couto HTZ (2012) Environmental suitability of a highly fragmented and heterogeneous landscape for forest bird species in south-eastern Brazil. Environ Conserv 39:316–324CrossRefGoogle Scholar
  46. Flynn DFB, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, Simpson N, Mayfield MM, DeClerck F (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12:22–33CrossRefPubMedGoogle Scholar
  47. Freitas CH, Justino CS, Setz EZF (2014) Road-kills of the giant anteater in south-eastern Brazil: 10 years monitoring spatial and temporal determinants. Wildl Res 41:673–680CrossRefGoogle Scholar
  48. Galetti M, Giacomini HC, Bueno RS, Bernardo CS, Marques RM, Bovendorp RS, Steffler CE, Rubim P, Gobbo SK, Donatti CI, Begotti RA, Meirelles F, Nobre RA, Chiarello AG, Peres CA (2009) Priority areas for the conservation of Atlantic forest large mammals. Biol Conserv 142:1229–1241CrossRefGoogle Scholar
  49. Galetti M, Eizirik E, Beisiegel B, Ferraz K, Cavalcanti S, Srbek-Araujo AC, Crawshaw P, Paviolo A, Galetti PM Jr, Jorge ML, Marinho-Filho J, Vercillo U, Morato R (2013) Atlantic rainforest’s jaguars in decline. Science 342:930–930CrossRefPubMedGoogle Scholar
  50. 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 91:223–229CrossRefGoogle Scholar
  51. Gaspar DA (1997) Ecologia e comportamento do bugio, Alouatta fusca (Geoffroyi, 1812; Primates: Cebidae) em fragmento de mata de Campinas, SP. Dissertation, Universidade Estadual Paulista Júlio de Mesquita Filho.Google Scholar
  52. Gheler-Costa C, Vettorazzi CA, Pardini R, Verdade LM (2012) The distribution and abundance of small mammals in agroecosystems of southeastern Brazil. Mammalia 76:185–191CrossRefGoogle Scholar
  53. Hannibal W (2014) Mammals of medium and large size from a fragmented seasonal forest landscape in Mato Grosso do Sul state, central-western Brazil. Check List 10:1430–1434CrossRefGoogle Scholar
  54. Huijser MP, Abra FD, Duffield JW (2013) Mammal road mortality and cost-benefit analyses of mitigation measures aimed at reducing collisions with capybara (Hydrochoerus hydrochaeris) in São Paulo State. Brazil Oecol Austral 17:129–146CrossRefGoogle Scholar
  55. IBGE – Instituto Brasileiro de Geografia e Estatística (2004a) Mapa de biomas do Brasil. ftp://ftp.ibge.gov.br/Cartas_e_Mapas/Mapas_Murais/biomas_pdf.zip. Accessed 10 December 2010
  56. IBGE – Instituto Brasileiro de Geografia e Estatística (2004b) Mapa da vegetação do Brasil. ftp://ftp.ibge.gov.br/Cartas_e_Mapas/Mapas_Murais/vegetacao_pdf.zip. Accessed 10 December 2010
  57. IUCN – International Union for Conservation of Nature and Natural Resources (2015) The IUCN Red List of Threatened Species. Version 2015–4. http://www.iucnredlist.org. Accessed on 10 February 2016
  58. Jiménez JE, Lucherini M, Novaro AJ (2008) Pseudalopex gymnocercus. In: IUCN 2014. IUCN Red List of Threatened Species. Version 2014.3. www.iucnredlist.org. Accessed 24 March 2015
  59. Jorge MLS, Galetti M, Ribeiro MC, Ferraz KMP (2013) Mammal defaunation as surrogate of trophic cascades in a biodiversity hotspot. Biol Conserv 163:49–57CrossRefGoogle Scholar
  60. Kasper CB, Mazim FD, Soares JBG, Oliveira TG, Fabián ME (2007) Composição e abundância relativa dos mamíferos de médio e grande porte no Parque Estadual do Turvo, Rio Grande do Sul, Brasil. Rev Bras Zool 24:1087–1100CrossRefGoogle Scholar
  61. Klink CA, Machado RB (2005) Conservation of the Brazilian Cerrado. Conserv Biol 19:707–713CrossRefGoogle Scholar
  62. Korschgen LJ (1980) Procedures for food-habits analyses. In: Schamnitz SD (ed) Wildlife management techniques manual. The Wildlife Society, Washington, pp 113–127Google Scholar
  63. Lessa LG, Alves H, Geise L, Barreto RM (2012) Mammals of medium and large size in a fragmented cerrado landscape in northeastern Minas Gerais state, Brazil. Check List 8:192–196CrossRefGoogle Scholar
  64. Lyra-Jorge MC, Ciocheti G, Pivello VR (2008) Carnivore mammals in a fragmented landscape in northeast of São Paulo State, Brazil. Biodiver Conserv 17:1573–1580CrossRefGoogle Scholar
  65. Lyra-Jorge MC, Ribeiro MC, Ciocheti G, Tambosi LR, Pivello VR (2010) Influence of multi-scale landscape structure on the occurrence of carnivorous mammals in a human-modified savanna, Brazil. Eur J Wildlife Res 56:359–368CrossRefGoogle Scholar
  66. Magioli M, Ferraz KMPMB, Rodrigues MG (2014a) Medium and large-sized mammals of an isolated Atlantic Forest remnant, southeast São Paulo State, Brazil. Check List 10:850–856CrossRefGoogle Scholar
  67. Magioli M, Moreira MZ, Ferraz KMB, Miotto RA, Camargo PB, Rodrigues MG, Canhoto MCS, Setz EZF (2014b) Stable isotope evidence of Puma concolor (Felidae) feeding patterns in agricultural landscapes in southeastern Brazil. Biotropica 46:451–460CrossRefGoogle Scholar
  68. Magioli M, Ribeiro MC, Ferraz KMPMB, Rodrigues MG (2015) Thresholds in the relationship between functional diversity and patch size for mammals in the Brazilian Atlantic Forest. Animal Conserv 18:499–511CrossRefGoogle Scholar
  69. Martensen AC, Ribeiro MC, Banks-Leite C, Prado PI, Metzger JP (2012) Associations of forest cover, fragment area, and connectivity with neotropical understory bird species richness and abundance. Conserv Biol 26:1100–1111CrossRefPubMedGoogle Scholar
  70. Martin PS (2007) Mamíferos de médio e grande porte em fragmentos de mata nativa na Bacia do Rio Corumbataí, SP. Monograph, Escola Superior de Agricultura Luiz de Queiroz – Universidade de São Paulo.Google Scholar
  71. Martin PS, Gheler-Costa C, Lopes PC, Rosalino LM, Verdade LM (2012) Terrestrial non-volant small mammals in agro-silvicultural landscapes of Southeastern Brazil. Forest Ecol Manag 282:185–195CrossRefGoogle Scholar
  72. Matias LF, Bargos D, Martins MI, Martins N, Galindo C (2012) Mapeamento do uso das terras na Região Metropolitana de Campinas (RMC) e hierarquização dos fragmentos florestais. http://www.icmbio.gov.br/corredordasoncas/images/stories/downloads/pub/Relatorios/Funbio/Relat_Uso_Terras.pdf. Accessed 12 December 2012
  73. Medri ÍM, Mourão G (2005) Home range of giant anteaters (Myrmecophaga tridactyla) in the Pantanal wetland, Brazil. J Zool 266:365–375CrossRefGoogle Scholar
  74. Miotto RA, Cervini M, Figueiredo MG, Begotti RA, Galetti PM Jr (2011) Genetic diversity and population structure of pumas (Puma concolor) in southeastern Brazil: implications for conservation in a human-dominated landscape. Conserv Genet 12:1447–1455CrossRefGoogle Scholar
  75. Miotto RA, Cervini M, Begotti RA, Galetti PM Jr (2012) Monitoring a puma (Puma concolor) population in a fragmented landscape in southeast Brazil. Biotropica 44:98–104CrossRefGoogle Scholar
  76. Mittermeier RA, Turner WR, Larsen FW, Brooks TM, Gascon C (2011) Global biodiversity conservation: the critical role of hotspots. In: Zachos FE, Habel JC (eds) Biodiversity hotspots. Springer Publishers, London, pp 3–22CrossRefGoogle Scholar
  77. MMA – Ministério do Meio Ambiente (2010) Plano de Manejo – ARIE Mata de Santa Genebra. Ministério do Meio Ambiente, Fundação José Pedro de Oliveira, Campinas. http://www.icmbio.gov.br/portal/images/stories/imgs-unidades-coservacao/arie_mata_de_santa_genebra.pdf. Accessed 20 November 2013.
  78. Monteiro-Filho ELA (1995) Os mamíferos da Santa Genebra. In: Morelatto LPC, Leitão-Filho HF (eds) Ecologia e preservação de uma floresta tropical urbana: reserva de Santa Genebra. UNICAMP, Campinas, pp 86–92Google Scholar
  79. Oliveira TG, Cassaro K (2006) Guia de campo dos felinos do Brasil. Instituto Pró-Carnívoros; Fundação do Parque Zoológico de São Paulo, Sociedade de Zoológicos do Brasil, Pró-Vida Brasil, São PauloGoogle Scholar
  80. Oliveira VB, Linares AM, Corrêa GLC, Chiarello AG (2008) Predation on the black capuccin monkey Cebus nigritus (Primates: Cebidae) by domestic dogs Canis lupus familiaris (Carnivora: Canidae) in the Parque Estadual Serra do Brigadeiro, Minas Gerais, Brazil. Rev Bras Zool 25:376–378CrossRefGoogle Scholar
  81. Paglia AP, Fonseca GAB, Rylands AB, Hermann G, Aguiar LMS, Chiarello AG, Leite YLR, Costa LP, Siciliano S, Kierulff MCM, Mendes SL, Tavares VC, Mittermeier RA, Patton JL (2012) Annotated Checklist of Brazilian Mammals. 2nd ed. Occasional Papers in Conservation Biology, No. 6. Conservation International, Arlington, VAGoogle Scholar
  82. Pardini R, 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 Conserv 124:253–266CrossRefGoogle Scholar
  83. Pardini R, Rossi RV, Munari DP (2009) Mamíferos não-voadores. In: Lopes MIMS, Kirizawa M, Melo MMRF (eds) Patrimônio da Reserva Biológica do Alto da Serra de Paranapiacaba. Instituto de Botânica, São Paulo, pp 639–658Google Scholar
  84. Pardini R, Bueno ADA, Gardner TA, Prado PI, Metzger JP (2010) Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. Plos One 5:e13666CrossRefPubMedPubMedCentralGoogle Scholar
  85. Pavoine S, Vallet J, Dufour AB, Gachet S, Daniel H (2009) On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118:391–402CrossRefGoogle Scholar
  86. Pedrosa F, Salerno R, Padilha FVB, Galetti M (2015) Current distribution of invasive feral pigs in Brazil: economic impacts and ecological uncertainty. Nat Conserv 13:84–87CrossRefGoogle Scholar
  87. Penido G, Zanzini ACS (2012) Checklist of large and medium-sized mammals of the Estação Ecológica Mata do Cedro, an Atlantic forest remnant of central Minas Gerais, Brazil. Check List 8:712–717Google Scholar
  88. Percequillo AR, Kierulff C (2009) Mamíferos. In: Breassan PM, Kierulff MCM, Sugieda AM (eds) Fauna ameaça de extinção do Estado de São Paulo: vertebrados. Fundação Parque Zoológico de São Paulo, Secretaria do Meio Ambiente, São Paulo, pp 31–41Google Scholar
  89. Percequillo AR, Hingst-Zaher E, Bonvicino CR (2008) Systematic review of genus Cerradomys Weksler, Percequillo and Voss, 2006 (Rodentia: Cricetidae: Sigmodontinae: Oryzomyini), with description of two new species from eastern Brazil. Am Mus Novit 3622: 1–46Google Scholar
  90. Petchey OL, Gaston KJ (2002) Functional diversity (FD), species richness and community composition. Ecol Lett 5:402–411CrossRefGoogle Scholar
  91. Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758CrossRefPubMedGoogle Scholar
  92. Portaria MMA n. 444 (2014) Reconhece como espécies da fauna brasileira ameaçadas de extinção aquelas constantes da “Lista Nacional Oficial de Espécies da Fauna Ameaçadas de Extinção”, trata de mamíferos, aves, répteis, anfíbios e invertebrados terrestres e indica o grau de risco de extinção de cada espécie. http://www.icmbio.gov.br/portal/images/stories/biodiversidade/fauna-brasileira/avaliacao-do-risco/PORTARIA_N%C2%BA_444_DE_17_DE_DEZEMBRO_DE_2014.pdf. Accessed 08 October 2015
  93. Prado MR, Rocha EC, Giudice GLM (2008) Mamíferos de médio e grande porte em um fragmento de Mata Atlântica, Minas Gerais, Brasil. R Árvore 32:741–749CrossRefGoogle Scholar
  94. Quadros J (2002) Identificação microscópica de pelos de mamíferos e sua aplicação no estudo da dieta de carnívoros. Universidade Federal do Paraná, ThesisGoogle Scholar
  95. Reale R, Fonseca RCB, Uieda W (2014) Medium and large-sized mammals in a private reserve of natural heritage in the municipality of Jaú, São Paulo, Brazil. Check List 10:997–1004CrossRefGoogle Scholar
  96. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distribuited? Implications for conservation. Biol Conserv 142:1141–1153CrossRefGoogle Scholar
  97. Ribeiro MC, Muylaert RL, Dodonov P, Ciocheti G, Magioli M, Martello F, Rocha A, Borges BD, Carvalho C, Kanda CZ, Rodríguez-Castro KG (2016) 4. Dealing with fragmentation and road effects in highly degraded and heterogeneous landscapes. In: Gheler-Costa C, Lyra-Jorge M, Verdade LM (eds) Biodiversity in agricultural landscapes of southeastern Brazil. De Gruyter Open, Berlin. doi:10.1515/9783110480849-006
  98. Robinson JG, Redford KH (1986) Body size, diet, and population density of Neotropical forest mammals. Amer Nat 128:665–680CrossRefGoogle Scholar
  99. Rocha EC, Dalponte JC (2006) Composição e caracterização da fauna de mamíferos de médio e grande porte em uma pequena reserva de Cerrado em Mato Grosso, Brasil. R Árvore 30:669–678CrossRefGoogle Scholar
  100. Rodrigues MG (2009) Relatório de Resultados – Campanha inicial de confirmação da presença de espécies ameaçadas na RMC - Área Piloto Usina Esther. Technical Report – ICMBio, AtibaiaGoogle Scholar
  101. Rodrigues RR, Gandolfi S (2007) Restoration actions. In: Rodrigues RR, Martins SV, Gandolfi S (eds) High diversity forest restoration in degraded areas. Nova, New York, pp 77–101Google Scholar
  102. Rylands AB, Mendes SL (2008) Callithrix penicillata. The IUCN Red List of Threatened Species 2008. doi:10.2305/IUCN.UK.2008.RLTS.T41519A10486326.en. Accessed 19 November 2015
  103. Rylands AB, Kierulff MCM, Mendes SL, Oliveira MM (2008a) Callithrix aurita. The IUCN Red List of Threatened Species 2008. doi:10.2305/IUCN.UK.2008.RLTS.T3570A9949843.en. Accessed 19 November 2015
  104. Rylands AB, Mittermeier RA, Oliveira MM, Kierulff MCM (2008b) Callithrix jacchus. The IUCN Red List of Threatened Species 2008. doi:10.2305/IUCN.UK.2008.RLTS.T41518A10485463.en. Accessed 19 November 2015
  105. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  106. Sambrook J, Fritschi EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  107. Silva AP Jr, Pontes AR (2008) The effect of a mega-fragmentation process on large mammal assemblages in the highly-threatened Pernambuco Endemism Centre, north-eastern Brazil. Biodiv Conserv 17:1455–1464CrossRefGoogle Scholar
  108. Silva JMC, Tabarelli M (2000) Tree species impoverishment and the future flora of the Atlantic forest of northeastern Brazil. Nature 404:72–74CrossRefGoogle Scholar
  109. Siviero MCB, Setz EZF (2011) Pegadas de mamíferos em parcelas de areia em fragmentos de vegetação da bacia do ribeirão Anhumas, Campinas, São Paulo. Rev Inst Flor 23:39–55Google Scholar
  110. Tabarelli M, Aguiar AV, Ribeiro MC, Metzger JP, Peres CA (2010) Prospects for biodiversity conservation in the Atlantic Forest: lessons from aging human-modified landscapes. Biol Conserv 143:2328–2340CrossRefGoogle Scholar
  111. Talamoni SA, Dias M (1999) Population and community ecology of small mammals in southeastern Brazil. Mammalia 63:167–181CrossRefGoogle Scholar
  112. Tambosi LR, Martensen AC, Ribeiro MC, Metzger JP (2014) A framework to optimize biodiversity restoration efforts based on habitat amount and landscape connectivity. Restor Ecol 22:169–177CrossRefGoogle Scholar
  113. Thornton DH, Branch LC, Sunquist ME (2011) The relative influence of habitat loss and fragmentation: Do tropical mammals meet the temperate paradigm? Ecol Appl 21:2324–2333CrossRefPubMedGoogle Scholar
  114. Tilman D (2001) Functional diversity. In: Levin SA (ed) Encyclopedia of biodiversity. Academic, Altham, pp 109–120CrossRefGoogle Scholar
  115. Trigo TC, Schneider A, Oliveira TG, Lehugeur LM, Silveira L, Freitas TR, Eizirik E (2013) Molecular data reveal complex hybridization and a cryptic species of Neotropical wild cat. Curr Biol 23:2528–2533CrossRefPubMedGoogle Scholar
  116. 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
  117. Upham NS, Hafner JC (2013) Do nocturnal rodents in the Great Basin Desert avoid moonlight? J Mamm 94:59–72CrossRefGoogle Scholar
  118. Varela DM, Trovati RG, Guzmán KR, Rossi RV, Duarte JMB (2010) Red brocket deer – Mazama americana. In: Duarte JMB, Gonzalez S (eds) Neotropical cervidology, biology and medicine of Latin American deer. Funep/IUCN, pp 151–159Google Scholar
  119. Vivo M, Carmignoto AP (2015) Family Sciuridae G. Fischer, 1987. In: Patton JL, Pardiñas UFJ, D’Elía G (eds) Mammals of South America, volume 2: Rodents. The University of Chicago Press, Chicago, pp 1–48Google Scholar
  120. Vivo M, Carmignotto AP, Gregorin R, Hingst-Zaher E, Iack-Ximenes GE, Miretski M, Percequillo AR, Rollo MM Jr, Rossi RV, Tadei VA (2011) Checklist dos mamíferos do Estado de São Paulo, Brasil. Biota Neotrop 11:1–21CrossRefGoogle Scholar
  121. Voss RS, Emmons LH (1996) Mammalian diversity in neotropical lowland rainforests: a preliminary assessment. Bull Am Mus Nat His 230.Google Scholar
  122. Zanon CM, Reis NR (2010) Ordem Lagomorpha. In: Reis NR, Peracchi AL, Fregonezi MN, Rossaneis BK (eds) Mamíferos do Brasil. Technical Books Editora, Rio de JaneiroGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Marcelo Magioli
    • 1
  • Katia Maria Paschoaletto Micchi de Barros Ferraz
    • 1
  • Eleonore Zulnara Freire Setz
    • 2
  • Alexandre Reis Percequillo
    • 3
  • Michelle Viviane de Sá Santos Rondon
    • 2
  • Vanessa Villanova Kuhnen
    • 2
  • Mariana Cristina da Silva Canhoto
    • 2
  • Karen Evelyn Almeida dos Santos
    • 2
  • Claudia Zukeran Kanda
    • 4
  • Gabriela de Lima Fregonezi
    • 4
  • Helena Alves do Prado
    • 4
  • Mitra Katherina Ferreira
    • 4
  • Milton Cezar Ribeiro
    • 4
  • Priscilla Marqui Schmidt Villela
    • 5
  • Luiz Lehmann Coutinho
    • 5
  • Márcia Gonçalves Rodrigues
    • 6
  1. 1.Escola Superior de Agricultura “Luiz de Queiroz” – ESALQ/USP, Departamento de Ciências Florestais, Laboratório de Ecologia, Manejo e Conservação de Fauna Silvestre (LEMaC)PiracicabaBrazil
  2. 2.Universidade Estadual de Campinas – UNICAMP, Instituto de Biologia, Departamento de Biologia Animal, Laboratório de Ecologia e Comportamento de Mamíferos (LAMA)Rua Monteiro Lobato 255, Cidade UniversitáriaCampinasBrazil
  3. 3.Escola Superior de Agricultura “Luiz de Queiroz” – ESALQ/USP, Departamento de Ciências Biológicas, Laboratório de Zoologia de VertebradosPiracicabaBrazil
  4. 4.Universidade Estadual Paulista “Júlio de Mesquita Filho” – UNESP, Instituto de Biologia, Departamento de Ecologia, Laboratório de Ecologia Espacial e Conservação (LEEC)Rio ClaroBrazil
  5. 5.Escola Superior de Agricultura “Luiz de Queiroz” – ESALQ/USP, Departamento de Zootecnia, Laboratório de Biotecnologia AnimalPiracicabaBrazil
  6. 6.ARIE Matão de Cosmópolis, Instituto Chico Mendes para Conservação da Biodiversidade, Ministério do Meio Ambiente, Rua Pitágoras, 353 – Cidade Universitária Zeferino VazCampinasBrazil

Personalised recommendations