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European Journal of Wildlife Research

, Volume 56, Issue 3, pp 359–368 | Cite as

Influence of multi-scale landscape structure on the occurrence of carnivorous mammals in a human-modified savanna, Brazil

  • Maria Carolina Lyra-Jorge
  • Milton Cezar Ribeiro
  • Giordano Ciocheti
  • Leandro Reverberi Tambosi
  • Vânia Regina Pivello
Original Paper

Abstract

São Paulo is the most developed state in Brazil and contains few fragments of native ecosystems, generally surrounded by intensive agriculture lands. Despite this, some areas still shelter large native animals. We aimed at understanding how medium and large carnivores use a mosaic landscape of forest/savanna and agroecosystems, and how the species respond to different landscape parameters (percentage of landcover and edge density), in a multi-scale perspective. The response variables were: species richness, carnivore frequency and frequency for the three most recorded species (Puma concolor, Chrysocyon brachyurus and Leopardus pardalis). We compared 11 competing models using Akaike's information criterion (AIC) and assessed model support using weight of AIC. Concurrent models were combinations of landcover types (native vegetation, “cerrado” formations, “cerradão” and eucalypt plantation), landscape feature (percentage of landcover and edge density) and spatial scale. Herein, spatial scale refers to the radius around a sampling point defining a circular landscape. The scales analyzed were 250 (fine), 1,000 (medium) and 2,000 m (coarse). The shape of curves for response variables (linear, exponential and power) was also assessed. Our results indicate that species with high mobility, P. concolor and C. brachyurus, were best explained by edge density of the native vegetation at a coarse scale (2,000 m). The relationship between P. concolor and C. brachyurus frequency had a negative power-shaped response to explanatory variables. This general trend was also observed for species richness and carnivore frequency. Species richness and P. concolor frequency were also well explained by a second concurrent model: edge density of cerradão at the fine (250 m) scale. A different response was recorded for L. pardalis, as the frequency was best explained for the amount of cerradão at the fine (250 m) scale. The curve of response was linearly positive. The contrasting results (P. concolor and C. brachyurus vs L. pardalis) may be due to the much higher mobility of the two first species, in comparison with the third. Still, L. pardalis requires habitat with higher quality when compared with other two species. This study highlights the importance of considering multiple spatial scales when evaluating species responses to different habitats. An important and new finding was the prevalence of edge density over the habitat extension to explain overall carnivore distribution, a key information for planning and management of protected areas.

Keywords

Brazilian savanna Mammal distribution Habitat use Landscape ecology Habitat heterogeneity 

Notes

Acknowledgments

The authors are thankful to Dr. Carlos Alberto Vettorazzi for his suggestions on a previous phase of this study and to Neotropical Grassland Conservancy and CNPQ for financial support. We are also very thankful to Patrick James, Danilo Boscolo and Tadeu Siqueira for their contributions in a later version of the paper. MCR thanks to Jean Paul Metzger's and Marie-Josee Fortin's research groups for all valuable discussions on landscape ecology and biodiversity conservation fields.

References

  1. Aberg J, Jansson G, Swenson JE, Angelstam P (1995) The effect of matrix on the occurrence of hazel grouse in isolated habitat fragments. Oecologia 103:265–269CrossRefGoogle Scholar
  2. Antongiovanni M, Metzger JP (2005) Influence of matrix habitats on the occurrence of insectivorous bird species in Amazonian forest fragments. Biol Conserv 122:441–451CrossRefGoogle Scholar
  3. Aragona M, Setz EZ (2001) Diet of the maned wolf, during wet and dry seasons at Ibitipoca state park. Brazil J Zool 254(1):131–136CrossRefGoogle Scholar
  4. Arrhenius O (1921) Species and area. J Ecol 9:95–99CrossRefGoogle Scholar
  5. Baldissera R, Ganade G, Brescovit AD, Hartz SM (2008) Landscape mosaic of Araucaria forest and forest monocultures influencing understorey spider assemblages in southern Brazil. Austral Ecol 33:45–54Google Scholar
  6. Bender DJ, Fahrig L (2005) Matrix structure obscures the relationship between interpatch movement and patch size and isolation. Ecology 86:1023–1033CrossRefGoogle Scholar
  7. Berry O, Mandy T, Gleeson DM, Sarres D (2005) Effect of vegetation matrix on animal dispersal: genetic evidence from a study of endangered skinks. Conserv Biol 19:855–864CrossRefGoogle Scholar
  8. Bietti MS, Paviolo A, Ângelo D (2006) Density, habitat use and activity patterns of ocelots in the Atlantic Forest of Missiones, Argentina. J Zool 270(1):153–163Google Scholar
  9. Bolker B (2008) Ecological Models and Data in R, 516p available at http://www.zoo.ufl.edu/bolker/emdbook. Accessed 22 April 2008
  10. Boscolo D, Metzger JP (2009) Is bird incidence in Atlantic forest fragments influenced by landscape patterns at multiple scales? Landscape Ecology. doi: 10.1007/s10980-009-9370-8, 12p
  11. Boscolo D, Candia-Gallardo C, Awade M, Metzger JP (2008) Importance of inter-habitat gaps and stepping-stones for a bird species in the Atlantic Forest, Brazil. Biotropica 40:273–276CrossRefGoogle Scholar
  12. Brannstrom C (2001) Conservation-with-development models in Brazil's agro-pastoral landscapes. World Dev 29:1345–1359CrossRefGoogle Scholar
  13. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information—theoretical approach. Springer, New YorkGoogle Scholar
  14. Cassandra LT, Zhang L, Mitsch WJ (2008) Aquatic metabolism as an indicator on the ecological effects of hydrologic pulsing in flow-through wetlands. Ecol Indic (2008). doi: 10.1016/j.ecolind.2007.09.005
  15. Castellon TD, Sieving KE (2005) An experimental test of matrix permeability and corridor use by and endemic understory bird. Conserv Biol 20:135–145CrossRefGoogle Scholar
  16. Coelho CM, Melo FB, Sábato AL, Magni EMV, Hirsch A, Young RJ (2008) Habitat use by wild maned wolves (Chrysocyon brachyurus) in a transition zone environment. J Mammal 89:97–104CrossRefGoogle Scholar
  17. Comiskey EJ, Bass Jr OL, Gross LJ, McBride RT, Salinas R (2002) Panthers and Forests in South Florida: an Ecological Perspective. Conservation Ecology 6(1): 18. Available at http://www.consecol.org/vol6/iss1/art18. Accessed 1 August 2009
  18. Coutinho LM (1978) O conceito de cerrado. Rev Bras Bot 1:17–23Google Scholar
  19. Crooks K (2002) Relative sensitivities of mammalian carnivores to habitat fragmentation. Conserv Biol 16:488–502CrossRefGoogle Scholar
  20. Devictor V, Julliard R, Jiguet F (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117(4):507–514CrossRefGoogle Scholar
  21. Dietz JM (1984) Ecology and social organization of the maned wolf (Chrysocyon brachyurus). Smithson Contrib Zool 392:1–51Google Scholar
  22. Dixo M, Metzger J, Morgante J, Zamudio K (2008) Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian Atlantic Coastal Forest. Biol Conserv 142:1560–1569CrossRefGoogle Scholar
  23. Downes SJ, Handasyde KA, Elgar MA (1997) The use of corridors by mammals in fragmented Australian eucalypt forests. Conserv Biol 11:718–726CrossRefGoogle Scholar
  24. Drakare S, Lennon JJ, Hillebrand H (2006) The imprint of the geographical, evolutionary and ecological context on species-area relationships. Ecol Lett 9(2):215–227CrossRefPubMedGoogle Scholar
  25. Durigan G, Siqueira MF, Franco GADC (2007) Threats to the cerrado remnants of the state of São Paulo, Brazil. Sci Agric 64:366–363CrossRefGoogle Scholar
  26. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Ann Rev Ecol Evol Syst 34:487–515CrossRefGoogle Scholar
  27. Fahrig L, Merriam G (1994) Conservation of fragmented populations. Conserv Biol 8:50–59CrossRefGoogle Scholar
  28. Fortin MJ, Dale MRT (2005) Spatial analysis: a guide for ecologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  29. Fortin MJ, Dale MRT (2009) Spatial autocorrelation in ecological studies—a legacy of solutions and myths. Geogr Anal 41:392–396CrossRefGoogle Scholar
  30. Garshelis DL (2000) Delusions in habitat evaluation: measuring use, selection and importance. Research techniques in animal ecology: controversies and consequences. Columbia University Press, New York, pp 111–164Google Scholar
  31. Goulart FVB, Cáceres NC, Graipel ME, Tortato MA, Ghizoni IR, Oliveira-Santos LGR (2009) Habitat selection by large mammals in a southern Brazilian atlantic forest. Mamm Biol 74(3):182–190CrossRefGoogle Scholar
  32. Hansbauer MM, Storch I, Leu S, Nieto-Holguin J-P, PimentelRG KF, Metzger JP (2008) Movements of neotropical understory passerines affected by anthropogenic forest edges in the Brazilian Atlantic Rainforest. Biol Conserv 141:782–791CrossRefGoogle Scholar
  33. Hilty JA, Merenlender AM (2004) Use of riparian Corridors and vineyards by mammalian predators in Northern California. Conserv Biol 18:126–135CrossRefGoogle Scholar
  34. IBGE-Instituto Brasileiro de Geografia e Estatística (1973) Cartas Topográficas Luis Pulador (folha SF-22-Z-B-IV-3). IBGE, Rio de JaneiroGoogle Scholar
  35. INPE—Instituto Nacional de Pesquisas Espaciais (2005) SPRING—Sistema de Processamento de Informações Georreferenciadas, version 4.1. Available at <www.dpi.inpr.br/spring>. Accessed 01 June 2005
  36. Lindenmayer D, Hobbs RJ, Montague-Drake R, Alexandra J, Bennett A, Burgman M, Cale P, Calhoun A, Cramer V, Cullen P, Driscoll D, Fahrig L, Fischer J, Franklin J, Haila Y, Hunter M, Gibbons P, Lake S, Luck G, MacGregor C, McIntyre S, Mac Nally R, Manning A, Miller J, Mooney H, Noss R, Possingham H, Saunders D, Schmiegelow F, Scott M, Simberloff D, Sisk T, Tabor G, Walker B, Wiens J, Woinarski J, Zavaleta E (2008) A checklist for ecological management of landscape for conservation. Ecol Lett 11:78–91PubMedGoogle Scholar
  37. Lomolino MV (2000) Ecology's most general, yet protean pattern: the species–area relationship. J Biogeogr 27(1):17–26CrossRefGoogle Scholar
  38. Lomolino MV (2001) The species–area relationship: new challenges for an old pattern. Progr Phys Geogr 25(1):1–21Google Scholar
  39. Lyra-Jorge MC, Ciocheti G, Pivello VR (2008) Carnivore mammals in a fragmented landscape in northeast of São Paulo State, Brazil. Biodivers Conserv 17:1573–1580CrossRefGoogle Scholar
  40. Marsden SJ, Symes CT (2008) Bird richness and composition along an agricultural gradient in New Guinea: the influence of land use, habitat heterogeneity and proximity to intact forest. Austral Ecol 33:784–793CrossRefGoogle Scholar
  41. Martensen AC, Pimentel RG, Metzger JP (2008) Relative effects of fragment size and connectivity on bird community in the Atlantic Rain Forest: implications for conservation. Biol Conserv 141:2184–2192CrossRefGoogle Scholar
  42. McAlpine CA, Bowen ME, Callaghan JG, Lunney D, Rhodes JR, Mitchell DL, Pullar DV, Poszingham HP (2006) Testing alternative models for the conservation of Koalas in fragmented rural–urban landscapes. Austral Ecol 31:529–544CrossRefGoogle Scholar
  43. Metzger JP, Martensen AC, Dixo M, Bernacci LC, Ribeiro MC, Teixeira AMG, Pardini R (2009) Time-lag in biological responses to landscape changes in a highly dynamic Atlantic forest region. Biol Conserv 142:1180–1191Google Scholar
  44. Michalski F, Peres CA (2005) Anthropogenic determinants of primate and carnivore local extinctions in a fragmented forest landscape of southern Amazonia. Biol Conserv 124:383–396CrossRefGoogle Scholar
  45. Miller B, Dugelby B, Foreman D, Del Rio CM, Noss R, Phillips M, Readding R, Soulé ME, Terborgh J, Willcox L (2001) The importance of large carnivores to healthy ecosystems. Endang Spec UPDATE 18:202–210Google Scholar
  46. Miotto RA, Pacheco FR, Ciocheti G, Galetti PM Jr (2007) Determination of the minimum population size of pumas (Puma concolor) through faecal DNA analysis in two protected cerrado areas in the Brazilian Southeast. Biotropica 39:647–654CrossRefGoogle Scholar
  47. Moreno RS, Kays RW, Samudio R Jr (2006) Competitive release in diets of ocelot (Leopardus pardalis) and puma (Puma concolor) after jaguar (Panthera onca) decline. J Mammal 84:808–816CrossRefGoogle Scholar
  48. Neteler M, Mitasova H (2008) Open Source GIS: a GRASS GIS approach. Springer, LLC, 3rd edn, p 406. Springer Science+Business Media, LCC, 233 Spring Street, New York, NY 10013, USAGoogle Scholar
  49. Oliveira TG, Cassaro K (1999) Guia de identificação dos felinos brasileiros, 2nd edn. Sociedade dos Zoológicos do Brasil, São Paulo, p 60Google Scholar
  50. Oliveira PS, Marquis RJ (2002) The cerrados os Brazil. Ecology and Natural history of a neotropical Savanna. Columbia University Press, New YorkGoogle Scholar
  51. R Development Core Team (2008) R: a language and environmental for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3- 900051-07-0. Available at <http://www.r-project.org>. Accessed 1 August 2009
  52. Rayfield B, Moilanen A, Fortin M-J (2009) Incorporating consumer-resource spatial interactions in reserve design. Ecol Modell 220:725–733CrossRefGoogle Scholar
  53. Ribeiro MC, Metzger JP, Ponzoni F, Martensen AC, Hirota M (2009) Brazilian Atlantic forest: how much is left and how the remaining forest is distributed? Implications for conservation. Biol Conserv 142:1141–1153CrossRefGoogle Scholar
  54. Ricketts TH (2001) The matrix matters: effective isolation in fragmented landscapes. Am Nat 158:87–99CrossRefPubMedGoogle Scholar
  55. Roque FO, Siqueira T, Bini LM, Ribeiro MC, Tambosi LR, Ciocheti G, Trivino-Strixino S Untangling chironomid taxon associations in Neotropical streams using local and landscape filters. Freshwater Biology (in press)Google Scholar
  56. Shida CN (2005) Evolução do uso da terras na região. In: Pivello VR, Varanda E (eds) O Cerrado Pé-de-Gigante. Parque Estadual de Vassununga—Ecologia e Conservação. Secretaria de Estado do Meio Ambiente, São Paulo, pp 30–42Google Scholar
  57. Smallwood KS, Fitzhugh EL (1995) A track count for estimating mountain lion Felis concolor californica population trend. Biol Conserv 71:251–259CrossRefGoogle Scholar
  58. Taylor PD, Fahrig L, Henein K, Merriam G (1993) Connectivity is a vital element of landscape structure. Oikos 68:571–573CrossRefGoogle Scholar
  59. Tigas LA, Van Vuren DH, Sauvajot RM (2002) Behavioral responses of bobcats and coyotes to habitat fragmentation and corridors in an urban environment. Biol Conserv 108:299–306CrossRefGoogle Scholar
  60. Uezu A, Metzger JP, Vielliard JM (2005) Effects of structural and functional connectivity and patch size on the abundance of seven Atlantic forest bird species. Biol Conserv 123:507–519CrossRefGoogle Scholar
  61. Uezu A, Beyer DD, Metzger JP (2008) Can agroforest woodlots work as stepping stones for birds in the Atlantic forest region? Biodiv Conserv 17:1907–1922CrossRefGoogle Scholar
  62. Umetsu F, Pardini R (2007) Small mammals in a mosaic of forest remnants and anthropogenic habitats—evaluating matrix quality in an Atlantic forest landscape. Landsc Ecol 22:517–530CrossRefGoogle Scholar
  63. Umetsu F, Metzger JP, Pardini R (2008) Importance of estimating matrix quality for modeling species distribution in complex tropical landscapes: a test with Atlantic forest small mammals. Ecography 31:359–370CrossRefGoogle Scholar
  64. Vandermeer J, Carvajal R (2001) Metapopulation dynamics and the quality of the matrix. Am Nat 158:211–220CrossRefPubMedGoogle Scholar
  65. Wang E (2002) Diets of acelots, margays and oncillas in the Atlantic rainforest in southeast Brazil. Stud Neotrop Faun Environ 37(3):207–212CrossRefGoogle Scholar
  66. Wagner HH, Fortin MJ (2005) Spatial analysis of landscape: concepts and statistics. Ecology 86:1975–1987CrossRefGoogle Scholar
  67. Walz U (2008) Monitoring landscape change and functions in Saxony (Eastern Germany)—methods and indicators. Ecol Indic (2008). doi: 10.1016/j.ecolind.2006.12.002
  68. Williams PH, Margules CR, Wilbert DW (2002) Data requirements and data sources for biodiversity priority area selection. Journal of Bioscience 27:327–338CrossRefGoogle Scholar
  69. Zaccarelli N, Riiters KH, Petrosillo I, Zurlini G (2008) Indicating disturbance contend and context for preserved areas. Ecol Indic (2008). doi: 10.1016/j.ecolind.2007.01.010
  70. Zurlini G, Girardin P (2008) Introduction of the special issue on “Ecological Indicators at multiple scales”. Ecol Indic (2008), doi. 10.1016/j.ecolind.2007.12.003
  71. Zuur AG, Ieno EN, Walker NJ, Savaliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with r. Springer, New York, USA, p 574CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Maria Carolina Lyra-Jorge
    • 1
  • Milton Cezar Ribeiro
    • 1
  • Giordano Ciocheti
    • 1
  • Leandro Reverberi Tambosi
    • 1
  • Vânia Regina Pivello
    • 1
  1. 1.Departamento de EcologiaUniversidade de São PauloSão PauloBrazil

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