Advertisement

Mammalian Biology

, Volume 99, Issue 1, pp 19–26 | Cite as

Implications of an agricultural mosaic in small mammal communities

  • Marina Falcão RodriguesEmail author
  • Maria Adélia B. de Oliveira
  • Martín Alejandro Montes
Original investigation

abstract

The ideas that larger fragments have greater species richness and abundance, when compared to smaller fragments and altered environments, and that assemblage composition is different, was tested in an agricultural mosaic using data on small mammals. To achieve this, we sampled ten forest fragments of different sizes, small and large, as well as five areas in a sugarcane matrix, through the capture-mark-recapture method. The study was conducted in a sugarcane plantation (Usina São José, Igarassu, Pernambuco, Brazil) from January to October 2016. There was a significant difference when comparing richness between small fragments (eight species) and the sugarcane matrix (four species). Abundance differed significantly between all areas, being influenced by fragment size and habitat type. We found that abundance was positively influenced by forested environments and, among them, larger fragments. The composition of assemblages in the forest fragments and the sugarcane matrix differed clearly for NMDS, MANOVA and SIMPER analyses. Between the habitats, assemblage parameters were also distinct. Lower abundance and richness were found in the sugarcane matrix, where the presence of rodents was associated with food availability and less competition; and higher abundance and richness was measured in forest fragments, where there was a strong association between marsupials and forest strata. The landscape configuration in an agricultural mosaic can compromise the level of interspecific interactions of small mammals, which negatively impacts the ecological processes of forested areas. In this case, the conservation of a matrix permeable to most species and the preservation of all fragments are necessary, since small and large fragments have different functions in the maintenance of species.

Keywords

Atlantic Forest Sugarcane Richness Abundance Composition and assemblage 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alvares, C.A., Stape, J.L., Sentelhas, P.C., de Moraes Goncalves, J.L., Sparovek, G., 2013. Köppen’s climate classification map for Brazil. Meteorol. Z. 22 (6), 711–728,  https://doi.org/10.1127/0941-2948/2013/0507.CrossRefGoogle Scholar
  2. Asfora, P.H., Mendes Pontes, A.R., 2009. The small mammals of the highly impacted North-eastern Atlantic Forest of Brazil, Pernambuco Endemism Center. Biota Neotrop. 9 (1), 31–35,  https://doi.org/10.1590/S1676-06032009000100004.CrossRefGoogle Scholar
  3. Benedek, A.M., Sirbu, I., 2018. Responses of small mammal communities to environment and agriculture in a rural mosaic landscape. Mammal. Biol. 90, 55–65,  https://doi.org/10.1016/j.mambio.2018.02.008.CrossRefGoogle Scholar
  4. Bonecker, S.T., Portugal, G.L., Costa-Neto, S.F., Gentile, R., 2009. A long term study of small mammal populations in a Brazilian agricultural landscape. Mammal. Biol. 74 (6), 467–477,  https://doi.org/10.1016/j.mambio.2009.05.010.CrossRefGoogle Scholar
  5. Bonvicino, C.R., Lindbergh, S.M., Maroja, L.S., 2002. Small non-flying mammals from conserved and altered areas of Atlantic Forest and Cerrado: comments on their potential use for monitoring environment. Braz. J. Biol. 62 (4B), 765–774,  https://doi.org/10.1590/S1519-69842002000500005.PubMedCrossRefGoogle Scholar
  6. Butler, R.A., Laurance, W.F., 2008. New strategies for conserving tropical forests. Trends Ecol. Evol. 23 (9), 469–472,  https://doi.org/10.1016/j.tree.2008.05.006.PubMedCrossRefGoogle Scholar
  7. Brito, D., 2009. Análise de viabilidade de populações: uma ferramenta para a conservação da biodiversidade no Brasil. Oecologia Bras. 13 (3), 452–469,  https://doi.org/10.4257/oeco.2009.1303.04.CrossRefGoogle Scholar
  8. Cáceres, N.C., Monteiro-Filho, E.L.A., 2007. Germination in seed species ingested by opossums: implications for seed dispersal and forest conservation. Braz. Arch. Biol. Technol. 50 (6), 921–928.CrossRefGoogle Scholar
  9. Cáceres, N.C., Weber, M.M., Melo, G.L., Meloro, C., Sponchiado, J., Carvalho, R.S., et al., 2016. Which factors determine spatial segregation in the South American opossums (Didelphis aurita and D. albiventris)? An ecological niche modelling and geometric morphometrics approach. PLoS ONE 11 (6), 1–19,  https://doi.org/10.1371/journal.pone.0157723.Google Scholar
  10. Castro, E.B.V., Fernandez, F.A.S., 2004. Determinants of differential extinction vulnerabilities of small mammals in Atlantic forest fragments in Brazil. Biol. Conserv. 119 (1), 73–80,  https://doi.org/10.1016/j.biocon.2003.10.023.CrossRefGoogle Scholar
  11. Costa, L.P., Leite, Y.L.R., Fonseca, G.A.B., Fonseca, M.T., 2000. Biogeography of South American Forest Mammals: endemism and diversity in the Atlantic Forest. Biotropica 32 (4b), 872–881,  https://doi.org/10.1646/0006-3606(2000)032[0872:BOSAFM]2.0.CO;2.CrossRefGoogle Scholar
  12. Dantas-Torres, F., Aléssio, F.M., Siqueira, D.B., Mauffrey, J.F., Marvulo, M.F.V., Martins, T.F., Moraes-Filho, J., Camargo, M.C.G.O., D’Auria, S.R.N., Labruna, M.B., Silva, J.C.R., 2012. Exposure of small mammals to ticks and rickettsiae in Atlantic Forest patches in the metropolitan area of Recife, North-eastern Brazil. Parasitology 139 (1), 83–91,  https://doi.org/10.1017/S0031182011001740.PubMedCrossRefPubMedCentralGoogle Scholar
  13. Dunn, R.R., 2004. Recovery of faunal communities during tropical forest regeneration. Conserv. Biol. 18 (2), 302–309 (Accessed 12 August 2016) https://www.jstor.org/stable/3589207.CrossRefGoogle Scholar
  14. Dixon, M., Metzger, J.P., Morgante, J.S., Zamudio, K.R., 2009. Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian Atlantic Coastal Forest. Biol. Conserv. 142 (8), 1560–1569,  https://doi.org/10.1016/j.biocon.2008.11.016.CrossRefGoogle Scholar
  15. Estavillo, C., Pardini, R., Rocha, P.L.B., 2013. Forest loss and the biodiversity threshold: an evaluation considering species habitat requirements and the use of matrix habitats. PLoS One 8 (12), 1–10,  https://doi.org/10.1371/journal.pone.0082369.CrossRefGoogle Scholar
  16. Estrada, A., Garber, P.A., Rylands, A.B., Roos, C., Fernandez-Duque, E., et al., 2017. Impending extinction crisis of the world’s primates: why primates matter. Sci. Adv. 3 (1), 1–16,  https://doi.org/10.1126/sciadv.1600946.CrossRefGoogle Scholar
  17. Fahrig, L., Baudry, J., Brotons, L., Burel, F.G., Crist, T.O., Fuller, R.J., Sirami, C., Siriwardena, G.M., Martin, J.L., 2011. Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol. Lett. 14 (2), 101–112,  https://doi.org/10.1111/j.1461-0248.2010.01559.x.PubMedCrossRefGoogle Scholar
  18. Flinday, C.S., Houlahan, J., 1997. Anthropogenic correlates of species richness in Southeastern Ontario wetlands. Conserv. Biol. 11, 1000–1009.CrossRefGoogle Scholar
  19. Fonseca, G.A.B., Robinson, J.G., 1990. Forest size and structure: competitive and predatory effects on small mammal communities. Biol. Conserv. 53, 265–294.CrossRefGoogle Scholar
  20. Gardner, A.L., 2007. Mammals of South America, Volume 1 - Marsupials, Xenarthrans, Shrews, and Bats. The University of Chicago Press Chicago and London, London.Google Scholar
  21. Gascon, C., Lovejoy, T.E., Bierregaard Jr., R.O., Lovejoy, T.E., Malcolm, J.R., 1999. Matrix habitat and species richness in tropical forest remnants. Biol. Conserv. 91 (2–3), 223–229,  https://doi.org/10.1016/S0006-3207(99)00080-4.CrossRefGoogle Scholar
  22. Geist, H.J., Lambin, E.F., 2002. Underlying Driving Forces of Tropical Deforestation: tropical forests are disappearing as the result of many pressures, both local and regional, acting in various combinations in different geographical locations. BioScience 52 (2), 143–150,  https://doi.org/10.1641/0006-3568(2002)052[0143:PCAUDF]2.0.CO;2.CrossRefGoogle Scholar
  23. Gheler-Costa, C., Vettorazzi, C.A., Pardini, R., Verdade, L.M., 2012. The distribution and abundance of small mammals in agroecosystems of southeastern Brazil. Mammalia 76, 185–191,  https://doi.org/10.1515/mammalia-2011-0109.CrossRefGoogle Scholar
  24. Hammer, Ø., Harpper, D.A.T., Ryan, D., 2001. PAST: (1999) paleontological statistics software package for education and data analysis. Palaeontol. Electron. (Accessed 23 October 2016) https://palaeo-electronica.org/20011/past/past.pdf.Google Scholar
  25. Hass, Al., Kormann, U.G., Tscharntke, T., Clough, Y., Baillod, A.B., Sirami, C., Fahrig, L., Martin, J.L., Baudry, J., Bertrand, C., Bosch, J., Brotons, L., Burel, F., Georges, R., Giralt, D., Marcos-García, M.A., Ricarte, A., Siriwardena, G., Batáry, P., 2018. Landscape configurational heterogeneity by small-scale agriculture, not crop diversity, maintains pollinators and plant reproduction in western Europe. Proc. R. Soc. B Biol. Sci. 285 (1872), 1–10,  https://doi.org/10.1098/rspb.2017.2242.CrossRefGoogle Scholar
  26. Heroldová, M., Bryja, J., Zejda, J., Tkadlec, E., 2007. Structure and diversity of small mammal communities in agriculture landscape. Agric. Ecosyst. Environ. 120 (2-4), 206–210,  https://doi.org/10.1016/j.agee.2006.09.007.CrossRefGoogle Scholar
  27. Holland, G.J., Bennett, J.F., 2007. Occurrence of small mammals in a fragmented landscape: the role of vegetation heterogeneity. Wildl. Res. 34 (5), 387–397,  https://doi.org/10.1071/WR07061.CrossRefGoogle Scholar
  28. Jordano, P., Galetti, M., Pizo, M.A., Silva, W.R., 2006. Ligando Frugivoria e Dispersão de Sementes à Biologia da Conservação (Accessed 12 June 2016) https://www.researchgate.net/publication/230801935_Ligando_Frugivoria_e_Dispersao_de_Sementes_a_Biologia_da_Conservacao.Google Scholar
  29. Jullien, M., Thiollay, J.M., 1996. Effect of rainforest disturbance and fragmentation: comparative changes of raptor community along natural and human-made gradients in French Guiana. J. Biogeogr. 34, 387–397,  https://doi.org/10.1046/j.1365-2699.1996.00963.x.Google Scholar
  30. Laurance, W.F., 1994. Rain forest fragmentation and the structure of small mammal communities intropical Queensland. Biol. Conserv. 69 (1), 23–32,  https://doi.org/10.1016/0006-3207(94)90325-5.CrossRefGoogle Scholar
  31. Laurance, W.F., Ferreira, L.Y., Merona, J.R., Laurance, S.G., 1998. Rain forest fragmentation and the dynamics of Amazonian tree communities. Ecology 79, 2032–2040,  https://doi.org/10.1890/0012-9658(1998)079[2032:RFFATD]2.0.CO;2.CrossRefGoogle Scholar
  32. Laurance, W.F., Vasconcelos, H.L., 2009. Conseqüências ecológicas da fragmentação florestal na Amazônia. Oecologia Bras. 13 (3), 434–451,  https://doi.org/10.4257/oeco.2009.1303.03.CrossRefGoogle Scholar
  33. Laurance, W.F., 2010. Habitat destruction: death by a thousand cuts. In: Shodi, N.S., Ehrlich, P.R. (Eds.), Conservation Biology for All. Oxford University Press, pp. 73–87.CrossRefGoogle Scholar
  34. Lins e Silva, A.C.B., 2010. Influência da área e da heterogeneidade de habitats na diversidade vegetal em fragmentos de floresta atlântica (Accessed 10 August 2015) http://livros01.livrosgratis.com.br/cp140629.pdf.Google Scholar
  35. Luza, A.L., Gonçalves, G.L., Pillar, V.D., Hartz, S.M., 2016. Processes related to habitat selection, diversity and niche similarity in assemblages of non-volant small mammals at grassland-forest ecotones. Braz. J. Nat. Conserv. 14 (2), 88–98,  https://doi.org/10.1016/j.ncon.2016.09.003.CrossRefGoogle Scholar
  36. Read, J.L., Moseby, K.E., 2001. Factors affecting pitfall capture rates of small ground vertebrates in arid South Australia. I. The influence of weather and moon phase on capture rates of reptiles. Wildl. Res. 28 (1), 53–60,  https://doi.org/10.1071/WR99057.Google Scholar
  37. Nagendra, H., Munroeb, D.K., Southworth, J., 2004. From pattern to process: landscape fragmentation and the analysis of land use/land cover change. Agric. Ecosyst. Environ. 101 (2-3), 111–115,  https://doi.org/10.1016/j.agee.2003.09.003.CrossRefGoogle Scholar
  38. Nupp, E.T., Swihart, R.T.K., 2000. Landscape-level correlates of small-mammal assemblages in forest fragments of farmland. J. Mammal. 81 (2), 512–526,  https://doi.org/10.1644/1545-1542(2000)081<0512:LLCOSM>2.0.CO;2.CrossRefGoogle Scholar
  39. OECD/Fao, 2015. Perspectivas Agrícolas no Brasil: desafios daagriculturabrasileira. IOP Publishing Physics Web (Accessed 4 September 2017) www.agri-outlook.orgGoogle Scholar
  40. Oliveira, F.F., Langguth, A., 2004. Pequenos mamíferos (Didelphimorphia e Rodentia) de Paraíba e Pernambuco, Brasil. Rev. Nord. Biol. 18 (2), 19–86.Google Scholar
  41. Paglia, A.P., Fonseca, G.A.B.D.A., Rylands, A.B., Herrmann, G., Aguiar, L.M.S., Chiarello, A.G., et al., 2012. Lista Anotada dos Mamíferos do Brasil / Annotated Check list of Brazilian Mammals, 2aedição/ 2nd edition. Occasional Papers in Conservation Biology, No. 6. Conservation International, Arlington.Google Scholar
  42. Pardini, R., 2004. Effects of forest fragmentation on small mammals in an Atlantic Forest landscape. Biodivers. Conserv. 13, 2567–2586.CrossRefGoogle Scholar
  43. Pardini, R., Souza, S.M., Braga-Neto, R., Metzger, J.P., 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 (2), 253–266,  https://doi.org/10.1016/j.biocon.2005.01.033.CrossRefGoogle Scholar
  44. Patton, J.L., Pardiñas, U.F.J., D’Elía, G., 2015. Mammals of South America, Volume 2 - Rodents. The University of Chicago Press Chicago and London, London.CrossRefGoogle Scholar
  45. Ranganathan, J., Ranjit Daniels, R.J., Chandran, M.D.S., Ehrlicha, P.R., Dailya, G.C., 2008. Sustaining biodiversity in ancient tropical countryside. PNAS 105 (46), 17852–17854,  https://doi.org/10.1073/pnas.0808874105.PubMedCrossRefGoogle Scholar
  46. Rappole, J.H., Morton, E.S., 1985. Effects of habitat alteration on atropical avian forest community. Ornithol. Monogr. 36, 1013–1021,  https://doi.org/10.2307/40168333.CrossRefGoogle Scholar
  47. Remsen, J.V., Parker, T.A., 1983. Contribution of river-created habitats to bird species richness in Amazonia. Biotropica 15 (3), 223–231,  https://doi.org/10.2307/2387833.CrossRefGoogle Scholar
  48. Ribeiro, M.C., Martensen, A.C., Metzger, J.P., Ponzoni, F.J., Hirota, M.M., 2009. The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142 (6), 1141–1153,  https://doi.org/10.1016/j.biocon.2009.02.021.CrossRefGoogle Scholar
  49. Ribeiro, M.C., Martensen, A.C., Metzger, J.P., Tabarelli, M., Scarano, F., Fortin, M.J., 2011. The Brazilian Atlantic Forest: a shrinking biodiversity hotspot. In: Zachos, F.E., Habel, J.C. (Eds.), Biodiversity Hotspots.,  https://doi.org/10.1007/978-3-642-20992-5_21.Google Scholar
  50. Rocha-Mendes, F., Mikich, S.B., Quadros, J., Pedro, W.A., 2010. Feeding ecology of carnivores (Mammalia, Carnivora) in Atlantic Forest remnants, Southern Brazil. Biota Neotrop. 10 (4), 21–30.CrossRefGoogle Scholar
  51. Sanchez-Cordero, V., Martinez-Gallargo, R., 1998. Post dispersal fruit and seed removal by forest-dwelling rodents in a lowland rainforest in Mexico. J. Trop. Ecol. 14 (2), 139–151,  https://doi.org/10.1017/S0266467498000121.CrossRefGoogle Scholar
  52. Santos, J.P., Steinke, V.A., García-Zapata, M.T.A., 2016. Espaço e doença: mudanças antrópicas e a hantavirose / environment and disease: anthropic changes and hantavírus. Hygeia 12 (22), 62–71.Google Scholar
  53. São José Agroindustrial, IOP Publishing Physics Web. http://www.usinasaojose.com.br/pt/usina/institucional. (Acessed 13 April 2016) 2017. A Usina.Google Scholar
  54. Silva, H.C.H., Lins e Silva, A.C.B., Gomes, J.S., Rodal, M.J.N., 2008. The effect of internal and external edges on vegetation physiognomy and structure in a remnant of Atlantic lowland rainforest in Brazil. Biorem. Biodiv. Bioavail. 2 (1), 47–55.Google Scholar
  55. Silva, M.F.A., Dissertation 2015. Influência do relevo na fragmentação e estrutura da vegetação na Floresta Atlântica, sub-região Pernambuco. University Federal Rural of Pernambuco.Google Scholar
  56. Silveira, L.F., Olmos, F., Long, A.J., 2003. Birds in Atlantic Forest fragments in north-east Brazil. Cotinga 20, 32–46 (Acessed 20 June 2017) http://www.ib.usp.br/~lfsilveira/pdf/a_2003_birdsnortheastbrazil.pdf.Google Scholar
  57. SOS Mata Atlântica and INPE, 2018. Atlas dos remanescentes florestais da Mata Atlântica mapeamento dos sistemas costeiros (Acessed 10 November 2018) http://mapas.sosma.org.br/site_media/download/SOSMA_Atlas-da-Costa_Final.pdf.Google Scholar
  58. Stoate, C., Báldi, A., Beja, P., Boatman, N.D., Herzon, I., Van Doorn, A., Snoo, G.R., Rakosy, L., Ramwell, C., 2009. Ecological impacts of early 21st century agricultural change in Europe - a review. J. Environ. Manage. 91 (1), 22–46,  https://doi.org/10.1016/jjenvman.2009.07.005.PubMedCrossRefPubMedCentralGoogle Scholar
  59. Tabarelli, M., Pinto, L.P., Silva, J.M.C., Hirota, M.M., Bedê, L.C., 2005. Desafios e oportunidades para a Conservação da biodiversidade na Mata Atlântica brasileira. Megadiversidade 1 (1), 132–138.Google Scholar
  60. Turner, I.M., Corllet, R.T., 1996. The conservation value of small, isolated fragments of low land tropical rainforest. Trends Ecol Evol. 11 (8), 330–333.PubMedCrossRefPubMedCentralGoogle Scholar
  61. Uezu, A., Metzger, J.P., Vielliard, J.M.E., 2005. Effects of structural and functional connectivity and patch size on the abundance of seven Atlantic Forest bird species. Biol. Conserv. 123 (4), 507–519,  https://doi.org/10.1016/j.biocon.2005.01.001.CrossRefGoogle 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 (4), 517–530.CrossRefGoogle Scholar
  63. Veloso, H.P., Góes-Filho, L., 1982. Classificação fisionômico-ecológica da vegetação neotropical. Boletins técnicos. Projeto Radambrasil 7.Google Scholar
  64. Verdade, L.M., Gheler-Costa, C., Penteado, M., Dotta, G., 2012. The impacts of sugarcane expansion on wildlife in the state of São Paulo, Brazil. J. Sustain. Bioenergy Syst. 2 (4), 138–144,  https://doi.org/10.4236/jsbs.2012.24020.Google Scholar
  65. Vieira, E.M., Monteiro-Filho, E.L.A., 2003. Vertical stratification of small mammals in the Atlantic rain forest of southeastern Brazil. J. Trop. Ecol. 19 (05), 501–507,  https://doi.org/10.1017/S0266467403003559.CrossRefGoogle Scholar
  66. Vivian-Smith, G., 1997. Microtopographic heterogeneity and floristic diversity in experimental wetland communities. J. Ecol. 85 (1), 71–82.CrossRefGoogle Scholar
  67. Wijesinghe, M.R., Brooke’s, M.D., 2005. Impact of habitat disturbance on the distribution of endemic species of small mammals and birds in a tropical rain forest in Sri Lanka. J. Trop. Ecol. 21, 661–668.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2019

Authors and Affiliations

  • Marina Falcão Rodrigues
    • 1
    Email author
  • Maria Adélia B. de Oliveira
    • 2
  • Martín Alejandro Montes
    • 3
  1. 1.Graduation Program in Ecology, Biology DepartmentFederal Rural University of PernambucoRecife/PernambucoBrazil
  2. 2.Laboratory of Ecophysiology and Animal Behavior, Department of Animal Morphology and PhysiologyFederal Rural University of PernambucoBrazil
  3. 3.Laboratory of Genetics, Department of BiologyFederal Rural University of PernambucoBrazil

Personalised recommendations