Small mammals and microhabitat selection in forest fragments in the transition zone between Atlantic Forest and Pampa biome
DOI:
https://doi.org/10.11606/1807-0205/2022.62.039Keywords:
Habitat use, Rodent, Marsupial, Community ecology, Vegetation StructureAbstract
Natural resources are depleted in fragmented landscapes that have their vegetation also altered. As a result, the microhabitat diversity and the composition and distribution of local species are affected. In this study, we evaluated the small mammals' community diversity, composition and microhabitat selection in two Atlantic Forest fragments, in an ecotone area with the Pampa biome, southern Brazil. We recorded five rodents (Akodon montensis, Oligoryzomys nigripes, Sooretamys angouya, Juliomys pictipes and the exotic Rattus rattus) and one marsupial (Didelphis albiventris). Both fragments were dominated by the generalist rodent A. montensis. Akodon montensis and O. nigripes showed similar habitat preferences: ground covered by rocks and higher values of vegetation obstruction. Sooretamys angouya preferred places with higher abundance of trees. Fruit availability was important for A. montensis and D. albiventris, highlighting the importance of this food resource for local wildlife, and the potential role of these species as seed predators and dispersers. Small species richness, the presence of an exotic species and high dominance level suggest that the study area is highly degraded.
Downloads
References
Abreu, M.S.L. & Oliveira, L.R. 2014. Patterns of arboreal and terrestrial space use by non-volant small mammals in an Araucaria forest of Southern Brazil. Anais da Academia Brasileira de Ciências, 86(2): 807-819. https://doi.org/10.1590/0001-3765201420130063.
Akers, A.A.; Islam, M.A. & Nijman, V. 2013. Habitat characterization of western hoolock gibbons Hoolock hoolock by examining home range microhabitat use. Primates, 54(4): 341-348. https://doi.org/10.1007/s10329-013-0352-8.
Almeida-Gomes, M. & Rocha, C.F.D. 2014. Landscape connectivity may explain anuran species distribution in an Atlantic forest fragmented area. Landscape Ecology, 29(1): 29-40. https://doi.org/10.1007/s10980-013-9898-5.
Almeida-Gomes, M.; Vieira, M.V.; Rocha, C.F.D. & Melo, A.S. 2019. Habitat amount drives the functional diversity and nestedness of anuran communities in an Atlantic Forest fragmented landscape. Biotropica, 51(6): 874-884. https://doi.org/10.1111/btp.12687.
Antunes, P.C.; Campos, M.A.A.; Oliveira-Santos, L.G.R. & Graipel, M.E. 2010. Population dynamics of Akodon montensis (Rodentia, Cricetidae) in the Atlantic forest of Southern Brazil. Mammalian Biology, 75(2): 186-190. https://doi.org/10.1016/j.mambio.2009.03.016.
Antunes, P.C.; Campos, M.A.A.; Oliveira-Santos, L.G.R. & Graipel, M.E. 2009. Population dynamics of Euryoryzomys russatus and Oligoryzomys nigripes (Rodentia, Cricetidae) in an Atlantic forest area, Santa Catarina Island, Southern Brazil. Biotemas, 22(2): 143-151. https://doi.org/10.5007/2175-7925.2009v22n2p143.
Bajaru, S.B.; Kulavmode, A.R. & Manakadan, R. 2019. Influence of microhabitat and landscape-scale factors on the richness and occupancy of small mammals in the northern Western Ghats: A multi-species occupancy modeling approach. Mammalian Biology, 99(1): 88-96. https://doi.org/10.1016/j.mambio.2019.10.003.
Barton, K. 2018. MuMIn: Multi-Model Inference. R package Version 1.42.1. https://cran.rproject.org/web/packages/MuMIn/index.html.
Bianchi, R.D.C.; Mendes, S.L. & Júnior, P.D.M. 2010. Food habits of the ocelot, Leopardus pardalis, in two areas in southeast Brazil. Studies on Neotropical Fauna and Environment, 45(3): 111-119. https://doi.org/10.1080/01650521.2010.514791.
Bonvicino, C.R.; Oliveira, J.D. & D'Andrea, P.S. 2008. Guia dos roedores do Brasil, com chaves para gêneros baseadas em caracteres externos. Rio de Janeiro, Ventro Pan-Americano de Febre Aftosa/OPAS/OMS. 122p. (Série de Manuais Técnicos; 11).
Bregman, T.P.; Sekercioglu, C.H. & Tobias, J.A. 2014. Global patterns and predictors of bird species responses to forest fragmentation: implications for ecosystem function and conservation. Biological Conservation, 169: 372-383. https://doi.org/10.1016/j.biocon.2013.11.024.
Bricker, M.; Pearson, D. & Maron, J. 2010. Small‐mammal seed predation limits the recruitment and abundance of two perennial grassland forbs. Ecology, 91(1): 85-92. https://doi.org/10.1890/08-1773.1.
Brito, D.; Oliveira, L.C.; Oprea, M. & Mello, M.A. 2009. An overview of Brazilian mammalogy: trends, biases and future directions. Zoologia, Curitiba, 26(1): 67-73. https://doi.org/10.1590/S1984-46702009000100011.
Burnham, K.P. & Anderson, D.R. 2002. Model Selection and Multimodel Inference. A Practical Information-Theoretic Approach. 2. ed. Heidelberg, Springer-Verlag.
Cáceres, N.C. 2002. Food habits and seed dispersal by the white-eared opossum, Didelphis albiventris, in southern Brazil. Studies on Neotropical Fauna and Environment, 37(2): 97-104. https://doi.org/10.1076/snfe.37.2.97.8582.
Cáceres, N.C. 2006. O papel dos marsupiais na dispersão de sementes. In: Cáceres, N.C. & Monteiro-Filho, E.L.A. (Eds.). Os marsupiais do Brasil – Biologia, Ecologia e Evolução. Campo Grande, Editora UFMS. p. 255-269.
Cáceres, N.C.; Dittrich, V.A.O. & Monteiro-Filho, E.L.A. 1999. Fruit consumption, distance of seed dispersal and germination of Solanaceous plants ingested by the common opossum (Didelphis aurita) in Southern Brazil. Revue d'écologie, La Terre et la Vie, 54(3): 225-234.
Camargo, N.F.D.; Sano, N.Y. & Vieira, E.M. 2018. Forest vertical complexity affects alpha and beta diversity of small mammals. Journal of Mammalogy, 99(6): 1444-1454. https://doi.org/10.1093/jmammal/gyy136.
Cantor, M.; Ferreira, L.A.; Silva, W.A. & Setz, E.Z.F. 2010. Potential seed dispersal by Didelphis albiventris (Marsupialia, Didelphidae) in highly disturbed environment. Biota Neotropica, 10(2): 45-51. https://doi.org/10.1590/S1676-06032010000200004.
Castro, E.B.V. & Fernandez, F.A.S. 2004. Determinants of differential extinction vulnerabilities of small mammals in Atlantic forest fragments in Brazil. Biological Conservation, 119: 73-80. https://doi.org/10.1016/j.biocon.2003.10.023.
Chazdon, R.L. 2003. Tropical forest recovery: legacies of human impact and natural disturbances. Perspectives in Plant Ecology, Evolution and Systematics, 6: 51-71. https://doi.org/10.1078/1433-8319-00042.
Corrêa, M.R.; Bellagamba, Y.M.; de Magalhães, A.P.; Martins, J.P.; Cruz, A.J.D.R.; Kozovitz, A.R.; Messias, M.C.T.B. & de Azevedo, C.S. 2018. Microhabitat structure and food availability modelling a small mammal assemblage in restored riparian forest remnants. Mammalia, 82(4): 315-327. https://doi.org/10.1515/mammalia-2017-0026.
Dalmaschio, J. & Passamani, M. 2003. Aspectos da ecologia de Marmosa murina (Linnaeus, 1758) (Mammalia, Didelphimorphia), em uma região de Mata Atlântica no estado do Espírito Santo. Biotemas, 16(2): 145-158. https://doi.org/10.5007/%25x.
Delciellos, A.C.; Barros, C.D.S.D.; Prevedello, J.A.; Ferreira, M.S.; Cerqueira, R. & Vieira, M.V. 2018. Habitat fragmentation affects individual condition: evidence from small mammals of the Brazilian Atlantic Forest. Journal of Mammalogy, 99(4): 936-945. https://doi.org/10.1093/jmammal/gyy078.
Delciellos, A.C.; Vieira, M.V.; Grelle, C.E.V.; Cobra, P. & Cerqueira, R. 2016. Habitat quality versus spatial variables as determinants of small mammal assemblages in Atlantic Forest fragments. Journal of Mammalogy, 97(1): 253-265. https://doi.org/10.1093/jmammal/gyv175.
Filgueiras, B.K.; Melo, D.H.; Andersen, A.N.; Tabarelli, M. & Leal, I.R. 2019. Cross-taxon congruence in insect responses to fragmentation of Brazilian Atlantic forest. Ecological Indicators, 98: 523-530. https://doi.org/10.1016/j.ecolind.2018.11.036.
Freitas, S.R.; Cerqueira, R. & Vieira, M.V. 2002. A device and standard variables to describe microhabitat structure of small mammals based on plant cover. Brazilian Journal of Biology, 62(4b): 795-800. https://doi.org/10.1590/S1519-69842002000500008.
Galiano, D.; Kubiak, B.B.; Marinho, J.R. & de Freitas, T.R.O. 2013. Population dynamics of Akodon montensis and Oligoryzomys nigripes in an Araucaria forest of southern Brazil. Mammalia, 77(2): 173-179. https://doi.org/10.1515/mammalia-2011-0128.
Grenha, V.; Macedo, M.V.; Pires, A.S. & Monteiro, R.F. 2010. The role of Cerradomys subflavus (Rodentia, Cricetidae) as seed predator and disperser of the palm Allagoptera arenaria. Mastozoología Neotropopical, 17(1): 61-68.
Hair, J.F.; Black, W.C.; Babin, B.J. & Anderson, R.E. 2010. Multivariate data analysis. 7 ed. New Jersey, Prentice Hall.
Hodara, K. & Busch, M. 2010. Patterns of macro and microhabitat use of two rodent species in relation to agricultural practices. Ecological Research, 25(1): 113-121. https://doi.org/10.1007/s11284-009-0638-x.
Kaunisto, S.; Kortet, R.; Härkönen, S.; Kaitala, A.; Laaksonen, S. & Ylönen, H. 2012. Do small mammals prey upon an invasive ectoparasite of cervids? Canadian Journal of Zoology, 90(8): 1044-1050. https://doi.org/10.1139/z2012-072.
Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxton, S.; Cooper, A.; Markowitz, S.; Duran, C.; Thierer, T.; Ashton, B.; Meintjes, P. & Drummond, A. 2012. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12): 1647-1649. https://doi.org/10.1093/bioinformatics/bts199.
Kuinchtner, A. & Buriol, G.A. 2001. Clima do Estado do Rio Grande do Sul segundo a classificação climática de Köppen e Thornthwaite. Disciplinarum Scientia – Ciencias Naturais e Tecnológicas, 2(1): 171-182.
Law, B.; Chidel, M.; Britton, A. & Threlfall, C. 2018. Comparison of microhabitat use in young regrowth and unlogged forest by the eastern pygmy-possum (Cercartetus nanus). Australian Mammalogy, 40(1): 1-9. https://doi.org/10.1071/AM16041.
Leal, I.R.; Filgueiras, B.K.; Gomes, J.P.; Iannuzzi, L. & Andersen, A.N. 2012. Effects of habitat fragmentation on ant richness and functional composition in Brazilian Atlantic forest. Biodiversity and Conservation, 21(7): 1687-1701. https://doi.org/10.1007/s10531-012-0271-9.
Leitman, P.; Amorim, A.M.; Sansevero, J.B. & Forzza, R.C. 2015. Floristic patterns of epiphytes in the Brazilian Atlantic Forest, a biodiversity hotspot. Botanical Journal of the Linnean Society, 179(4): 587-601. https://doi.org/10.1111/boj.12342.
Lima, D.O.D.; Azambuja, B.O.; Camilotti, V.L. & Cáceres, N.C. 2010. Small mammal community structure and microhabitat use in the austral boundary of the Atlantic Forest, Brazil. Zoologia, Curitiba, 27: 99-105. https://doi.org/10.1590/S1984-46702010000100015.
Lira, P.K.; Tambosi, L.R.; Ewers, R.M. & Metzger, J.P. 2012. Land-use and land-cover change in Atlantic Forest landscapes. Forest Ecology and Management, 278: 80-89. https://doi.org/10.1016/j.foreco.2012.05.008.
Lôbo, D.; Leão, T.; Melo, F.P.; Santos, A.M. & Tabarelli, M. 2011. Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Diversity and Distribution, 17(2): 287-296. https://doi.org/10.1111/j.1472-4642.2010.00739.x.
Maestri, R.; Galiano, D.; Kubiak, B.B. & Marinho, J.R. 2014. Diversity of small land mammals in a subtropical Atlantic forest in the western region of the state of Santa Catarina, southern Brazil. Biota Neotropica, 14(4): 1-7. https://doi.org/10.1590/1676-06032014012914.
Matthews, T.J.; Cottee‐Jones, H.E. & Whittaker, R.J. 2014. Habitat fragmentation and the species-area relationship: a focus on total species richness obscures the impact of habitat loss on habitat specialists. Diversity and Distribution, 20(10): 1136-1146. https://doi.org/10.1111/ddi.12227.
Melo, G.L.; Miotto, B.; Peres, B. & Caceres, N.C. 2013. Microhabitat of small mammals at ground and understorey levels in a deciduous, southern Atlantic Forest. Anais da Academia Brasileira de Ciências, 85(2): 727-736. https://doi.org/10.1590/S0001-37652013000200017.
Melo, G.L.; Sponchiado, J.; Machado, A.F. & Cáceres, N.C. 2011. Small-mammal community structure in a South American deciduous Atlantic Forest. Community Ecology, 12(1): 58-66. https://doi.org/10.1556/comec.12.2011.1.8.
Morris, D.W. 1987. Ecological scales and habitat use. Ecology, 68(2): 362-369. https://doi.org/10.2307/1939267.
Paglia, A.P.; Fonseca, G.A.B. da.; Rylands, A.B.; Herrmann, G.; Aguiar, L.M.S.; Chiarello, A.G.; Leite, Y.L.R.; Costa, L.P.; Siciliano, S.; Kierulff, M.C.M.; Mendes, S.L.; Tavares, V. da. C.; Mittermeier, R.A. & Patton, J.L. 2012. Lista Anotada dos Mamíferos do Brasil/Annotated Checklist of Brazilian Mammals. 2. ed. Arlington, VA.,Conservation International, 76p. (Occasional Papers in Conservation Biology, No. 6).
Pardini, R. 2004. Effects of forest fragmentation on small mammals in an Atlantic Forest landscape. Biodiversity and Conservation, 13(13): 2567-2586. https://doi.org/10.1023/B:BIOC.0000048452.18878.2d.
Pardini, R.; De Arruda Bueno, A.; Gardner, T.A.; Prado, P.I. & Metzger, J.P. 2010. Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. PloS ONE, 5(10): e13666. https://doi.org/10.1371/journal.pone.0013666.
Pardini, R.; De 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. Biological Conservation, 124(2): 253-266. https://doi.org/10.1016/j.biocon.2005.01.033.
Peel, M.C.; Finlayson, B.L. & McMahon, T.A. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences Discussions, European Geosciences Union, 4(2): 439-473. https://doi.org/10.5194/hess-11-1633-2007.
Pinotti, B.T.; Naxara, L. & Pardini, R. 2011. Diet and food selection by small mammals in an old-growth Atlantic forest of south-eastern Brazil. Studies on Neotropical Fauna and Environment, 46(1): 1-9. https://doi.org/10.1080/01650521.2010.535250.
Püttker, T.; Bueno, A.A.; dos Santos de Barros, C.; Sommer, S. & Pardini, R. 2013. Habitat specialization interacts with habitat amount to determine dispersal success of rodents in fragmented landscapes. Journal of Mammalogy, 94(3): 714-726. https://doi.org/10.1644/12-MAMM-A-119.1.
Quintela, F.M.; da Rosa, C.A. & Feijó, A. 2020. Updatd and annotated checklist of recent mammals from Brazil. Anais da Academia Brasileira de Ciências, 92(Supl. 2): 1-57. https://doi.org/10.1590/0001-3765202020191004.
R Core Team. 2018. Version 3.5.1. Vienna, R Foundation for Statistical Computing. https://www.r-project.org.
Ribeiro, M.C.; Metzger, J.P.; Martensen, A.C.; 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. Biological Conservation, 142(6): 1141-1153. https://doi.org/10.1016/j.biocon.2009.02.021.
Richards, P.W. 1996. The tropical rain forest. 2 ed. Cambridge, Cambridge University Press,.
Rodrigues, D.P.; Skupien, F.L.; Sausen, J.O. & Lima, D.O. 2020. Small mammals in fragments of Atlantic Forest: species richness answering to field methods and environment. Journal of Tropical Ecology, 36(3): 101-108. https://doi.org/10.1017/S0266467420000048.
Rosenzweig, M.L. 1981. A theory of habitat selection. Ecology, 62(2): 327-335. https://doi.org/10.2307/1936707.
Santo-Silva, E.E.; Almeida, W.R.; Tabarelli, M. & Peres, C.A. 2016. Habitat fragmentation and the future structure of tree assemblages in a fragmented Atlantic forest landscape. Plant Ecology, 217(9): 1129-1140. https://doi.org/10.1007/s11258-016-0638-1.
Schirmer, A.; Herde, A.; Eccard, J.A. & Dammhahn, M. 2019. Individuals in space: personality-dependent space use, movement and microhabitat use facilitate individual spatial niche specialization. Oecologia, 189(3): 647-660. https://doi.org/10.1007/s00442-019-04365-5.
Schoener, T.W. 1974. Resource partitioning in ecological communities. Science, 185: 27-39. https://doi.org/10.1126/science.185.4145.27.
Smith, M.F. & Patton, J.L. 1993. The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biological Journal of the Linnean Society, 50(3): 149-177. https://doi.org/10.1111/j.1095-8312.1993.tb00924.x.
SOS Mata Atlântica (Fundação SOS Mata Atlântica) & INPE (Instituto Nacional de Pesquisas Espaciais). 2011. Atlas dos remanescentes florestais da Mata Atlântica, período de 2008-2010 (p. 122). São Paulo, Fundação SOS Mata Atlântica; INPE. p. 122.
Souza, S.S.; Ramos, R.F.; Bremm, N.; Garcia, P.B.; Grzybowski, N.; Ferrera, T.S.; Chassot, T. & Pinheiro, T. 2020. Estrutura arbórea de um fragmento de floresta estacional decidual na região fisiográfica Missões, Rio Grande do Sul, Brasil. Pesquisas, Botânica, 74: 133-145.
Sponchiado, J.; Melo, G.L. & Cáceres, N.C. 2012. Habitat selection by small mammals in Brazilian Pampas biome. Journal of Natural History, 46(21-22): 1321-1335. https://doi.org/10.1080/00222933.2012.655796.
Stevens, R.D.; Gavilanez, M.M.; Tello, J.S. & Ray, D.A. 2012. Phylogenetic structure illuminates the mechanistic role of environmental heterogeneity in community organization. Journal of Animal Ecology, 81(2): 455-462. https://doi.org/10.1111/j.1365-2656.2011.01900.x.
Tabarelli, M.; Pinto, L.P.; Silva, J.M.; Hirota, M. & Bede, L. 2005. Challenges and opportunities for biodiversity conservation in the Brazilian Atlantic Forest. Conservation Biology, 19(3): 695-700. https://doi.org/10.1111/j.1523-1739.2005.00694.x.
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 Ecology, 22(4): 517-530. https://doi.org/10.1007/s10980-006-9041-y.
Vieira, E.M.; Iob, G.; Briani, D.C. & Palma, A.R.T. 2005. Microhabitat selection and daily movements of two rodents (Nectomys lasiurus and Oryzomys scotti) in Brazilian Cerrado, as revealed by a spool-and-line device. Mammalian Biology, 70(6): 359-365. https://doi.org/10.1016/j.mambio.2005.08.002.
Vieira, E.M.; Paise, G. & Machado, P.H.D. 2006. Feeding of small rodents on seeds and fruits: a comparative analysis of three species of rodents of the Araucaria forest, southern Brazil. Acta Theriologica, 51(3): 311-318. https://doi.org/10.1007/BF03192683.
Vieira, M.V.; Olifiers, N.; Delciellos, A.C.; Antunes, V.Z.; Bernardo, L.R.; Grelle, C.E. & Cerqueira, R. 2009. Land use vs. fragment size and isolation as determinants of small mammal composition and richness in Atlantic Forest remnants. Biological Conservation, 142(6): 1191-1200. https://doi.org/10.1016/j.biocon.2009.02.006.
Wang, E. 2002. Diets of ocelots (Leopardus pardalis), margays (L. wiedii), and oncillas (L. tigrinus) in the Atlantic rainforest in southeast Brazil. Studies on Neotropical Fauna and Environment, 37(3): 207-212. https://doi.org/10.1076/snfe.37.3.207.8564.
Warrick, G.D.; Kato, T.T. & Rose, B.R. 1998. Microhabitat use and home range characteristics of blunt-nosed leopard lizards. Journal of Herpetology, 32(2): 183-191. https://doi.org/10.2307/1565295.
Zhang, Z.; Schwartz, S.; Wagner, L. & Miller, W. 2000. A greedy algorithm for aligning DNA sequences. Journal of Computational Biology, 7(1-2): 203-214. https://doi.org/10.1089/10665270050081478.
Downloads
Published
Issue
Section
License
Copyright (c) 2022 Papéis Avulsos de Zoologia
This work is licensed under a Creative Commons Attribution 4.0 International License.
Responsibility: The scientific content and the opinions expressed in the manuscript are the sole responsibility of the author(s).
Copyrights: Papéis Avulsos de Zoologia. The journal is licensed under a Creative Commons attribution-type CC-BY.
How to Cite
Funding data
-
Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul
Grant numbers 0423-2551/15-7;0528-2551/16-7
