HABITAT SELECTION OF Marmosops incanus (LUND, 1841) (DIDELPHIMORPHIA, DIDELPHIDAE) IN THE SERRA DOS ÓRGÃOS NATIONAL PARK, ATLANTIC FOREST, SOUTHEAST BRAZIL
DOI:
https://doi.org/10.4257/oeco.2023.2702.07Keywords:
small mammals, scansorial, habitat use, national park, montane forestAbstract
Habitat selection is one of the mechanisms responsible for allowing species coexistence and,
therefore, local richness of communities. This study investigates microhabitat selection by the opossum, Marmosops incanus, in a forested area in the Brazilian Atlantic Forest. We measured microhabitat variables related to vegetation structure and inferred M. incanus abundance as a measure of habitat use. Eight microhabitat variables were measured in each trap station: litter, herbaceous and woody stems, rock outcropping, canopy cover, foliar vertical obstruction at three heights (FOV), and number of fallen trunks. Based on a correlation matrix, we selected four microhabitat variables (litter, rock outcropping cover, FOV, and number of fallen trunks) and performed a Poisson regression using the selected variables and M. incanus abundance. Litter and rock outcropping cover were positively related to abundance, thus representing the habitat characteristics selected by the species. We infer that litter represents a source of food items, since it can support an abundant fauna of macroinvertebrates, especially arthropods. Rock outcroppings can be used as shelter and protection against predators. Other studies have recorded M. incanus using habitat in a unique way, either by changing the frequency of ground/understory use, or habitats with high/few herbaceous and litter cover, as the habitat varied from restinga to fragmented forests. Different habitat selection patterns were observed in areas where M. incanus and M. paulensis are sympatric, or Gracilinanus microtarsus, both of which have comparable size and ecology. We suppose the selection patterns recorded in this study are a result of the absence of a congener species in the study area. It may allow M. incanus to use more frequently areas where near-ground strata are clear and highly covered with litter. It remains to be evaluated if habitat simplification leads to behavior homogenization.
References
Alho, C. J. R. (1981). Small Mammal Populations of Brazilian Cerrado: The Dependence of Abundance and Diversity on Habitat Complexity. Revista Brasileira de Biologia, 41(1), 223–230. http://md1.csa.com/partners/viewrecord.php?requester=gs&collection=ENV&recid=238222&q=Small+mammal+populations+of+Brazilian+Cerrado:+the+dependence+of+abundance+and+diversity+on+habitat+complexity&uid=790935104&setcookie=yes
Astúa, D., Santori, R. T., Finotti, R., & Cerqueira, R. (2003). Nutritional and fibre contents of laboratory-established diets of neotropical opossums (Didelphidae). In M. Jones, C. Dickman, & M. Archer (Eds.), Predators with pouches: the biology of carnivorous marsupials (1st ed., pp. 229–237). Csiro Publishing.
Atramentowicz, M. (1982). Disponibilités trophiques et rythmes de reproduction chez trois marsupiaux didelphidés de Guyane. Mémoires Du Muséum National D’Histoire Naturelle, 132, 123–130.
August, P. V. (1983). The Role of Habitat Complexity and Heterogeneity in Structuring Tropical Mammal Communities. Ecology, 64(6), 1495–1507. https://doi.org/10.2307/1937504
Braz, A.G., Grelle, C.E.V., Figueiredo, M. & Weber, M. (2020). Interspecific competition constrains local abundance in highly suitable areas. Ecography 43, 1560–1570. https://doi.org/10.1111/ecog.04898.
Calazans, J. de F., & Bocchiglieri, A. (2019). Microhabitat use by Rhipidomys mastacalis and Marmosops incanus (Mammalia) in a restinga areas in north-eastern Brazil. Austral Ecology, 44(8), 1471–1477. https://doi.org/10.1111/aec.12821
Câmara, E. M. V. C., Oliveira, L. de C., & Meyer, R. L. L. (2003). Occurrence of the mouse opossum, Marmosops incanus in Cerrado « stricto sensu » area, and new locality records for the Cerrado and Caatinga biomes in Minas Gerais State, Brazil. Mammalia, 67(4), 617–619. http://www.scopus.com/inward/record.url?eid=2-s2.0-1942423227&partnerID=40&md5=b16b08f03794949c593454d746eff820
Cassini, M. H., & Galante, M. L. (1992). Foraging under predation risk in the wild guinea pig: the effect of vegetation height on habitat utilization. Annales Zoologici Fennici, 29(4), 285–290.
Cerqueira, R., & Freitas, S. R. (1999). A new study method of microhabitat structure of small mammals. Revista Brasileira de Biologia, 59(2), 219–223. https://doi.org/10.1590/S0034-71081999000200006
Corbalán, V. (2006). Microhabitat selection by murid rodents in the Monte desert of Argentina. Journal of Arid Environments, 65(1), 102–110. https://doi.org/10.1016/j.jaridenv.2005.07.006
Costa, L. P., & Patton, J. L. (2006). Diversidade e limites geográficos e sistemáticos de marsupiais brasileiros. In N. C. Cáceres (Ed.), Os Marsupiais do Brasil: Biologia, Ecologia e Evolução (1st. ed., pp. 321–342). Editora UFMS.
Cunha, A. A., & Vieira, M. V. (2002). Support diameter, incline, and vertical movements of four didelphid marsupials in the Atlantic forest of Brazil. Journal of Zoology, 258(4), 419–426. https://doi.org/10.1017/S0952836902001565
Dalloz, M. F., Loretto, D., Papi, B. S., Cobra, P. de P. A., & Vieira, M. V. (2012). Positional behaviour and tail use by the bare-tailed woolly opossum Caluromys philander. Mammalian Biology, 77(5), 307–313. https://doi.org/10.1016/j.mambio.2012.03.001
Dalmagro, A. D., & Vieira, E. M. (2005). Patterns of habitat utilization of small rodents in an area of Araucaria forest in Southern Brazil. Austral Ecology, 30, 353–362.
Delciellos, A. C., Loretto, D., & Vieira, M. V. (2006). Novos métodos o estudo da estratificação vertical de marsupiais neotropicais. Oecologia Brasiliensis, 10(2), 135–153.
Dueser, R. D., & Shugart Jr., H. H. (1978). Microhabitat in a florest-floor small mammal fauna. Ecology, 59(1), 89–98.
Ellwood, M. D. F., & Foster, W. A. (2004). Doubling the estimate of invertebrate biomass in a rainforest canopy. Nature, 429(6991), 549–551. https://doi.org/10.1038/nature02560
Erwin, T. L. (1982). Tropical Forests: Their Richness in Coleoptera and Other Arthropod Species. The Coleopterists Society, 36(1), 74–75. http://books.google.com/books?hl=en&lr=&id=IhMVs2m9Z4oC&oi=fnd&pg=PA438&dq=Tropical+Forests+:+Their+Richness+in+Coleoptera+and+Other+Arthropod+Species&ots=4c4OVvuIS4&sig=NxRcefdA-Xmq_HI8sD7M3RRPnvQ
Ferreira, P. (2009). Importância do habitat em estudos com mamíferos terrestres neotropicais: uma revisão do conceito e um estudo de caso na Serra dos Órgãos, RJ. Universidade Federal do Rio de Janeiro.
Figueiredo, M. de S. L., Weber, M. M., Brasileiro, C. A., Cerqueira, R., Grelle, C. E. V., Jenkins, C. N., Solidade, C. V., Thomé, M. T. C., Vale, M. M., & Lorini, M. L. (2021). Tetrapod Diversity in the Atlantic Forest: Maps and Gaps. In The Atlantic Forest. https://doi.org/10.1007/978-3-030-55322-7_9
Fowler, C. W. (1981). Density Dependence as Related to Life History Strategy. Ecology, 62(3), 602–610. https://doi.org/10.2307/1937727
Freitas, S. R. (1998). Variação Espacial e Temporal na Estrutura do Habitat e Preferência de Microhabitat por Pequenos Mamíferos na Mata Atlântica. Universidade Federal do Rio de Janeiro.
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
Fretwell, S. D. (1972). Theory of habitat distribution. In S. D. Fretwell (Ed.), Populations in a seasonal environment (pp. 79–114). Princeton University Press.
Gallardo-Santis, A., Simonetti, J. a., & Vásquez, R. a. (2005). Influence of tree diameter on climbing ability of small mammals. Journal of Mammology, 86(5), 969–973. https://doi.org/10.1644/1545-1542(2005)86[969:IOTDOC]2.0.CO;2
Gentile, R., Finotti, R., Rademaker, V., & Cerqueira, R. (2004). Population dynamics of four marsupials and its relation to resource production in the Atlantic forest in southeastern Brazil. Mammalia, 68(2–3), 109–119. https://doi.org/10.1515/mamm.2004.012
Gonzalez, L. A., Murua, R., & JOFRE, C. (2000). Habitat utilization of two muroid species in relation to population outbreaks in southern temperate forests of Chile. Revista Chilena de Historia Natural, 73(3). https://doi.org/10.4067/S0716-078X2000000300012
Grelle, C. E. V. (2003). Forest Structure and Vertical Stratification of Small Mammals in a Secondary Atlantic Forest, Southeastern Brazil. Studies on Neotropical Fauna and Environment, 38(2), 81–85. https://doi.org/10.1076/snfe.38.2.81.15926
Hodara, K., Busch, M., Kittlein, M. J., & Kravetz, F. O. (2000). Density-dependent habitat selection between maize cropfields and their borders in two rodent species (Akodon azarae and Calomys laucha) of Pampean agroecosystems. Evolutionary Ecology 2000 14:7, 14(7), 571–593. https://doi.org/10.1023/A:1010823128530
Hosmer, D. W., Lemeshow, S., & Sturdivant, R. (2000). Applied Logistic Regression (3rd. ed.). John Wiley & Sons, Inc.
IBGE. (2012). Manual técnico da vegetação brasileira. In Produção da Pecuária Municipal (2nd ed., Vol. 39). IBGE. https://doi.org/ISSN 0101-4234
Jorgensen, E. E. (2004). Small mammal use of microhabitat reviewed. Journal of Mammology, 85(3), 531–539. https://doi.org/10.1644/BER-019
Jorgensen, E. E., & Demarais, S. (1999). Spatial Scale Dependence of Rodent Habitat Use. Journal of Mammology, 80(2), 421. https://doi.org/10.2307/1383290
Julien-Laferrière, D., & Atramentowicz, M. (1990). Feeding and reproduction of three didelphid marsupials in two neotropical forests (French Guiana). Biotropica, 22(4), 404–415. http://www.jstor.org/stable/2388558
Kajin, M., Cerqueira, R., Vieira, M. V., & Gentile, R. (2008). Nine-year demography of the black-eared opossum Didelphis aurita (Didelphimorphia: Didelphidae) using life tables. Revista Brasileira de Zoologia, 25(2), 206–213. https://doi.org/10.1590/S0101-81752008000200007
Leiner, N. O. (2005). Ecologia alimentar e reprodutiva de Marmosops paulensis (Didelphimorphia: Didelphidae) em uma área de Mata Atlântica no sudeste de São Paulo. Universidade Estadual de Campinas.
Leiner, N. O., Dickman, C. R., & Silva, W. R. (2010). Multiscale habitat selection by slender opossums (Marmosops spp.) in the Atlantic forest of Brazil. Journal of Mammology, 91(3), 561–565. https://doi.org/10.1644/09-MAMM-A-328.1
Leiner, N. O., & Silva, W. R. (2007). Seasonal variation in the diet of the Brazilian slender opossum (Marmosops paulensis) in a montane Atlantic forest area, Southeastern Brazil. Journal of Mammology, 88(1), 158–164. https://doi.org/10.1644/06-MAMM-A-088R2.1
Lessa, L. G., & Geise, L. (2010). Hábitos alimentares de marsupiais didelfídeos brasileiros: análise do estado de conhecimento atual. Oecologia Australis, 14(04), 901–910. https://doi.org/10.4257/oeco.2010.1404.07
Loretto, D., & Vieira, M. V. (2005). The effects of reproductive and climatic seasons on movements in the black-eared opossum (Didelphis aurita Wied-Neuwied, 1826). Journal of Mammology, 86(2), 287–293. https://doi.org/10.1644/BEH-117.1
Loretto, D., & Vieira, M. V. (2008). Use of space by the marsupial Marmosops incanus (Didelphimorphia, Didelphidae) in the Atlantic Forest, Brazil. Mammalian Biology, 73(4), 255–261. https://doi.org/10.1016/j.mambio.2007.11.015
Lorini, M. L., Oliveira, J. A. De, & Persson, V. G. (1994). Annual age structure and reproductive patterns in Marmosa incana (Lund, 1841)(Didelphidae, Marsupialia). Zeitschrift Für Säugetierkunde, 59, 65–73.
Macedo, J. (2007). Reprodução, fator de condição e dinâmica temporal de uma população do marsupial Didelfídeo Marmosops incanus na Serra dos Órgãos (Issue September). Universidade Federal do Rio de Janeiro.
Macedo, J., Loretto, D., Mello, M. C. S., Freitas, S. R., Vieira, M. V., & Cerqueira, R. (2007). História Natural dos mamíferos de uma área perturbada do Parque Nacional da Serra dos Órgãos. In Cecilia Cronemberger & E. B. Viveiros de Castro (Eds.), Ciência e Conservação na Serra dos Órgãos (pp. 165–182). Ministério do Meio Ambiente.
Macedo, J., Loretto, D., Vieira, M. V., & Cerqueira, R. (2006). Classes de desenvolvimento em marsupiais: um método para animais vivos. Mastozoología Neotropical, 13(1), 133–136. http://www.redalyc.org/html/457/45713111/index.html
McNab, B. K. (1966). The Metabolism of Fossorial Rodents: A Study of Convergence. Ecology, 47(5), 712–733. http://www.jstor.org/stable/1934259
Melo, G. L., & Sponchiado, J. (2012). Distribuição geográfica dos marsupiais no Brasil. In N. C. Cáceres (Ed.), Os Marsupiais do Brasil: Biologia, Ecologia e Evolução (2nd. ed., pp. 95–112). Editora UFMS.
Mittermeier, R. A., Fonseca, G. A. B., Rylands, A. B., & Brandon, K. (2005). A Brief History of Biodiversity Conservation in Brazil. Conservation Biology, 19(3), 601–607. https://doi.org/10.1111/j.1523-1739.2005.00709.x
Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. B., & Worm, B. (2011). How Many Species Are There on Earth and in the Ocean? PLoS Biology, 9(8), e1001127. https://doi.org/10.1371/journal.pbio.1001127
Morris, D. W. (1996). Coexistence of specialist and generalist rodents via habitat selection. Ecology, 77(8), 2352–2364. http://www.jstor.org/stable/10.2307/2265737
Morris, D. W. (2003). Toward an ecological synthesis: a case for habitat selection. Oecologia, 136, 1–13. https://doi.org/10.1007/s00442-003-1241-4
Moura, M. C., Caparelli, A. C., Freitas, S. R., & Vieira, M. V. (2005). Scale-dependent habitat selection in three didelphid marsupials using the spool-and-line technique in the Atlantic forest of Brazil. Journal of Tropical Ecology, 21(3), 337–342. https://doi.org/10.1017/S0266467405002270
Mustrangi, M. A., & Patton, J. L. (1997). Phylogeography and systematics of the slender mouse opossum Marmosops (Marsupialia, Didelphidae). University of California Publications in Zoology, 130, 130. http://library.wur.nl/WebQuery/clc/937076
Nimer, E. (1989). Climatologia do Brasil. In Série Recursos Naturais e Meio Ambiente (Issue 4). Instituto Brasileiro de Geografia e Estatística.
Ødegaard, F. (2000). How many species of arthropods? Erwin’s estimate revised. Biological Journal of the Linnean Society, 71(4), 583–597. https://doi.org/10.1006/bijl.2000.0468
Olifiers, N., Gentile, R., & Fiszon, J. T. (2005). Relation between small-mammal species composition and anthropic variables in the Brazilian Atlantic Forest. Brazilian Journal of Biology, 65(3), 495–501. https://doi.org/10.1590/S1519-69842005000300015
Paglia, A. P., Fonseca, G. A. B., Rylands, A. B., Herrmann, G., Aguiar, L. M. de S., Chiarello, A. G., Leite, Y. L. R., Costa, L. P., Siciliano, S., Kierulff, M. C. M., Mendes, S. L., Tavares, V. D. C., Mittermeier, R. A., L.Patton, J., Patton, J. L., Da Fonseca, G. A. B., Rylands, A. B., Herrmann, G., Aguiar, L. M. de S., … Patton, J. L. (2012). Annotated Checklist of Brazilian Mammals. In Occasional Papers in Conservation Biology (Vol. 6, Issue 6). http://www.conservation.org/global/brasil/publicacoes/Documents/annotated_checklist_of_brazilian_mammals_2nd_edition.pdf
Pellens, R., & Garay, I. (1999). Edaphic macroarthropod communities in fast-growing plantations of Eucalyptus grandis Hill ex Maid (Myrtaceae) and Acacia mangium Wild (Leguminosae) in Brazil. European Journal of Soil Biology, 35(2), 77–89. https://doi.org/10.1016/S1164-5563(99)00209-5
Price, M. V., & Kramer, K. A. (1984). On measuring microhabitat affinities with special reference to small mammals. Oikos, 42(3), 9–354. http://www.jstor.org/stable/10.2307/3544404
Ricklefs, R. E., & Donald, M. (1994). Ecological and Evolutionary Inferences in Morphology: An Ecological perpestive. In Ecological Morphology: Integrative Organismal Biology. (p. 367). University Of Chicago Press.
Rocha, L. G. M. da. (2007). The land tenure situation of Serra Órgãos National Park. In Cecília Cronemberger & E. B. Viveiros de Castro (Eds.), Ciência e Conservação na Serra dos Órgãos (1st. ed., pp. 39–54). IBAMA.
Rosenzweig, M. L. (1981). A theory of habitat selection. Ecology, 62(2), 327–335. http://www.esajournals.org/doi/abs/10.2307/1936707
Rosenzweig, M. L. (1985). Some theoretical aspects of habitat selection. In M. L. Cody (Ed.), Habitat Selection in Birds (pp. 517–540). Academic Press, NY.
Santori, R. T., Rocha-Barbosa, O., Vieira, M. V., Magnan-Neto, J. A., & Loguercio, M. F. de C. (2005). Locomotion in aquatic, terrestrial, and arboreal habitat of thick-tailed opossum, Lutreolina crassicaudata (Desmarest, 1804). Journal of Mammology, 86(5), 902–908. https://doi.org/10.1644/1545-1542(2005)86[902:LIATAA]2.0.CO;2
Schmitt, D., & Lemelin, P. (2002). Origins of primate locomotion: gait mechanics of the woolly opossum. American Journal of Physical Anthropology, 118(3), 231–238. https://doi.org/10.1002/ajpa.10048
Sokal, R. R., & Rohlf, F. J. (2011). Biometry (4th. ed.). W. H. Freeman; 4th edition. http://www.amazon.com/Biometry-Robert-R-Sokal/dp/0716786044
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 theAraucaria forest, southern Brazil. Acta Theriologica, 51(3), 311–318. https://doi.org/10.1007/BF03192683
Walter, H. (1986). Vegetação e zonas climáticas: tratado de ecologia global. Editora Pedagógica e Universitária.
