Influence of forest type on the diversity, abundance, and naïve occupancy of the mammal assemblage in the southeastern Brazilian Atlantic Forest

Authors

  • Alejandra Soto-Werschitz Programa de Pós-Graduação em Ecologia Aplicada, Instituto de Ciências Naturais, Departamento de Ecologia e Conservação, Laboratório de Ecologia e Conservação de Mamíferos, Universidade Federal de Lavras. Universidad de Los Andes, Departamento de Biología.
  • Salvador Mandujano Red de Biología y Conservación de Vertebrados, Instituto de Ecología. A.C.
  • Marcelo Passamani Programa de Pós-Graduação em Ecologia Aplicada, Instituto de Ciências Naturais, Departamento de Ecologia e Conservação, Laboratório de Ecologia e Conservação de Mamíferos, Universidade Federal de Lavras.

Keywords:

Biodiversity, Brazil, conservation, habitat use, mammals, relative abundance index.

Abstract

The Brazilian Atlantic Forest has the highest rate of native vegetation destruction, which is one of the principal drivers of mammal extinctions. Therefore, reducing information gaps regarding diversity patterns, abundance, and habitat use is crucial to understand mammal persistence in fragmented landscapes. Our objective was to establish the γ diversity and to assess the extent to which the α, and β diversity, the relative abundance, and naïve occupation of medium and large-sized mammal communities differ between seasonal and ombrophilous forests. Between January 2019 and March 2020, we placed 22 camera traps in the Atlantic Forest of Minas Gerais. We calculate Hill's numbers using iNEXT.4steps package, the β-diversity with the Betapart package, as well as the relative abundance index (RAI), and naïve occupancy (PAO). We used Kruskal-Wallis and Mann-Whitney statistical tests to compare the RAIs between different species and forest types. Finally, we calculated the correlation between the RAIs and PAOs. We found 32 species, principally from the orders Carnivora and Artiodactyla. The alpha diversity and evenness profiles were not different between the two forest types (seasonal q0 = 0.91, q1 = 0.99, q2 = 1, J = 0.83; ombrophilous q0 = 0.96, q1 = 0.99, q2 = 1, J = 0.85). The beta diversity was low (βJAC = 0.37) which was mostly associated with species turnover (βJTU = 0.34), while nestedness was almost non-existent (βJNE = 0.02). The RAIs varied among mammalian species (H = 115.24, P = 0.000), with the highest values for Didelphis aurita (RAI = 4.55 ± 7.66) and Cuniculus paca (RAI = 2.35 ± 3.73) and the minor values for Speothos venaticus (RAI = 0.04 ± 0.24) and Galictis cuja (RAI = 0.06 ± 1.19). The RAIs of species was not significantly different between forests (U = 453.5; Z = 0.37; P = 0.70), and only Leopardus wiedii showed significant differences between forests (U = 84.5; P = 0.01). Most of the mammalian species had restricted occupancy to a few localities (< 50 %). The species Eira barbara and Didelphis aurita had the highest PAOs in both forests (> 50 %), and the species Tayassu pecari, Tamandua tetradactyla, and Speothos venaticus, the lowest values (5 %). We found a correlation of 75 % between the average RAI and naïve occupancy. The γ diversity was representative and consistent with the species found in the Atlantic Forest, and the relative abundance and naïve occupancy reflected the rarity of most species in the area. Additionally, the only difference between the two forests corresponds to species turnover. Therefore, we must conserve native remnants of both forests to ensure the existence of native mammals, mainly the most threatened species, to prevent more dramatic scenarios of local extinction in Minas Gerais.

Author Biographies

Alejandra Soto-Werschitz, Programa de Pós-Graduação em Ecologia Aplicada, Instituto de Ciências Naturais, Departamento de Ecologia e Conservação, Laboratório de Ecologia e Conservação de Mamíferos, Universidade Federal de Lavras. Universidad de Los Andes, Departamento de Biología.

Programa de Pós-Graduação em Ecologia Aplicada,Instituto de Ciências Naturais, Departamento de Ecologia e Conservação, Laboratório de Ecologia e Conservação de Mamíferos, Universidade Federal de Lavras.Estudiante de Doctorado.

Salvador Mandujano, Red de Biología y Conservación de Vertebrados, Instituto de Ecología. A.C.

Red de Biología y Conservación de VertebradosInvestigador Titular B.

Marcelo Passamani, Programa de Pós-Graduação em Ecologia Aplicada, Instituto de Ciências Naturais, Departamento de Ecologia e Conservação, Laboratório de Ecologia e Conservação de Mamíferos, Universidade Federal de Lavras.

Instituto de Ciências Naturais, Departamento de Ecologia e ConservaçãoProfessor

References

ABREU, E. F., ET AL. 2021-2. Lista de Mamíferos do Brasil. Dataset Open Access. Zenodo. Comitê de Taxonomia da Sociedade Brasileira de Mastozoologia (CT-BMz). https://doi.org/10.5281/zenodo.5802047.

DE ASSIS MORAIS, T., et al. 2020. The influence of population-control methods and seasonality on the activity pattern of wild boars (Sus scrofa) in high-altitude forests. Mammalian Biology 100:101-106.

DE BARROS, R.A., ET AL. 2021. The value of a small urban green area to the medium and large-sized mammals conservation. Research, Society and Development 10:e11710817043.

BECA, G., et al. 2017. High mammal species turnover in forest patches immersed in biofuel plantations. Biological Conservation 210:352-359.

BASELGA, A., 2010. Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography 19:134-143.

BASELGA, A., AND C. D. L. ORME. 2012. Betapart: an R package for the study of beta diversity. Methods in Ecology and Evolution 3:808–812.

BASELGA, A., ET AL. 2021. Betapart: partitioning beta diversity into turnover and nestedness components. R package ver. 1.5.2.

BOGONI, J. A., et al. 2016. Landscape features lead to shifts in communities of medium- to large-bodied mammals in subtropical Atlantic Forest. Journal of Mammalogy 97:713-725.

BOGONI, J. A., ET AL. 2017. What would be the diversity patterns of medium- to large-bodied mammals if the fragmented Atlantic Forest was a large metacommunity? Biological Conservation 211:85-94.

BOGONI, J. A., ET AL. 2018. Wish you were here: How defaunated is the Atlantic Forest biome of its medium- to large-bodied mammal fauna? Plos One 13:e0204515.

BOGONI, J. A., C.A. PERES, AND K. M. FERRAZ. 2020. Extent, intensity and drivers of mammal defaunation: a continental-scale analysis across the Neotropics. Scientific Reports 10:14750.

BOGONI, J. A., C.A. PERES, AND K. M. FERRAZ. 2020a. Effects of mammal defaunation on natural ecosystem services and human well being throughout the entire Neotropical realm. Ecosystem Services 45:101173.

BOTHELO, A. L. M., L. H. M. BORGES, AND B. MCFARLAND. 2018. Abundance and composition of the medium to large-sized mammals in a private area of a REDD+ project in Acre, Brazil. Biota Neotropica 18:e20170487.

BRANCALION, P. H., ET AL. 2016. A critical analysis of the Native Vegetation Protection Law of Brazil (2012): updates and ongoing initiatives. Natureza and Conservação14:1-15.

BURNHAM, K. P., AND W. S. OVERTON. 1979. Robust estimation of population size when capture probabilities vary among animals. Ecology 60:927-936.

CAMPANILI, M., AND W. B. SCHÄFFER (EDS.). 2010. Mata Atlântica: patrimônio nacional dos brasileiros. Ministério do Meio Ambiente. Secretaria de Biodiversidade e Florestas. Núcleo Mata Atlântica e Pampa. Brasília, Brazil.

CHAO, A., C. H. CHIU, AND L. JOST. 2014. Unifying species diversity, phylogenetic diversity, functional diversity, and related similarity and differentiation measures through Hill Numbers. Annual Review of Ecology, Evolution, and Systematics 45:297-324.

CHAO, A., ET AL. 2020. Quantifying sample completeness and comparing diversities among assemblages. Ecological Research 35:292-314.

CONSERVATION INTERNATIONAL. 2018. Wild.ID 0.9.31. TEAM Network Supercomputer Center. San Diego U.S.A.

COOKE, R. S. C., F. EINGENBROD, AND A. E. BATES. 2019. Projected losses of global mammal and bird ecological strategies. Nature Communications 10:1-8.

CORRȆA, T. C. V., ET AL. 2021. Medium and large-sized mammals in Private Natural Heritage Reserves in the Quadrilátero Ferrífero of Minas Gerais, Brazil. Neotropical Biology and Conservation 16:383-396.

CROOKS, K. R., AND M. E. SOULÉ. 1999. Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563-566.

FAHARIG, L., ET AL. 2019. Is habitat fragmentation bad for biodiversity? Biological Conservation 230:179-186.

FERREIRA, A. S., ET AL. 2020. Multi-scale mammal responses to agroforestry landscapes in the Brazilian Atlantic Forest: the conservation value of forest and traditional shade plantations. Agroforestry Systems 94:2331-2341.

FIGUEREIDO, M. D. S. L., ET AL. 2021. Tetrapod Diversity in the Atlantic Forest: Maps and Gaps. Pp. 185–204 in The Atlantic Forest (M.C.M. Marques and C.E.V. Grelle, eds.). Springer International Publishing, Cham.

GALETTI, M., ET AL. 2009. Priority areas for the conservation of Atlantic Forest large mammals. Biological Conservation 142:1229-1241.

GALETTI, M., ET AL. 2021. Causes and Consequences of Large-Scale Defaunation in the Atlantic Forest. Pp. 297–324 in The Atlantic Forest (Marques, M. C. M. and C. E. V. Grelle, eds.). Springer International Publishing, Cham.

HADDAD, N. M., ET AL. 2015. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Science Advances 1:e1500052.

HSIEH, T. C., K. H. MA, AND A. CHAO. 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution 7:1451-1456.

IKIN, K., ET AL. 2014. Multi-scale associations between vegetation cover and woodland bird communities across a large agricultural region. Plos One 9: e97029.

INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA (EDS.). 2012. Manual técnico da vegetação brasileir. Instituto Brasileiro de Geografia e Estatística-IBGE, Rio de Janeiro, Brazil.

INSTITUTO CHICO MENDES DE CONSERVAÇÃO DA BIODIVERSIDADE (ICMBIO, EDS.). 2018. Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Brasilia, Brazil.

INTERNATIONAL UNION FOR CONSERVATION OF NATURE AND NATURAL RESOURCES (IUCN). 2021. IUCN Red List categories. IUCN.

INVASIVE SPECIES SPECIALIST GROUP (ISSG). 2015. The Global Invasive Species Database. University of Auckland, New Zealand.

KÉRY, M. AND J. A. ROYLE. 2015. Applied Hierarchical Modeling in Ecology: Analysis of Distribution, Abundance and Species Richness in R and BUGS. Academic Press, Londres, Reino Unido.

KINDT, R., AND R. COE. 2005. Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi, Kenya.

LISTA DAS ESPÉCIES DA FAUNA AMEAÇADAS DE EXTINÇÃO NO ESTADO DE MINAS GERAIS, COPAM. 2010. Deliberação Normativa Conselho Estadual de Política Ambiental Nº 147. Diário do Executivo, Minas Gerais, Brazil.

MACKENZIE, D. I. AND W. L. KENDALL. 2002. How should detection probability be incorporated into estimates of relative abundance? Ecology 83:2387-2393.

MANDUJANO, S. AND L. A. PÉREZ-SOLANO. 2019. Fototrampeo en R: organización y análisis e datos. Instituto de Ecología A. C., Xalapa, México.

DE MATOS, T. P. V., ET AL. 2021. Protected areas and forest fragmentation: sustainability index for prioritizing fragments for landscape restoration. Geology, Ecology, and Landscapes 5:19-31.

MYERS, N., ET AL. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858.

OLIVEIRA, R. F., A. R. DE MORAIS, AND L. C. TERRIBILE. 2020. Effects of landscape and patch attributes on the functional diversity of medium and large-sized mammals in the Brazilian Cerrado. Mammal Research 65:301-308.

OKSANEN, J., ET AL. 2013. Package 'vegan'. R Package.

PORFIRIO, G., ET AL. 2014. Medium to large size mammals of southern Serra do Amolar, Mato Grosso do Sul, Brazilian Pantanal. Check List 10:473-482.

PÃœTTKER, T., ET AL. 2020. Indirect effects of habitat loss via habitat fragmentation: A cross-taxa analysis of forest-dependent species. Biological Conservation 241:108368.

QUINTELA, F. M., C. A. DA ROSA, AND A. FEIJÓ. 2020. Updated and annotated checklist of recent mammals from Brazil. Anais da Academia Brasileira de Ciências 92:e20191004.

R CORE TEAM 4.1.0. 2021. R: A language and environment for statistical computing. R for Statistical Computing, Vienna, Austria.

RÍOS, E., ET AL. 2022. Spatial predictors and species’ traits: evaluating what really matters for mediumâ€sized and large mammals in the Atlantic Forest, Brazil. Mammal Review 52:236-251.

REGOLIN, A. L., ET AL. 2020. Spatial heterogeneity and habitat configuration overcome habitat composition influences on alpha and beta mammal diversity. Biotropica 52:969-980.

RIBEIRO, M. C., ET AL. 2009. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142:1141-1153.

ROVERO, F., AND D. SPITALE. 2016. Presence/absence and species inventory. Pp. 43-67 in Camera Trapping for Wildlife Research (Rovero, F., and F. Zimmermann, eds.). Pelagic Publishing, U.K.

ROSA, C. A., ET AL. 2017. Alien terrestrial mammals in Brazil: current status and management. Biological Invasions 19:2101-2123.

SANTOS, K. K., G. S. M. PACHECO, AND M. PASSAMANI. 2016. Medium-sized and large mammals from Quedas do Rio Bonito Ecological Park, Minas Gerais, Brazil. Check List 12:1830.

SANTOS, F., ET AL. 2021. Site and species contribution to β-diversity in terrestrial mammal communities: Evidence from multiple Neotropical Forest sites. Science of the Total Environment 789:147946.

DA SILVA, P. G., M. I. M. HERNÁNDEZ, AND J. HEINO. 2018. Disentangling the correlates of species and site contributions to beta diversity in dung beetle assemblages. Diversity and Distributions 24:1674-686.

SOUZA, Y., ET AL. 2019. Atlantic mammals: a data set of assemblages of medium- and large-sized mammals of the Atlantic Forest of South America. Ecology 100:e02785.

SOTO-WERSCHITZ, A., S. MANDUJANO AND M. PASSAMANI. 2023. First record of the bush dog Speothos venaticus in the Atlantic Forest of Minas Gerais, Brazil. Oryx, 1-3. doi:10.1017/S0030605323000236.

SRBEK-ARAUJO, A. C., AND A. G. CHIARELLO. 2005. Is camera-trapping an efficient method for surveying mammals in Neotropical forests? A case study in south-eastern Brazil. Journal of Tropical Ecology 21:121-125.

STEINBEISER, C. M., ET AL. 2019. Relative abundance and activity patterns explain method-related differences in mammalian species richness estimates. Journal of Mammalogy 100:192-201.

TOMCZAK, M., AND E. TOMCZAK. 2014. The need to report effect size estimates revisited. An overview of some recommended measures of effect size. Trends in Sport Sciences, 1:19-25.

TROLLIET, F., ET AL. 2014. Use of camera traps for wildlife studies: a review. Biotechnologie, Agronomie, Société et Environnement 18:446-454.

VILAS BOAS, A. H., ET AL. 2022. Survey of medium-and large-sized mammals in Atlantic Forest remnants of Conceição dos Ouros, Minas Gerais, Brazil. Biodiversity Data Journal 10:e82139.

WEARN, O. R., ET AL. 2017. Mammalian species abundance across a gradient of tropical land-use intensity: A hierarchical multi-species modelling approach. Biological Conservation 212:162-71.

WEARN, O. R. AND GLOVER-KAPFER. 2019. Snap happy: camera traps are an effective sampling tool when compared with alternative methods. Royal Society open science, 6:181-748.

WHITTAKER, R. H. 1972. Evolution and measurement of species diversity. Taxon 21:213-251.

Published

2023-08-29

Issue

Section

Articles