Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-30T20:22:29.883Z Has data issue: false hasContentIssue false

Small mammals in fragments of Atlantic Forest: species richness answering to field methods and environment

Published online by Cambridge University Press:  27 March 2020

Daniele Pereira Rodrigues
Affiliation:
Universidade Federal da Fronteira Sul (UFFS), Campus Cerro Largo, Rua Jacob Reinaldo Haupenthal, 1580, São Pedro, CEP 97900-000, Cerro Largo, RS, Brasil Programa de Pós-Graduação em Ciência e Tecnologia Ambiental, Universidade Federal da Fronteira Sul (UFFS), Campus Erechim, ERS 135 – Km 72, 200, CEP 99700-970, Erechim, RS, Brasil
Fabrício Luiz Skupien
Affiliation:
Universidade Federal da Fronteira Sul (UFFS), Campus Cerro Largo, Rua Jacob Reinaldo Haupenthal, 1580, São Pedro, CEP 97900-000, Cerro Largo, RS, Brasil Programa de Pós-Graduação em Ecologia, Universidade Federal do Rio de Janeiro (UFRJ), Ilha do Fundão, Caixa Postal 68020, CEP 21941-902, Rio de Janeiro, RJ, Brasil
Jady de Oliveira Sausen
Affiliation:
Universidade Federal da Fronteira Sul (UFFS), Campus Cerro Largo, Rua Jacob Reinaldo Haupenthal, 1580, São Pedro, CEP 97900-000, Cerro Largo, RS, Brasil
Daniela Oliveira de Lima*
Affiliation:
Universidade Federal da Fronteira Sul (UFFS), Campus Cerro Largo, Rua Jacob Reinaldo Haupenthal, 1580, São Pedro, CEP 97900-000, Cerro Largo, RS, Brasil
*
Author for correspondence: *Daniela Oliveira de Lima, Email: [email protected]

Abstract

Small mammals can be used as environmental indicators and have been intensively studied in fragmented landscapes of Atlantic Forest, with a wide range of field methods. Our aim in this study was two-fold: we tested for the effects of methods and for the effects of the main environmental variables on observed small mammal richness in fragments of Atlantic Forest. We gathered information on small mammal richness, methods and environmental variables from 122 fragments of Atlantic Forest through literature review. These data were analysed using linear models and model selection based on AIC values along with a regression tree analysis. We found that studies will record more species with bigger trapping effort, using pitfall traps and sampling all forest strata. We also confirmed two important ecological assumptions: fragments at lower latitudes and bigger fragments were the ones with higher species richness. Methodological and environmental variables were analysed together on a regression tree, where trapping effort was the most important variable, surpassing any environmental effect. Considering that a significant number of the studies on Atlantic Forest fragments did not use pitfall traps or sample all forest strata, their results on forest fragmentation were affected by sampling bias.

Type
Research Article
Copyright
© The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature cited

Abreu, MSL and Oliveira, LR (2014) Patterns of arboreal and terrestrial space use by non-volant small mammals in an Araucaria Forest of southern Brazil. Annals of the Brazilian Academy of Sciences 86, 807819.CrossRefGoogle Scholar
Andren, H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71, 355366.CrossRefGoogle Scholar
Ardente, NC, Ferreguetti, AC, Gettinger, D, Leal, P, Martins-Hatano, F and Bergallo, HG (2017) Differential efficiency of two sampling methods in capturing non-volant small mammals in an area in eastern Amazonia. Acta Amazonica 47, 123132.CrossRefGoogle Scholar
Balieiro, P, Behs, D, Graipel, ME, Dornelles, SS, Tiepolo, LM and Cremer, MJ (2015) Riqueza de pequenos mamíferos não voadores em florestas de restinga do sul do Brasil. Mastozoolia Neotropical 22, 367373.Google Scholar
Banks-Leite, C, Ewers, RM and Metzger, JP (2010) Edge effects as the principal cause of area effects on birds in fragmented secondary forest. Oikos 119, 918926.CrossRefGoogle Scholar
Banks-Leite, C, Pardini, R, Tambosi, LR, Pearse, WD, Bueno, AA, Bruscagin, RT, Condez, TH, Dixo, M, Igari, AT, Martensen, AC and Metzger, JP (2014) Using ecological thresholds to evaluate the costs and benefits of set-asides in a biodiversity hotspot. Science 345, 10411045.CrossRefGoogle Scholar
Barros, CS, Puttker, T, Pinotti, BT and Pardini, R (2015) Determinants of capture-recapture success: an evaluation of trapping methods to estimate population and community parameters for Atlantic forest small mammals. Zoologia 32, 334344.CrossRefGoogle Scholar
Barton, K (2018) MuMIn: Multi-Model Inference. R package version 1.42.1. https://cran.rproject.org/web/packages/MuMIn/index.html.Google Scholar
Bregman, TP, Sekercioglu, CH and Tobias, JA (2014) Global patterns and predictors of bird species responses to forest fragmentation: implications for ecosystem function and conservation. Biological Conservation 169, 372383.CrossRefGoogle Scholar
Bovendorp, RS, McCleery, RA and Galetti, M (2017) Optimizing sampling methods for small mammals communities in Neotropical Rain Forest. Mammal Review 47, 148158.CrossRefGoogle Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (2nd edn). New York, NY: Springer Science & Business Media.Google Scholar
Castro, EBV and Fernandez, FAS (2004) Determinants of differential extinction vulnerabilities of small mammals in Atlantic forest fragments in Brazil. Biological Conservation 119, 7380.CrossRefGoogle Scholar
Chiarello, AG (1999) Effects of fragmentation of the Atlantic forest on mammal communities in south-eastern Brazil. Biological Conservation 89, 7182.CrossRefGoogle Scholar
Costa, LP, Leite, YL, Da Fonseca, GA and Da Fonseca, MT (2000) Biogeography of South American forest mammals: endemism and diversity in the Atlantic Forest. Biotropica 32, 872881.CrossRefGoogle Scholar
Dalmagro, AD and Vieira, EM (2005) Patterns of habitat utilization of small rodents in an area of Araucaria forest in Southern Brazil. Austral Ecology 30, 353362.CrossRefGoogle Scholar
Dauber, J, Hirsch, M, Simmering, D, Waldhardt, R, Otte, A and Wolters, V (2003) Landscape structure as an indicator of biodiversity: matrix effects on species richness. Agriculture, Ecosystems and Environment 98, 321329.CrossRefGoogle Scholar
De Bondi, N, White, JG, Stevens, M and Cooke, R (2010) A comparison of the effectiveness of camera trapping and live trapping for sampling terrestrial small-mammal communities. Wildlife Research 37, 456465.CrossRefGoogle Scholar
Dean, W (1996) A ferro e fogo: a história e a devastação da Mata Atlântica Brasileira. São Paulo: Companhia das Letras.Google Scholar
Delciellos, AC, Barros, CS, Prevedello, JA, Ferreira, MS, Cerqueira, R and Vieira, MV (2018) Habitat fragmentation affects individual condition: evidence from small mammals of the Brazilian Atlantic Forest. Journal of Mammalogy 99, 936945.CrossRefGoogle Scholar
Driscoll, DA, Banks, SC, Barton, PS, Lindenmayer, DB and Smith, AL (2013) Conceptual domain of the matrix in fragmented landscapes. Trends in Ecology and Evolution 28, 605613.CrossRefGoogle ScholarPubMed
Fahrig, L (2003) Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics 34, 487515.CrossRefGoogle Scholar
Fahrig, L (2017) Ecological responses to habitat fragmentation per se. Annual Review of Ecology, Evolution, and Systematics 48, 123.CrossRefGoogle Scholar
Fahrig, L, Arroyo-Rodríguez, V, Bennett, JR, Boucher-Lalonde, V, Cazetta, E, Currie, DJ, Eigenbrod, F, Ford, AT, Harrison, SP, Jaeger, JAG, Koper, N, Martin, AE, Martin, JL, Metzger, JP, Morrison, P, Rhodes, JR, Saunders, DA, Simberloff, D, Smith, AC, Tischendorf, L, Vellend, M and Watling, JI (2019) Is habitat fragmentation bad for biodiversity? Biological Conservation 230, 179186.CrossRefGoogle Scholar
Feliciano, BR, Fernandez, FAS, Freitas, D and Figueiredo, MSL (2002) Population dynamics of small rodents in a grassland between fragments of Atlantic Forest in southeastern Brazil. Mammalian Biology 67, 304314.CrossRefGoogle Scholar
Figueiredo, MS, Barros, CS, Delciellos, AC, Guerra, EB, Cordeiro-Estrela, P, Kajin, M, Alvarez, MR, Asfora, PH, Astúa, D, Bergallo, HG, Cerqueira, R, Geise, L, Gentile, R, Grelle, CEV, Iack-Ximenes, GE, Oliveira, LC, Weksler, M and Vieira, MV (2017) Abundance of small mammals in the Atlantic Forest (ASMAF): a data set for analyzing tropical community patterns. Ecology 98, 2981.CrossRefGoogle ScholarPubMed
Fletcher, Jr, RJ, Didham, RK, Banks-Leite, C, Barlow, J, Ewers, RM, Rosindell, J, Holt, RD, Gonzalez, A, Pardini, R, Damschen, EI, Melo, FPL, Ries, L, Prevedello, JA, Tscharntke, T, Laurance, WF, Lovejoy, T and Haddad, NM (2018) Is habitat fragmentation good for biodiversity? Biological Conservation 226, 915.CrossRefGoogle Scholar
Gascon, C, Lovejoy, TE, Bierregaard, Jr, RO, Malcolm, JR, Stouffer, PC, Vasconcelos, HL, Laurance, WF, Zimmerman, B, Tocher, M and Borges, S (1999) Matrix habitat and species richness in tropical forest remnants. Biological Conservation 91, 223229.CrossRefGoogle Scholar
Gaston, KJ (2000) Global patterns in biodiversity. Nature 405, 220227.CrossRefGoogle ScholarPubMed
Graipel, ME, Cherem, JJ, Monteiro-Filho, ELA and Glock, L (2006) Dinâmica populacional de marsupiais e roedores no parque municipal da lagoa do peri, ilha de Santa Catarina, sul do Brasil. Mastozoologia Neotropical 13, 3149.Google Scholar
Grazzini, G, Mochi-Junior, CM, De Oliveira, H, Pontes, JS, Gatto-Almeida, F and Tiepolo, LM (2015) Identidade, riqueza e abundância de pequenos mamíferos (Rodentia e Didelphimorphia) de área de Floresta com Araucária no estado do Paraná, Brasil. Papéis Avulsos de Zoologia 55, 217230.CrossRefGoogle Scholar
Haddad, NM, Brudvig, LA, Clobert, J, Davies, KF, Gonzalez, A, Holt, RD, Lovejoy, TE, Sexton, JO, Austin, MP, Collins, CD, Cook, WM, Damschen, EI, Ewers, RM, Foster, BL, Jenkins, CN, King, AJ, Laurance, WF, Levey, DJ, Margules, CR, Melbourne, BA, Nicholls, AO, Orrock, JL, Song, DX and Townshend, JR (2015) Habitat fragmentation and its lasting impact on Earthʼs ecosystems. Science Advances 1, e1500052.CrossRefGoogle ScholarPubMed
Hill, JK and Hamer, KC (2004) Determining impacts of habitat modification on diversity of tropical forest fauna: the importance of spatial scale. Journal of Applied Ecology 41, 744754.CrossRefGoogle Scholar
ICMBIO (2016) Sumário executivo do livro vermelho da fauna brasileira ameaçada de extinção. Disponível em. https://www.icmbio.gov.br/portal/images/stories/comunicacao/publicacoes/publicacoes-diversas/dcom_sumario_executivo_livro_vermelho_ed_2016.pdf.Google Scholar
Karp, DS, Rominger, AJ, Zook, J, Ranganathan, J, Ehrlich, PR and Daily, GC (2012) Intensive agriculture erodes betadiversity at large scales. Ecology Letters 15, 963970.CrossRefGoogle Scholar
Krauss, J, Bommarco, R, Guardiola, M, Heikkinen, RK, Helm, A, Kuussaari, M, Lindborg, R, Ockinger, E, Partel, M, Pino, J, Poyry, J, Raatikainen, KM, Sang, A, Stefanescu, C, Teder, T, Zobel, M and Steffan-Dewenter, I (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecology Letters 13, 597605.CrossRefGoogle ScholarPubMed
Kupfer, JA, Malanson, GP and Franklin, SB (2006) Not seeing the ocean for the islands: the mediating influence of matrix-based processes on forest fragmentation effects. Global Ecology and Biogeography 15, 820.CrossRefGoogle Scholar
Lyra-Jorge, MC and Pivello, VR (2001) Combining live traps and pitfalls to survey small mammals in cerrado (Brazilian savanna) habitats. Mammalia 65, 524530.Google Scholar
Magioli, M, Ribeiro, MC, Ferraz, KMPMB and Rodrigues, MG (2015) Thresholds in the relationship between functional diversity and patch size for mammals in the Brazilian Atlantic Forest. Animal Conservation 18, 499511.CrossRefGoogle Scholar
Meixler, MS, Fisher, K and Sanderson, EW (2019) Latitude-enhanced species-area relationships for conservation planning. Landscape Ecology 34, 18771888.CrossRefGoogle Scholar
Milborrow, S (2017) rpart.plot: Plot ‘rpart’ Models: An Enhanced Version of ‘plot. rpart’. R package version 2.1.2. https://mran.microsoft.com/snapshot/2017-12-15/web/packages/rpart.plot/index.html.Google Scholar
Moura, MC, Grelle, CEV and Bergallo, HG (2008) How does sampling protocol affect the richness and abundance of small mammals recorded in tropical forest? An example from the Atlantic Forest, Brazil. Neotropical Biology and Conservation 3, 5158.Google Scholar
Olifiers, N, Gentile, R and Fiszon, JT (2005) Relation between small-mammal species composition and anthropic variables in the Brazilian Atlantic Forest. Brazilian Journal of Biology 65, 495501.CrossRefGoogle ScholarPubMed
Pardini, R (2004) Effects of forest fragmentation on small mammals in an Atlantic Forest landscape. Biodiversity and Conservation 13, 25672586.CrossRefGoogle Scholar
Pardini, R, de Souza, SM, Braga-Neto, R and Metzger, JP (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, 253266.CrossRefGoogle Scholar
Pardini, R, Faria, D, Accacio, GM, Laps, RR, Mariano-Neto, E, Paciencia, ML, Dixo, M and Baumgarten, J (2009) The challenge of maintaining Atlantic forest biodiversity: a multi-taxa conservation assessment of specialist and generalist species in an agro-forestry mosaic in southern Bahia. Biological Conservation 142, 11781190.CrossRefGoogle Scholar
Pardini, R, Bueno, AA, Gardner, TA, Prado, PI and Metzger, JP (2010) Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. PLoS ONE 5, e13666.CrossRefGoogle ScholarPubMed
Passamani, M (1995) Vertical stratification of small mammals in Atlantic Hill forest. Mammalia 59, 276279.Google Scholar
Passamani, M and Fernandez, FAS (2011) Abundance and richness of small mammals in fragmented Atlantic Forest of southeastern Brazil. Journal of Natural History 45, 553565.CrossRefGoogle Scholar
Paviolo, A, De Angelo, C, Ferraz, KM, Morato, RG, Pardo, JM, Srbek-Araujo, AC, Beisiegel, BM, Lima, F, Sana, D, da Silva, MX, Velázquez, MC, Cullen, L, Crawshaw, Jr, P, Jorge, MLSP, Galetti, P, Di Bitetti, MS, de Paula, RC, Eizirik, E, Aide, TM, Cruz, P, Perilli, MLL, Souza, ASM, Quiroga, V, Nakano, E, Pinto, FR, Fernández, S, Costa, S, Moraes, Jr, EA and Azevedo, F (2016) A biodiversity hotspot losing its top predator: the challenge of jaguar conservation in the Atlantic Forest of South America. Scientific Reports 6, 37147.CrossRefGoogle ScholarPubMed
Pfeifer, M, Lefebvre, V, Peres, CA, Banks-Leite, C, Wearn, OR, Marsh, CJ, Butchart, SHM, Arroyo- Rodríguez, , Barlow, J, Cerezo, A, Cisneros, L, D’Cruze, N, Faria, D, Hadley, A, Harris, S, Klingbeil, BT, Kormann, U, Leans, L, Medina-Rangel, GF, Morante-Filho, JC, Olivier, P, Peters, SL, Pidgeon, A, Ribeiro, DB, Scherber, C, Schneider-Maunory, L, Struebig, M, Urbina-Cardona, N, Watlling, JI, Willig, MR, Wood, EM and Ewers, RM (2017) Creation of forest edges has a global impact on forest vertebrates. Nature 551, 187191.CrossRefGoogle Scholar
Pianka, ER (1966) Latitudinal gradients in species diversity: a review of concepts. American Naturalist 100, 3346.CrossRefGoogle Scholar
Pires, AS, Fernandez, FAS, Barros, CS, Rocha, CFD and Bergallo, HG (2006) Vivendo em um mundo em pedaços: efeitos da fragmentação florestal sobre comunidades e populações animais. In Rocha, CFD, Bergallo, HG, Van-Sluys, M, Alves, MAS (eds), Biologia da conservação: essências. São Carlos: Rima Editora, pp. 231260.Google Scholar
Pires, AS, Lira, PK, Fernandez, FAS, Schittini, GM and Oliveira, LC (2002) Frequency of movements of small mammals among Atlantic Coastal Forest fragments in Brazil. Biological Conservation 108, 229237.CrossRefGoogle Scholar
Prevedello, JA and Vieira, MV (2010) Does the type of matrix matter? A quantitative review of the evidence. Biodiversity and Conservation 19, 12051223.CrossRefGoogle Scholar
Püttker, T, Pardini, R, Meyer-Lucht, Y and Sommer, S (2008) Responses of five small mammal species to micro-scale variations in vegetation structure in secondary Atlantic Forest remnants, Brazil. BMC Ecology 8, 9.CrossRefGoogle ScholarPubMed
Püttker, T, Bueno, AA, Barros, CS, Sommer, S and Pardini, R (2011) Immigration rates in fragmented landscapes – empirical evidence for the importance of habitat amount for species persistence. PLoS ONE 6, e27963.CrossRefGoogle ScholarPubMed
Püttker, T, Bueno, AA, Barros, CS, Sommer, S and Pardini, R (2013) Habitat specialization interacts with habitat amount to determine dispersal success of rodents in fragmented landscapes. Journal of Mammalogy 94, 714726.CrossRefGoogle Scholar
Pyron, RA and Wiens, JJ (2013) Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity. Proceedings of the Royal Society B: Biological Sciences 280, 20131622.CrossRefGoogle ScholarPubMed
Ribeiro, MC, Metzger, JP, Martensen, AC, Ponzoni, FJ and Hirota, MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142, 11411153.CrossRefGoogle Scholar
Ribeiro, MC, Martensen, AC, Metzger, JP, Tabarelli, M, Scarano, F and Fortin, MJ (2011) The Brazilian Atlantic Forest: a shrinking biodiversity hotspot. In Zachos, F and Habel, J (eds), Biodiversity Hotspots. Berlin: Springer, pp. 405434.CrossRefGoogle Scholar
R Core Team (2018) Version 3.5.1. Vienna: R Foundation for Statistical Computing. https://www.r-project.org.Google Scholar
Ribeiro-Júnior, MA, Rossi, RV, Miranda, CL and Ávila-Pires, TC (2011) Influence of pitfall trap size and design on herpetofauna and small mammal studies in a Neotropical Forest. Zoologia 28, 8091.CrossRefGoogle Scholar
Rohde, K (1992) Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65, 514527.CrossRefGoogle Scholar
Santos-Filho, MD, Lázari, PRD, Sousa, CPFD and Canale, GR (2015) Trap efficiency evaluation for small mammals in the southern Amazon. Acta Amazon 45, 187194.CrossRefGoogle Scholar
Silva, JMC and Tabarelli, M (2000) Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature 404, 72.CrossRefGoogle Scholar
Silva, JMC, de Sousa, MC and Castelletti, CH (2004) Areas of endemism for passerine birds in the Atlantic forest, South America. Global Ecology and Biogeography 13, 8592.CrossRefGoogle Scholar
Sigrist, MS and Carvalho, CJBD (2008) Detection of areas of endemism on two spatial scales using Parsimony Analysis of Endemicity (PAE): the Neotropical region and the Atlantic Forest. BiotaNeotropica 8. https://doi.org/10.1590/S1676-06032008000400002.Google Scholar
Sólymos, P and Lele, SR (2012) Global pattern and local variation in species–area relationships. Global Ecology and Biogeography 21, 109120.CrossRefGoogle Scholar
Souza, JB and Alves, RRN (2014) Hunting and wildlife use in an Atlantic Forest remnant of northeastern Brazil. Tropical Conservation Science 7, 145160.CrossRefGoogle Scholar
Stevens, GC (1989) The latitudinal gradient in geographical range: how so many species coexist in the tropics. American Naturalist 133, 240256.CrossRefGoogle Scholar
Therneau, T, Atkinson, B, Ripley, B and Ripley, MB (2018) Package ‘rpart’. cran.ma.ic.ac.uk/web/packages/rpart/rpart.pdf.Google Scholar
Umetsu, F and 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, 517530.CrossRefGoogle Scholar
Umetsu, F, Naxara, L and Pardini, R (2006) Evaluating the efficiency of pitfall traps for sampling small mammals in the Neotropics. Journal of Mammalogy 87, 757765.CrossRefGoogle Scholar
Vieira, EM and Monteiro-Filho, ELA (2003) Vertical stratification of small mammals in the Atlantic rain forest of south-eastern Brazil. Journal of Tropical Ecology 19, 501507.CrossRefGoogle Scholar
Vieira, MV, Grelle, CEV and Gentile, R (2004) Differential trappability of small mammals in three habitats of southeastern Brazil. Brazilian Journal of Biology 64, 895900.CrossRefGoogle ScholarPubMed
Vieira, MV, Olifiers, N, Delciellos, AC, Antunes, VZ, Bernardo, LR, Grelle, CE and 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, 11911200.CrossRefGoogle Scholar
Willig, MR, Kaufman, DM and Stevens, RD (2003) Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annual Review of Ecology, Evolution, and Systematics 34, 273309.CrossRefGoogle Scholar
Zhang, H and Singer, BH (2010) Recursive Partitioning and Applications. New York, NY: Springer Science & Business Media.CrossRefGoogle Scholar
Supplementary material: File

Rodrigues et al. supplementary material

Rodrigues et al. supplementary material 3

Download Rodrigues et al. supplementary material(File)
File 87.8 KB
Supplementary material: File

Rodrigues et al. supplementary material

Rodrigues et al. supplementary material 1

Download Rodrigues et al. supplementary material(File)
File 26.6 KB
Supplementary material: File

Rodrigues et al. supplementary material

Rodrigues et al. supplementary material 2

Download Rodrigues et al. supplementary material(File)
File 18.2 KB