Skip to main content

Advertisement

Log in

Testing the habitat amount hypothesis and fragmentation effects for medium- and large-sized mammals in a biodiversity hotspot

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Context

Habitat loss is widely recognized as the main driver of biodiversity loss around the globe, yet the effects of habitat fragmentation on biodiversity have been extensively debated in recent years.

Objectives

We used a robust dataset of medium and large-sized mammals to test (a) the Habitat Amount Hypothesis, which postulates that species richness can be mainly predicted by the total amount of habitat surrounding the sampling site, and (b) the effects of habitat fragmentation per se, which may be expected to be weak or mainly positive on species richness.

Methods

We compiled information on the occurrence of mammal species in 166 forest fragments across the Atlantic Forest. For each forest fragment, we extracted information on patch size, percentage of forest cover (a proxy for habitat amount), and edge density and number of fragments (fragmentation metrics). We related these metrics to mammalian richness considering separately for all species, forest-dependent species, disturbance-tolerant species, and different trophic guilds.

Results

All richness measures strongly declined with decreasing forest cover, yet were unaffected by patch size, number of patches and edge density. The only exception occurred with herbivore richness, which was affected by number of patches. However, we found fragmentation per se effects only for herbivore richness.

Conclusions

Our results show that mammal richness increased with habitat amount at the landscape, whereas habitat fragmentation per se had significant negative impacts on herbivores only. We therefore recommend maintaining highly forested landscapes and restoring severely deforested areas, being essential for ensuring high richness of mammals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Data will be available from the Figshare Repository.

References

  • Arroyo-Rodríguez V, Fahrig L, Tabarelli M, Watling JI, Tischendorf L, Benchimol M, Cazetta E, Faria D, Leal IR, Melo FPL, Morante-Filho JC, Santos BA, Arasa-Gisbert R, Arce-Peña N, Cervantes-López MJ, Cudney-Valenzuela S, Galán-Acedo C, San-José M, Vieira ICG, Slik JWF, Nowakowski AJ, Tscharntke T (2020) Designing optimal human-modified landscape for forest biodiversity conservation. Ecol Lett 23:1404–1420

  • Barton K (2020) Multi-Model Inference: Package 'MuMIn'. R package version 1.43.17. https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48

    Google Scholar 

  • Beca G, Vancine MH, Carvalho CS, Pedrosa F, Alves RSC, Buscariol D, Peres CA, Ribeiro MC, Galetti M (2017) High mammal species turnover in forest patches immersed in biofuel plantations. Biol Conserv 210:352–359

    Google Scholar 

  • Bello C, Galetti M, Pizo MA, Magnago LFS, Rocha MF, Lima RAF, Peres CA, Ovaskainen O, Jordano P (2015) Defaunation affects carbon storage in tropical forests. Sci Adv 1:e1501105

    PubMed  PubMed Central  Google Scholar 

  • Benchimol M, Peres CA (2015) Widespread forest vertebrate extinctions induced by a mega hydroelectric dam in lowland Amazonia. PLoS ONE 10:e0129818

    PubMed  PubMed Central  Google Scholar 

  • Bogoni JA, Cherem JJ, Giehl ELH, Oliveira-Santos LG, De Castilho PV, Filho VP, Fantacini FM, Tortato MA, Luiz MR, Rizzaro R, Graipel ME (2016) Landscape features lead to shifts in communities of medium-to large-bodied mammals in subtropical Atlantic Forest. J Mamm 97:713–725

    Google Scholar 

  • Brady MJ, McAlpline CA, Possingham HP, Miller CJ, Baxter GS (2011) Matrix is important for mammals in landscapes with small amounts of native forest habitat. Landsc Ecol 26:617–628

    Google Scholar 

  • Bueno AS, Peres CA (2019) Patch-scale biodiversity retention in fragmented landscapes: Reconciling the habitat amount hypothesis with the island biogeography theory. J Biogeogr 46:621–632

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model Selection and Multimodel Inference: a pratical information—theoric approach, 2nd edn. Springer, New York

    Google Scholar 

  • Canale GR, Peres CA, Guidorizzi CE, Gatto CAF, Kierulff MCM (2012) Pervasive defaunation of forest remnants in a tropical biodiversity hotspot. PLoS ONE 7:e41671

    CAS  PubMed  PubMed Central  Google Scholar 

  • Core Team R (2018) R: A language and Environment for Statistical Computing. Viena, Austria: R Foundation for Statistical Computing. Retrieved from https://www.r-project.org/

  • Cullen L Jr, Bodmer RE, Pádua CV (2000) Effects of hunting in habitat fragments of the Atlantic forests, Brazil. Biol Cons 95:49–56

    Google Scholar 

  • Curtis PG, Slay CM, Harris NL, Tyukavina A, Hansen MC (2018) Classifying drivers of global forest loss. For Ecol 361:1108–1111

    CAS  Google Scholar 

  • De Camargo RX, Boucher-Lalonde V, Currie DJ (2018) At the landscape level, birds respond strongly to habitat amount but weakly to fragmentation. Divers Distrib 24:629–639

    Google Scholar 

  • Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46

    Google Scholar 

  • Emmons L, Feer F (1997) Neotropical rainforest mammals: a field guide, 2nd edn. University of Chicago Press, Chicago

    Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Google Scholar 

  • Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40:1649–1663

    Google Scholar 

  • Fahrig L (2017) Ecological responses to habitat fragmentation per se. Annu Rev Ecol Evol Syst 48:1–23

    Google Scholar 

  • Fahrig L, Arroyo-Rodríguez V, Bannett 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, Watling JI (2019) Is habitat fragmentation bad for biodiversity? Biol Conserv 230:179–186

  • Fletcher RJ, Didham RK, Ewers RM, Ries L, Laurance WF, 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, Haddad NM (2018) Is habitat fragmentation good for biodiversity? Biol Conserv 226:9–15

  • Galetti M, Keuroghlian A, Hanada L, Morato MI (2001) Frugivory and seed dispersal by the lowland tapir (Tapirus terrestris) in Southeast Brazil. Biotropica 33:723–726

    Google Scholar 

  • Galetti M, Giacomini HC, Bueno RS, Bernardo CSS, Marques RM, Bovendorp RS, Steffer CE, Rubim P, Gobbo SK, Donatti CI, Begotti RA, Meirelles F, Nobre RA, Chiarello AG, Peres CA (2009) Priority areas for the conservation of Atlantic forest large mammals. Biol Conserv 142:1229–1241

    Google Scholar 

  • Galetti M, Dirzo R (2013) Ecological and evolutionary consequences of living in a defaunated world. Biol Conserv 163:1–6

    Google Scholar 

  • Galetti M, Guevara R, Neves CL, Rodarte RR, Bovendorp R, Moreira M, Hopkins JB III, Yeakel JD (2015) Defaunation affects the populations and diets of rodents in Neotropical rainforests. Biol Conserv 190:2–7

    Google Scholar 

  • Gibbs HK, Ruesch AS, Clayton MK, Holmgren P, Foley JA, Ramankutty N, Achard F (2010) Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. Proc Natl Acad Sci USA 107:16732–16737

    CAS  PubMed  Google Scholar 

  • Graipel ME, Cherem JJ, Monteiro-Filho ELA, Carmignotto AP (2017) Mamíferos da Mata Atlântica. In: Monteiro-Filho ELA, Conte CE (eds) Revisões de Zoologia: Mata Atlântica (pp 391–482). Ed. UFPR

  • Haddad NM, Gonzalez A, Brudvig LA, Burt MA, Levey DJ, Damschen EI (2016) Experimental evidence does not support the Habitat Amount Hypothesis. Ecography 40:48–55

    Google Scholar 

  • Harper KA, Macdonald SE, Burton PK, Chen JQ, Brosofske KD, Saunders SC, Euskirchen ES, Roberts D, Jaiteh MS, Esseen PA (2005) Edge influence on forest structure and composition in fragmented landscapes. Conserv Biol 19:768–782

    Google Scholar 

  • Huais PY (2018) Multifit: an R function for multi-scale analysis in landscape ecology. Landsc Ecol 33:1023–1028

    Google Scholar 

  • IBGE (2017) Base cartográfica Nacional IBGE. http://forest-gis.com/download-de-shapefiles/

  • IUCN (2019) The IUCN red list of threatened species. https://www.iucnredlist.org/

  • Jorge MLSP, Galetti M, Ribeiro MC, Ferraz KMPMB (2013) Mammal defaunation as surrogate of trophic cascades in a biodiversity hotspot. Biol Conserv 163:49–57

    Google Scholar 

  • Lees AC, Peres CA (2009) Gap-crossing movements predict species occupancy in Amazonian forest fragments. Oikos 118:280–290

    Google Scholar 

  • Lima F, Beca G, Muylaert RL, Jenkins CN, Perili MLL, Paschoal AMO, Massara RL, Paglia AP, Chiarello AG, Graipel ME, Cherem JJ, Regolin AL, Santos LGRO, Brocardo CR, Paviolo A, Di Bitetti MS, Scoss LM, Rocha FL, Fusco-Costa R, Rosa CA, Da Silva MX, Hufnagell L, Santos PM, Duarte GT, Guimarães LN, Bailey LL, Rodrigues FHG, Cunha HM, Fantacini FM, Batista GO, Bogoni JA, Tortato MA, Luiz MR, Peroni N, De Castilho PV, Maccarini TB, Filho VP, De Angelo C, Cruz P, Quiroga V, Iezzi ME, Varela D, Cavalcanti SMC, Martensen AC, Maggiorini EV, Keesen FF, Nunes AV, Lessa GM, Cordeiro-Estrela P, Beltrão MG, De Albuquerque ACF, Ingberman B, Cassano CR, Cullen Jr LC, Ribeiro MC, Galetti M (2017) ATLANTIC-CAMTRAPS: a dataset of medium and large terrestrial mammal communities in the Atlantic Forest South America. Ecology 98:1–32

  • Lindenmayer DB, Fischer J (2007) Tackling the habitat fragmentation panchreston. Trends Ecol Evol 22:127–132

    PubMed  Google Scholar 

  • Lindenmayer DB, Blanchard W, Foster CN, Scheele BC, Westgate MJ, Stein J, Crane M, Florance D (2020) Habitat amount versus connectivity: an empirical study of bird responses. Biol Conserv 241:108377

  • Lyra-Jorge MC, Ribeiro MC, Ciochete G, Tambosi LR, Pivello VR (2010) Influence of multi-scale landscape structure on the occurrence of carnivorous mammals in a human-modified savanna, Brazil. Eur J Wild Res 56:359–368

    Google Scholar 

  • MacArthur RH, Wilson EO (1963) An equilibrium theory of insular zoogeography. Evolution (NY) 17: 373–387.

  • Magioli M, Ribeiro MC, Ferraz KMPM, Rodrigues MG (2015) Thresholds in the relationship between functional diversity and patch size for mammals in the Brazilian Atlantic Forest. Anim Conser 18:499–511

    Google Scholar 

  • Martin AE, Fahrig L (2012) Measuring and selecting scales of effect for landscape predictors in species–habitat models. Ecol Appl 22:2277–2292

    PubMed  Google Scholar 

  • Melo GL, Sponchiado J, Cáceres NC, Fahrig L (2017) Testing the habitat amount hypothesis for South American small mammals. Biol Conserv 209:304–314

    Google Scholar 

  • Merckx T, Miranda MD, Pereira HM (2019) Habitat amount, not patch size and isolation, drives species richness of macro-moth communities in countryside landscapes. J Biogeogr 46:956–967

    Google Scholar 

  • Michalski F, Peres CA (2007) Disturbance-mediated mammal persistence and abundance-area relationships in Amazonian Forest fragments. Conserv Biol 21:1626–1640

    PubMed  Google Scholar 

  • Miller-Rushing AJ, Primack RB, Devictor V, Corlett RT, Cumming GS, Loyola R, Maas B, Pejchar L (2019) How does habitat fragmentation affect biodiversity? A controversial question at the core of conservation biology. Biol Conser 232:271–273

    Google Scholar 

  • MMA (2014) Lista Nacional Oficial de Espécies Ameaçadas de Extinção. http://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?jornal=1&pagina=121&data=18/12/2014

  • Morante-Filho JC, Benchimol M, Faria D (2020) Landscape composition is the strongest determinant of bird occupancy patterns in tropical forest patches. Landsc Ecol. https://doi.org/10.1007/s10980-020-01121-6

    Article  Google Scholar 

  • Mortelliti A, Fagiani S, Battisti C, Capizzi D, Boitani L (2010) Independents effects of habitat loss, habitat fragmentation and structural connectivity on forest-dependent birds. Divers Distrib 16:941–951

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    CAS  Google Scholar 

  • Murcia C (1995) Edge effects in fragmented forests: implications for conservation. TREE 10:58–62

    CAS  PubMed  Google Scholar 

  • Newbold T, Hudson LN, Arnell AP, Contu S, Palma A, Ferrier S, Hill SLL, Hoskins AJ, Lysenko I, Phillips HRP, Burton VJ, Chng CWT, Emerson S, Gao D, Pask-Hale G, Hutton J, Jung M, Sanchez-Ortiz K, Simmons BI, Whitmee S, Zhang H, Scharlemann JPW, Purvis A (2016) Has land use pushed terrestrial biodiversity beyond the planetary boundary? A global assessment. Science 353:288–291

  • Newbold T, Ingram DJ, Collen B, Newbold T, Mace GM, De Palma A , Díaz S, Echeverria-Londoño S, Edgar MJ, Feldman A, Garon M, Harrison MLK, Alhusseini T, Ingram DJ, Itescu Y, Kattge J, Kemp V, Kirkpatrick L, Kleyer M, Correia DLP, Martin CD, Meiri S, Novosolov M, Pan Y, Phillips HRP, Purves DW, Robinson A, Simpson J, Tuck SL, Weiher E, White HJ, Ewers RM, Mace GM, Scharlemann JPW, Purvis A (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50

  • Paglia AP, da Fonseca GA, Rylands AB, Herrmann G, Aguiar LM, Chiarello AG, Leite YLR, Costa LP, Siciliano S, Kierulff MCM, Mendes SL, Tavares VC, Mittermeier RA, Patton JL (2012) Lista anotada dos mamíferos do Brasil/Annotated checklist of Brazilian mammals (2nd ed.). Arlington, Occasional Papers in Conservation Biology, 6

  • Palmeirim AF, Figueiredo MSL, Grelle CEV, Carbone C, Vieira MV (2019) When does habitat fragmentation matter? A biome-wide analysis of small mammals in the Atlantic Forest. J Biogeogr 46:2811–2825

    Google Scholar 

  • Pfeifer M, Lefebvre V, Peres CA, Banks-Leite C, Wearn OR, Marsh CJ, Butchart SHM, Arroyo-Rodríguez V, Barlow J, Cerezo A, Cisneros L, D'Cruze N, Faria D, Hadley A, Harris SM, Klingbeil BT, Kormann U, Lens L, Medina-Rangel GF, Morante-Filho JC, Olivier P, Peters SL, Pidgeon A, Ribeiro DB, Scherber C, Schneider-Maunoury L, Struebig M, Urbina-Cardona N, Watling JI, Willing MR, Wood EM, Ewers RM (2017) Creation of forest edges has a global impact on forest vertebrates. Nature 551:187–191

  • Projeto MapBiomas (2019) MapBiomas Project, Collection [4] of the Annual Land Use Land Cover Maps of Brazil. http://mapbiomas.org

  • QGIS Development Team (2019) Quantum GIS Geographic Information System. Open Source Geospatial Foundation Project. https://qgis.org/en/site/

  • Regolin AL, Cherem JJ, Graipel ME, Bogoni JA, Ribeiro JW, Vancine MH, Tortato MA, Oliveira-Santos LG, Fantacini FM, Luiz MR, De Castilho PV, Ribeiro MC, Cáceres NC (2017) Forest cover influences occurrence of mammalian carnivores within Brazilian Atlantic Forest. J Mammal 98:1721–1731

    Google Scholar 

  • Regolin AL, Ribeiro MC, Martello F, Melo GL, Sponchiado J, Campanha LFC, Sugai LSM, Silva TSF, Cáceres NC (2020) Spatial heterogeneity and habitat configuration overcome habitat composition influences on alpha and beta mammal diversity. Biotropica. https://doi.org/10.1111/btp.12800

  • Reino L, Beja P, Araújo MB, Dray S, Segurado P (2013) Does local habitat fragmentation affect large-scale distributions? The case of a specialist grassland bird. Divers Distrib 19:423–432

    Google Scholar 

  • Rezende CL, Scarano FR, Assad ED, Joly CA, Metzger JP, Strassburg BBN, Tabarelli M, Fonseca GA, Mittermeier RA (2018) From hotspot to hopespot : An opportunity for the Brazilian Atlantic. PECON 16:208–214

  • Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153

    Google Scholar 

  • Ries L, Sisk TD (2004) A predictive model of edge effects. Ecology 85:2917–2926

    Google Scholar 

  • Rueda M, Hawkins BA, Morales-Castilla I, Vidanes RM, Ferrero M, Rodríguez MÁ (2013) Does fragmentation increase extinction thresholds ? A European-wide test with seven forest birds. Glob Ecol Biogeogr 22:1282–1292

    Google Scholar 

  • Seibold S, Bässler C, Brandl R, Fahrig L, Heurich M, Hothorn T, Scheipl F, Thorn S, Müller J (2017) An experimental test of the habitat-amount hypothesis for saproxylic beetles in a forested region. Ecology 98:1613–1622

  • Souza Y, Gonçalves F, Lautenschlager L, Akkawi P, Mendes C, Carvalho MM, Bovendorp RS, Fernandes-Ferreira H, Rosa C, Graipel ME, Peroni N, Cherem JJ, Bogoni JA, Brocardo CR, Miranda J, Silva LZ, Melo G, Cáceres N, Sponchiado J, Ribeiro MC, Galetti M  (2019) ATLANTIC MAMMALS: a data set of assemblages of medium- and large-sized mammals of the Atlantic Forest of South America. Ecology 100:e02785

  • Venables WN, Ripley BD (2002) Modern Applied Statistics with S. (4nd ed.) ISBN 0-387-95457-0. Springer, New York.

  • Vieira MV, Almeida-Gomes M, Delciellos AC, Cerqueira R, Crouzeilles R (2018) Fair tests of the habitat amount hypothesis require appropriate metrics of patch isolation: An example with small mammals in the Brazilian Atlantic Forest. Biol Conser 226:264–270

    Google Scholar 

  • Watling JI, Arroyo-Rogríguez V, Pfeifer M, Baeten L, Banks-Leite C, Cisneros LM, Fang R, Hamel-Leigue AC, Lachat T, Leal IR, Lens L, Possingham HP, Raheem DC, Ribeiro DB, Slade EM, Urbina-Cardona JN, Wood EM, Fahrig L (2020) Support for the habitat amount hypothesis from a global synthesis of species density studies. Ecol Lett 23:674–681

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GH (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Google Scholar 

Download references

Acknowledgements

We thank the Centre for Research and Conservation, Royal Zoological Society of Antwerp for the doctoral scholarship, the Universidade Estadual de Santa Cruz—(PROPP, 00220.1100.1840), The Rufford Foundation (24655-1) and Idea Wild for funding. E.C. thanks the Conselho Nacional de Desenvolvimento Científico for the productivity fellowship (306373/2018-1). We thank the anonymous reviewer and Victor Arroyo-Rodríguez for their valuable comments on an earlier version of the ms.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elaine Rios.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Electronic supplementary material 1 (DOCX 78 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rios, E., Benchimol, M., Dodonov, P. et al. Testing the habitat amount hypothesis and fragmentation effects for medium- and large-sized mammals in a biodiversity hotspot. Landscape Ecol 36, 1311–1323 (2021). https://doi.org/10.1007/s10980-021-01231-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-021-01231-9

Keywords

Navigation