Abstract
Objectives
Harmful effects of habitat loss and fragmentation can be detected across multiple spatial scales, yet most studies that aim to characterize these effects take place at a single spatial scale. Here we investigated responses in ant diversity to forest fragmentation across three spatial scales.
Methods
We sampled ant diversity in a fragmented landscape in southeastern Brazil. We set transects with 15 pitfall traps (local scale response) within 16 forest fragments (fragment scale response) distributed in eight paired fragments separated by roads (mesoscale response). We measured habitat features at local, fragment and mesoscales and across the landscape. For each spatial scale, we then assessed the effects of ecological drivers measured at the same and subsequent higher spatial scales.
Results
Local diversity was higher with closer proximity to the matrix, and in fragments with high vegetation density. Both fragment species richness and β-diversity were higher in less circular fragments. However, at the mesoscale (pairs of fragments), total species richness decreased with increasing pasture matrix in the landscape (landscape driver).
Conclusions
Edge and matrix effects lead to increased ant species richness at small spatial scales (due to an increase in generalist ants). However, when analyzed at a higher spatial scale, the responses to these effects were in fact reversed, leading to a decrease in ant diversity. Thus, we suggest that conservation efforts should take a multi-scale perspective (from local to landscape) and aim to protect both local and fragment characteristics that can buffer edge effects, as well as improve matrix quality in the landscape.
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References
Ahuatzin DA, Corro EJ, Jaimes AA et al (2019) Forest cover drives leaf litter ant diversity in primary rainforest remnants within human-modified tropical landscapes. Biodivers Conserv 28:1091–1107. https://doi.org/10.1007/s10531-019-01712-z
ArcMap ESRI Version 10.1. Environmental Systems Research Institute, Redlands, California
Arroyo-Rodríguez V, Saldaña-Vázquez RA, Fahrig L, Santos BA (2017) Does forest fragmentation cause an increase in forest temperature? Ecol Res 32:81–88. https://doi.org/10.1007/s11284-016-1411-6
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 JF, Nowakowski AJ, Tscharntke T (2020) Designing optimal human‐modified landscapes for forest biodiversity conservation. Ecol Lett. https://doi.org/10.1111/ele.13535
Baccaro FB, Feitosa RM, Fernandez F, Fernandes IO, Izzo TJ, Souza JLP, Solar R (2015) Guia para gêneros de formigas do Brasil. INPA Publishing Company, Manaus
Barton K (2014) MuMIn: Multi-model inference. R package version 1.10.5. https://cran.r-project.org/package=MuMIn
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bestelmeyer BT, Agosti D, Leeanne F, Alonso T, Brandão CRF, Brown WL, Delabie JHC, Silvestre R (2000) Field techniques for the study of ground-living ants: an overview, description, and evaluation. In: Agosti D, Majer JD, Tennant A, Schultz T (eds) Ants: standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press, Washington, pp 122–144
Boesing AL, Nichols E, Metzger JP (2018) Biodiversity extinction thresholds are modulated by matrix type. Ecography 41:1520–1533. https://doi.org/10.1111/ecog.03365
Bolker BM, Brooks ME, Clark CJ et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. https://doi.org/10.1016/j.tree.2008.10.008
Burnham KP, Anderson D (2002) Model Selection and Multimodel Inference. A practical information-theoretic approach. Springer-Verlag, New York
Câmara T, Almeida WR, Tabarelli M, Andersen AN, Leal IR (2017) Habitat fragmentation, EFN-bearing trees and ant communities: Ecological cascades in Atlantic Forest of northeastern Brazil. Austral Ecol 42:31–39. https://doi.org/10.1111/aec.12393
Crist TO (2009) Biodiversity, species interactions, and functional roles of ants (Hymenoptera: Formicidae) in fragmented landscapes: a review. Myrmecol News 12:3–13
Cornell HV, Harrison SP (2014) What Are Species Pools and When Are They Important? Annu Rev Ecol Evols Syst 45:45–67. https://doi.org/10.1146/annurev-ecolsys-120213-091759
Cuissi RG, Lasmar CJ, Moretti TS, Schmidt FA, Fernandes WD, Falleiros AB, Schoereder JH, Ribas CR (2015) Ant community in natural fragments of the Brazilian wetland: species–area relation and isolation. J Insect Conserv 19:531–537. https://doi.org/10.1007/s10841-015-9774-5
Debuse VJ, King J, House AP (2007) Effect of fragmentation, habitat loss and within-patch habitat characteristics on ant assemblages in semi-arid woodlands of eastern Australia. Landsc Ecol 22:731–745. https://doi.org/10.1007/s10980-006-9068-0
Didham RK, Kapos V, Ewers RM (2012) Rethinking the conceptual foundations of habitat fragmentation research. Oikos 121:161–170. https://doi.org/10.1111/j.1600-0706.2011.20273.x
Driscoll DA, Banks SC, Barton PS, Lindenmayer DB, Smith AL (2013) Conceptual domain of the matrix in fragmented landscapes. Trends Ecol Evol 28:605–613. https://doi.org/10.1016/j.tree.2013.06.010
ENVI (2009) ITT Visual Information Solutions. “ENVI user’s guide
Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40:1649–1663. https://doi.org/10.1111/jbi.12130
Fahrig L (2017) Ecological responses to habitat fragmentation per se. Annu Rev Ecol Evol Syst 48:1–23. https://doi.org/10.1146/annurev-ecolsys-110316-022612
Fahrig L (2019) Habitat fragmentation: a long and tangled tale. Global Ecol Biogeogr 28:33–41. https://doi.org/10.1111/geb.12839
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 et al (2019) Is habitat fragmentation bad for biodiversity? Biol Conserv 230:179–186. https://doi.org/10.1016/j.biocon.2018.12.026
Fahrig L (2020) Why do several small patches hold more species than few large patches? Global Ecol Biogeogr 29:615–628. https://doi.org/10.1111/geb.13059
Fardila D, Kelly LT, Moore JL, McCarthy MA (2017) A systematic review reveals changes in where and how we have studied habitat loss and fragmentation over 20 years. Biol Conserv 212:130–138. https://doi.org/10.1016/j.biocon.2017.04.031
Fletcher RJ, Acevedo MA, Robertson EP (2014) The matrix alters the role of path redundancy on patch colonization rates. Ecology 95:1444–1450. https://doi.org/10.1890/13-1815.1
Fletcher RJ, Didham RK, Banks-Leite C, Barlow J, Ewers RM, Rosindell J et al (2018) Is habitat fragmentation good for biodiversity? Biol Conserv 226:9–15. https://doi.org/10.1016/j.biocon.2018.07.022
González E, Buffa L, Defagó MT, Molina SI, Salvo A, Valladares G (2018) Something is lost and something is gained: loss and replacement of species and functional groups in ant communities at fragmented forests. Landsc Ecol 33:2089–2102. https://doi.org/10.1007/s10980-018-0724-y
Haddad NM, Brudvig LA, Clobert J, Davies KF et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:e1500052. https://doi.org/10.1126/sciadv.1500052
Haddad NM, Gonzalez A, Brudvig LA, Burt MA, Levey DJ, Damschen EI (2017) Experimental evidence does not support the habitat amount hypothesis. Ecography 40:48–55. https://doi.org/10.1111/ecog.02535
Hagen M, Kissling WD, Rasmussen C et al (2012) Biodiversity, Species Interactions and Ecological Networks in a Fragmented World. Adv Ecol Res 46:89–210. https://doi.org/10.1016/B978-0-12-396992-7.00002-2
Hendershot JN, Smith JR, Anderson CB, Letten AD, Frishkoff LO, Zook JR et al (2020) Intensive farming drives long-term shifts in avian community composition. Nature 579:393–396. https://doi.org/10.1038/s41586-020-2090-6
Hölldobler B, Wilson EO (1990) The Ants. Harvard University Press, Cambridge
IBGE (2013) Technical manual of Brazilian vegetation. http://www.ibge.gov.br/home/geociencias/recursosnaturais/vegetacao/manual_vegetacao.shtm. Accessed February 2013
Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174
Lasmar CJ, Queiroz ACM, Rabello AM et al (2017) Testing the effect of pitfall-trap installation on ant sampling. Insect Soc 64:445–451. https://doi.org/10.1007/s00040-017-0558-7
Lasmar CJ, Bishop TR, Parr CL, Queiroz ACM, Schmidt FA, Ribas CR (2021) Geographical variation in ant foraging activity and resource use is driven by climate and net primary productivity. J Biogeogr. https://doi.org/10.1111/jbi.14089
Leal IR, Filgueiras BK, Gomes JP, Iannuzzi L, Andersen AN (2012) Effects of habitat fragmentation on ant richness and functional composition in Brazilian Atlantic forest. Biodivers Conserv 21:1687–1701. https://doi.org/10.1007/s10531-012-0271-9
Magnago LFS, Rocha MF, Meyer L et al (2015) Microclimatic conditions at forest edges have significant impacts on vegetation structure in large Atlantic forest fragments. Biodivers Conserv 24:2305–2318. https://doi.org/10.1007/s10531-015-0961-1
MMA. Ministério do Meio Ambiente (2015) Geocatalogo MMA-Rapideye Imagery; MMA: Brasília, Brazil. Available online: http://geocatalogo.mma.gov.br/ (accessed on May 2015)
Martin AE, Fahrig L (2012) Measuring and selecting scales of effect for landscape predictors in species–habitat models. Ecol Appl 22:2277–2292. https://doi.org/10.1890/11-2224.1
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 Conserv 232:271–273
Morante-Filho JC, Arroyo‐Rodríguez V, Faria D (2016) Patterns and predictors of b-diversity in the fragmented Brazilian Atlantic forest: a multiscale analysis of forest specialist and generalist birds. J Anim Ecol 85:240–250. https://doi.org/10.1111/1365-2656.12448
Moreau CS, Bell CD (2013) Testing the museum versus cradle tropical biological diversity hypothesis: phylogeny, diversification, and ancestral biogeographic range evolution of the ants. Evolution 67:2240–2257. https://doi.org/10.1111/evo.12105
Muñoz PT, Torres FP, Megías AG (2015) Effects of roads on insects: a review. Biodivers Conserv 24:659–682. https://doi.org/10.1007/s10531-014-0831-2
Nams VO (2012) Shape of patch edges affects edge permeability for meadow voles. Ecol Appl 22:1827–1837. https://doi.org/10.1890/11-1034.1
Oliveira M, Grillo A, Tabarelli M (2004) Forest edge in the Brazilian Atlantic forest: Drastic changes in tree species assemblages. Oryx 38(4):389–394. https://doi.org/10.1017/S0030605304000754
Peter F, Berens DG, Farwig N (2014) Effects of Local Tree Diversity on Herbivore Communities Diminish with Increasing Forest Fragmentation on the Landscape Scale. PLoS ONE 9(4):e95551. https://doi.org/10.1371/journal.pone.0095551
Pfeifer M, Lefebvre V, Peres CA, Banks-Leite C, Wearn OR, Marsh CJ et al (2017) Creation of forest edges has a global impact on forest vertebrates. Nature 551:187–191. https://doi.org/10.1038/nature24457
Philpott SM, Perfecto I, Armbrecht I, Parr CL (2010) Disturbance and habitat transformation. In: Lach L, Parr CL, Abbott KL (eds) Ant Ecology. Oxford University Press, Oxford, pp 137–156. https://doi.org/10.1093/acprof:oso/9780199544639.003.0008
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and SPLUS. Springer, New York
Queiroz ACM, Rabello AM, Braga DL et al (2020) Cerrado vegetation types determine how land use impacts ant biodiversity. Biodivers Conserv 29:2017–2034. https://doi.org/10.1007/s10531-017-1379-8
R Development Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.rproject.org
Reider IJ, Donnelly MA, Watling JI (2018) The influence of matrix quality on species richness in remnant forest. Landsc Ecol 33:1147–1157. https://doi.org/10.1007/s10980-018-0664-6
Resasco J, Bruna EM, Haddad NM, Banks-Leite C, Margules CR (2017) The contribution of theory and experiments to conservation in fragmented landscapes. Ecography 40:109–118. https://doi.org/10.1111/ecog.02546
Ribas CR, Schoereder JH, Pic M, Soares SM (2003) Tree heterogeneity, resource availability, and larger scale processes regulating arboreal ant species richness. Austral Ecol 28:305–314. https://doi.org/10.1046/j.1442-9993.2003.01290.x
Ribas CR, Campos RBF, Schmidt FA, Solar RRC (2012) Ants as indicators in Brazil: A review with suggestions to improve the use of ants in environmental monitoring programs. Psyche. https://doi.org/10.1155/2012/636749
Ries L, Fletcher RJ, Battin J, Sisk TD (2004) Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu Rev Ecol Evol Syst 35:491–522. https://doi.org/10.1146/annurev.ecolsys.35.112202.130148
Rosa CA, Secco H, Carvalho N, Maia AC et al (2018) Edge effects on small mammals: Differences between arboreal and ground-dwelling species living near roads in Brazilian fragmented landscapes. Austral Ecol 43:117–126. https://doi.org/10.1111/aec.12549
Schiesari L, Matias MG, Prado PI, Leibold MA, Albert CH, Howeth JG et al (2019) Towards na applied metaecology. Perspect Ecol Conserv 17:172–181. https://doi.org/10.1016/j.pecon.2019.11.001
Schneider-Maunoury L, Lefebvre V, Ewers RM, Medina-Rangel GF, Peres CA, Somarriba E, Urbina-Cardona N, Pfeifer M (2016) Abundance signals of amphibians and reptiles indicate strong edge effects in Neotropical fragmented forest landscapes. Biol Conserv 200:207–215. https://doi.org/10.1016/j.biocon.2016.06.011
Socolar JB, Gilroy JJ, Kunin WE, Edwards DP (2016) How should beta-diversity inform biodiversity conservation? Trends Ecol Evol 31:67–80. https://doi.org/10.1016/j.tree.2015.11.005
Solar RRC, Barlow J, Andersen AN, Schoereder JH, Berenguer E, Ferreira JN, Gardner TA (2016) Biodiversity consequences of land-use change and forest disturbance in the Amazon: A multi-scale assessment using ant communities. Biol Conserv 197:98–107. https://doi.org/10.1016/j.biocon.2016.03.005
Spiesman BJ, Cumming GS (2008) Communities in context: the influences of multiscale environmental variation on local ant community structure. Landsc Ecol 23:313–325. https://doi.org/10.1007/s10980-007-9186-3
Taubert F, Fischer R, Groeneveld J, Lehmann S, Müller MS, Rödig E et al (2018) Global patterns of tropical forest fragmentation. Nature 554:519–522. https://doi.org/10.1038/nature25508
Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L et al (2012) Landscape moderation of biodiversity patterns and processes - eight hypotheses. Biol Rev 87:661–685. https://doi.org/10.1111/j.1469-185X.2011.00216.x
Vasconcelos HL, Maravalhas JB, Feitosa RM, Pacheco R, Neves KC, Andersen AN (2018) Neotropical savanna ants show a reversed latitudinal gradient of species richness, with climatic drivers reflecting the forest origin of the fauna. J Biogeogr 45:248–258. https://doi.org/10.1111/jbi.13113
Villaseñor NR, Blanchard W, Driscoll DA, Gibbons P, Lindenmayer DB (2015) Strong influence of local habitat structure on mammals reveals mismatch with edge effects models. Landsc Ecol 30:229–245. https://doi.org/10.1007/s10980-014-0117-9
Watling JI, Arroyo-Rodríguez 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. https://doi.org/10.1111/ele.13471
Wei T (2017) Package ‘corrplot’. Version 0.84. https://cran.r-project.org/web/packages/corrplot/corrplot.pdf
Whittaker RH (1972) Evolution and the measurement of species diversity. Taxon 21:213–251
Wilson MC, Chen XY, Corlett RT, Didham RK. Ding P et al (2016) Habitat fragmentation and biodiversity conservation: key findings and future challenges. Landsc Ecol 31:219–227. https://doi.org/10.1007/s10980-015-0312-3
Acknowledgements
We are thankful for funding grants from Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG - CRA PPM 00243/14, CRA PPM 00121/12, CRA APQ − 03868-10) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq – processo 303509/20122-0). We thank Vinícius Yoshino, Fernanda Tanure, Tamara Moretti for fieldwork assistance, Vilany Carneiro for tree species identification, Rodrigo Feitosa for ant species identification, Victor Hugo Fonseca Oliveira for reading early versions of this manuscript and Natalie Swan for revising the English of the manuscript. CJL is supported by PNPD fellowship grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior CAPES (Finance code: 001), CR from Cnpq/PCI, NSC from CNPq (Processo 140379/2018-5), ACMQ received a Post-Doctoral fellowship from CEMIG - Companhia Energética de Minas Gerais S.A. (P&D 611 - Descomissionamento da PCH Pandeiros: uma experiencia inédita na América do Sul), FAS received a Post-Doctoral fellowship from CNPq (150356/2012-9 - Pós-doutorado Júnior (PDJ) and RS is supported by a CNPq fellowship grant (305739/2019-0). This study was part of the Bachelor's Thesis of CJL at the Universidade Federal de Lavras.
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Lasmar, C.J., Queiroz, A.C.M., Rosa, C. et al. Contrasting edge and pasture matrix effects on ant diversity from fragmented landscapes across multiple spatial scales. Landscape Ecol 36, 2583–2597 (2021). https://doi.org/10.1007/s10980-021-01258-y
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DOI: https://doi.org/10.1007/s10980-021-01258-y