Abstract
Urbanization causes species loss around the world, but its effects on phylogenetic diversity are poorly known in tropical forests. Using a patch-landscape approach in an urbanizing region of the Brazilian Atlantic Forest, we tested whether the increase in landscape urbanization reduces plant species density, phylogenetic richness and divergence, and increases the relatedness among co-occurring individuals and species. We assessed plant responses to urbanization in adult (diameter at breast height > 10 cm) and sapling communities (2.5–10 cm diameter) separately, as saplings are proxies of the future flora. We sampled 2860 woody plants belonging to 155 species in nine circular landscapes with urbanization level varying from 0% to 45%, and estimated the relatedness among the species that have increased and decreased in relative abundance in more urbanized landscapes (winner and losers, respectively). As expected, species density and phylogenetic richness decreased with the increase in urbanization. These responses were consistent for adult and sapling communities, suggesting a persistent loss of species and lineages in more urbanized landscapes. Contrary to our expectations, phylogenetic divergence and structure did not respond to urbanization, indicating that the more urbanized landscapes still retain much evolutionary history. However, because the relatedness among winners was greater than among losers, it is likely that the phylogenetic divergence gradually reduces and the relatedness increases, resulting in impoverished forests with uncertain ability to provide ecosystem services such as carbon storage and pest control. This environmental cost should be taken into account to align urban sprawl with biodiversity conservation.
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References
Amici V, Rocchini D, Filibeck G, Bacaro G, Santi E, Geri F, Landi S, Scoppola A, Chiarucci A (2015) Landscape structure effects on forest plant diversity at local scale: exploring the role of spatial extent. Ecol Complex 21:44–52. https://doi.org/10.1016/j.ecocom.2014.12.004
Andrade ER, Jardim JG, Santos BA, Melo FPL, Talora DC, Faria D, Cazetta E (2015) Effects of habitat loss on taxonomic and phylogenetic diversity of understory Rubiaceae in Atlantic forest landscapes. Forest Ecol Manag 349:73–84. https://doi.org/10.1016/j.foreco.2015.03.049
Angiosperm Phylogeny Group (APG) (2009) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121. https://doi.org/10.1111/j.1095-8339.2009.00996.x
Arroyo-Rodríguez V, Fahrig L (2014) Why is a landscape perspective important in studies of primates? Am J Primatol 76:901–909. https://doi.org/10.1002/ajp.22282
Arroyo-Rodríguez V, Pineda E, Escobar F, Benítez-Malvido J (2009) Value of small patches in the conservation of plant-species diversity in highly fragmented rainforest. Conserv Biol 23:729–739. https://doi.org/10.1111/j.1523-1739.2008.01120.x
Arroyo-Rodríguez V, Cavender-Bares J, Escobar F, Melo FPL, Tabarelli M, Santos BA (2012) Maintenance of tree phylogenetic diversity in a highly fragmented rain forest. J Ecol 100:702–711. https://doi.org/10.1111/j.1365-2745.2011.01952.x
Arroyo-Rodríguez V, Melo FPL, Martínez-Ramos M, Bongers F, Chazdon RL, Meave JA, Norden N, Santos BA, Leal IR, Tabarelli M (2017) Multiple successional pathways in human-modified tropical landscapes: new insights from forest succession, forest fragmentation and landscape ecology research. Biol Rev 92:326–340. https://doi.org/10.1111/brv.12231
Beninde J, Veith M, Hochkirch A (2015) Biodiversity in cities needs space: a meta-analysis of factors determining intra-urban biodiversity variation. Ecol Lett 18:581–592. https://doi.org/10.1111/ele.12427
Brennan JM, Bender DJ, Contreras TA, Fahrig L (2002) Focal patch landscape studies for wildlife management: optimizing sampling effort across sacles. In: Liu J, Taylor WW (eds) Integrating landscape ecology into natural resource management. Cambridge University Press, Cambridge, pp 68–91
Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715. https://doi.org/10.1111/j.1461-0248.2009.01314.x
Chao A, Chiu C-H, Jost L (2010) Phylogenetic diversity measures based on hill numbers. Philos Trans R Soc B Biol Sci 365:3599–3609
Chao A, Ma KH, Hsieh TC (2013) iNEXT online: interpolation and extrapolation (version 1.0) [software]. http://chao.stat.nthu.edu.tw/blog/software401 download/. Acessed 10 Oct 2016
Chiu C-H, Chao A (2012) Program PhD (phylogenetic diversity). Program and User’s Guide at http://chao.stat.nthu.edu.tw/softwareCE.html. Acessed 19 Jun 2016
Cincotta RP, Wisnewski J, Engelman R (2000) Human population in the biodiversity hotspots. Nature 404:990–992. https://doi.org/10.1038/35010105
Enedino TR, Loures-Ribeiro A, Santos BA (2018) Protecting biodiversity in urbanizing regions: the role of urban reserves for the conservation of Brazilian Atlantic Forest birds. Perspect Ecol Conserv in press 16:17–23. https://doi.org/10.1016/j.pecon.2017.11.001
Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142. https://doi.org/10.1017/S1464793105006949
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. https://doi.org/10.1146/132419
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
Gentry AH (1982) Patterns of Neotropical plant species diversity. Evol Biol 15:1–85. https://doi.org/10.1007/978-1-4615-6968-8_1
Girão LC, Lopes AV, Tabarelli M, Bruna EM (2007) Changes in tree reproductive traits reduce functional diversity in a fragmented Atlantic forest landscape. PLoS One 2:e908. https://doi.org/10.1371/journal.pone.0000908
Guerra TNF, Araújo EL, Sampaio EVSB, Ferraz EMN (2017) Urban or rural areas: which types of surrounding land use induce stronger edge effects on the functional traits of tropical forests plants? Appl Veg Sci 20:538–548. https://doi.org/10.1111/avsc.12315
Instituto Brasileiro de Geografia e Estatística (2013) Banco de dados agregados. http://www.sidra.ibge.gov.br. Accessed 30 Mar 2013
Knapp S, Dinsmore L, Fissore C, Hobbie SE, Jakobsdottir I, Kattge J, King JY, Klotz S, McFadden JP, Cavender-Bares J (2012) Phylogenetic and functional characteristics of household yard floras and their changes along an urbanization gradient. Ecology 93:83–98. https://doi.org/10.1890/11-0392.1
Knapp S, Winter M, Klotz S (2017) Increasing species richness but decreasing phylogenetic richness and divergence over a 320-year period of urbanization. J Appl Ecol 54:1152–1160. https://doi.org/10.1111/1365-2664.12826
Laurance WF, Nascimento HEM, Laurance SG, Andrade A, Ribeiro JELS, Giraldo JP, Lovejoy TE, Condit R, Chave J, Harms KE, D’Angelo S (2006) Rapid decay of tree-community composition in Amazonian forest fragments. Proc Natl Acad Sci U S A 103:19010–19014. https://doi.org/10.1073/pnas.0609048103
Laurance WF, Camargo JLC, Luizão RCC, Laurance SG, Pimm SL, Bruna EM, Stouffer PC, Bruce WG, Benítez-Malvido J, Vasconcelos HL (2011) The fate of Amazonian forest fragments: a 32-year investigation. Biol Conserv 144:56–67. https://doi.org/10.1016/j.biocon.2010.09.021
Lôbo D, Leão T, Melo FPL, Santos AMM, Tabarelli M (2011) Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Divers Distrib 17:287–296. https://doi.org/10.1111/j.1472-4642.2010.00739.x
Lopes AV, Girão LC, Santos BA, Peres CA, Tabarelli M (2009) Long-term erosion of tree reproductive trait diversity in edge-dominated Atlantic forest fragments. Biol Conserv 142:1154–1165. https://doi.org/10.1016/j.biocon.2009.01.007
Matos FAR, Magnago LFS, Gastauer M, Carreiras JMB, Simonelli M, Meira-Neto JAA, Edwards DP (2017) Effects of landscape configuration and composition on phylogenetic diversity of trees in a highly fragmented tropical forest. J Ecol 105:265–276. https://doi.org/10.1111/1365-2745.12661
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260. https://doi.org/10.1016/j.biocon.2005.09.005
McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urb Ecosys 11:161–176. https://doi.org/10.1007/s11252-007-0045-4
Melo FPL, Arroyo-Rodríguez V, Fahrig L, Martínez-Ramos M, Tabarelli M (2013) On the hope for biodiversity-friendly tropical landscapes. Trends Ecol Evol 28:461–468. https://doi.org/10.1016/j.tree.2013.01.001
Müller N, Ignatieva M, Nilon CH, Werner P, Zipperer WC (2013) Patterns and trends in urban biodiversity and landscape design. In: Elmqvist T, Fragkias M, Goodness J, Güneralp B, Marcotullio PJ, McDonald RI, Parnell S, Haase D, Sendstad M, Seto KC, Wilkinson C (eds) Urbanization, biodiversity and ecosystem services: challenges and opportunities. Springer Netherlands, Dordrecht, pp 453–459
Munguía-Rosas MA, Jurado-Dzib SG, Mezeta-Cob CR, Montiel S, Rojas A, Pech-Canché JM (2014) Continuous forest has greater taxonomic, functional and phylogenetic plant diversity than an adjacent naturally fragmented forest. J Trop Ecol 30:323–333. https://doi.org/10.1017/S0266467414000194
Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Norden N, Letcher SG, Boukili V, Swenson NG, Chazdon R (2012) Demographic drivers of successional changes in phylogenetic structure across life-history stages in plant communities. Ecology 93:s70–s82. https://doi.org/10.1890/10-2179.1
Palma E, Catford JA, Corlett RT, Duncan RP, Hahs AK, Mccarthy MA, Mcdonnell MJ, Thompson K, Williams NSG, Vesk PA (2017) Functional trait changes in the floras of 11 cities across the globe in response to urbanization. Ecography 40:875–886. https://doi.org/10.1111/ecog.02516
Pôrto KC, Almeida-Cortez JS, Tabarelli M (2005) Diversidade Biológica e Conservação da Floresta Atlântica ao Norte do Rio São Francisco. Ministério do Meio Ambiente, Brasília
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
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. https://doi.org/10.1016/j.biocon.2009.02.021
Ribeiro EMS, Santos BA, Arroyo-Rodríguez V, Tabarelli M, Souza G, Leal IR (2016) Phylogenetic impoverishment of plant communities following chronic human disturbances in the Brazilian Caatinga. Ecology 97:1583–1592. https://doi.org/10.1890/15-1122.1
Ricotta C, La Sorte FA, Pyšek P, Rapson GL, Celesti-Grapow R, Thompson K (2011) Phylogenetic beta diversity of native and alien species in European urban floras. Glob Ecol Biogeogr 21:751–759. https://doi.org/10.1111/j.1466-8238.2011.00715.x
Santos BA, Peres CA, Oliveira MA, Grillo A, Alves-Costa CP, Tabarelli M (2008) Drastic erosion in functional attributes of tree assemblages in Atlantic forest fragments of northeastern Brazil. Biol Conserv 141:249–260. https://doi.org/10.1016/j.biocon.2007.09.018
Santos BA, Arroyo-Rodríguez V, Moreno CE, Tabarelli M (2010) Edge-related loss of tree phylogenetic diversity in the severely fragmented brazilian atlantic forest. PLoS One 5:e12625. https://doi.org/10.1371/journal.pone.0012625
Santos BA, Tabarelli M, Melo FPL, Camargo JLC, Andrade A, Laurance SG, Laurance WF (2014) Phylogenetic impoverishment of Amazonian tree communities in an experimentally fragmented forest landscape. PLoS One 9:e113109. https://doi.org/10.1371/journal.pone.0113109
Seto KC, Parnell S, Elmqvist T (2013) A global outlook on urbanization. In: Elmqvist T, Fragkias M, Goodness J, Güneralp B, Marcotullio PJ, McDonald RI, Parnell S, Haase D, Sendstad M, Seto KC, Wilkinson C (eds) Urbanization, biodiversity and ecosystem services: challenges and opportunities. Springer Netherlands, Dordrecht, pp 1–12
Silva-Junior V, Santos BA (2017) Using environmental perception and local knowledge to improve the effectiveness of an Urban Park in Northeast Brazil. Ethnobiol Conserv 6:2. https://doi.org/10.15451/ec2017-03-6.2-1-24
Stevens PO (2014) Dinâmica da paisagem no geossistema do estuário do Rio Paraiba - Extremo Oriental das Américas : estimativas de perdas de habitat e cenários de recuperação da biodiversidade. Universidade Federal da Paraíba, Dissertation
Tabarelli M, Lopes AV, Peres CA (2008) Edge-effects drive tropical forest fragments towards an early-successional system. Biotropica 40:657–661. https://doi.org/10.1111/j.1744-7429.2008.00454.x
Tucker CM, Cadotte MW, Carvalho SB, Davies TJ, Ferrier S, Fritz SA, Grenyer R, Helmus MR, Jin LS, Mooers AO, Pavoine S, Purschke O, Redding DW, Rosauer DF, Winter M, Mazel F (2017) A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol Rev 92:698–715. https://doi.org/10.1111/brv.12252
United Nations (2014) World urbanization prospects: the 2014 revision. Department of Economic and Social Affairs United Nations, New York
Vamosi SM, Heard SB, Vamosi JC, Webb CO (2009) Emerging patterns in the comparative analysis of phylogenetic community structure. Mol Ecol 18:572–592. https://doi.org/10.1111/j.1365-294X.2008.04001.x
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100. https://doi.org/10.1093/bioinformatics/btn358
Williams NSG, Schwartz MW, Vesk PA, McCarthy MA, Hahs AK, Clemants SE, Corlett RT, Duncan RP, Norton BA, Thompson K, McDonnell MJ (2009) A conceptual framework for predicting the effects of urban environments on floras. J Ecol 97:4–9. https://doi.org/10.1111/j.1365-2745.2008.01460.x
Winter M, Devictor V, Schweiger O (2013) Phylogenetic diversity and nature conservation: where are we? Trends Ecol Evol 28:199–204. https://doi.org/10.1016/j.tree.2012.10.015
Acknowledgements
This work was supported by the National Council for Scientific and Technological Development (CNPq) (grant numbers 476135/2013-3 and 310340/2016-0 to BAS). CNPq also provided graduate scholarship to VSJ (130604/2015-1) and postdoctoral fellowship to DGS (313272/2015-8). We thank the Chico Mendes Institute for Biodiversity Conservation (ICMBio) and the Paraíba Environment Administration (SUDEMA) for authorization to carry out the fieldwork within the protected areas. We are also grateful to Pamela Stevens for producing the figure of the study area and Orione Alvares da Silva for discussing ideas and supporting fieldwork. Nicholas Williams and an anonymous reviewer provided valuable comments on earlier versions of the manuscript.
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Silva-Junior, V., Souza, D.G., Queiroz, R.T. et al. Landscape urbanization threatens plant phylogenetic diversity in the Brazilian Atlantic Forest. Urban Ecosyst 21, 625–634 (2018). https://doi.org/10.1007/s11252-018-0745-y
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DOI: https://doi.org/10.1007/s11252-018-0745-y