Abstract
The Cerrado is one of the most threatened biomes in Brazil, with little spatial representation within the Protected Area network. Recently, proposed conservation plans worldwide have advocated for the use of multiple biodiversity facets to protect unique evolutionary and functional processes. Our aim was to identify areas with high biodiversity representativeness applying this multifaceted perspective, and propose conservation plans based on the joint analysis of taxonomic, functional and phylogenetic diversity. We used a database of the Brazilian National Program for Research in Biodiversity, which employs a standard protocol for sampling tadpoles. The Cerrado database includes samples from 165 water bodies spread over 15 localities, covering most of the Central Brazilian Cerrado. We selected four morphological traits to calculate functional diversity and used a dated phylogeny available in the literature to compute phylogenetic diversity. Our approach selected five priority areas for conservation, one of which is already protected. Our results highlighted the importance of four new areas which show high values of diversity, including original lineages and traits, and urgently need conservation prioritization. Furthermore, unlike the current protected network, our approach performs significantly better than random at protecting sites with high phylogenetic and functional diversity. We therefore discuss how the multifaceted indices considered can help protect key ecosystem functions and evolutionary legacy in anuran communities of the Brazilian Cerrado.
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References
Balvanera P, Pfisterer AB, Bucmann N et al (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156
Becker CG, Loyola RD (2008) Extinction risk assessments at the population and species level: implications for amphibian conservation. Biodivers Conserv 17:2297–2304. https://doi.org/10.1007/s10531-007-9298-8
Becker CG, Fonseca CR, Haddad CFB et al (2007) Habitat split and the global decline of amphibians. Science 318:1775–1777. https://doi.org/10.1126/science.1149374
Bowatte G, Perera P, Senevirathne G et al (2013) Tadpoles as dengue mosquito (Aedes aegypti) egg predators. Biol Control 67:469–474. https://doi.org/10.1016/j.biocontrol.2013.10.005
Bruner AG, Gullison RE, Balmford A (2004) Financial costs and shortfalls of managing and expanding preotected-area systems in developing countries. Bioscience 54:1119–1126. https://doi.org/10.1641/0006-3568(2004)054
Bustamante MR, Ron SR, Coloma LA (2005) Changes in diversity of seven anuran communities in the Ecuadorian Andes. Biotropica 37:180–189. https://doi.org/10.1111/j.1744-7429.2005.00025.x
Cadotte MW (2017) Functional traits explain ecosystem function through opposing mechanisms. Ecol Lett 20:989–996. https://doi.org/10.1111/ele.12796
Cadotte MW, Jonathan Davies T, Regetz J et al (2010) Phylogenetic diversity metrics for ecological communities: integrating species richness, abundance and evolutionary history. Ecol Lett 13:96–105. https://doi.org/10.1111/j.1461-0248.2009.01405.x
Caramaschi U, Sazima I (1984) Uma nova espécie deThoropa da Serra do Cipó, Minas Gerais, Brasil (Amphibia, Leptodactylidae). Rev Bras Zool 2:139–146. https://doi.org/10.1590/S0101-81751983000300004
Chamberlain SA, Hovick SM, Dibble CJ et al (2012) Does phylogeny matter? Assessing the impact of phylogenetic information in ecological meta-analysis. Ecol Lett 15:627–636. https://doi.org/10.1111/j.1461-0248.2012.01776.x
Chen Y, Zhang J, Jiang J et al (2017) Assessing the effectiveness of China’s protected areas to conserve current and future amphibian diversity. Divers Distrib 23:146–157. https://doi.org/10.1111/ddi.12508
de Dias BFS (1992) Cerrados: uma caracterização. In: Alternativas de desenvolvimento dos Cerrados: manejo e conservação dos recursos naturais renováveis, pp 11–25
de Sousa VTT, Nomura F, Venesky MD et al (2014) Flexible feeding kinematics of a tropical carnivorous anuran tadpole. J Zool 293:204–2010. https://doi.org/10.1111/jzo.12135
Devictor V, Mouillot D, Meynard C et al (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 13:1030–1040. https://doi.org/10.1111/j.1461-0248.2010.01493.x
Díaz S, Lavorel S, de Bello F et al (2007) Incorporating plant functional diversity effects in ecosystem service assessments. Proc Natl Acad Sci 104:20684–20689. https://doi.org/10.1073/pnas.0704716104
Dirzo R, Young HS, Galetti M et al (2014) Defaunation in the anthropocene. Science 345:401–406. https://doi.org/10.1126/science.1251817
Eiten G (1972) The Cerrado vegetation of Brazil. Bot Rev 38:201–338. https://doi.org/10.1007/BF02859158
Erwin TL (1991) An evolutionary basis for conservation strategies. Science 253:750–752. https://doi.org/10.1126/science.253.5021.750
Eterovick PC, Barros IS (2003) Niche occupancy in south-eastern Brazilian tadpole communities in montane-meadow streams. J Trop Ecol 19:439–448. https://doi.org/10.1017/S026646740300347X
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Faith DP (2008) Threatened species and the potential loss of phylogenetic diversity: conservation scenarios based on estimated extinction probabilities and phylogenetic risk analysis. Conserv Biol 22:1461–1470. https://doi.org/10.1111/j.1523-1739.2008.01068.x
Faivovich J (2002) A cladistic analysis of Scinax (Anura: Hylidae). Cladistics 18:367–393
Faivovich J, Haddad CFB, Garcia PCA et al (2005) Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bull Am Museum Nat Hist 294:1–240
Forest F, Grenyer R, Rouget M et al (2007) Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445:757–760. https://doi.org/10.1038/nature05587
Gillespie R (2004) Community assembly through adaptive radiation in Hawaiian spiders. Science (80-) 303:356–359.
Gonçalves-Souza T, Santos AJ, Romero GQ, Lewinsohn TM (2015) Conservation along a hotspot rim: spiders in Brazilian coastal restingas. Biodivers Conserv 24:1131–1146. https://doi.org/10.1007/s10531-014-0846-8
Gosner KL (1960) A simplified table for staging anuran embryos larvae with notes on identification. Herpetodologists’ Leag 16:183–190. https://doi.org/10.2307/3890061
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391. https://doi.org/10.1046/j.1461-0248.2001.00230.x
Haddad CFB, Martins M (1994) Four Species of Brazilian Frogs Related to Epipedobates pictus (Dendrobatidae): Taxonomy and Natural History Observations. Herpetologica 50:282–295
Hautier Y, Isbell F, Borer ET et al (2018) Local loss and spatial homogenization of plant diversity reduce ecosystem multifunctionality. Nat Ecol Evol 2:50–56. https://doi.org/10.1038/s41559-017-0395-0
Hidasi-Neto J, Loyola RD, Cianciaruso MV (2013) Conservation actions based on red lists do not capture the functional and phylogenetic diversity of birds in Brazil. PLoS ONE 8:e73431. https://doi.org/10.1371/journal.pone.0073431
Hooper DU, Chapin FS, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35
Iknayan KJ, Tingley MW, Furnas BJ, Beissinger SR (2014) Detecting diversity: emerging methods to estimate species diversity. Trends Ecol Evol 29:97–106. https://doi.org/10.1016/j.tree.2013.10.012
Isbell F, Cowles J, Dee LE et al (2018) Quantifying effects of biodiversity on ecosystem functioning across times and places. Ecol Lett 21:763–778. https://doi.org/10.1111/ele.12928
IUCN (2016) The IUCN red list of threatened species. http://www.iucnredlist.org. Accessed 7 Dec 2016
IUCN (2017) The IUCN red list of threatened species. http://www.iucnredlist.org. Accessed 11 Nov 2017
Klink CA, Machado RB (2005) Conservation of the Brazilian Cerrado. Conserv Biol 19:707–713. https://doi.org/10.1111/j.1523-1739.2005.00702.x
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305
Lavorel S, McIntyre S, Landsberg J, Forbes TDA (1997) Plant functional classifications: from general groups to specific groups based on response to disturbance. Trends Ecol Evol 12:474–478. https://doi.org/10.1016/S0169-5347(97)01219-6
Legendre P, Legendre L (2012) Numerical Ecology, 3rd edn. Elsevier, Amsterdam
Lips KR, Reeve JD, Witters LR (2003) Population declines in Central America. Conserv Biol 17:1078–1088. https://doi.org/10.1046/j.1523-1739.2003.01623.x
Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci 100:12765–12770
Loyola RD, Becker CG, Kubota U et al (2008) Hung out to dry: choice of priority ecoregions for conserving threatened neotropical anurans depends on life-history traits. PLoS ONE 3:e2120. https://doi.org/10.1371/journal.pone.0002120
Mace GM, Gittleman JL, Purvis A (2003) Preserving the tree of life. Science 300:1707–1709. https://doi.org/10.1126/science.1085510
Mace GM, Norris K, Fitter AH (2012) Biodiversity and ecosystem services: a multilayered relationship. Trends Ecol Evol 27:19–26. https://doi.org/10.1016/j.tree.2011.08.006
Maire A, Buisson L, Biau S et al (2013) A multi-faceted framework of diversity for prioritizing the conservation of fish assemblages. Ecol Indic 34:450–459. https://doi.org/10.1016/j.ecolind.2013.06.009
Margules CR, Pressey RL (2000) Systematic conservation planning. Nature 405:243–253. https://doi.org/10.1038/35012251
Mason NWH, MacGillivray K, Steel JB, Wilson JB (2003) An index of functional diversity. J Veg Sci 14:571–578
Mason NWH, Mouillot D, Lee WG, Wilson JB (2005) Functional richness, functional evenness and functional divergence: the primary of functional components diversity. Oikos 111:112–118. https://doi.org/10.1111/j.0030-1299.2005.13886.x
Meynard CN, Devictor V, Mouillot D et al (2011) Beyond taxonomic diversity patterns: How do α, β and γ components of bird functional and phylogenetic diversity respond to environmental gradients across France? Glob Ecol Biogeogr 20:893–903. https://doi.org/10.1111/j.1466-8238.2010.00647.x
Ministério do Meio Ambiente (2004) Portaria 126
Ministério do Meio Ambiente (2017) Biomas. http://www.mma.gov.br/biomas. Accessed 15 Dec 2017
Mokany A (2007) Impact of tadpoles and mosquito larvae on ephemeral pond structure and processes. Mar Freshw Res 58:436–444
Mouquet N, Devictor V, Meynard CN et al (2012) Ecophylogenetics: advances and perspectives. Biol Rev Camb Philos Soc 87:769–785. https://doi.org/10.1111/j.1469-185X.2012.00224.x
Myers N, Mittermeier RA, Mittermeier CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Pardo I, Roquet C, Lavergne S et al (2017) Spatial congruence between taxonomic, phylogenetic and functional hotspots: true pattern or methodological artefact? Divers Distrib 23:209–220. https://doi.org/10.1111/ddi.12511
Pavoine S, Ollier S, Dufour A-B (2005) Is the originality of a species measurable? Ecol Lett 8:579–586. https://doi.org/10.1111/j.1461-0248.2005.00752.x
Peel MC, Finlayson BL, Mcmahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644
Pollock LJ, Thuiller W, Jetz W (2017) Large conservation gains possible for global biodiversity facets. Nature 546:141–144. https://doi.org/10.1038/nature22368
Pressey RL, Cabeza M, Watts ME et al (2007) Conservation planning in a changing world. Trends Ecol Evol 22:583–591. https://doi.org/10.1016/j.tree.2007.10.001
Pyron RA (2014) Biogeographic analysis reveals ancient continental vicariance and recent oceanic dispersal in amphibians. Syst Biol 63:779–797. https://doi.org/10.1093/sysbio/syu042
Raghavendra K, Sharma P, Dash AP (2008) Biological control of mosquito populations through frogs: opportunities & constrains. Indian J Med Res 128:22–25
Rangel TFLVB, Diniz-Filho JAF, Bini LM (2006) Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Glob Ecol Biogeogr 15:321–327. https://doi.org/10.1111/j.1466-822X.2006.00237.x
Rangel TF, Diniz-Filho JAF, Bini LM (2010) SAM: a comprehensive application for spatial analysis in macroecology. Ecography (Cop) 33:46–50. https://doi.org/10.1111/j.1600-0587.2009.06299.x
Ranvestel AW, Lips KR, Pringle CM et al (2004) Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations. Freshw Biol 49:274–285. https://doi.org/10.1111/j.1365-2427.2004.01184.x
Rao CR (1982) Diversity and dissimilarity coefficients: a unified approach. Theor Popul Biol 21:24–43
Redding DW, Mooers AØ (2006) Incorporating evolutionary measures into conservation prioritization. Conserv Biol 20:1670–1678. https://doi.org/10.1111/j.1523-1739.2006.00555.x
Reiss J, Bridle JR, Montoya JM, Woodward G (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol Evol 24:505–514. https://doi.org/10.1016/j.tree.2009.03.018
Ricotta C, Bacaro G, Marignani M et al (2012) Computing diversity from dated phylogenies and taxonomic hierarchies: does it make a difference to the conclusions? Oecologia 170:501–506. https://doi.org/10.1007/s00442-012-2318-8
Rodrigues ASL, Pilgrim JD, Lamoreux JF et al (2006) The value of the IUCN Red List for conservation. Trends Ecol Evol 21:71–76. https://doi.org/10.1016/j.tree.2005.10.010
Roelants K, Gower DJ, Wilkinson M et al (2007) Global patterns of diversification in the history of modern amphibians. Proc Natl Acad Sci 104:887–892
Sgrò CM, Lowe AJ, Hoffmann AA (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evol Appl 4:326–337. https://doi.org/10.1111/j.1752-4571.2010.00157.x
Silva JMC, Bates JM (2002) Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. Bioscience 52:225–233. https://doi.org/10.1641/0006-3568(2002)052[0225:BPACIT]2.0.CO;2
Silva JF, Farinas MR, Felfili JM, Klink CA (2006) Spatial heterogeneity, land use and conservation in the Cerrado region of Brazil. J Biogeogr 33:536–548. https://doi.org/10.1111/j.1365-2699.2005.01422.x
Silvano DL, Valdujo PH, Colli GR (2016) Priorities for conservation of the evolutionary history of amphibian in the Cerrado. In: Pellens R, Grandcolas P (eds) Biodiversity conservation and phylogenetic systematics. Springer International Publishing, Berlin, pp 287–304
Skelly DK, Richardson JL (2010) Larval sampling. In: Kenneth Dodd (Ed) Amphibian ecology and conservation: a handbook of techniques. Oxford University Press, Oxford, pp 55–70
Srivastava DS, Bell T (2009) Reducing horizontal and vertical diversity in a foodweb triggers extinctions and impacts functions. Ecol Lett 12:1016–1028. https://doi.org/10.1111/j.1461-0248.2009.01357.x
Strassburg BBN, Brooks T, Feltran-Barbieri R et al (2017) Moment of truth for the Cerrado. Nature 1:1–3. https://doi.org/10.1038/s41559-017-0099
Strecker ALS, Olden JD, Whittier JB, Paukert CP (2011) Defining conservation priorities for freshwater fishes according to taxonomic, functional, and phylogenetic diversity. Ecol Appl 21:3002–3013
Swenson NG, Enquist BJ, Thompson J, Zimmerman JK (2007) The influence of spatial and size scale on phylogenetic relatednesss in tropical forest communities. Ecology 88:1770–1780. https://doi.org/10.1890/06-1499.1
Toledo LF, Guimarães LDA, Lima LP et al (2004) Notes on courtship, egg-laying site, and defensive behavior of Epipedobates flavopictus (Anura, Dendrobatidae) from two mountain ranges of central and southeastern Brazil. Phyllomedusa 3:145–147
Trindade-Filho J, Landa Sobral F, Cianciaruso MV, Loyola RD (2012) Using indicator groups to represent bird phylogenetic and functional diversity. Biol Conserv 146:155–162. https://doi.org/10.1016/j.biocon.2011.12.004
Tucker CM, Cadotte MW, Carvalho SB et al (2016) A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol Rev 92:698–715. https://doi.org/10.1111/brv.12252
Vellend M, Cornwell WK, Magnuson-Ford K, Mooers AØ (2011) Measuring phylogenetic biodiversity. In: Magurran AE, Mcgill BJ (eds) Biological diversity. Columbia University Press, New York
Venail P, Gross K, Oakley TH et al (2015) Species richness, but not phylogenetic diversity, influences community biomass production and temporal stability in a re-examination of 16 grassland biodiversity studies. Funct Ecol 29:615–626. https://doi.org/10.1111/1365-2435.12432
Villéger S, Mason H, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework. Ecology 89:2290–2301
Volkmann L, Martyn I, Moulton V et al (2014) Prioritizing populations for conservation using phylogenetic networks. PLoS ONE. https://doi.org/10.1371/journal.pone.0088945
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
Weinstein BG, Tinoco B, Parra JL et al (2014) Taxonomic, phylogenetic, and trait beta diversity in South American hummingbirds. Am Nat 184:211–224. https://doi.org/10.1086/676991
Wells KD (1977) The social behaviour of anuran amphibians. Anim Behav 25:666–693. https://doi.org/10.1016/0003-3472(77)90118-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
Zina J (2006) Communal nests in Physalaemus pustulosus (Amphibia: Leptodactylidae): experimental evidence for female oviposition preferences and protection against desiccation. Amphibia-Reptilia 27:148–150. https://doi.org/10.1163/156853806776052092
Acknowledgements
We want to thank C.F.B. Haddad, Nomura, F. and L.F. Toledo for loaning the tadpoles for this study; ECOFFUN members, D.B. Provete and M.V. Garey for useful discussion and suggestions during the development of this manuscript; and all the people involved with the SISBIOTA database, who made this study possible. L.S.O.M was supported by a scholarship from “Fundação de Amparo à Pesquisa do Estado de São Paulo”- FAPESP (2013/26101-8); D.C.R.F was supported by SISBIOTA, a research grant from Coordenadoria Nacional de Desenvolvimento Científico e Técnológico-CNPq and Fundação de Amparo à Pesquisa do estado de São Paulo – FAPESP support (CNPq 563075/2010-4 and FAPESP 2010/52321-7). DCRF is a CNPq fellow (# 302328/2017-3).
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Communicated by David Hawksworth.
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Ouchi-Melo, L.S., Meynard, C.N., Gonçalves-Souza, T. et al. Integrating phylogenetic and functional biodiversity facets to guide conservation: a case study using anurans in a global biodiversity hotspot. Biodivers Conserv 27, 3247–3266 (2018). https://doi.org/10.1007/s10531-018-1600-4
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DOI: https://doi.org/10.1007/s10531-018-1600-4