Abstract
Chronic anthropogenic disturbance (CAD) and climate change represent two of the major threats to biodiversity globally, but their combined effects are not well understood. Here we investigate the individual and interactive effects of increasing CAD and decreasing rainfall on the composition and taxonomic (TD), functional (FD) and phylogenetic diversity (PD) of plants possessing extrafloral nectaries (EFNs) in semi-arid Brazilian Caatinga. EFNs attract ants that protect plants against insect herbivore attack and are extremely prevalent in the Caatinga flora. EFN-bearing plants were censused along gradients of disturbance and rainfall in Catimbau National Park in north-eastern Brazil. We recorded a total of 2243 individuals belonging to 21 species. Taxonomic and functional composition varied along the rainfall gradient, but not along the disturbance gradient. There was a significant interaction between increasing disturbance and decreasing rainfall, with CAD leading to decreased TD, FD and PD in the most arid areas, and to increased TD, FD and PD in the wettest areas. We found a strong phylogenetic signal in the EFN traits we analysed, which explains the strong matching between patterns of FD and PD along the environmental gradients. The interactive effects of disturbance and rainfall revealed by our study indicate that the decreased rainfall forecast for Caatinga under climate change will increase the sensitivity of EFN-bearing plants to anthropogenic disturbance. This has important implications for the availability of a key food resource, which would likely have cascading effects on higher trophic levels.
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Availability of data and material
The datasets generated and/or analysed during the current study will be available in the Dryad repository: https://doi.org/10.5061/dryad.5mkkwh776.
Code availability
The codes used during the current study are available from the corresponding author on reasonable request.
References
Allen K, Dupuy JM, Gei MG, Catherine Hulshof C, Medvigy D, Pizano C et al (2017) Will seasonally dry tropical forests be sensitive or resistant to future changes in rainfall regimes? Environ Res Lett 12:023001. https://doi.org/10.1088/1748-9326/aa5968
Apple JL, Fenner DHJR (2001) Ant visitation of extrafloral nectaries of Passiflora: the effects of nectary attributes and ant behavior on patterns in facultative ant-plant mutualisms. Oecologia 127:409–416. https://doi.org/10.1007/s004420000605
Arnan X, Arcoverde GB, Pie MR, Ribeiro-Neto JD, Leal IR (2018a) Increased anthropogenic disturbance and aridity reduce phylogenetic and functional diversity of ant communities in Caatinga dry forest. Sci Total Environ 631–632:429–438. https://doi.org/10.1016/j.scitotenv.2018.03.037
Arnan X, Leal IR, Tabarelli M, Andrade JF, Barros MF, Câmara T et al (2018b) A framework for deriving measures of chronic anthropogenic disturbance: surrogate, direct, single and multi-metric indices in Brazilian Caatinga. Ecol Ind 94:274–282. https://doi.org/10.1016/j.ecolind.2018.07.001
Athiê-Souza SM, Miranda de Melo JI, da Silva LP, Lima dos Santos L, Silva dos Santos J, Dias de Oliveira LS et al (2019) Phanerogamic flora of the Catimbau National Park, Pernambuco, Brazil. Biota Neotrop 19:1–27. https://doi.org/10.1590/1676-0611-BN-2018-0622
Bairlein F, Winkel W (2001) Birds and climate change. In: Lozan JL, Grassl H, Hupfer P (eds) Climate of the 21st century: changes and risks. Wissenschaftliche Auswertungen, Hamburg
de Bello F, Lavergne S, Thuiller W (2010) The partitioning of diversity: showing Theseus a way out of the labyrinth. J Veg Sci 21:992–1000. https://doi.org/10.1111/j.1654-1103.2010.01195.x
Bentley BL (1977) Extrafloral nectaries and protection by pugnacious bodyguards. Ecology 57:815–820. https://doi.org/10.1146/annurev.es.08.110177.002203
Blüthgen N, Reifenrath K (2003) Extrafloral nectaries in an Australian rainforest: structure and distribution. Aust J Bot 51:515–527. https://doi.org/10.1071/BT02108
Burkett VR, Suarez AG (2014) Point of departure. In: Field CB, Barros VR, Dokken DJ (eds) Climate Change 2014: Impacts, adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York
Byk J, Del-Claro K (2011) Ant-plant interaction in the Neotropical savanna: direct beneficial effects of extrafloral nectar on ant colony fitness. Popul Ecol 53:327–332. https://doi.org/10.1007/s10144-010-0240-7
Caddy-Retalic AAN, Aspinwall MJ, Breed MF, Byrne M, Christmas MJ et al (2017) Bioclimatic transect networks: powerful observatories of ecological change. Ecol Evol 7:4607–4619. https://doi.org/10.1002/ece3.2995
Calixto ES, Lange D, Del-Claro K (2021a) Net benefits of a mutualism: influence of the quality of extrafloral nectar on the colony fitness of a mutualistic ant. Biotropica 53:846–856. https://doi.org/10.1111/btp.12925
Calixto ES, Novaes LR, dos Santos DFB, Lange D, Moreira X, Del-Claro K (2021b) Climate seasonality drives ant-plant-herbivore interactions via plant phenology in an extrafloral nectary-bearing plant community. J Ecol 109:639–651. https://doi.org/10.1111/1365-2745.13492
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
Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310. https://doi.org/10.1126/science.199.4335.1302
Crowther TW, Glick HB, Covey KR, Bettigole C, Maynard DS, Thomas SM et al (2015) Map** tree density at a global scale. Nature 525:201–205. https://doi.org/10.1038/nature14967
Câmara T, Almeida W, 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
Câmara T, Leal IR, Blüthgen N, Oliveira FMP, Arnan X (2019) Anthropogenic disturbance and rainfall variation threaten the stability of plant-ant interactions in the Brazilian Caatinga. Ecography 42:1960–1972. https://doi.org/10.1111/ecog.04531
Câmara T, Leal IR, Blüthgen N, Oliveira FMP, de Queiroz R, Arnan X (2018) Effects of chronic anthropogenic disturbance and rainfall on the specialization of ant-plant mutualistic networks in the Caatinga, a Brazilian dry forest. J Anim Ecol 87:1022–1033. https://doi.org/10.1111/1365-2656.12820
Davidson DW, Cook SC, Snelling RR, Chua TH (2003) Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300:969–972. https://doi.org/10.1126/science.1082074
Devictor V, Mouillot D, Meynard C, Jiguet F, Thuiller W, Nl M (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
Drummond AJ, Suchard MA, **e D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075
Díaz-Castelazo C, Rico-Gray V, Ortega F, Ángeles J (2005) Morphological and secretory characterization of extrafloral nectaries in plants of Coastal Veracruz, Mexico. Ann Bot 96:1175–1189. https://doi.org/10.1093/aob/mci270
Elias TS (1983) Extrafloral nectaries: their structure and distribution. In: Bentley BL, Elias TS (eds) The biology of nectaries. Columbia University Press, New York, pp 174–203
Engelbrecht BM, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL et al (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–82. https://doi.org/10.1038/nature05747
Fiala B, Linsenmaier KE (1995) Distribution and abundance of plants with extrafloral nectarines in the woody floral of a lowland primary forest in Malaysia. Biodivers Conserv 4:165–182. https://doi.org/10.1007/BF00137783
Frishkoff LO, Karp DS, Flanders JR, Zook J, Hadly EA, Daily GC et al (2016) Climate change and habitat conversion favour the same species. Ecol Lett 19:1081–1090. https://doi.org/10.1111/ele.12645
Frith CB, Frith DW (1985) Seasonality of insect abundance in an Australian upland tropical rainforest. Aust J Ecol 10:237–248. https://doi.org/10.1111/j.1442-9993.1985.tb00886.x
Frith CB, Frith DW (2005) A long-term banding study in upland tropical rainforest, Paluma Range, north-eastern Queensland with notes on breeding. Corella 29:25–48
Grime JP (1973) Competitive exclusion in herbaceous vegetation. Nature 242:244–247. https://doi.org/10.1038/242344a0
Gutiérrez AG, Armesto JJ, Díaz MF, Huth A (2014) Increased drought impacts on temperate rainforests from southern South America: results of a process-based, dynamic forest model. PLoS One 9:e103226. https://doi.org/10.1371/journal.pone.0103226
Harringon R, Stork N (1995) Insects in a changing environment. Academic Press
Heil M, Fiala B, Baumann B, Linsenmair KE (2000) Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Funct Ecol 14:749–757. https://doi.org/10.1046/j.1365-2435.2000.00480.x
Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE (2001) Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc Natl Acad Sci 98:1083–1088. https://doi.org/10.1073/pnas.98.3.1083
Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453. https://doi.org/10.1146/annurev.ecolsys.34.011802.132410
Hermant M, Hennion F, Barlish I, Yguel B, Prinzing A (2012) Disparate relatives: life histories vary more in genera occupying intermediate environments. Perspect Plant Ecol Evol Syst 14:283–301. https://doi.org/10.1016/J.PPEES.2012.02.001
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–2197. https://doi.org/10.1002/joc.1276
Hiltner U, Braüning A, Gebrekirstos A, Huth A, Fischer R (2016) Impacts of precipitation variability on the dynamics of a dry tropical montane forest. Ecol Model 320:92–101. https://doi.org/10.1016/j.ecolmodel.2015.09.021
Kersh MF, Fonseca CR (2005) Abiotic factors and the conditional outcome of an ant–plant mutualism. Ecology 86:2117–2126. https://doi.org/10.1890/04-1916
Lange D, Calixto ES, Del-Claro K (2017) Variation in extrafloral nectary productivity influences the ant foraging. PLoS ONE 12:e0169492. https://doi.org/10.1371/journal.pone.0169492
Leal LC, Andersen AN, Leal IR (2015) Disturbance winners or losers? Plants bearing extrafloral nectaries in Brazilian Caatinga. Biotropica 47:468–474. https://doi.org/10.1111/btp.12230
Leal IR, Lopes AV, Machado IC, Tabarelli M (2017) Plant-animal interactions in the Caatinga: current overview and future perspectives. In: Silva JMC, Leal IR, Tabarelli M (eds) Caatinga: the largest tropical dry forest region in South America. Springer, pp 255–278
Leal LC, Peixoto PEC (2017) Decreasing water availability across the globe improves the effectiveness of protective ant–plant mutualisms: a meta-analysis. Biol Rev 92:1785–1794. https://doi.org/10.1111/brv.12307
Legendre P, Oksanen J, Ter Braak CJF (2011) Testing the significance of canonical axes in redundancy analysis. Methods Ecol Evol 2:269–277. https://doi.org/10.1111/j.2041-210X.2010.00078.x
Leps J, de Bello F, Lavorel S, Berman S (2006) Quantifying and interpreting functional diversity of natural communities: practical considerations matter. Preslia 78:481–501
Maddison WP, Slatkin M (1991) Null models for the number of evolutionary steps in a character on a phylogenetic tree. Evolution 45:1184–1197. https://doi.org/10.1111/j.1558-5646.1991.tb04385.x
Magrin GO, Marengo JA, Boulanger JP, Buckeridge MS, Castellanos E, Poveda G, Scarano FR, Vicuna S (2014) Central and South America. In: Climate change 2014: impacts, adaptation and vulnerability. Contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, UK
Mair L, Hill JK, Fox R, Botham M, Brereton T, Thomas CD (2014) Abundance changes and habitat availability drive species’ responses to climate change. Nat Clim Chang 4:127–131. https://doi.org/10.1038/nclimate2086
Marazzi B, Bronstein JL, Koptur S (2013) The diversity, ecology and evolution of extrafloral nectaries: current perspectives and future challenges. Ann Bot 111:1243–1250. https://doi.org/10.1093/aob/mct109
Marazzi B, Sanderson MJ (2010) Large-scale patterns of diversification in the widespread legume genus Senna and the evolutionary role of extrafloral nectaries. Evolution 64:3570–3592. https://doi.org/10.1111/j.1558-5646.2010.01086.x
Martorell C, Peters EM (2005) The measurement of chronic disturbance and its effects on the threatened cactus Mammillaria pectinifera. Biol Conserv 124:199–207. https://doi.org/10.1016/j.biocon.2005.01.025
Melo Y, Machado SR, Alves M (2010) Anatomy of extrafloral nectaries in Leguminosae from dry-seasonal forest in Brazil. Bot J Linn Soc 163:87–98. https://doi.org/10.1111/j.1095-8339.2010.01047.x
Mouchet MA, Villeger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876. https://doi.org/10.1111/j.1365-2435.2010.01695.x
Nascimento VT, Vasconcelos MA, Maciel MIS, Albuquerque UP (2012) Famine foods of Brazil’s seasonal dry forests: ethnobotanical and nutritional aspects. Econ Bot 66:22–34. https://doi.org/10.1007/s12231-012-9187-2
Nogueira A, Baccaro FB, Leal LC, Rey PJ, Lohmann LG, Bronstein JL (2020) Variation in the production of plant tissues bearing extrafloral nectaries explains temporal patterns of ant attendance in Amazonian understory plants. J Ecol 108:1578–1591. https://doi.org/10.1111/1365-2745.13340
Oliveira FMP, Câmara T, Durval JIF, Oliveira CLS, Arnan X, Andersen AN et al (2021) Plant protection services mediated by extrafloral nectaries in Brazilian Caatinga: the roles of chronic anthropogenic disturbance, aridity, nectar production and ant species composition. J Ecol 109:260–272. https://doi.org/10.1111/1365-2745.13469
Pavoine S, Dufuor AB, Chessel D (2004) From dissimilarities among species to dissimilarities among communities: a double principal coordinate analysis. J Theor Biol 228:523–537. https://doi.org/10.1016/j.jtbi.2004.02.014
Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrakei TC, Chen C et al (2017) Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science 355:1–9. https://doi.org/10.1126/science.aai9214
Petchey OL, Gaston AJ (2002) Functional diversity (FD), species richness and community composition. Ecol Lett 5:402–411. https://doi.org/10.1046/j.1461-0248.2002.00339.x
Prober SM, Thiele K (2004) Floristic patterns along an east-west gradient in grassy box woodlands of Central New South Wales. Cunninghamia 8:306–325
Purschke O, Schmid BC, Sykes MT, Poschlod P, Michalski SG, Durka W et al (2013) Contrasting changes in taxonomic, phylogenetic and functional diversity during a long-term succession: insights into assembly processes. J Ecol 101:857–866. https://doi.org/10.1111/1365-2745.12098
Queiroz LP (2009) Leguminosas da Caatinga. Feira de Santana. Universidade Estadual de Feira de Santana, Associação de Plantas do Nordeste-APNE. Kew, Royal Botanic Gardens, 467
R Core Team (2014) R: a language and environment for statistical computing, Version 3.1.2. Foundation for Statistical Computing, Vienna, Austria.
Rao CR (1982) Diversity and dissimilarity coefficients: a unified approach. Theor Popul Biol 21:24–43. https://doi.org/10.1016/0040-5809(82)90004-1
Ribeiro EMS, Arroyo-Rodríguez V, Santos BA, Tabarelli M, Leal IR (2015) Chronic anthropogenic disturbance drives the biological impoverishment of the Brazilian Caatinga vegetation. J Appl Ecol 52:611–620. https://doi.org/10.1111/1365-2664.12420
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
Ribeiro LF, Solar RRC, Muscardi DC, Schoereder JH, Andersen AN (2018) Extrafloral nectar as a driver of arboreal ant communities at the site-scale in Brazilian savanna. Austral Ecol 43:672–680. https://doi.org/10.1111/aec.12612
Ribeiro LF, Solar RRC, Sobrinho T, Muscardi DC, Schoereder JH, Andersen AN (2019) Different trophic groups of arboreal ants show differential responses to resource supplementation in a neotropical savanna. Oecologia 190:433–443. https://doi.org/10.1007/s00442-019-04414-z
Ribeiro-Neto JD, Arnan X, Tabarelli M, Leal IR (2016) Chronic anthropic disturbance causes homogenization of plant and ant communities in the Brazilian Caatinga. Biodivers Conserv 25:943–956. https://doi.org/10.1007/s10531-016-1099-5
Rico-Gray V, García-Franco JG, Palacios-Rios M, Díaz-Castelazo C, Parra-Tabla V, Navarro JA (1998) Geographical and seasonal variation in the richness of ant-plant interactions in Mexico. Biotropica 30:190–200. https://doi.org/10.1111/j.1744-7429.1998.tb00054.x
Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant plant interactions. University of Chicago Press, Chicago
Rito KF, Arroyo-Rodríguez V, Quieroz RT, Leal IR, Tabarelli M (2017a) Precipitation mediates the effect of human disturbance on the Brazilian Caatinga vegetation. J Ecol 105:828–838. https://doi.org/10.1111/1365-2745.12712
Rito KF, Tabarelli M, Leal IR (2017b) Euphorbiaceae responses to chronic anthropogenic disturbances in Caatinga vegetation: from species proliferation to biotic homogenization. Plant Ecol 218:749–759. https://doi.org/10.1007/s11258-017-0726-x
Rotem G, Gavish Y, Schacham B, Giladi I, Bouskila A, Ziv Y (2015) Combined effects of climatic gradient and domestic livestock grazing on reptile community structure in a heterogeneous agroecosystem. Oecologia 180:231–242. https://doi.org/10.1007/s00442-015-3435-y
Rubenstein DI (1992) The greenhouse effect and changes in animal behavior: effects on social structure and life- history strategies. In: Peters RL, Lovejoy TE (eds) Global warming and biological diversity. Yale University Press, New Haven
Rudgers JA, Gardener MC (2004) Extrafloral nectar as a resource mediating multispecies interactions. Ecology 85:1495–1502. https://doi.org/10.1890/03-0391
Safi K, Cianciaruso MV, Loyola RD, Brito D, Armour-Marshall K, Diniz-Filho JAF (2011) Understanding global patterns of mammalian functional and phylogenetic diversity. Philos Trans R Soc B 366:2536–2544. https://doi.org/10.1098/rstb.2011.0024
Sagar R, Raghubanshi A, Singh J (2003) Tree species composition, dispersion and diversity along a disturbance gradient in a dry tropical forest region of India. For Ecol Manage 186:61–71. https://doi.org/10.1016/s0378-1127(03)00235-4
Schultz K, Voigt K, Beusch C, Almeida-Cortez JS, Kowarik I, Walz A et al (2016) Grazing deteriorates the soil carbon stocks of Caatinga forest ecosystems in Brazil. For Ecol Manage 367:62–70. https://doi.org/10.1016/j.foreco.2016.02.011
Seiler C, Hutjes RWA, Kruijt B, Hickler T (2015) The sensitivity of wet and dry tropical forests to climate change in Bolivia. J Geophys Res Biogeosci 120:399–413. https://doi.org/10.1002/2014JG002749
da Silva CHF, Arnan X, Andersen AN, Leal IR (2019a) Extrafloral nectar as a driver of ant community spatial structure along disturbance and rainfall gradients in Brazilian Caatinga. J Trop Ecol 35:280–287. https://doi.org/10.1017/S0266467419000245
Silva ILH, Leal IR, Ribeiro-Neto JD, Arnan X (2019b) Spatiotemporal responses of ant communities across a disturbance gradient: the role of behavioral traits. Insect Soc 66:623–635. https://doi.org/10.1007/s00040-019-00717-9
Silva JMC, Tabarelli M, Leal IR (2017) The Caatinga: understanding the challenges. In: Silva JMC, Leal IR, Tabarelli M (eds) Caatinga: the largest Tropical Dry Forest region in South America. Springer Verlag, Berlim, pp 3–19
Singh SP (1998) Chronic disturbance, a principal cause of environmental degradation in develo** countries. Environ Conserv 25:1–2. https://doi.org/10.1017/S0376892998000010
Specht MJ, Santos BA, Marshall N, Melo FPL, Leal IR, Tabarelli M et al (2019) Socioeconomic differences among residents, users and neighbour populations of a protected areas in the Brazilian dry forest. J Environ Manage 232:607–614. https://doi.org/10.1016/j.jenvman.2018.11.101
Tilman D, Clark M, Williams DR, Kimmel K, Polasky S, Packer C (2017) Future threats to biodiversity and pathways to their prevention. Nature 546:73–81. https://doi.org/10.1038/nature22900
Tilman D, Knops J, Wedin D, Reicj P, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302. https://doi.org/10.1126/science.277.5330.1300
Torres RR, Lapola DM, Gamarra NLR (2017) Future climate change in the Caatinga. In: Silva JMC, Leal IR, Tabarelli M (eds) Caatinga: the largest Tropical Dry Forest region in South America. Springer Verlag, Berlim, pp 383–410
Travis JMJ (2003) Climate change and habitat destruction a deadly anthropogenic cocktail. Proc R Soc Lond 270:467–473. https://doi.org/10.1098/rspb.2002.2246
Vilela AA, Del Claro VTS, Torezan-Silingardi HM, Del-Claro K (2017) Climate changes affecting biotic interactions, phenology, and reproductive success in a savanna community over a 10-year period. Arthropod-Plant Interact 12:215–227. https://doi.org/10.1007/s11829-017-9572-y
Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC et al (2002) Ecological responses to recent climate change. Nature 16:389–395. https://doi.org/10.1038/416389a
Warren MS, Hill JK, Thomas C, Asher J, Fox R, Huntley B et al (2001) Climate versus habitat change: opposing forces underlay rapid changes to the distribution and abundances of British butterflies. Nature 414:65–69. https://doi.org/10.1038/35102054
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
Weber GW, Keeler KH (2012) The phylogenetic distribution of extrafloral nectaries in plants. Ann Bot 12:1–11. https://doi.org/10.1093/aob/mcs225
Weber MG, Porturas LD, Keeler, KH (2015) World list of plants with extrafloral nectaries. www.extrafloralnectaries.org. Accessed 29 Jan 2015
Williams SE, Middleton J (2008) Climatic seasonality, resource bottlenecks, and abundance of rainforest birds: implications for global climate change. Divers Distrib 14:69–77. https://doi.org/10.1111/j.1472-4642.2007.00418.x
Yu Q, Jia DR, Tian B, Yang YP, Duan YW (2016) Changes of flowering phenology and flower size in rosaceous plants from a biodiversity hotspot in the past century. Sci Rep 6:283–302. https://doi.org/10.1038/srep28302
Acknowledgements
We are grateful to L.B. Gonçalves and the many students who assisted with fieldwork, to Prof. Luiz Gustavo Souza from Plant Cytogenetics Laboratory, who gently helped with the phylogenetic tree construction and to K.F. Rito for hel** with the phylogenetic data. We also thank Catimbau National Park landowners for giving us permission to work on their proprieties.
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This study was supported by grants from Coordenação de Aperfeiçoamento de Pessoal de Nível superior (CAPES, PVE-88881.030482/2013-01), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, PELD-441386/2016-4 and Universal-470480/2013-0), Fundação de Amparo à Pesquisa à Ciência e Tecnologia do Estado de Pernambuco (FACEPE, APQ-0738-2.05/12 and PRONEX-0138-2.05/14), and Rufford Small Grants Foundation (RSG 17372-1). C.H.F.S. acknowledges the Commonwealth Scientific and Industrial Research Organization (CSIRO) in Darwin for support and cooperation. X.A. thanks CNPq for post-doc grants (PDS-167533/2013-4 and PDS-165623/2015-2), F.M.P.O thanks CAPES and FACEPE for post-doc grant (PNPD-88887.163451/2018-00), E.M.S.R. thanks CAPES and CNPq for post-doc grants (CSF/PVE-88887.094728/2015-00 and PDJ-165867/2015-9) and I.R.L. for productivity grants (PQ-308300/2018-1).
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XA, CHFS, ANA and IRL conceived the ideas and designed methodology; CHFS, DQAR, FMPO and TC collected the data; XA, CHFS, TC and EMSR analysed the data; XA, CHFS and IRL led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
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Arnan, X., Silva, C.H.F., Reis, D.Q.A. et al. Individual and interactive effects of chronic anthropogenic disturbance and rainfall on taxonomic, functional and phylogenetic composition and diversity of extrafloral nectary-bearing plants in Brazilian Caatinga. Oecologia 198, 267–277 (2022). https://doi.org/10.1007/s00442-021-05074-8
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DOI: https://doi.org/10.1007/s00442-021-05074-8