Climatic drivers of dry grassland phylogenetic diversity in the Republic of Macedonia

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Abstract

Climatic gradients can be used to predict the extent to which climate drives biodiversity and to which biodiversity may be affected by global climate changes. Climate and evolutionary history are linked by the ecological adaptations of species and the history of Earth’s climate. If so, phylogenetic diversity may be a good metric to estimate biodiversity. We aimed to test whether the phylogenetic diversity of Macedonian dry grasslands was related to climatic variables. We sampled 575 plots, identifying the species and building a phylogenetic tree for them. We calculated two metrics of phylogenetic diversity and regressed them against climatic variables. We also tested whether there were nodes in the tree responsible for the main observed spatial patterns of phylogenetic diversity. We found a strong signature of evolutionary history in species sorting across a gradient driven by climate in Macedonian dry grasslands. First, the amount of evolutionary history decreased towards drier and more seasonal climates, suggesting a phylogenetic niche conservatism. Second, there was an air temperature filter and a temperature seasonality filter, acting in opposite directions and leading to phylogenetic clustering. Third, there were few nodes in the phylogenetic tree with high degrees of allopatry, associated with clades that differed not only in their geographic distribution, but also in their climatic preferences. Macedonian dry grassland communities developed over centuries of traditional land use but are threatened nowadays by human activities. The use of phylogenetic approaches may lead to more effective conservation policies and help us preserve this highly diverse vegetation.

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  • Ackerly D. D. 2003: Community assembly niche conservatism and adaptive evolution in changing environments. International Journal of Plant Sciences 16 S165-S184.

  • Andersen A. N. Toro I. Parr C. L. 2015: Savanna ant species richness is maintained along a bioclimatic gradient of increasing latitude and decreasing rainfall in northern Australia. Journal of Biogeography 42 2313–2322.

  • Baldi M. Dalu G. Maracchi G. Pasqui M. Cesarone F. 2006: Heat waves in the Mediterranean: a local feature or a larger-scale effect? International Journal of Climatology 26 1477–1487.

  • Beaulieu J. M. Ree R. H. Cavender-Bares J. Weiblen G. D. Donoghue M. J. 2012: Synthesizing phylogenetic knowledge for ecological research. Ecology 93 S4-S13.

  • Begon M. Townsend C. R. Harper J. L. 2006: Ecology: from individuals to ecosystems. Blackwell Malden.

  • Bell C. D. Soltis D. E. Soltis P. S. 2010: The age and diversification of the angiosperms re-revisited. American Journal of Botany 97 1296–1303.

  • Bergant K. 2006: Climate change scenarios for Macedonia. University of Nova Gorica Nova Gorica.

  • Bivand R. Keitt T. Rowlingson B. 2015: Rgdal: bindings for the geospatial data abstraction library. R Foundation for Statistical Computing Vienna. Retrieved from http://CRAN.R-project.org/package=rgdal.

  • Borregaard M. K. Rahbek C. Fjeldså J. Parra J. L. Whittaker R. J. Graham C. H. 2014: Node-based analysis of species distributions. Methods in Ecology and Evolution 5 1225–1235.

  • Braun-Blanquet J. 1964: Pflanzensoziologie: Grundzüge der Vegetationskunde. Springer Vienna.

  • Bremer K. Friis E. M. Bremer B. 2004: Molecular phylogenetic dating of asterid flowering plants shows early Cretaceous diversification. Systematic Biology 53 496–505.

  • Carvalho G. H. Cianciaruso M. V. Batalha M. A. 2010: Plant-miner: a web tool for checking and gathering plant species taxonomic information. Environmental Modelling and Software 25 815–816.

  • Cavender-Bares J. Kozak K. H. Fine P. A. Kembel S. W. 2009:

  • The merging of community ecology and phylogenetic biology. Ecology Letters 12 693–715.

  • Chang C. 1993: Pastoral transhumance in the southern Balkans as a social ideology: ethnoarcheological research in northern Greece. American Anthropologist 95 687–703.

  • Chao A. Chiu C. H. Hsieh T. C. Davis T. Nipperess D. A. Faith D. P. 2015: Rarefaction and extrapolation of phylogenetic diversity. Methods in Ecology and Evolution 6 380–388.

  • Chemonics International 2001: Biodiversity assessment for Macedonia. Chemonics International Washington.

  • Čarni A. Matevski V. 2015: Impact of climate change on mountain flora and vegetation in the Republic of Macedonia (central part of the Balkan Peninsula). In: Öztürk M. Hakeem K. R. Faridah-Hanum I. Efe R. (eds.) Climate change impacts on high-altitude ecosystems 189–213. Springer Cham.

  • Ćušterevska R. 2016: Dry grassland vegetation in the Galičica Mountain (SW Macedonia). Contributions Section of Natural Mathematical and Biotechnical Sciences 37 105–126.

  • Ćušterevska R. Matevski V. Kostadinovski M. Čarni A. 2012: Dry grasslands communities of Erysimo-Trifolietum in the north-eastern part of the Republic of Macedonia. Hacquetia 11 91–111.

  • Davis C. C. Webb C. O. Wurdack K. J. Jaramillo C. A. Donoghue M. J. 2005: Explosive radiation of Malpighiales supports a mid-Cretaceous origin of modern tropical rain forests. American Naturalist 165 E36–E65.

  • Donoghue M. J. 2008: A phylogenetic perspective on the distribution of plant diversity. Proceedings of the National Academy of Science 105 11549–11555.

  • Filipovski G. Rizovski R. Ristevski P. 1996: The characteristic of the climate-vegetation-soil zones (regions) in the Republic of Macedonia. Macedonian Academy of Sciences and Arts Skopje.

  • Francis A. P. Currie D. J. 2003: A globally consistent richness-climate relationship for angiosperms. American Naturalist 161 523–536.

  • Gaston K. J. David R. 1994: Hotspots across Europe. Biodiversity Letters 2 108–116.

  • Graham C. H. Machac A. Storch D. 2016: Phylogenetic scale in ecology and evolution. BioRxiv: 10.1101/063560.

  • Grunewald K. Scheithauer J. 2010: Europe’s southernmost glaciers: response and adaptation to climate change. Journal of Glaciology 56 129–142.

  • Harmon L. J. Weir J. T. Brock C. D. Glor R. E. Challenger W. 2008: Geiger: investigating evolutionary radiations. Bioinformatics 24 129–131.

  • Harvey P. H. Pagel M. 1991: The comparative method in evolutionary biology. Oxford University Oxford.

  • Hawkins B. A. 2001: Ecology’s oldest pattern? Trends in Ecology and Evolution 16 470.

  • Helmus M. R. Bland T. J. Williams C. K. Ives A. R. 2007: Phylogenetic measures of biodiversity. American Naturalist 169 E68–E83.

  • Hijmans R. J. 2015: Raster: geographic data analysis and modeling. R Foundation for Statistical Computing Vienna. Retrieved from: http://CRAN.R-project.org/package=raster.

  • Hijmans R. J. Cameron S. E. Parra J. L. Jones P. G. Jarvis A. 2005: Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25 1965–1978.

  • Hoiss B. Krauss J. Potts S. G. Roberts S. Steffan-Dewenter I. 2012; Altitude acts as an environmental filter on phylogenetic composition traits and diversity in bee communities. Proceedings of the Royal Society B 79 4447–4456.

  • Huber P. J. Ronchetti E. M. 2009: Robust statistics. John Wiley New Jersey.

  • Janišová M. Bartha S. Kiehl K. Dengler J. 2011: Advances in the conservation of dry grasslands: Introduction to contributions from the seventh European Dry Grassland Meeting. Plant Biosystems 145 507–513.

  • Jombart T. Pavoine S. Devillard S. Pontier D. 2010: Putting phylogeny into the analysis of biological traits: a methodological approach. Journal of Theoretical Biology 264 693–701.

  • Jongman R. H. G. Braak C. J. F. Tongeren O. F. R. 1995: Data analysis in community and landscape ecology. Cambridge University Cambridge.

  • Kahle D. Wickham H. 2013: Ggmap: spatial visualization with ggplot2. R Journal 5 144–161.

  • Karanfilovski A. 2012: Climate change scenarios for Macedonia. Ministry of Agriculture Forestry and Water Economy Skopje.

  • Kembel S. W. Cowan P. D. Helmus M. R. Cornwell W. K. Morlon H. Ackerly D. D. Blomberg S. P. Webb C. O. 2010: Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26 1463–1464.

  • Kerkhoff A. J. Moriarty P. E. Weiser M. D. 2014: The latitudinal species richness gradient in New World woody angiosperms is consistent with the tropical conservatism hypothesis. Proceedings of the National Academy of Sciences 111 8125–8130.

  • Lean C. Maclaurin J. 2016: The value of phylogenetic diversity. Topics in Biodiversity and Conservation 14 19–37.

  • Marchese C. 2015: Biodiversity hotspots: A shortcut for a more complicated concept. Global Ecology and Conservation 3 297–309.

  • Matevski V. Petkovski S. Andonov S. Melovski L. Krstić S. 2003: Country study for biodiversity of the Republic of Macedonia. Ministry of Environmental and Physical Planning Skopje.

  • Matevski V. Lozanovski R. Kostadinovski M. 2007: Silene-Thymetum ciliatopubescentis ass. nova in the vegetation on highland pastures in the Republic of Macedonia. In: Filipovski G. Lozanovski R. Matevski. V. (eds.) Collection of papers devoted to academician Kiril Micevski. Macedonian Academy of Sciences and Arts Skopje.

  • Matevski V. Čarni A. Kostadinovski M. Košir P. Šilc U. Zelnik I. 2008: Flora and vegetation of the Macedonian steppe. Založba Ljubljana.

  • Matevski V. Čarni A. Avramoski O. Juvan N. Kostadinovski M. Košir P. Marinšek A. Paušič A. Šilc U. 2011: Forest vegetation of the Galičica mountain range in Macedonia. Založba Ljubljana.

  • Matevski V. Čarni A. Ćušterevska R. Kostadinovski M. Mucina L. 2015: Syntaxonomy of the rocky grasslands on carbonate bedrocks in the west and southwest of the Republic of Macedonia. Applied Ecology and Environmental Research 13 1197–1214.

  • McGill B. J. Enquist B. J. Weiher E. Westoby M. 2006: Rebuilding community ecology from functional traits. Trends in Ecology and Evolution 21 178–185.

  • Naeem S. Chapin III C. F. S. Costanza R. Ehrlich P. R. Golley F. B. Hooper D. U. Lawton J. H. O’Neill R. V. Mooney H. A. Sala O. E. Symstad A. J. Tilman D. 1999: Maintaining natural life support processes. Issues in Ecology 4 2–11.

  • Oksanen J. Blanchet F. G. Kindt R. Legendre P. Minchin P. R. O’Hara R. B. Simpson G. L. Solymos P. Stevens M. H. H. Wagner H. 2013: Vegan: community ecology package. R Foundation for Statistical Computing Vienna. Retrieved from http://CRAN.R-project.org/package=vegan.

  • Palpurina S. Chytrý M. Tzonev R. Danihelka J. Axmanová I. Merunková K. Duchon M. Karakiev T. 2015: Patterns of fine-scale plant species richness in dry grasslands across the eastern Balkan Peninsula. Acta Oecologica 63 36–46.

  • Paradis E. Claude J. Strimmer K. 2004: APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20 289–290.

  • Parra J. L. McGuire J. A. Graham C. A. 2010: Incorporating clade identity in analyses of phylogenetic community structure: an example with hummingbirds. American Naturalist 176 573–587.

  • Pavoine S. Love M. S. Bonsall M. B. 2009: Hierarchical partitioning of evolutionary and ecological patterns in the organization of phylogenetically-structured species assemblages: application to rockfish (genus: Sebastes) in the Southern California Bight. Ecology Letters 12 898–908.

  • Purvis A. Agapow P. M. Gittleman J. L. Mace G. M. 2000: Nonrandom extinction and the loss of evolutionary history. Science 288 328–330.

  • Qian H. Zhang Y. Zhang J. Wang X. 2013: Latitudinal gradients in phylogenetic relatedness of angiosperm trees in North America. Global Ecology and Biogeography 22 1183–1191.

  • R Development Core Team 2015: Foreign: read data stored by Minitab S SAS SPSS Stata Systat Weka dBase. R Foundation for Statistical Computing Vienna. Retrieved from http://CRAN.R-project.org/package=foreign.

  • R Development Core Team 2016: R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna. Retrieved from http://www.r-project.org.

  • Rothwell G. W. Erwin D. M. 1987: Origin of seed plants: an aneurophyte-seed fern link elaborated. American Journal of Botany 74 970–973.

  • Stevanović V. Matevski V. Tan K. 2009: Helianthemum marmoreum (Cistaceae) a new species from the Central Balkans. Botanica Serbica 33 13–19.

  • Tucker C. M. Cadotte M. W. Carvalho S. B. Davies T. J. Ferrier S. Fritz S. A. Grenyer R. Helmus M. R. Jin L. S. Mooers A. O. Pavoine S. Purschke O. Redding D. W. Rosauer D. F. Winter M. Mazel F. 2017: A guide to phylogenetic metrics for conservation community ecology and macroecology. Biological Reviews 92 698–715.

  • Vellend M. Cornwell W. K. Magnuson-Ford K. Mooers A. O. 2011: Measuring phylogenetic biodiversity. In: Magurran A. E. McGill B. J. (eds.) Biological diversity: frontiers in measurement and assessment 193–206. Oxford University Oxford.

  • Venables W. N. Ripley B. D. 2002: Modern applied statistics with S. Springer New York.

  • Webb C. O. 2000: Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. American Naturalist 156 145–155.

  • Webb C. O. 2002: Phylogenies and community ecology. Annual Review of Ecology and Systematics 33 475–505.

  • Webb C. O. Ackerly D. D. Kembel S. W. 2008: Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24 2098–2100.

  • Weigelt P. Kissling W. D. Kisel Y. Fritz S. A. Karger D. N. Kessler M. Lehtonen S. Svenning J. C. Kreft H. 2015: Global patterns and drivers of phylogenetic structure in island floras. Scientific Reports 5 12213.

  • Williams R. J. Cook G. D. Braithwaite R. W. Andersen A. N. Corbett L. K. 1995: Australia’s wet-dry tropics: identifying the sensitive zones. In: Pernetta J. Leemans R. Elder D. Humphrey S. (eds.) The impact of climate change on ecosystems and species: terrestrial ecosystems 39–65. IUCN Gland.

  • WWF 2016: Living planet report. WWF International Gland.

  • Zhang J. Nielsen S. E. Stolar J. Chen Y. Thuiller W. 2015: Gains and losses of plant species and phylogenetic diversity for a northern high-latitude region. Diversity and Distributions 21 1441-1454.

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