Island biogeographical models consider islands either as geologically static with biodiversity resulting from ecologically neutral immigration–extinction dynamics1, or as geologically dynamic with biodiversity resulting from immigration–speciation–extinction dynamics influenced by changes in island characteristics over millions of years2. Present climate and spatial arrangement of islands, however, are rather exceptional compared to most of the Late Quaternary, which is characterized by recurrent cooler and drier glacial periods. These climatic oscillations over short geological timescales strongly affected sea levels3,4 and caused massive changes in island area, isolation and connectivity5, orders of magnitude faster than the geological processes of island formation, subsidence and erosion considered in island theory2,6. Consequences of these oscillations for present biodiversity remain unassessed5,7. Here we analyse the effects of present and Last Glacial Maximum (LGM) island area, isolation, elevation and climate on key components of angiosperm diversity on islands worldwide. We find that post-LGM changes in island characteristics, especially in area, have left a strong imprint on present diversity of endemic species. Specifically, the number and proportion of endemic species today is significantly higher on islands that were larger during the LGM. Native species richness, in turn, is mostly determined by present island characteristics. We conclude that an appreciation of Late Quaternary environmental change is essential to understand patterns of island endemism and its underlying evolutionary dynamics.
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MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton University Press, 1967)
Whittaker, R. J., Triantis, K. A. & Ladle, R. J. A general dynamic theory of oceanic island biogeography. J. Biogeogr. 35, 977–994 (2008)
Bintanja, R., van de Wal, R. S. & Oerlemans, J. Modelled atmospheric temperatures and global sea levels over the past million years. Nature 437, 125–128 (2005)
Miller, K. G. et al. The Phanerozoic record of global sea-level change. Science 310, 1293–1298 (2005)
Fernández-Palacios, J. M. et al. Towards a glacial-sensitive model of island biogeography. Glob. Ecol. Biogeogr. (2015)
Borregaard, M. K. et al. Oceanic island biogeography through the lens of the general dynamic model: assessment and prospect. Biol. Rev. Camb. Philos. Soc. (2016)
Warren, B. H. et al. Islands as model systems in ecology and evolution: prospects fifty years after MacArthur-Wilson. Ecol. Lett. 18, 200–217 (2015)
Dynesius, M. & Jansson, R. Evolutionary consequences of changes in species´ geographical distributions driven by Milankovitch climate oscillations. Proc. Natl Acad. Sci. USA 97, 9115–9120 (2000)
Sandel, B. et al. The influence of Late Quaternary climate-change velocity on species endemism. Science 334, 660–664 (2011)
Ali, J. R. & Aitchison, J. C. Exploring the combined role of eustasy and oceanic island thermal subsidence in shaping biodiversity on the Galápagos. J. Biogeogr. 41, 1227–1241 (2014)
Rijsdijk, K. F. et al. Quantifying surface-area changes of volcanic islands driven by Pleistocene sea-level cycles: biogeographical implications for the Macaronesian archipelagos. J. Biogeogr. 41, 1242–1254 (2014)
Weigelt, P. & Kreft, H. Quantifying island isolation – insights from global patterns of insular plant species richness. Ecography 36, 417–429 (2013)
Heaney, L. R. Dynamic disequilibrium: a long-term, large-scale perspective on the equilibrium model of island biogeography. Glob. Ecol. Biogeogr. 9, 59–74 (2000)
Weigelt, P., Jetz, W. & Kreft, H. Bioclimatic and physical characterization of the world’s islands. Proc. Natl Acad. Sci. USA 110, 15307–15312 (2013)
Svenning, J.-C. & Skov, F. Ice age legacies in the geographical distribution of tree species richness in Europe. Glob. Ecol. Biogeogr. 16, 234–245 (2007)
Kisel, Y. & Barraclough, T. G. Speciation has a spatial scale that depends on levels of gene flow. Am. Nat. 175, 316–334 (2010)
Whitehead, D. R. & Jones, C. E. Small islands and the equilibrium theory of insular biogeography. Evolution 23, 171–179 (1969)
Brown, J. H. & Kodric-Brown, A. Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58, 445–449 (1977)
Ricklefs, R. E. & Bermingham, E. Nonequilibrium diversity dynamics of the Lesser Antillean avifauna. Science 294, 1522–1524 (2001)
Nogué, S. et al. The ancient forests of La Gomera, Canary Islands, and their sensitivity to environmental change. J. Ecol. 101, 368–377 (2013)
Losos, J. B. & Schluter, D. Analysis of an evolutionary species-area relationship. Nature 408, 847–850 (2000)
Gillespie, R. G. & Roderick, G. K. Evolution: geology and climate drive diversification. Nature 509, 297–298 (2014)
Steinbauer, M. J., Irl, S. D. H. & Beierkuhnlein, C. Elevation-driven ecological isolation promotes diversification on Mediterranean islands. Acta Oecol. 47, 52–56 (2013)
Stohlgren, T. J., Barnett, D. T., Jarnevich, C. S., Flather, C. & Kartesz, J. The myth of plant species saturation. Ecol. Lett. 11, 313–322 (2008)
Jackson, S. T. & Sax, D. F. Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol. Evol. 25, 153–160 (2010)
Triantis, K., Mylonas, M. & Whittaker, R. Evolutionary species–area curves as revealed by single-island endemics: insights for the inter-provincial species–area relationship. Ecography 31, 401–407 (2008)
Price, J. P. & Clague, D. A. How old is the Hawaiian biota? Geology and phylogeny suggest recent divergence. Proc. R. Soc. Lond. B 269, 2429 (2002)
Cabral, J. S., Weigelt, P., Kissling, W. D. & Kreft, H. Biogeographic, climatic and spatial drivers differentially affect α-, β- and γ-diversities on oceanic archipelagos. Proc. R. Soc. Lond. B 281, 20133246 (2014)
Price, J. P. & Wagner, W. L. A phylogenetic basis for species–area relationships among three Pacific Island floras. Am. J. Bot. 98, 449–459 (2011)
Kier, G. et al. A global assessment of endemism and species richness across island and mainland regions. Proc. Natl Acad. Sci. USA 106, 9322–9327 (2009)
Amante, C. & Eakins, B. W. ETOPO1 1 arc-minute global relief model: procedures, data sources and analysis. NOAA Technical Memorandum NESDIS NGDC-24 (2009)
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005)
Braconnot, P. et al. Results of PMIP2 coupled simulations of the mid-Holocene and Last Glacial Maximum – part 1: experiments and large-scale features. Clim. Past 3, 261–277 (2007)
Harter, D. E. V. et al. Impacts of global climate change on the floras of oceanic islands - Projections, implications and current knowledge. Perspect. Plant Ecol. Evol. Syst. 17, 160–183 (2015)
Sax, D. F., Gaines, S. D. & Brown, J. H. Species invasions exceed extinctions on islands worldwide: a comparative study of plants and birds. Am. Nat. 160, 766–783 (2002)
Weigelt, P. et al. Global patterns and drivers of phylogenetic structure in island floras. Sci. Rep. 5, 12213 (2015)
Weigelt, P. The macroecology of island floras. Frontiers of Biogeography 7, 119–125 (2015)
Abe, T. Threatened pollination systems in native flora of the Ogasawara (Bonin) Islands. Ann. Bot. (Lond.) 98, 317 (2006)
Acevedo-Rodríguez, P. & Strong, M. T. Catalogue of the seed plants of the West Indieshttp://botany.si.edu/antilles/WestIndies/index.htm
Arechavaleta, M., Zurita, N., Marrero, M. C. & Martín, J. L. Lista preliminar de especies silvestres de Cabo Verde (hongos, plantas y animales terrestres) (Consejería de Medio Ambiente y Ordenación Territorial, Gobierno de Canarias, 2005)
Arechavaleta, M., Rodríguez, S., Zurita, N. & García, A. Lista de especies silvestres de Canarias. Hongos, plantas y animales terrestres (Consejería de Medio Ambiente y Ordenación Territorial, Gobierno de Canarias, 2009)
Ashmole, P. & Ashmole, M. St Helena and Ascension Island: a Natural History (Anthony Nelson Ltd, 2000)
Athens, J. S., Blinn, D. W. & Ward, J. V. Vegetation history of Laysan Island, northwestern Hawaiian islands. Pac. Sci. 61, 17–37 (2007)
Baker, M. L. & Duretto, M. F. A Census of The Vascular Plants of Tasmania (Tasmanian Herbarium, Tasmanian Museum and Art Gallery, 2011)
Borges, P. A. V. et al. Listagem dos fungos, flora e fauna terrestres dos arquipélagos da Madeira e Selvagens (Direcção Regional do Ambiente da Madeira and Universidade dos Açores, 2008)
Borges, P. A. V. et al. A List of the Terrestrial and Marine Biota from the Azores (Princípia, Cascais, 2010)
Brofas, G., Karetsos, G., Panitsa, M. & Theocharopoulos, M. The flora and vegetation of Gyali Island, SE Aegean, Greece. Willdenowia 31, 51–70 (2001)
Broughton, D. A. & McAdam, J. H. A checklist of the native vascular flora of the Falkland Islands (Islas Malvinas): new information on the species present, their ecology, status and distribution. J. Torrey Bot. Soc. 132, 115–148 (2005)
Burton, F. J. Red List Assessment of Cayman Islands’ Native Flora for Legislation and Conservation Planning (Royal Botanic Gardens Kew, 2007)
Caribbean Research and Management of Biodiversity Foundation. Dutch Caribbean Biodiversity Explorerhttp://www.dcbiodata.net/explorer/home
Case, T. J., Cody, M. L. & Ezcurra, E. A new island biogeography of the Sea of Cortés (Oxford University Press, 2002)
Charters, M. Flora of Bermudahttp://www.calflora.net/floraofbermuda/index.html
Christmas Island National Park. Third Christmas Island National Park Management Plan (Parks Australia North, Christmas Island, Australia, 2002)
Cronk, Q. C. B. The past and present vegetation of St Helena. J. Biogeogr. 16, 47–64 (1989)
D’Arcy, W. G. The island of Anegada and its flora. Atoll Res. Bull. 139, 1–21 (1971)
de Lange, P. J., Heenan, P. B. & Rolfe, J. R. Checklist of Vascular Plants Recorded from Chatham Islands (Department of Conservation, Wellington Hawke’s Bay Conservancy, 2011)
de Miranda Freitas, A. M. A Flora Fanerogâmica Atual do Arquipélago de Fernando de Noronha - Brasil (Universidade Estadual, 2007)
Du Puy, D. J. Christmas Island: species listshttp://www.environment.gov.au/biodiversity/abrs/online-resources/flora/50/index.html
Exell, A. W. Catalogue of the Vascular Plants of S. Tome (with Principe and Annobon) (Trustees of the British Museum, 1944)
Florence, J., Chevillotte, H., Ollier, C. & Meyer, J.-Y. Base de données botaniques Nadeaud de l'Herbier de la Polynésie française (PAP)http://www.herbier-tahiti.pf
Fosberg, F. R., Renvoize, S. A. & Townsend, C. C. The flora of Aldabra and neighbouring islands (HMSO, 1980)
Fosberg, F. R. & Sachet, M. H. Flora of Maupiti, Society Islands. Atoll Res. Bull. 294, 1–70 (1987)
Green, P. S. Lord Howe Island: species listshttp://www.environment.gov.au/biodiversity/abrs/online-resources/flora/49/index.html
Greene, S. & Walton, D. An annotated check list of the sub-Antarctic and Antarctic vascular flora. Polar Rec. (Gr. Brit.) 17, 473–484 (1975)
Hill, M. J. Biodiversity Surveys and Conservation Potential of Inner Seychelles Islands (Smithsonian Institution, 2002)
Hnatiuk, R. J. Subantarctic Islands: species listshttp://www.environment.gov.au/biodiversity/abrs/online-resources/flora/50/index.html
Imada, C. T. Hawaiian Native and Naturalized Vascular Plants Checklist. Bishop Musem Technical Report 60 (2012)
Jaramillo Díaz, P. & Guézou, A. CDF checklist of Galapagos vascular plantshttp://www.darwinfoundation.org/datazone/checklists/vascular-plants/
Johnson, P. N. & Campbell, D. J. Vascular plants of the Auckland Islands. N.Z. J. Bot. 13, 665–720 (1975)
Johnston, I. M. The flora of the Revillagigedo Islands. Proc. Calif. Acad. Sci. 20, 9–104 (1931)
Junak, S., Philbrick, R., Chaney, S. & Clark, R. A Checklist of Vascular Plants of Channel Islands National Park. 2nd edn (Southwest Parks and Monuments Association, 1997)
Kingston, N., Waldren, S. & Bradley, U. The phytogeographical affinities of the Pitcairn Islands – a model for south-eastern Polynesia? J. Biogeogr. 30, 1311–1328 (2003)
Kirchner, F., Picot, F., Merceron, E. & Gigot, G. Flore vasculaire de La Réunion (Conservatoire Botanique National de Mascarin, 2010)
Levin, G. A. & Moran, R. The vascular flora of Socorro, Mexico. Memoirs of the San Diego Society of Natural History 16, 1–71 (1989)
Marticorena, C., Stuessy, T. F. & Baeza, C. M. Catalogue of the vascular flora of the Robinson Crusoe or Juan Fernández islands, Chile. Gayana Botanica 55, 187–211 (1998)
Miller, A. G. & Morris, M. Ethnoflora of the Soqotra Archipelago (Royal Botanic Garden, 2004)
Moran, R. The Flora of Guadalupe Island, Mexico (California Academy of Sciences, 1996)
Renvoize, S. A. A floristic analysis of the western Indian Ocean coral islands. Kew Bull. 30, 133–152 (1975)
Sáez, L. & Rosselló, J. A. Llibre vermell de la flora vascular de les Illes Balears (Direcció General de Biodiversitat, Conselleria de Medi Ambient, Govern de les Illes Balears, 2001)
St John, H. Census of the Flora of the Gambier Islands, Polynesia: Pacific Plant Studies 43 (1988)
Strahm, W. A. The Conservation and Restoration of the Flora of Mauritius and Rodrigues (University of Reading, 1993)
Sykes, W. R. Contributions to the Flora of Niue. Department of Scientific and Industrial Research, New Zealand. Bulletin; 200 (1970)
Takahashi, H. et al. A preliminary checklist of the vascular plants of Chirinkotan, Kuril Islands. Journal of Phytogeography and Taxonomy 47, 131–137 (1999)
Taylor, R. Straight Through from London: the Antipodes and Bounty Islands, New Zealand (Heritage Expeditions New Zealand, 2006)
Universitat de les Illes Balears. Herbario virtual del Mediterráneo Occidentalhttp://herbarivirtual.uib.es/cas-med/index.html
University of Kent. Cook Islands Biodiversity and Ethnobiology Databasehttp://cookislands.bishopmuseum.org/search.asp
Wace, N. M. The vegetation of Gough Island. Ecol. Monogr. 31, 337–367 (1961)
Wace, N. M. & Dickson, J. H. The terrestrial botany of the Tristan da Cunha Islands. Phil. Trans. R. Soc. Lond. B 249, 273–360 (1965)
Wagner, W. L. & Lorence, D. H. Flora of the Marquesas Islandshttp://botany.si.edu/pacificislandbiodiversity/marquesasflora/index.htm
Wagner, W. L., Herbst, D. R. & Lorence, D. H. Flora of the Hawaiian Islandshttp://botany.si.edu/pacificislandbiodiversity/hawaiianflora/index.htm
Whistler, W. A. A Study of the Rare Plants of American Samoa (US Fish and Wildlife Service, 1998)
Gerlach, J. The biodiversity of the granitic islands of Seychelles. Phelsuma 11 (Supplement A), 1–47 (2003)
Shaw, J. D., Spear, D., Greve, M. & Chown, S. L. Taxonomic homogenization and differentiation across Southern Ocean Islands differ among insects and vascular plants. J. Biogeogr. 37, 217–228 (2010)
Dormann, C. F. et al. Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30, 609–628 (2007)
Crase, B., Liedloff, A. C. & Wintle, B. A. A new method for dealing with residual spatial autocorrelation in species distribution models. Ecography 35, 879–888 (2012)
Bivand, R. spdep: spatial dependence: weighting schemes, statistics and models v.0.5-77 (Package for R statistical software, 2014)
Kreft, H., Jetz, W., Mutke, J., Kier, G. & Barthlott, W. Global diversity of island floras from a macroecological perspective. Ecol. Lett. 11, 116–127 (2008)
Burnham, K. P. & Anderson, D. R. Model selection and multimodel inference: a practical information-theoretic approach. 2nd edn (Springer, 2002)
Guisan, A. & Zimmermann, N. E. Predictive habitat distribution models in ecology. Ecol. Modell. 135, 147–186 (2000)
McFadden, D. in Frontiers in Economics (ed P. Zarembka ) (Academic Press, 1974)
Efron, B. Regression and ANOVA with zero-one data: measures of residual variation. J. Am. Stat. Assoc. 73, 113–121 (1978)
P.W., J.S.C. and H.K. acknowledge funding by the German Research Council (DFG) Free Floater Program in the Excellence Initiative at the University of Göttingen. P.W. and H.K. additionally acknowledge funding by the BEFmate project from the Ministry of Science and Culture of Lower Saxony. M.J.S. was supported by the Danish Carlsbergfondet (CF14-0148). We are grateful to S. L. Chown, J. Gerlach, Y. Kisel, J. P. Price and J. D. Shaw for providing species lists. We thank R. J. Whittaker for helpful discussions and J.-C. Svenning for comments on a previous version of the manuscript.
The authors declare no competing financial interests.
Extended data figures and tables
Extended Data Figure 1 Frequency distributions of differences between last glacial maximum and present characteristics of 184 oceanic islands worldwide.
a–e, Variables depicted by Δ give differences between island characteristics during the last glacial maximum and today in island area (a), stepping-stone isolation (b), temperature (c), precipitation (d), and elevation (e). In f, no. of entities represents the number of present island entities that made up single past island units during the LGM owing to lower sea levels.
Extended Data Figure 2 Geologic age and area of the four main geologic complexes of the Hawaiian Islands exemplifying the rate of area decrease with time due to subsidence and erosion for volcanic islands.
In this example scenario, we assume that the four major complexes of the Hawaiian Islands (Fig. 2b) all reached approximately the same maximum area size and that the youngest complex, Big Island, already reached its full extent. The area decrease from Big Island to Maui Nui equals −0.0072 km2 per year and from Maui Nui to O’ahu −0.0016 km2 per year (see map in Fig. 2b). The linear fit over all points has a slope of −0.0016 km2 per year. The negative exponential curve has a slope of −0.0034 km2 per year at the beginning and of −0.0006 km2 per year at the end. For comparison, the 184 islands used for this paper experienced an area decrease due to rising sea levels of 0.5035 km2 per year over 10,000 years on average and the post-LGM decrease in island area for islands like Anegada or Mahé, was up to 1,000 times faster than the area decrease indicated here for the Hawaiian Islands. The notion that post-LGM changes have been much faster than average rates of geologic processes of island formation and erosion, therefore, most likely holds true even if the assumptions above are not perfectly met.
Extended Data Figure 3 Pearson correlation coefficients (r) of last glacial maximum and present characteristics of 184 oceanic islands worldwide.
a–f, Island area (a), stepping-stone isolation (b), isolation measured as proportion of surrounding landmass (c), temperature (d), precipitation (e), and elevation (f). See Methods for variable descriptions. Diagonals indicate hypothetically equal last glacial maximum and present values. ***P < 0.001.
Extended Data Figure 4 Effects of post-LGM changes in biophysical island characteristics on the proportion of endemic species on 184 islands worldwide.
a, b, Regression lines were predicted for changes in area (Δarea) (a) and stepping-stone isolation (Δisolation) (b) after accounting for all past and present covariables which were held constant at the mean of their empirical values across the islands (see Fig. 3 and Extended Data Fig. 5). Relationships are shown for single-island endemics (light green) and species endemic to past island units (differs from single-island endemics in cases where several present islands originated from one island during the last glacial maximum) (green). Dashed lines indicate 95% confidence intervals.
Extended Data Figure 5 Effects of post-LGM changes in biophysical island characteristics on angiosperm diversity on 184 islands worldwide.
Post-LGM changes (with Δ) give the difference in island characteristics from the LGM to today. No. of entities, number of present-island entities that made up single past island units during the LGM. Regression lines were predicted after accounting for all past and present covariables which were held constant at the mean of their empirical values across the islands (for Δarea and Δisolation see Fig. 3 and Extended Data Fig. 4). In a, c, e and g, relationships are shown for species numbers of natives (black), native-non-endemics (blue), single-island endemics (light green) and species endemic to past island units (green; differs from single-island endemics in cases where several present islands originated from one island during the LGM). In b, d, f and h, relationships are shown for proportions of single-island endemics (light green) and species endemic to past island units (green). Dashed lines indicate 95% confidence intervals. *P < 0.05, **P < 0.01, ***P < 0.001, n.s., not significant (P ≥ 0.05).
Extended Data Figure 6 Species richness of native and endemic angiosperms on the 184 islands worldwide used for this study.
a–f, Native species (a), single-island endemics (SIE) (b), past-island-unit endemics (PIE; differs from SIE in cases where several present islands originated from one island during the last glacial maximum) (c), native non-endemics (d), proportion of single-island endemics (pSIE) (e), and proportion of species endemic to past island units (pPIE) (f). Species richness is given in numbers of species. Numbers in legends indicate category borders. World maps are based on the GADM database of Global Administrative Areas, version 1 (http://www.gadm.org/version1). See Supplementary Data for values and see Methods for references used to compile the data set.
Extended Data Figure 7 Relationships and Pearson correlation coefficients (r) of native and endemic species richness of angiosperms on 184 islands worldwide.
a–c, Correlations of native species richness (S) with native non-endemics (N) (a), single-island endemics (SIE) (b) and past-island-unit endemics (PIE; differs from SIE in cases where several present islands originated from one island during the last glacial maximum) (c). d–f, Correlations of native non-endemic species richness (N) with single-island endemics (SIE) (d) and past-island-unit endemics (PIE) (e) as well as richness of single-island endemics (SIE) with past-island-unit endemics (PIE) (f). Diagonals indicate lines of equal values. ***P < 0.001.
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Weigelt, P., Steinbauer, M., Cabral, J. et al. Late Quaternary climate change shapes island biodiversity. Nature 532, 99–102 (2016). https://doi.org/10.1038/nature17443
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