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The unrealized potential of herbaria for global change biology
Corresponding Author
Emily K. Meineke
Department of Organismic and Evolutionary Biology, Harvard University Herbaria, 22 Divinity Avenue, Cambridge, Massachusetts, 02138 USA
Department of Biology, McGill University, 1205 Dr. Penfield Avenue, Montreal, Quebec, H3A 1B1 Canada
E-mail: [email protected]Search for more papers by this authorCharles C. Davis
Department of Organismic and Evolutionary Biology, Harvard University Herbaria, 22 Divinity Avenue, Cambridge, Massachusetts, 02138 USA
Search for more papers by this authorT. Jonathan Davies
Department of Biology, McGill University, 1205 Dr. Penfield Avenue, Montreal, Quebec, H3A 1B1 Canada
Search for more papers by this authorCorresponding Author
Emily K. Meineke
Department of Organismic and Evolutionary Biology, Harvard University Herbaria, 22 Divinity Avenue, Cambridge, Massachusetts, 02138 USA
Department of Biology, McGill University, 1205 Dr. Penfield Avenue, Montreal, Quebec, H3A 1B1 Canada
E-mail: [email protected]Search for more papers by this authorCharles C. Davis
Department of Organismic and Evolutionary Biology, Harvard University Herbaria, 22 Divinity Avenue, Cambridge, Massachusetts, 02138 USA
Search for more papers by this authorT. Jonathan Davies
Department of Biology, McGill University, 1205 Dr. Penfield Avenue, Montreal, Quebec, H3A 1B1 Canada
Search for more papers by this authorAbstract
Plant and fungal specimens in herbaria are becoming primary resources for investigating how plant phenology and geographic distributions shift with climate change, greatly expanding inferences across spatial, temporal, and phylogenetic dimensions. However, these specimens contain a wealth of additional data, including nutrients, defensive compounds, herbivore damage, disease lesions, and signatures of physiological processes, that capture ecological and evolutionary responses to the Anthropocene but which are less frequently utilized. Here, we outline the diversity of herbarium data, global change topics to which they have been applied, and new hypotheses they could inform. We find that herbarium data have been used extensively to study impacts of climate change and invasive species, but that such data are less commonly used to address other drivers of biodiversity loss, including habitat conversion, pollution, and overexploitation. In addition, we note that fungal specimens are under-explored relative to vascular plants. To facilitate broader application of plant and fungal specimens in global change research, we consider the limitations of these data and modern sampling and statistical tools that may be applied to surmount challenges they present. Using a case study of insect herbivory, we illustrate how novel herbarium data may be employed to test hypotheses for which few data exist. With the goal of positioning herbaria as hubs for global change research, we suggest future research directions and curation priorities.
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Literature Cited
- Ainsworth, E. A., and S. P. Long. 2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy. New Phytologist 165: 351–371.
- Antonovics, J., M. E. Hood, H. Thrall, J. Y. Abrams, and G. M. Duthie. 2003. Herbarium studies on the distribution of anther-smut fungus (Microbotryum violaceum) and Silene species (Caryophyllaceae) in the eastern United States. American Journal of Botany 90: 1522–1531.
- Aono, Y., and K. Kazui. 2008. Phenological data series of cherry tree flowering in Kyoto, Japan, and its application to reconstruction of springtime temperatures since the 9th century. International Journal of Climatology 28: 905–914.
- Applequist, W. L., and L. M. Campbell. 2014. DNA Banking for the 21st Century. in Proceedings of the US Workshop on DNA Banking, Vol. 194. The William L. Brown Center at the Missouri Botanical Garden, St. Louis, Missouri, USA.
- Atha, D. E., T. Forrest, R. F. C. Naczi, M. C. Pace, M. Rubin, J. A. Schuler, and M. Nee. 2016. The historic and extant spontaneous vascular flora of The New York Botanical Garden. Brittonia 68: 245–277.
- Baker, T. R., et al. 2017. Maximising synergy among tropical plant systematists, ecologists, and evolutionary biologists. Trends in Ecology and Evolution 32: 258–267.
- Barney, J. N. 2006. North American history of two invasive plant species: phytogeographic distribution, dispersal vectors, and multiple introductions. Biological Invasions 8: 703–717.
- Bertin, R. I. 2002. Losses of native plant species from Worcester, Massachusetts. Rhodora 104: 325–349.
- Bolmgren, K., and K. Lonnberg. 2005. Herbarium data reveal an association between fleshy fruit type and earlier flowering time. International Journal of Plant Sciences 166: 663–670.
- Bonal, D., et al. 2011. Leaf functional response to increasing atmospheric CO2 concentrations over the last century in two northern Amazonian tree species: A historical δ13C and δ18O approach using herbarium samples. Plant, Cell and Environment 34: 1332–1344.
- Bonan, G. B. 2008. Forests and climate change: Forcings, feedbacks, and the climate benefits of forests. Science 320: 1444–1449.
- Both, C., M. van Asch, R. G. Bijlsma, A. B. van den Burg, and M. E. Visser. 2009. Climate change and unequal phenological changes across four trophic levels: Constraints or adaptations? Journal of Animal Ecology 78: 73–83.
- Burns, K. C., N. Herold, and B. Wallace. 2012. Evolutionary size changes in plants of the south-west Pacific. Global Ecology and Biogeography 21: 819–828.
- Buswell, J. M., A. T. Moles, and S. Hartley. 2011. Is rapid evolution common in introduced plant species? Journal of Ecology 99: 214–224.
- Calinger, K. M. 2015. A functional group analysis of change in the abundance and distribution of 207 plant species across 115 years in north-central North America. Biodiversity and Conservation 24: 2439–2457.
- Calinger, K. M., S. Queenborough, and P. S. Curtis. 2013. Herbarium specimens reveal the footprint of climate change on flowering trends across north-central North America. Ecology Letters 16: 1037–1044.
- Celesti-Grapow, L., G. Capotorti, E. Del Vico, E. Lattanzi, A. Tilia, and C. Blasi. 2013. The vascular flora of Rome. Plant Biosystems 147: 1059–1087.
- Clark, D. A. 2004. Tropical forests and global warming: Slowing it down or speeding it up? Frontiers in Ecology and the Environment 2: 73–80.
- Corney, D., J. Y. Clark, H. L. Tang, and P. Wilkin. 2012a. Automatic extraction of leaf characters from herbarium specimens. Taxon 61: 231–244.
- Corney, D. P., H. L. Tang, J. Y. Clark, Y. Hu, and J. Jin. 2012b. Automating digital leaf measurement: the tooth, the whole tooth, and nothing but the tooth. PLoS ONE 7: e42112.
- Crawford, P. H. C., and B. W. Hoagland. 2009. Can herbarium records be used to map alien species invasion and native species expansion over the past 100 years? Journal of Biogeography 36: 651–661.
- D'Andrea, L., O. Broennimann, G. Kozlowski, A. Guisan, X. Morin, J. Keller-Senften, and F. Felber. 2009. Climate change, anthropogenic disturbance and the northward range expansion of Lactuca serriola (Asteraceae). Journal of Biogeography 36: 1573–1587.
- Daru, B. H., et al. 2018. Widespread sampling biases in herbaria revealed from large-scale digitization. New Phytologist 217: 939–955.
- Davis, C. C., C. G. Willis, B. Connolly, C. Kelly, and A. M. Ellison. 2015. Herbarium records are reliable sources of phenological change driven by climate and provide novel insights into species’ phenological cueing mechanisms. American Journal of Botany 102: 1599–1609.
- DeCandido, R., A. A. Muir, and M. B. Gargiullo. 2004. A first approximation of the historical and extant vascular flora of New York City: Implications for native plant species conservation. Journal of the Torrey Botanical Society 131: 243–251.
- Diamond, S. E., L. M. Nichols, N. McCoy, C. Hirsch, S. L. Pelini, N. J. Sanders, A. M. Ellison, N. J. Gotelli, and R. R. Dunn. 2012. A physiological trait-based approach to predicting the responses of species to experimental climate warming. Ecology 93: 2305–2312.
- Diez, J. M., T. Y. James, M. McMunn, and I. Ibanez. 2013. Predicting species-specific responses of fungi to climatic variation using historical records. Global Change Biology 19: 3145–3154.
- Dolan, R. W., M. E. Moore, and J. D. Stephens. 2011. Documenting effects of urbanization on flora using herbarium records. Journal of Ecology 99: 1055–1062.
- Drew, J. A., C. S. Moreau, and M. L. J. Stiassny. 2017. Digitization of museum collections holds the potential to enhance researcher diversity. Nature Ecology and Evolution 1: 1789–1790.
- Elith, J., and J. R. Leathwick. 2009. Species distribution models: ecological explanation and prediction across space and time. Annual Review of Ecology Evolution and Systematics 40: 677–697.
- Everill, P. H., R. B. Primack, E. R. Ellwood, and E. K. Melaas. 2014. Determining past leaf-out times of New England's deciduous forests from herbarium specimens. American Journal of Botany 101: 1293–1300.
- Farnsworth, E. J., and D. E. Ogurcak. 2006. Biogeography and decline of rare plants in New England: Historical evidence and contemporary monitoring. Ecological Applications 16: 1327–1337.
- Feeley, K. J. 2012. Distributional migrations, expansions, and contractions of tropical plant species as revealed in dated herbarium records. Global Change Biology 18: 1335–1341.
- Feeley, K. J., and M. R. Silman. 2010. Land-use and climate change effects on population size and extinction risk of Andean plants. Global Change Biology 16: 3215–3222.
- Feeley, K. J., and M. R. Silman. 2011. Keep collecting: accurate species distribution modelling requires more collections than previously thought. Diversity and Distributions 17: 1132–1140.
- Feeley, K. J., J. Hurtado, S. Saatchi, M. R. Silman, and D. B. Clark. 2013. Compositional shifts in Costa Rican forests due to climate-driven species migrations. Global Change Biology 19: 3472–3480.
- Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125: 1–15.
- Futuyma, D. J., and A. A. Agrawal. 2009. Macroevolution and the biological diversity of plants and herbivores. Proceedings of the National Academy of Sciences USA 106: 18054–18061.
- Gilman, S. E., M. C. Urban, J. Tewksbury, G. W. Gilchrist, and R. D. Holt. 2010. A framework for community interactions under climate change. Trends in Ecology and Evolution 25: 325–331.
- Gotelli, N. J., and G. R. Graves. 1996. Null models in ecology. Smithsonian Institution Press, Washington, DC, USA.
- Graham, C. H., S. Ferrier, F. Huettman, C. Moritz, and A. T. Peterson. 2004. New developments in museum-based informatics and applications in biodiversity analysis. Trends in Ecology and Evolution 19: 497–503.
- Gregor, T., D. Bönsel, I. Starke-Ottich, and G. Zizka. 2012. Drivers of floristic change in large cities – A case study of Frankfurt/Main (Germany). Landscape and Urban Planning 104: 230–237.
- Guerin, G. R., H. Wen, and A. J. Lowe. 2012. Leaf morphology shift linked to climate change. Biology Letters 8: 882–886.
- Gugerli, F., L. Parducci, and R. J. Petit. 2005. Ancient plant DNA: review and prospects. New Phytologist 166: 409–418.
- Harris, L. W., and T. J. Davies. 2016. A complete fossil-calibrated phylogeny of seed plant families as a tool for comparative analyses: testing the ‘time for speciation’ hypothesis. PLoS ONE 11: e0162907.
- Haston, E., J. E. Richardson, P. F. Stevens, M. W. Chase, and D. J. Harris. 2009. The Linear Angiosperm Phylogeny Group (LAPG) III: a linear sequence of the families in APG III. Botanical Journal of the Linnean Society 161: 128–131.
- Hegland, S. J., A. Nielsen, A. Lazaro, A. L. Bjerknes, and O. Totland. 2009. How does climate warming affect plant-pollinator interactions? Ecology Letters 12: 184–195.
- Johnson, K. G., et al. 2011. Climate change and biosphere response: unlocking the collections vault. BioScience 61: 147–153.
- Joly, M., P. Bertrand, R. Y. Gbangou, M. C. White, J. Dubé, and C. Lavoie. 2011. Paving the way for invasive species: Road type and the spread of Common ragweed (Ambrosia artemisiifolia). Environmental Management 48: 514–522.
- Kauserud, H., L. C. Stige, J. O. Vik, R. H. Okland, K. Hoiland, and N. C. Stenseth. 2008. Mushroom fruiting and climate change. Proceedings of the National Academy of Sciences USA 105: 3811–3814.
- Kauserud, H., E. Heegaard, M. A. Semenov, L. Boddy, R. Halvorsen, L. C. Stige, T. H. Sparks, A. C. Gange, and N. Chr. Stenseth. 2010. Climate change and spring-fruiting fungi. Proceedings of the Royal Society B 277: 1169–1177.
- Kavanagh, P. H., C. A. Lehnebach, M. J. Shea, and K. C. Burns. 2011. Allometry of sexual size dimorphism in dioecious plants: Do plants obey Rensch's rule? American Naturalist 178: 596–601.
- Keane, R. M., and M. J. Crawley. 2002. Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17: 164–170.
- Keeling, C., and T. Whorf. 2005. Atmospheric carbon dioxide record from Mauna Loa. Carbon Dioxide Research Group, Scripps Institution of Oceanography, University of California, La Jolla, California, USA.
- Kharouba, H. M., and M. Vellend. 2015. Flowering time of butterfly nectar food plants is more sensitive to temperature than the timing of butterfly adult flight. Journal of Animal Ecology 84: 1311–1321.
- Kingsolver, J. G., S. E. Diamond, and L. B. Buckley. 2013. Heat stress and the fitness consequences of climate change for terrestrial ectotherms. Functional Ecology 27: 1415–1423.
- Kozlov, M. V., E. J. van Nieukerken, V. Zverev, and E. L. Zvereva. 2013. Abundance and diversity of birch-feeding leafminers along latitudinal gradients in northern Europe. Ecography 36: 1138–1149.
- Labandeira, C. C., and E. D. Currano. 2013. The fossil record of plant-insect dynamics. Annual Review of Earth and Planetary Sciences 41: 287–311.
- Lavoie, C. 2013. Biological collections in an ever changing world: Herbaria as tools for biogeographical and environmental studies. Perspectives in Plant Ecology Evolution and Systematics 15: 68–76.
- Lavoie, C., and D. Lachance. 2006. A new herbarium-based method for reconstructing the phenology of plant species across large areas. American Journal of Botany 93: 512–516.
- Lavoie, C., Y. Jodoin, and A. G. de Merlis. 2007. How did common ragweed (Ambrosia artemisiifolia L.) spread in Quebec? A historical analysis using herbarium records. Journal of Biogeography 34: 1751–1761.
- Law, W., and J. Salick. 2005. Human-induced dwarfing of Himalayan snow lotus, Saussurea laniceps (Asteraceae). Proceedings of the National Academy of Sciences USA 102: 10218–10220.
- Lees, D. C., H. W. Lack, R. Rougerie, A. Hernandez-Lopez, T. Raus, N. D. Avtzis, S. Augustin, and C. Lopez-Vaamonde. 2011. Tracking origins of invasive herbivores through herbaria and archival DNA: The case of the horse-chestnut leaf miner. Frontiers in Ecology and the Environment 9: 322–328.
- Leger, E. A. 2013. Annual plants change in size over a century of observations. Global Change Biology 19: 2229–2239.
- Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans, M. Clout, and F. A. Bazzaz. 2000. Biotic invasions: Causes, epidemiology, global consequences, and control. Ecological Applications 10: 689–710.
- Malmstrom, C. M., R. Shu, E. W. Linton, L. A. Newton, and M. A. Cook. 2007. Barley yellow dwarf viruses (BYDVs) preserved in herbarium specimens illuminate historical disease ecology of invasive and native grasses. Journal of Ecology 95: 1153–1166.
- Matthews, E. R., and S. J. Mazer. 2016. Historical changes in flowering phenology are governed by temperature x precipitation interactions in a widespread perennial herb in western North America. New Phytologist 210: 157–167.
- McLauchlan, K. K., C. J. Ferguson, I. E. Wilson, T. W. Ocheltree, and J. M. Craine. 2010. Thirteen decades of foliar isotopes indicate declining nitrogen availability in central North American grasslands. New Phytologist 187: 1135–1145.
- Meyer, C., P. Weigelt, and H. Kreft. 2016. Multidimensional biases, gaps and uncertainties in global plant occurrence information. Ecology Letters 19: 992–1006.
- Millennium Ecosystem Assessment. 2005. Ecosystems and human well-being: synthesis. Island Press, Washington, D.C., USA.
- Miller-Rushing, A. J., R. B. Primack, D. Primack, and S. Mukunda. 2006. Photographs and herbarium specimens as tools to document phenological changes in response to global warming. American Journal of Botany 93: 1667–1674.
- Miller-Rushing, A. J., R. B. Primack, P. H. Templer, S. Rathbone, and S. Mukunda. 2009. Long-term relationships among atmospheric CO2, stomata, and intrinsic water use efficiency in individual trees. American Journal of Botany 96: 1779–1786.
- Miller-Struttmann, N. E., J. C. Geib, J. D. Franklin, P. G. Kevan, R. M. Holdo, D. Ebert-May, A. M. Lynn, J. A. Kettenbach, E. Hedrick, and C. Galen. 2015. Functional mismatch in a bumble bee pollination mutualism under climate change. Science 349: 1541–1544.
- Mitchell, C. E., and A. G. Power. 2003. Release of invasive plants from fungal and viral pathogens. Nature 421: 625–627.
- Moffett, R. 2014. A biographical dictionary of contributors to the natural history of the Free State and Lesotho. SUN MeDIA Bloemfontein, Bloemfontein, South Africa.
10.18820/9781920382353 Google Scholar
- Morrow, P. A., and L. R. Fox. 1989. Estimates of pre-settlement insect damage in Australian and North American forests. Ecology 70: 1055–1060.
- Neil, K. L., L. Landrum, and J. Wu. 2010. Effects of urbanization on flowering phenology in the metropolitan phoenix region of USA: Findings from herbarium records. Journal of Arid Environments 74: 440–444.
- Newbold, T. 2010. Applications and limitations of museum data for conservation and ecology, with particular attention to species distribution models. Progress in Physical Geography 34: 3–22.
- Norby, R. J., et al. 2016. Model–data synthesis for the next generation of forest free-air CO2 enrichment (FACE) experiments. New Phytologist 209: 17–28.
- Oerke, E.-C., and H.-W. Dehne. 2004. Safeguarding production—losses in major crops and the role of crop protection. Crop Protection 23: 275–285.
- Park, D. S., and C. C. Davis. 2017. Implications and alternatives of assigning climate data to geographical centroids. Journal of Biogeography 44: 2188–2198.
- Park, D. S., and D. Potter. 2013. A test of Darwin's naturalization hypothesis in the thistle tribe shows that close relatives make bad neighbors. Proceedings of the National Academy of Sciences USA 110: 17915–17920.
- Parolo, G., and G. Rossi. 2008. Upward migration of vascular plants following a climate warming trend in the Alps. Basic and Applied Ecology 9: 100–107.
- Pauw, A., and J. A. Hawkins. 2011. Reconstruction of historical pollination rates reveals linked declines of pollinators and plants. Oikos 120: 344–349.
- Pearse, W. D., D. W. Inouye, R. B. Primack, C. C. Davis, and T. J. Davies. 2017. A statistical estimator for determining the limits of contemporary and historic phenology. Nature Ecology and Evolution 1: 1876.
- Pelini, S. L., F. P. Bowles, A. M. Ellison, N. J. Gotelli, N. J. Sanders, and R. R. Dunn. 2011. Heating up the forest: open-top chamber warming manipulation of arthropod communities at Harvard and Duke Forests. Methods in Ecology and Evolution 2: 534–540.
- Plant, R. E. 2012. Spatial data analysis in ecology and agriculture using R. CRC Press, Boca Raton, Florida, USA.
10.1201/b11769 Google Scholar
- Post, E., C. Pedersen, C. C. Wilmers, and M. C. Forchhammer. 2008. Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores. Proceedings of the Royal Society B 275: 2005–2013.
- Primack, D., C. Imbres, R. B. Primack, A. J. Miller-Rushing, and P. Del Tredici. 2004. Herbarium specimens demonstrate earlier flowering times in response to warming in Boston. American Journal of Botany 91: 1260–1264.
- Pyke, G. H., and P. R. Ehrlich. 2010. Biological collections and ecological/environmental research: a review, some observations and a look to the future. Biological Reviews 85: 247–266.
- Reef, R., and C. E. Lovelock. 2014. Historical analysis of mangrove leaf traits throughout the 19th and 20th centuries reveals differential responses to increases in atmospheric CO2. Global Ecology and Biogeography 23: 1209–1214.
- Renberg, I., M. W. Persson, and O. Emteryd. 1994. Preindustrial atmospheric lead contamination detected in Swedish lake sediments. Nature 368: 323–326.
- Riera, R., C. Sangil, and M. Sanson. 2015. Long-term herbarium data reveal the decline of a temperate-water algae at its southern range. Estuarine Coastal and Shelf Science 165: 159–165.
- Robbirt, K. M., A. J. Davy, M. J. Hutchings, and D. L. Roberts. 2011. Validation of biological collections as a source of phenological data for use in climate change studies: a case study with the orchid Ophrys sphegodes. Journal of Ecology 99: 235–241.
- Romeiras, M. M., R. Figueira, M. C. Duarte, P. Beja, and I. Darbyshire. 2014. Documenting biogeographical patterns of African timber species using herbarium records: A conservation perspective based on native trees from Angola. PLoS ONE 9: e103403.
- Sakai, A. K., et al. 2001. The population biology of invasive species. Annual Review of Ecology and Systematics 32: 305–332.
10.1146/annurev.ecolsys.32.081501.114037 Google Scholar
- Saltonstall, K. 2002. Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proceedings of the National Academy of Sciences USA 99: 2445–2449.
- Särkinen, T., M. Staats, J. E. Richardson, R. S. Cowan, and F. T. Bakker. 2012. How to open the treasure chest? Optimising DNA extraction from herbarium specimens. PLoS ONE 7: e43808.
- Schaefer, H., O. J. Hardy, L. Silva, T. G. Barraclough, and V. Savolainen. 2011. Testing Darwin's naturalization hypothesis in the Azores. Ecology Letters 14: 389–396.
- Sigal, L. L., and T. H. Nash. 1983. Lichen communities on conifers in southern California Mountains: an ecological survey relative to oxidant air pollution. Ecology 64: 1343–1354.
- Southwood, T. R. E., and P. A. Henderson. 2009. Ecological methods. Methuen and Co. Limited, London, UK.
- Spellman, K. V., and C. P. H. Mulder. 2016. Validating herbarium-based phenology models using citizen-science data. BioScience 66: 897–906.
- Steffen, W., P. J. Crutzen, and J. R. McNeill. 2007. The Anthropocene: Are humans now overwhelming the great forces of nature. Ambio 36: 614–621.
- Stewart, G. R., M. P. M. Aidar, C. A. Joly, and S. Schmidt. 2002. Impact of point source pollution on nitrogen isotope signatures (delta N-15) of vegetation in SE Brazil. Oecologia 131: 468–472.
- Syfert, M. M., L. Serbina, D. Burckhardt, S. Knapp, and D. M. Percy. 2017. Emerging new crop pests: ecological modelling and analysis of the South American potato psyllid Russelliana solanicola (Hemiptera: Psylloidea) and its wild relatives. PLoS ONE 12: e0167764.
- Thessen, A. 2016. Adoption of machine learning techniques in ecology and earth science. One Ecosystem 1: e8621.
10.3897/oneeco.1.e8621 Google Scholar
- Thiers, B. (continuously updated). 2016. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden's Virtual Herbarium. http://sweetgum.nybg.org/science/ih/
- Turcotte, M. M., T. J. Davies, C. J. M. Thomsen, and M. T. J. Johnson. 2014. Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants. Proceedings of the Royal Society B 281: 20140555.
- Unger, J., D. Merhof, and S. Renner. 2016. Computer vision applied to herbarium specimens of German trees: testing the future utility of the millions of herbarium specimen images for automated identification. BMC Evolutionary Biology 16: 248.
- United Nations, Department of Economic and Social Affairs, Population Division. 2008. World Urbanization Prospects: The 2007 Revision. New York.
- Vandepitte, K., T. D. Meyer, K. Helsen, K. V. Acker, I. Roldan-Ruiz, J. Mergeay, and O. Honnay. 2014. Rapid genetic adaptation precedes the spread of an exotic plant species. Molecular Ecology 23: 2157–2164.
- Vellend, M., C. D. Brown, H. M. Kharouba, J. L. McCune, and I. H. Myers-Smith. 2013. Historical ecology: using unconventional data sources to test for effects of global environmental change. American Journal of Botany 100: 1294–1305.
- Wandeler, P., P. E. A. Hoeck, and L. F. Keller. 2007. Back to the future: museum specimens in population genetics. Trends in Ecology and Evolution 22: 634–642.
- Warren, M. S., et al. 2001. Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414: 65–69.
- Wearn, O. R., D. C. Reuman, and R. M. Ewers. 2012. Extinction debt and windows of conservation opportunity in the Brazilian Amazon. Science 337: 228–232.
- Weiss, D., W. Shotyk, J. D. Kramers, and M. Gloor. 1999. Sphagnum mosses as archives of recent and past atmospheric lead deposition in Switzerland. Atmospheric Environment 33: 3751–3763.
- Wernberg, T., B. D. Russell, M. S. Thomsen, C. F. D. Gurgel, C. J. A. Bradshaw, E. S. Poloczanska, and S. D. Connell. 2011. Seaweed communities in retreat from ocean warming. Current Biology 21: 1828–1832.
- Wilf, P., and C. C. Labandeira. 1999. Response of plant-insect associations to Paleocene-Eocene warming. Science 284: 2153–2156.
- Wilf, P., S. Zhang, S. Chikkerur, S. A. Little, S. L. Wing, and T. Serre. 2016. Computer vision cracks the leaf code. Proceedings of the National Academy of Sciences USA 113: 3305–3310.
- Williams, A. C., J. Goh, C. G. Willis, J. Goh, A. M. Ellison, J. H. Brusuelas, C. C. Davis, and E. Law. 2017. Deja Vu: characterizing work reliability using task consistency. Proceedings of the AAAI Conference on Human Computation (HCOMP 2017), Quebec City, Canada.
- Willis, C. G., B. Ruhfel, R. B. Primack, A. J. Miller-Rushing, and C. C. Davis. 2008. Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proceedings of the National Academy of Sciences USA 105: 17029–17033.
- Willis, C. G., et al. 2017a. Old plants, new tricks: phenological research using herbarium specimens. Trends in Ecology and Evolution 32: 531–546.
- Willis, C. G., et al. 2017b. CrowdCurio: an online crowdsourcing platform to facilitate climate change studies using herbarium specimens. New Phytologist 215: 479–488.
- Wolkovich, E. M., and E. E. Cleland. 2011. The phenology of plant invasions: a community ecology perspective. Frontiers in Ecology and the Environment 9: 287–294.
- Wolkovich, E. M., et al. 2012. Warming experiments underpredict plant phenological responses to climate change. Nature 485: 494–497.
- Woodward, F. I. 1987. Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327: 617–618.
- Wu, Z. T., P. Dijkstra, G. W. Koch, J. Penuelas, and B. A. Hungate. 2011. Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Global Change Biology 17: 927–942.
- Yaakub, S. M., L. J. McKenzie, P. L. A. Erftemeijer, T. Bouma, and P. A. Todd. 2014. Courage under fire: Seagrass persistence adjacent to a highly urbanised city-state. Marine Pollution Bulletin 83: 417–424.
- Youngsteadt, E., A. G. Dale, A. J. Terando, R. R. Dunn, and S. D. Frank. 2015. Do cities simulate climate change? A comparison of herbivore response to urban and global warming. Global Change Biology 21: 97–105.
- Zangerl, A. R., and M. R. Berenbaum. 2005. Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore. Proceedings of the National Academy of Sciences USA 102: 15529–15532.
- Zarnetske, P. L., D. K. Skelly, and M. C. Urban. 2012. Biotic multipliers of climate change. Science 336: 1516–1518.
- Ziska, L. H., J. S. Pettis, and J. Edwards. 2016. Rising atmospheric CO2 is reducing the protein concentration of a floral pollen source essential for North American bees. Proceedings of the Royal Society B 283: 20160414.