Lords of the biosphere: Plant winners and losers in the Anthropocene

Societal Impact Statement The impact of humans on Earth's biodiversity varies across the Tree of Life. The extirpation and extinction of species is often determined by compatibility with human activities. Here we classify, where data are available, a significant portion (~30%) of vascular plant species as winners or losers with respect to this compatibility and show that currently losers greatly outnumber winners and that these losers will continue to exceed winners in the future even if species now deemed tentative winners succeed. In a rapidly changing world, species may tolerate shifting conditions, adapt, or migrate to new habitats. Species that benefit humankind may have an additional advantage of survival. Those that cannot tolerate, adapt, migrate, or prove useful will be the ultimate losers in the Anthropocene and may become extinct. Summary The impact of humans on the Earth continues to accelerate, affecting climate, land use, resource exploitation, species migrations, and habitat pollution. All of these changes have the potential to result in a massive extinction of populations and species of plants, fungi, and animals. However, the impact will vary across the diversity of life: some species, the “losers,” will decline and become extinct while others, the “winners,” will thrive as a result of human activities. We surveyed a variety of sources of information on economic uses, environmental tolerances, and conservation status and were able to classify 86,592 species of vascular plant into seven categories of winners and losers as follows: winners useful to humans and winners not useful to humans, losers useful to humans and losers not useful to humans, and currently neutral species. We also recognized tentative winners and potential losers, which we could not confidently categorize into the above five classes. We then mapped, both taxonomically and phylogenetically, the clear winners and losers across the major groups of vascular plants. The results suggest that currently many more species are losers than winners and that if the tentative winners and potential losers realize their projected trajectories, losers in the future will continue to greatly outnumber future winners. Furthermore, although winners and losers are today distributed across nearly all orders of vascular plants, all but two of the nine major phylogenetic lineages favor losers over winners. A significant phylogenetic signal was detected for percentages of both winners and losers and some of the smaller ancestral orders with a high percentage of losers may be at risk of extinction. In a rapidly changing world, plant species that tolerate human pressures, adapt, or shift distributions will continue to be the winners and survive the extinction bottleneck while the many more species that cannot do so will become the ultimate losers in the Anthropocene.