Economic use of plants is key to their naturalization success

The study investigates how human economic use of plants influences their success at naturalizing beyond native ranges. While alien plants establish self-sustaining populations via both unintentional and intentional introductions, a large share are cultivated deliberately for economic purposes (food, medicine, materials, ornamentals, etc.). Established drivers of naturalization include propagule pressure, residence time, and species traits; economically used plants likely experience high propagule pressure and frequent, widespread planting. However, contributions may vary by type and number of uses. The authors pose five key questions: (1) Are economic plants more likely to naturalize than non-economic plants, and do particular use categories associate more strongly with naturalization? (2) Are Northern Hemisphere continents overrepresented as donors of economic plants? (3) Are economic plants from Northern Hemisphere continents more likely to naturalize? (4) Do tropical regions and islands have larger proportions of economic plants in their naturalized floras? (5) Do phylogenetic biases in economically used plants underlie phylogenetic patterns in naturalization success?

Prior work indicates increasing numbers of naturalized alien organisms in the Anthropocene and identifies cultivation as a major introduction pathway in regional floras. Propagule pressure, residence time, and species traits are key determinants of invasion success. Northern Hemisphere continents, especially Europe, have been overrepresented as donors of naturalized plants; explanations include evolutionary history, adaptation to human disturbance, and colonial-era deliberate introductions of economically valuable taxa. Certain plant families (e.g., Poaceae, Pinaceae, Rosaceae) are overrepresented among naturalized species, potentially reflecting both shared traits and introduction biases. Tropical regions often have lower proportions of naturalized plants and islands higher, potentially due to resistance or introduction pressures. These studies suggest that economic use and introduction history may structure global naturalization patterns, yet the global contribution of economic uses and their phylogenetic and biogeographic patterns had not been comprehensively assessed.

Data sources and integration: The authors combined the World Economic Plants (WEP) database (accessed 7 Jan 2016) for economic use information and the Global Naturalized Alien Flora (GloNAF) database for naturalization records across 861 regions covering >80% of the ice-free terrestrial surface. Taxonomy was standardized to The Plant List (version 1.1, Sept 2013; accessed 1 Oct 2019) using the R package Taxonstand. Sample: Of 326,101 accepted seed plant taxa, 11,685 had economic uses (after excluding four non-use categories and ferns) and 12,013 were recorded as naturalized in at least one region. Native continents of origin (TDWG scheme; splitting Asia into temperate and tropical, and including Pacific Islands) were compiled for 11,485 of the economic taxa using GRIN-GLOBAL and, where needed, WCSP. Phylogeny: A global seed plant phylogeny was constructed based on Smith & Brown (2018), standardized to The Plant List. Missing taxa were added at the genus or family root where necessary (20.47% added to genus roots; 1.34% to family roots). A WEP-specific tree was pruned from this global phylogeny. Analytical framework: - Naturalization likelihood of economic vs non-economic plants: resampling tests drawing random sets equal to WEP size from the global flora (9,999 iterations); alternative binomial GLM and phylogenetic binomial GLM. - Per-use category effects: resampling within WEP comparing observed naturalized counts per category to random draws; analyses repeated on taxa with single use only; alternative binomial and phylogenetic GLMs. - Number of uses: naturalization incidence modeled with (phylogenetic) binomial GLM; for naturalized economic taxa, naturalization extent (number of GloNAF regions, log10-transformed) analyzed with Kendall–Theil Sen Siegel regression and phylogenetic linear model. - Combinations of two uses: (phylogenetic) binomial GLM including main effects and all two-way interactions among uses for taxa with 0, 1, or 2 uses. - Geographic biases: resampling tests to evaluate over/under-representation of native continents among economic plants, accounting for taxa with single native continent; inter- and intra-continental flows of naturalized economic plants evaluated against expectations from random draws within WEP (9,999 iterations). Native flora sizes per continent were extrapolated from WCSP species to the total global taxa. - Regional composition: binomial GLM relating proportion of economic plants in each region’s naturalized flora to absolute latitude and island vs mainland (with quasi-binomial to account for overdispersion). - Phylogenetic structure: Faith’s phylogenetic diversity (PD) of economic and naturalized taxa compared to random expectations (9,999 draws) to compute SES; repeated while constraining the economic-use proportion among naturalized draws to test whether economic-use clustering explains naturalization clustering. Significance: Unless noted, two-sided tests were used; multiple-comparisons corrections were not applied.

- Overall naturalization: 12,013 of 326,101 seed plant taxa (3.7%) are naturalized globally. Of 11,685 economic taxa, 4,792 are naturalized (41.0%), making economic plants far more likely to naturalize than non-economic plants (approximately 18-fold increase). Venn counts indicate 7,221 naturalized taxa have no recorded economic use and 6,893 economic taxa have not naturalized. - Use categories: All 12 use categories have higher proportions of naturalized taxa than the global flora baseline; however, relative to WEP overall, materials do not differ, and gene sources have significantly fewer naturalized taxa. Highest proportions occur for bee plants and non-vertebrate poisons (>70%). In the single-use subset, animal food (fodder/forage) and environmental uses (ornamentals, erosion control, soil improvement, agroforestry) have the highest naturalization proportions; materials, gene sources, fuels, social, invertebrate food, and non-vertebrate poisons show lower prevalence when only single-use taxa are considered. Phylogenetic GLMs corroborate that animal food and environmental uses confer the highest naturalization probabilities. - Number of uses: Naturalization likelihood increases with the number of economic uses (GLM: z=29.34, p<0.001; phylogenetic GLM: z=32.09, p<0.001; n=11,685). Among naturalized economic taxa, naturalization extent (number of GloNAF regions) increases with number of uses (nonparametric regression V=7,937,443, p<0.001; phylogenetic LM: F≈122.09, p<0.001; n=4,792). Combinations of uses show diminishing returns (negative interaction terms) with especially high probabilities when an environmental use is involved, and lower when paired with materials. - Geographic patterns: Northern temperate regions contribute disproportionately to the pool of economic plants. Considering only taxa with a single native continent, temperate Asia, Europe, and North America are overrepresented donors of economic plants. As donors of naturalized economic taxa, temperate Asia is overrepresented to almost all continents; tropical Asia is also often overrepresented (underrepresented in Europe; not overrepresented in Australasia and North America). Africa and Europe show larger-than-expected intracontinental flows; other continents are mostly underrepresented. - Regional floras: Although 39.9% of global naturalized taxa have an economic use, 848/861 regions have a higher proportion in their naturalized floras (median 70.2%), indicating that economic plants are shared widely among regions. The proportion of economic plants in regional naturalized floras increases toward the equator (binomial GLM: t=-12.88, p<0.001); island vs mainland differences are not significant. - Phylogenetic structure: Economic plants are phylogenetically clustered (SES=-37.07, p<0.001); naturalized taxa are also clustered (SES=-33.49, p<0.001). After constraining randomizations to match the observed proportion of economic plants, clustering among naturalized taxa remains but is reduced (SES=-25.72, p<0.001), indicating that phylogenetic biases in economic use partly underlie naturalization clustering.

The findings demonstrate that intentional cultivation for economic purposes is a dominant driver of plant naturalization worldwide. Economic plants are disproportionately likely to establish outside their native ranges, particularly those cultivated as animal fodder/forage or for environmental uses (notably ornamentals, but also erosion control, soil improvement, and agroforestry). Increased numbers of uses likely reflect higher planting frequency and propagule pressure, enhancing both the likelihood and geographic extent of naturalization. Combinations involving environmental uses further elevate naturalization probability, whereas materials-related uses often associate with lower probabilities, consistent with more limited cultivation intensity. Biogeographically, Northern Hemisphere floras contribute disproportionately to the global pool of economic plants. However, when focusing on donors of naturalized economic taxa, temperate and tropical Asia are most overrepresented, suggesting intrinsic naturalization potential for many Asian taxa. The high proportion of economic plants in regional naturalized floras, especially in the tropics, implies that directed, repeated introductions have homogenized floras across regions; island regions do not show higher proportions of economic plants than mainlands, suggesting substantial unintentional introductions to islands as well. Phylogenetically, clustering among naturalized taxa is partly explained by the clustered selection of plants for economic uses. Nevertheless, even after accounting for economic-use clustering, significant phylogenetic structure remains, implying that both introduction biases and intrinsic lineage-level traits shape global naturalization patterns.

Economic use is a key predictor of global plant naturalization. Plants cultivated for animal food and environmental purposes, and those with multiple uses, are most likely to naturalize and to do so across many regions. Northern temperate regions supply a disproportionate share of economic plants, but Asian taxa, especially from temperate Asia, contribute most strongly to the pool of naturalized economic plants globally, indicating elevated innate naturalization potential. Phylogenetic analyses reveal that the clustering of naturalized taxa is partly due to biases in which lineages humans cultivate. Future directions include monitoring how shifts in cultivation (e.g., expansion of biofuel crops) and climate-driven changes in suitability and demand alter naturalization risks, disentangling mechanisms underlying higher innate naturalization potential in some donor regions (e.g., Asia), and integrating introduction effort, trait syndromes, and pathway management into risk assessments to mitigate future naturalizations.

- Economic-use data coverage: The WEP database, though extensive, is not fully comprehensive; many additional species are cultivated (e.g., ornamental garden species), potentially leading to underestimation of economic-use status for some taxa. - Native range data: Continental native ranges were incomplete for some taxa and supplemented from additional sources; WCSP coverage is partial and may be geographically biased, and native flora sizes per continent were extrapolated, introducing uncertainty. - Phylogeny construction: Many taxa missing from the backbone phylogeny were placed at genus or family roots, which may affect estimates of phylogenetic diversity and clustering. - Statistical considerations: Multiple comparisons were not corrected in some analyses; interaction estimates for rare use-category combinations (e.g., invertebrate food, non-vertebrate poisons) are uncertain due to small sample sizes. - Pathway intensity proxies: Number and type of uses serve as proxies for propagule pressure and cultivation extent; direct measures of planting frequency, quantities, and residence times were not available globally. - Scope: Analyses focus on naturalization occurrence and extent, not subsequent invasion impacts or spread dynamics within regions.