Economic use of plants is key to their naturalization success

The Anthropocene is characterized by a rapid increase in the number of naturalized alien species, many of which are introduced intentionally for economic purposes. Economic plants, defined as those with value to humans (e.g., food, medicine, ornamentals), have been cultivated outside their native ranges since the Late Pleistocene. However, their introduction drastically increased after the 15th century with European exploration. Royal houses and professional plant hunters actively sought economically valuable plants, and botanical gardens played a crucial role in acclimatizing them. While escape from cultivation is a known pathway for naturalization, the global contribution of economic taxa to this pattern remains unassessed. Key drivers of naturalization success include propagule pressure, residence time, and species-specific traits. Economic plants are expected to have higher propagule pressure due to active propagation and widespread planting. However, the type and number of uses influence cultivation intensity and species traits. For example, fodder plants are usually sown over large areas and possess traits often associated with invasive species. Previous regional studies have identified cultivation as a major pathway for naturalization, but global patterns remain unknown. Tropical regions, often showing lower naturalization rates, might depend more on high propagule pressure. Additionally, the Northern Hemisphere, particularly Europe, is overrepresented as a donor of naturalized plants; this might be partly due to the deliberate introduction of economic plants to colonies. This study uses the World Economic Plants (WEP) and Global Naturalized Alien Flora (GloNAF) databases to assess the role of economic use in global plant naturalization, addressing five key questions: (1) Naturalization percentage differences between economic and non-economic plants and variations among economic use categories; (2) Overrepresentation of Northern Hemisphere continents as donors of economic plants; (3) Naturalization likelihood of economic plants from the Northern Hemisphere; (4) Proportion of economic plants in tropical regions and islands; (5) Underlying phylogenetic biases in economic uses and naturalization success.

Existing research highlights several factors influencing plant naturalization success. Propagule pressure, the frequency and magnitude of introduction events, is a significant driver, with higher pressure leading to increased establishment probability. Residence time, the duration a species has been present in a non-native area, also plays a crucial role, allowing for adaptation and spread. Species traits, such as growth rate, reproductive capacity, and competitive ability, are further intrinsic factors influencing naturalization potential. Previous studies have established cultivation as a significant pathway for the introduction of alien plants, particularly in regional contexts. However, the extent to which this pattern applies globally remains unclear. Existing literature also points towards latitudinal patterns in naturalization, with temperate regions often exhibiting higher rates compared to the tropics. Furthermore, the role of phylogenetic bias in naturalization is acknowledged; certain plant families are frequently overrepresented in naturalized floras, suggesting that shared evolutionary history might confer a predisposition to successful invasion. The overrepresentation of Northern Hemisphere plants as successful invaders has been linked to both higher competitive ability and the legacy of past human disturbances. However, the contribution of deliberate introductions of economic plants to this pattern requires further investigation. This study builds upon previous work by conducting a comprehensive global-scale analysis, incorporating the most extensive datasets on both economic uses and naturalization success to fully understand the complex interplay of factors influencing plant naturalization.

This research combined data from the World Economic Plants (WEP) database and the Global Naturalized Alien Flora (GloNAF) database. The WEP database provides information on economic uses for over 15,000 vascular plant taxa, categorized into 12 economic use categories (excluding those not representing true economic uses, such as harmful organism hosts and weeds). Taxonomic names were harmonized using The Plant List to ensure consistency between datasets. The GloNAF database contains lists of naturalized vascular plant taxa for 861 regions globally, covering over 80% of the terrestrial ice-free surface. For each taxon in WEP, the continents of origin were identified using data from the National Plant Germplasm System GRIN-GLOBAL and supplemented with information from other sources such as the World Checklist of Selected Plant Families (WCSP). Phylogenetic trees were constructed using the seed plant phylogeny of Smith and Brown (2018) supplemented to incorporate taxa missing in the original phylogeny. The analyses used several statistical methods. Resampling tests were employed to compare the percentage of naturalized taxa between economic and non-economic plants, and to assess variations across economic use categories. Binomial generalized linear models (GLMs) and phylogenetic binomial GLMs were used to account for phylogenetic non-independence. The latter analysis used the phyloglm and phylolm functions from the "phylolm" R package. A binomial GLM and a phylogenetic GLM assessed the relationship between naturalization success and the number of economic uses, supplemented by a Kendall-Theil Sen Siegel nonparametric regression and a phylogenetic linear model. To investigate the effects of combinations of economic uses, a binomial GLM and a phylogenetic binomial GLM were used. Further resampling tests examined biases in the continents of origin of economic plants and the continents of origin of naturalized economic plants. A binomial GLM evaluated the relationship between the proportion of economic plants in regional naturalized floras and latitude. Finally, resampling tests were conducted to analyze phylogenetic structures in economic use and naturalization success. Faith's phylogenetic diversity was calculated and compared to randomly sampled distributions to identify significant phylogenetic clustering. The standardized effect size (SES) quantified the strength of phylogenetic structure. The analyses accounted for the phylogenetic structure of economic use in the analyses of phylogenetic structure in naturalization success to separate out the effects.

The study's key findings reveal a strong link between economic plant use and naturalization success. Of the 326,101 seed plant taxa, 11,685 have known economic uses, and 12,013 are naturalized. While only 3.7% of the global flora is naturalized, 41.0% of economic plants are, showing a significantly higher naturalization probability (p < 0.001). All 12 economic use categories exhibited higher naturalization percentages than the global average, with the highest percentages observed for bee plants and non-vertebrate poisons. However, considerable variation exists among categories. Resampling tests confirmed that the proportion of naturalized taxa was significantly higher than expected for most economic use categories, with animal food and environmental uses showing the strongest associations with naturalization success (p < 0.001). Considering only taxa with a single economic use, animal food and environmental plants continued to exhibit high naturalization rates (p<0.001). Both the probability of naturalization and the number of regions where a taxon is naturalized increased with the number of economic uses. The analysis of taxa with one or two economic uses indicated that the combination of uses influences naturalization success, with environmental uses positively impacting naturalization. Regarding geographic patterns, the Northern Hemisphere continents, especially temperate Asia, Europe, and North America, were overrepresented as sources of economic plants, and temperate Asia showed disproportionately high naturalization success. The percentage of economic plants in regional naturalized floras exceeded the global average (median 70.2%), increasing towards the equator. The analysis demonstrated significant phylogenetic clustering for both economic use and naturalization success. However, after accounting for phylogenetic clustering of economic plants, the naturalized taxa still showed significant phylogenetic clustering indicating that phylogenetic biases in economic use partly explain the patterns in naturalization success.

The findings strongly support the hypothesis that economic use is a major driver of plant naturalization. The significantly higher naturalization rate of economic plants compared to non-economic plants underscores the role of intentional human introduction. The variation among economic use categories highlights the importance of considering the specific ways plants are used. Plants used for animal feed and environmental purposes (particularly ornamentals) exhibited the highest naturalization rates, likely due to widespread and repeated cultivation resulting in high propagule pressure. The positive relationship between the number of economic uses and naturalization success further emphasizes the influence of cultivation intensity. The geographic patterns observed, with higher representation of Northern Hemisphere plants as economic plants and higher naturalization success in Asia, reflect historical trade and cultivation practices. However, the high naturalization success of Asian plants suggests an inherent potential for invasion. The increasing proportion of economic plants in regional naturalized floras toward the equator may be due to greater resistance to invasion in species-rich tropical regions that can be overcome by high propagule pressure. The phylogenetic clustering of both economic plants and naturalized plants underscores the influence of shared evolutionary traits; however, these results also indicate that the role of economic factors are paramount.

This study provides robust evidence for the significant role of economic use in driving plant naturalization patterns globally. The high naturalization rates of economically valuable plants, particularly those for animal food and environmental purposes, are primarily attributed to the large-scale and repeated cultivation practices. The study highlights the need to consider human economic activities when understanding naturalization processes, emphasizing that the unique relationship between plants and human use is a key factor driving global patterns of plant naturalization. Future research should investigate how changes in cultivation patterns, such as increasing biofuel crop production, may alter future naturalization trends and explore the complexities of plant invasion processes further. Further research could also focus on the specific traits that confer naturalization success across different categories of economic use.

While the study uses comprehensive databases, the WEP database does not claim to be entirely exhaustive, and some biases in recording economic uses may exist. The GloNAF database, while extensive, may not capture every instance of naturalization globally. Further, the study relies on existing databases; therefore, the accuracy of the data relies on the underlying data collection efforts. The analysis focuses on seed plants, excluding other plant groups. Therefore, the findings might not be generalizable to all plant taxa. The study does not incorporate environmental factors like climate, competition, and environmental impact independently. Therefore, the results solely focus on the influence of economic factors on naturalization without considering the influence of environmental factors.