Abstract
Nitrogen (N) has been considered a crucial factor influencing plant invasions. Many studies have assessed responses of alien plants to different N availabilities. However, in natural soils, N comes in different inorganic and organic forms. Few studies have explored yet whether responses of alien species to different N forms are related to their naturalization success globally. We selected 22 common herbaceous species native to Germany that have all become naturalized elsewhere in the world, but vary in their naturalization extent. We grew the species under six N conditions that differed in the availability or form of N, and assessed their growth performance. We found that neither biomass production nor promiscuity to different N forms was related to naturalization success of the species. However, the biomass response to inorganic N, relative to organic N, was stronger for the widely naturalized species than for the less widely naturalized ones. Our comparative multi-species source-area study shows that although the widely naturalized species were not more promiscuous than the less widely naturalized species, they took more advantage of the inorganic-N forms. This indicates that naturalization success might be partly driven by a species’ ability to take advantage of increased inorganic N levels.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Over thirteen thousand alien plant species have already become naturalized (i.e. established self-sustaining populations outside cultivation) beyond their native ranges (van Kleunen et al. 2015). The number of these naturalized alien plant species continues to rise with no signs of saturation (Seebens et al. 2017), and is projected to increase by about 18% from 2005 to 2050 (Seebens et al. 2021). As naturalization is a major step in the plant invasion process, the increase in the number of naturalized species may also result in more species becoming invasive, and thus having severe environmental, economic and human health impacts (Vilà et al. 2011; Schaffner et al. 2020; Diagne et al. 2021). Concerns over the impacts of plant invasions have stimulated considerable interest in the mechanisms underlying plant invasions (van Kleunen et al. 2010; Funk 2013; Zhang et al. 2020a, b; Liu et al. 2021). However, despite considerable progress in our understanding of invasions, it is still unclear why some plant species, despite similar degrees of commonness in their native range, are more successful as aliens than others.
The fluctuating-resource hypothesis poses that an alien plant species could establish more easily in a community if the availability of a limiting resource (e.g. nitrogen) increases (Davis and Thompson 2000). Several studies found support for this hypothesis, and indicated that many successful alien species are opportunists that capitalize more strongly on additional resources than less successful species (Richards et al. 2006; Dawson et al. 2012b). For example, common alien species showed stronger biomass increases in response to nutrient addition than rare alien species (Dawson et al. 2012a). Similarly, Parepa et al. (2013) found that invasive Fallopia spp. became more dominant after an increase in nutrients. It was also shown that Central European plant species from more productive habitats are more likely to be invasive elsewhere in the world than species from less productive habitats (Dostál et al. 2013). However, although Liu and van Kleunen (2019) showed that Central European plant species that are widely naturalized elsewhere grow faster than the ones that are not widely naturalized, this was not related to differences in nitrogen-acquisition ability of the species. Therefore, more research is needed to explain how some species are able to take more advantage of additional nutrients than others, and how this relates to their naturalization success.
Nitrogen (N) is a macronutrient essential for plant growth, and has been considered a crucial factor driving the increase in local abundance of naturalized alien plants (Seabloom et al. 2015; Liu et al. 2017a, b). Generally, species with high local abundances have large populations, which can produce and disperse higher numbers of seeds in the landscape, resulting in more populations and a larger geographical range (Primack and Miao 1992; Schupp et al. 2010; Ramírez-Rodríguez and Amich 2017; Liu et al. 2018). Indeed, a comprehensive assessment of the different dimensions of invasion success for the European alien seed plant flora showed that the maximum local abundance of alien plant species in vegetation plots is positively correlated with their naturalization extent (number of regions where naturalized; Fristoe et al. 2021). Consequently, N use and response is also frequently considered to drive global naturalization success of alien species (Dostál et al. 2013; Liu and van Kleunen 2019).
Nitrogen comes in different forms. Beside the the two inorganic N forms (ammonium [NH4+] and nitrate [NO3−]), it also comes in multiple organic forms. Actually, more than 20 forms of free amino acids in the soil are N sources for plants (Persson and Näsholm 2001). For some amino acids (e.g. glycine and histidine), it has been shown that their contribution to the total N take up could range from 0.5% for crops to 82% for arctic/alpine plants (Kielland 1994; Xu et al. 2006, 2008). Due to atmospheric N deposition and fertilizer run-off from agricultural land, as well as by changes in microbial activity induced by climate change, both the availability of soil N and the the relative amounts of the different N forms are becoming highly heterogeneously distributed (Krupa 2003; Liu et al. 2016a, b; Homyak et al. 2021). It is frequently assumed that variation in preferences for various soil N forms could allow plant species to decrease their niche overlap, and to promote coexistence (McKane et al. 2002; Ashton et al. 2010). Following this logic, a species that can successfully invade, and thus coexist with the resident species, might be more promiscuous in the use of different nitrogen forms than less-successful alien species. In other words, those alien plants that can maintain a high performance under varying N-availability levels and take advantage of multiple N forms should be able to establish at more locations and thus have a larger non-native geographic range. This would also be in line with the long-standing idea that generalists, with a high environmental tolerance, have higher invasion potential than specialists (Baker 1965; Richards et al. 2006).
The preferences for various N forms are species-specific (Ashton et al. 2010; Boudsocq et al. 2012; Liu et al. 2017a, b; Liu et al. 2020). For example, the invasive species Mikania micrantha, Ipomoea cairica, Wedelia trilobata and Bidens pilosa performed better when supplied with NO3− than with NH4+ (Chen and Chen 2019). However, the invasive species Flaveria bidentis is able to use NO3− and NH4+, depending on which form is most available in the environment, and this promiscuity probably has contributed to its dominance in many communities (Huangfu et al. 2019). To test whether a preference for a certain N form or promiscuity generally contributes to naturalization success at the global scale, we need studies that compare successful with less successful alien plant species. However, there are many different factors that might determine the naturalization success of a species. Variation in naturalization success caused by these other factors can be reduced by comparing species that are native to the same region but differ in their invasion success elsewhere (i.e. the source-area approach) (Pyšek et al. 2004; van Kleunen et al. 2010; Liu and van Kleunen 2019). Furthermore, as species that are common in their native range might have a higher chance to be picked up and introduced elsewhere (e.g. van Kleunen et al. 2007; Pyšek et al. 2009), one can reduce this source of variation by selecting species that are equally common and occur in similar habitats in their native range.
To test whether preferences for certain N forms or promiscuity with regard to N forms could drive variation in naturalization success of alien species, we exposed 22 common Central European herbaceous grassland species that differ in their global naturalization success to six different N treatments. The six N treatments included one low and five high N-availability treatments: (1) low availability with equal amounts of nitrate-nitrogen (NO3−-N), ammonium nitrogen (NH4+-N), glycine (Gly-N) and histidine (His-N). (2) high availability with equal amounts of NO3−-N, NH4+-N, Gly-N and His-N, (3) high availability of NO3−-N only, (4) high availability of NH4+-N only, (5) high availability of Gly-N only, (6) high availability of His-N only. We compared how biomass and root allocation responses to the N treatments related to the global naturalization success of the species. Specifically, we tested the following questions: (i) Do widely naturalized species overall show a stronger response to increasing N availability than less widely naturalized species? (ii) Do the preferences for the different inorganic and organic N forms differ between widely and less widely naturalized species? (iii) Are widely naturalized species overall more promiscuous with regard to the different N forms than less widely naturalized species?
Materials and methods
Study species
To increase our ability to generalize the results on N-preference differences among species varying in their global naturalization success (van Kleunen et al. 2014), we selected 22 herbaceous plant species from eight families, and with different life spans (Table S1). All 22 species are common natives in Germany (occuring in at least 1928 of the 3000 German grid cells; Table S1), but have become naturalized to different extents in the rest of the world. All the naturalized species exhibit similar Ellenberg N‐indicator values (Fig. S1; Table S1), reflecting the N‐conditions in the natural habitats of the species in Europe (Ellenberg 1974). This measure is pertinent as species originating from N‐rich habitats are likely to have a higher naturalization success (Dostál et al. 2013). We determined the number of regions in which each species has become naturalized from the Global Naturalised Alien Flora (GloNAF) database, version 1.2 (van Kleunen et al. 2019), which includes data on naturalization success of 13,939 plant species across a total of 1029 regions. The number of GloNAF regions in which the selected species are recorded as naturalized ranged from 1 to 283 (Table S1), thereby including some of the globally most widely naturalized species (Pyšek et al. 2017). The number of naturalized regions of the 22 species is also strongly positively correlated with the number of countries where the species are considered invasive according to the Global Register of Introduced and Invasive Species (Pagad et al. 2022; r = 0.77, p < 0.001; Fig. S2). This implies that the more widely naturalized a species is, the higher its invasiveness worldwide. The seeds of all but two study species, which were collected from a field site in Konstanz, were bought from a commercial seed company (Rieger-Hofmann GmbH, Germany; Table S1). The company produces native seeds, representative of natural genotypes, for grassland-restoration and agricultural purposes (i.e. sowing of pastures and meadows).
Pre-cultivation and experimental set-up
To test whether the global naturalization success of the study species is related to their N-preferences, we did a greenhouse experiment in the botanical garden of the University of Konstanz (Germany). On 18 and 19 May 2020, seeds were sown into trays (12.0 cm × 12.0 cm × 4.5 cm) filled with potting soil (Topferde®, Einheitserde Co., Sinntal‐Altengronau, Germany; pH 5.8; 2.0 g/L KCl; 340 mg/L N; 380 mg/L P2O6; 420 mg/L K2O; 200 mg/L S; 700 mg/L Mg) for each of the 22 species separatately. We then placed the trays in a greenhouse at a temperature between 22 and 28 °C, and a day:night cycle of 16:8 h.
On 2 June 2020, two weeks after sowing, we selected 18 similarly sized seedlings per species, and transplanted each of them separately into circular 2-L plastic pots (i.e. one individual per pot) filled with a 1:1 nutrient-poor mixture of sand and fine vermiculite. In total, the experiment included 396 pots (i.e., 18 pots per species × 22 species), which were randomly assigned to positions on four greenhouse benches. To test whether responses to the amount of N and the different forms of N vary among the study species and relate to their naturalization success, we assigned the 18 pots of each species to six different N treatments. In other words, there were three replicate pots per species under each N treatment. As we were interested in promiscuity to different N forms between widely naturalized and less widely naturalized species, rather than in differences among the individual species, we had maximized the number of species over the number of replicate pots per species (van Kleunen et al. 2014). Although in nature, plants frequently grow in competition with other plants and have their roots intertwined, we chose to grow each plant individiually so that we were able to harvest all belowground parts and thus could determine total biomass production and root allocation responses to the varying N conditions.
The N treatments started two weeks after transplanting, and lasted for eight weeks. The six N treatments included one low N-availability treatment and five high N-availability treatments. Each week, we applied the six different N treatments using six modified Hoagland solutions that only differed from each other in the amount or form of N (for details, see Method S1). In other words, all nutrient solutions contained the same amounts of the other nutrients (e.g. P, K). Since the study species have become naturalized in diverse habitats across various regions of the world, it is unfeasible to manipulate all different N forms they encounter in naturalized soil. Therefore, we focused our study on two common inorganic N forms (ammonium [NO3−-N], stock-solution pH = 5.26; nitrate [NH4+-N], pH = 5.05) and two common organic forms (glycine [Gly-N], pH = 5.35; histidine [His-N], pH = 7.30). The low N availability treatment (further referred to as ‘low mixed N’) included a 1:1:1:1 mixture of NO3−-N, NH4+-N, Gly-N and His-N. For the five high N-availability treatments, the N forms differed: (i) a 1:1:1:1 mixture of NO3−-N, NH4+-N, Gly-N and His-N (further referred to as 'high mixed N'), (ii) only NO3−-N, (iii) only NH4+-N, (iv) only Gly-N, (v) only His-N. Because the charge of amino acids might determine their diffusion rates in soil (e.g. Homyak et al. 2021), we chose glycine, a neutrally charged amino acid, and histidine, a positively charged amino acid. We supplied 40 ml of each of the nutrient solutions to each pot once a week, so that 0.24 mmol and 2.4 mmol of N were provided each time for low mixed N and the five high N availability treatments, respectively. In other words, for the high nitrogen treatments, the nitrogen fertilizer applied during the experiment was equivalent to a total of 118.5 kg N per ha. This amount is slightly higher than the annual atmospheric N deposition in highly industrialized countries and comparable to the levels of agricultural fertilizer applications in many parts of the world (Galloway et al. 2008).
During the entire experiment, we kept all pots at temperatures between 22 and 28 °C, and provided supplemental lighting to extend the daily light period to 14 h. We watered each pot when the soil looked dry, and supplied the same amounts of water to all plants each time. To avoid that the nutrients leaked from the pots after watering or nutrient supply, we put a plastic dish under each pot.
Measurements
To be able to account for variation in initial sizes of the plants in the analyses, we counted, at the start of the experiment, the number of true leaves, and measured the length and width of the longest leaf on each plant. Based on these measurements, we calculated a proxy of initial leaf area as the length × width of the largest leaf × the number of true leaves. On 5 August 2020 (i.e. 8 weeks after the start of the N treatments), we assessed survival of the plants, and then started to harvest the ones that had survived. As 35 plants died during the experiment (Table S1), we finally harvested a total of 361 pots instead of 396 pots. We first harvested the aboveground biomass of each plant, and then washed their roots clean of substrate. The entire belowground biomass harvest took three days, from 6 to 8 August 2020. All aboveground and belowground biomass was dried at 70 °C for 72 h and then weighed. Based on the final aboveground and belowground biomass, we calculated the total biomass and root weight ratio (belowground biomass/total biomass) for each plant.
Statistical analyses
To test how survival related to naturalization success (i.e., the number of regions in which the species naturalized) and the different N treatments, we fitted a binomial generalized linear mixed-effects model using the glmer function in the package "lme4" (Bates et al. 2015) in R 4.0.3 (R Core Team 2020). Similarly, to test how total biomass and root weight ratio were related to naturalization success and the different N treatments, we fitted linear mixed-effects models using the lme function in the package “nlme” (Pinheiro 2011).
Survival, total biomass and root mass fraction of plants were the response variables in the models. To meet the normality assumption, total biomass was cubic-transformed. We included naturalization success (i.e. the number of naturalized regions per species), the different N treatments (i.e. low mixed N, high mixed N, high NO3−-N, high NH4+-N, high Gly-N and high His-N) and their interactions as fixed effects in the models. To test more specifically which of the N treatments differed from each other, we created a priori five orthogonal contrasts by coding dummy variables (Schielzeth 2010, Table S2): the mean of low mixed N vs. the mean of all high N treatments (Nlow-high), the mean of high mixed N vs. the mean of the non-mixed high N treatments (Nmix-nonmix), the mean of the two high inorganic N treatments vs. the mean of the two high organic N treatments (Ninorganic-organic), the mean of high NO3−-N vs. the mean of high NH4+-N (NNO3-NH4), the mean of high Gly-N vs. the mean high His-N (Ngly-his). Because variation in initial plant size might contribute to differences in final plant performance, we also added initial leaf area as a scaled natural‐log‐transformed covariate in the models. To account for phylogenetic non-independence of species and for non-independence of replicates of the same species, we included species nested within family as random factors in all models.
As the homoscedasticity assumption of linear mixed models was violated, we included variance structures in the models to allow different variances per species using the function "varIdent" in the R package nlme (Pinheiro 2011). As species with different naturalization success might vary in their responses to the N treatments, we also ran models with random slopes for family and species with respect to N treatment. However, because this led to a singular fit for the survival model, and increased the AIC-values (i.e. decreased model fit) for the total biomass model and the RWR model, we did not include the random slopes in the final models. In all models, we considered an estimated parameter as significant when its 95% confidence interval did not overlap zero. In addition, we also extracted the χ2 and p values of each parameter using the Anova function with type-III errors from the R package car (Fox and Weisberg 2018).
To assess whether promiscuity to the different N forms was related to naturalization success of the species, we needed an index indicating whether the biomass responses of a species to the different N forms was relatively constant (indicating promiscuity) or very variable. We therefore first calculated for each species in each of the five high N treatments the response ratio of the average biomass in the respective high N treatment vs. the average biomass of the species in the low N treatment. Then as measure of how variable this response was, we calculated the standard deviation (SD) across the five response ratios of each species. As the SD of the response ratios only considers the variation in the response ratios and not the magnitude, we additionally calculated the coefficient of variation (CV) as the SD of the response ratio divided by the mean value of the response ratio. A low CV value would indicate promiscuity as low values arise due to low variation (small SD) and/or a high mean of the response ratio (i.e. a strong response to N availability). Finally, to test whether the SDs and C vs. of the response ratios were related to naturalization success of the species, we calculated Pearson’s correlation coefficients. As the choice of p-value cutoffs for significance testing is arbitrary, we followed the suggestion of Muff et al. (2022) to translate the p-values into the language of evidence.
Results
Of the initial 396 plants, 35 (8.8%) had died by the end of the experiment. Survival was not related to naturalization success of the species (Table S3). However, we found moderate evidence that survival was lower in the high N treatments than in the low N treatment, and was lowest when plants received N in organic form as glycine (Table S3, Fig. S3).
Among the surviving plants, and averaged across the six N treatments, there was no evidence that total biomass was related to naturalization success of the species (Table 1; Fig. S4A). Averaged across all species, plants produced more biomass (+ 159.7%) when grown under high N levels than under low N levels (Fig. 1A). The response patterns to nitrogen addition were similar for legume and non-legume species (Fig. S5). The increase in biomass production in response to low vs. high N was similar for the widely and less widely naturalized species (Fig. 1A). In other words, the 95% CIs of the Nat × Nlow-high coefficient estimate overlapped with zero (Table 1). Among the high non-mixed N treatments, plants also produced more total biomass (+ 73.4%) when N was provided in inorganic form than when provided in organic form (Table 1; Fig. 1A, B). There was moderate evidence that the increase in biomass production in response to inorganic vs. organic N was larger for the widely naturalized species than for the less widely naturalized species (see the Nat × Ninorganic-organic interaction in Table 1; Fig. 1B). Furthermore, there was moderate evidence that widely naturalized species preferred high glycine conditions over high histidine conditions, and that the less widely naturalized species has no preference for any of the two organic N treatments (see the Nat × Ngly-his interaction in Table 1; Fig. 1C).
The root weight ratio of plants was also not related to naturalization success of the species (Fig. S4B), and was decreased (− 33.1%) when plants were grown at high N levels (Fig. 2A). Averaged across all species, there was no evidence that root weight ratio varied among the different high N treatments (Table 1; Fig. 2A, S3B). There was moderate evidence that while root weight ratio decreased with increasing naturalization success for the high N mixture treatment and the high glycine treatment, it increased for the other high N treatments (Table 1, Fig. 2B–E, Fig. S4B). Moreover, there was moderate evidence that the root weight ratio increased more strongly with increasing naturalization success for the inorganic than for the organic high N treatments.
The species’ standard deviation and coefficient of variation for the response ratios of biomass in the high N treatments vs. biomass in the low N treatment were not significantly related to the naturalization success of the species (SD: r = 0.219, n = 22, p = 0.328; CV: r = 0.139, n = 22, p = 0.526; Fig. 2). In other words, there was no evidence that promiscuity to the different N forms was related to naturalization success (Fig. 3).
Discussion
We tested whether preferences for and promiscuity with regard to different N forms of common Central European plant species were related to their naturalization success elsewhere. Not surprisingly, plants increased their performance when they had access to more N. However, we found that they benefited more from additional inorganic N than from organic N, and that high levels of glycine even increased mortality. The widely naturalized species did, averaged over the different N forms, not show a stronger response to increasing N availability than less widely naturalized species. Moreover, neither average biomass production nor promiscuity to different N forms was related to naturalization success of the species. However, the biomass response to inorganic N was, relative to the biomass response to organic N, and particularly to glycine, stronger for the widely naturalized species than for the less widely naturalized ones. These results indicate that naturalization success is not driven by N promiscuity, but might be partly driven by a species’ ability to take advantage of increased inorganic N.
Overall, plants increased their biomass production when growing under high N conditions relative to when grown under low N. This is not surprising because N availability is generally a limiting factor for plant growth (LeBauer and Treseder 2008). We also found that plants allocated less biomass to their root systems under high N conditions than under low N. This is in line with the predictions of resource-limitation theory, which states that plants should invest relatively more biomass into those structures that allow them to acquire more of the most limiting resource (Bloom et al. 1985; Poorter et al. 2012; Liu et al. 2016a, b; Liu and van Kleunen 2019). To assess whether the species can actually use each of the different N forms, we focused in this study on the single N forms and a mixture with equal ratios of the different N forms at both low and high levels. However, as in nature the different N-forms may occur at varying ratios, future studies should assess plant responses to a broader range of combinations and ratios of different N forms.
Numerous studies have shown that species that are more successful, either as natives or aliens, take more advantage of additional nutrients (Dawson et al. 2012b; Parepa et al. 2013; Liu and van Kleunen 2017). We found moderate evidence that widely naturalized species, relative to less widely naturalized species, decreased their biomass allocation to the root system more strongly in response to high N when compared to the low N-mixture treatment. However, this difference in root-allocation response among species varying in global naturalization success was apparently not large enough to result in a difference in overall biomass response to high N availability. The lack of a relationship between the naturalization success and the biomass response to high N availability could partly reflect that we only used species that are relatively successful in their native range and that some of them have not reached their full global naturalization potential yet. It could also be that the native genotypes that we used in our experiment are not representative for the genotypes that have become naturalized. Regardless of the exact reasons, futher studies should consider commonness in the native range and include a broader genotypic diversity of the study species. The lack of an association between global naturalization success and the response to high N availability, however, corroborates one of our previous studies, which showed that global naturalization success of Central European plants is not related to their N-acquisition ability (Liu and van Kleunen 2019). However, although we did not find a clear relationship between naturalization success and the overall response to an increased N availability, we found that biomass of the widely naturalized species increased more strongly in response to the inorganic N forms than was the case for the less widely naturalized species. So, the response to N addition might matter for naturalization success, but only if one considers inorganic N, which arguably are the most important N forms for plant growth.
While it was long thought that plants take up N exclusively in inorganic form, evidence is accumulating that many species are able to take up organic N forms (Kielland 1994; Persson and Näsholm 2001; Näsholm et al. 2009; Ashton et al. 2010; Boudsocq et al. 2012; Liu et al. 2017a, b; Homyak et al. 2021). Indeed, we found that most species increased their biomass when they were provided with the amino acids glycine or histidine instead of a low-N mixture. Nevertheless, plants benefited more from inorganic nitrogen (NO3−, NH4+) than from organic N. The latter is in line with previous studies, and might indicate that inorganic-N is the dominant N form in nature to which most species have adapted (Liu et al. 2017a, b).
Although most plant species produced more biomass in the high organic N treatments than on the low-N mixture, this does not necessarily mean that the plants took up the amino acids. Microbial turn-over of free amino acids is relatively rapid in natural soils. For example, it has been estimated that the half-lives of glycine and leucine in the field are normally less than 24 h (Henry and Jefferies 2003). Given the relative sterility of the sand:vermiculite mixture that we used in the present study, we expect that microbial conversion of organic to inorganic N was relatively limited. Still, we cannot fully exclude the possibility that some of the organic N in our treatments was mineralized by microbes, and that the plants took up the resulting inorganic N. However, if that would have been the case, we would expect that all species would have benefited from organic N addition and subsequent mineralization. Because there were also several species that produced less biomass in response to organic N additon (Fig. 1A and B), and because survival was lowest in the high glycine treatment (Fig. S3), it seems likely that the species that benefited took up the organic N forms directly.
Soil pH can also have a strong effect on plant growth. As the different N forms may inherently result in different soil pHs, the direct effects of the different N forms and the indirect effects through changes in soil pH cannot be separated in our study. So, it could be that the lower survival and biomass production of plants in the high glycine treatment than in the high histidine treatment, could be due to the lower pH values of glycine (stock-solution pH = 5.35) than histidine (pH = 7.30). However, this seems unlikely because the stock-solution pH of glycine was similar to the ones of nitrate (pH = 5.05) and ammonium (pH = 5.26), which were the most beneficial for plant performance. A case study on Ambrosia artemisiifolia indicated that plants grown in various natural soils with pH values between 5 and 7 had similar germination rates and growth performance (Gentili et al. 2018). Therefore, the different effects of glycine and histidine are unlikely caused by pH differences, although we cannot exclude that the differences in responses to glycine and histidine of the widely and less widely naturalized species (Fig. 1C) are caused by differences in pH sensitivities of the study species.
As mentioned above, the widely naturalized species benefited more from inorganic N, relative to organic N, than less widely naturalized species. In particular, the widely naturalized plants benefited less from the addition of glycine, relative to histidine. These biomass-response patterns are consistnet with root-weight-ratio responses to these different N treatments. This is not suprising because the more biomass is allocated to the root system, the more nutrients can be taken up and the more a plant can grow. Overall, these results suggest that there is a trade off between species’ responses to inorganic and organic N forms, and that those that benefit the most from inorganic N have the highest naturalization potential. Additionally, previous studies have shown that the different inorganic-N forms, NO3− and NH4+, could affect plant performance differently (Ashton et al. 2010; Huangfu et al. 2016; Chen and Chen 2019; Liu et al. 2020). We found that performance of our study species overall did not significantly differ between the NO3− and NH4+ treatments. Although plant responses to different N forms in nature may also depend on competition (Ashton et al. 2010), our findings highlight that changes in the NO3−/NH4+ ratio induced by atmospheric N deposition (Boxman et al. 2008) might not affect the absolute performance of the plants.
In all five high N treatments, plants invested on average less biomass in their roots than in the low N treatment. Averaged across species, root weight ratios did not differ among the different high N treatments. However, we found that in the high N mixture and high glycine treatments, the relative biomass investment into roots declined with the extent of naturalization of the species, while the reverse was true for the other N treatments. The reasons for these differences are unknown. However, the fact that the widely naturalized species produced low root weight ratios in the high glycine treatment might have contributed to their low biomass production in this treatment. On the other hand, the widely naturalized species invested more biomass in roots, and also produced more biomass than the less widely naturalized species in the high histidine treatment. This shows that plants do not benefit equally from all organic N forms, and this might be related to the charges of the amino acids and the differences in pH (Homyak et al. 2021). Although glycine is often considered to be a common amino acid in soils, the same can be true for histidine, as well as for amino acids that we did not included in our experiment (e.g. lysine, arginine and serine) (Lipson and Näsholm 2001; Tian et al. 2020). Future studies on N responses of plant species differing in their naturalization success should also consider these other amino acids as well as other organic N forms that could be taken up by some plants, such as urea and quaternary ammonium compounds (Warren 2013).
Conclusions
Our study is, to the best of our knowledge, the first multi-species experiment, using the source-area approach, that compared preferences for specific N forms and promiscuity to different N forms among species differing in their global naturalization success. While the widely naturalized alien species were not more promiscuous than the less widely naturalized species, they took more advantage of the inorganic-N forms, nitrate and ammonium. As these forms have globally increased due to atmospheric nitrogen deposition, our results suggest that one does not have to be a N generalist in order to become widely naturalized around the world. Instead, it helps to specialize in the most common forms of N available to plants.
Data availability
All data and code available from the Dryad Digital Repository https://datadryad.org/stash/share/CqgdA2tt1JNc4GrTbSnu11MG1d3iqdROMoBotBcHCUo.
References
Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–3260. https://doi.org/10.1890/09-1849.1
Baker HG (1965) Characteristics and modes of origin of weeds. Academic Press, New York, pp 147–172
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.48550/arXiv.1406.5823
Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants - an economic analogy. Annu Rev Ecol Syst 16:363–392. https://doi.org/10.1146/annurev.es.16.110185.002051
Boudsocq S, Niboyet A, Lata JC, Raynaud X, Loeuille N, Mathieu J, Blouin M, Abbadie L, Barot S (2012) Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? Am Nat 180:60–69. https://doi.org/10.1086/665997
Boxman AW, Peters RC, Roelofs JG (2008) Long term changes in atmospheric N and S throughfall deposition and effects on soil solution chemistry in a Scots pine forest in the Netherlands. Environ Pollut 156:1252–1259. https://doi.org/10.1016/j.envpol.2008.03.017
Chen WB, Chen BM (2019) Considering the preferences for nitrogen forms by invasive plants: a case study from a hydroponic culture experiment. Weed Res 59:49–57. https://doi.org/10.1111/wre.12344
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534. https://doi.org/10.1046/j.1365-2745.2000.00473.x
Dawson W, Fischer M, van Kleunen M (2012a) Common and rare plant species respond differently to fertilisation and competition, whether they are alien or native. Ecol Lett 15:873–880. https://doi.org/10.1111/j.1461-0248.2012.01811.x
Dawson W, Rohr RP, van Kleunen M, Fischer M (2012b) Alien plant species with a wider global distribution are better able to capitalize on increased resource availability. New Phytol 194:859–867. https://doi.org/10.1111/j.1469-8137.2012.04104.x
Diagne C, Leroy B, Vaissière AC, Gozlan RE, Roiz D, Jarić I, Salles JM, Bradshaw CJ, Courchamp F (2021) High and rising economic costs of biological invasions worldwide. Nature 592:571–576. https://doi.org/10.6084/m9.figshare.12668570.v1
Dostál P, Dawson W, van Kleunen M, Keser LH, Fischer M (2013) Central European plant species from more productive habitats are more invasive at a global scale. Global Ecol Biogeogr 22:64–72. https://doi.org/10.1111/j.1466-8238.2011.00754.x
Ellenberg H (1974) Zeigerwerte Der Gefäßpflanzen Mitteleuropas. Scripta Geobotanica 9(1):97
Fox J, Weisberg S (2018) An R companion to applied regression. SAGE Publications Inc, Cambridge
Fristoe TS, Chytrý M, Dawson W, Essl F, Heleno R, Kreft H, Maurel N, Pergl J, Pyšek P, Seebens H, Weigelt P, Vargas P, Yang Q, Attorre F, Bergmeier E, Bernhardt-Römermann M, Biurrun I, Boch S, Bonari G, Botta-Dukát Z, Bruun HH, Byun C, Čarni A, Carranza ML, Catford JA, Cerabolini BEL, Chacón-Madrigal E, Ciccarelli D, Ćušterevska R, de Ronde I, Dengler J, Golub V, Haveman R, Hough-Snee N, Jandt U, Jansen F, Kuzemko A, Küzmič F, Lenoir J, Macanović A, Marcenò C, Martin AR, Michaletz ST, Mori AS, Niinemets Ü, Peterka T, Pielech R, Rašomavičius V, Rūsiņa S, Dias AS, Šibíková M, Šilc U, Stanisci A, Jansen S, Svenning JC, Swacha G, van der Plas F, Vassilev K, van Kleunen M (2021) Dimensions of invasiveness: Links between local abundance, geographic range size, and habitat breadth in Europe’s alien and native floras. PNAS 118:e2021173118. https://doi.org/10.1073/pnas.20211731
Funk JL (2013) The physiology of invasive plants in low-resource environments. Conserv Physiol 1:cot026. https://doi.org/10.1093/conphys/cot026
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892
Gentili R, Ambrosini R, Montagnani C, Caronni S, Citterio S (2018) Effect of soil pH on the growth, reproductive investment and pollen allergenicity of Ambrosia artemisiifolia L. Front Plant Sci 9:1335. https://doi.org/10.3389/fpls.2018.01335
Henry HAL, Jefferies RL (2003) Plant amino acid uptake, soluble N turnover and microbial N capture in soils of a grazed Arctic salt marsh. J Ecol 91:627–636. https://doi.org/10.1046/j.1365-2745.2003.00791.x
Homyak PM, Slessarev EW, Hagerty S, Greene AC, Marchus K, Dowdy K, Iverson S, Schimel JP (2021) Amino acids dominate diffusive nitrogen fluxes across soil depths in acidic tussock tundra. New Phytol 231:2162–2173. https://doi.org/10.1111/nph.17315
Huangfu C, Li H, Chen X, Liu H, Wang H, Yang D (2016) Response of an invasive plant, Flaveria bidentis, to nitrogen addition: a test of form-preference uptake. Biol Invasions 18:3365–3380. https://doi.org/10.1007/s10530-016-1231-1
Huangfu C, Li K, Hui D (2019) Influences of plant interspecific competition and arbuscular mycorrhizal fungi on nitrogen form preference of an invasive plant. Biogeochemistry 145:295–313. https://doi.org/10.1007/s10533-019-00607-z
Kielland K (1994) Amino acid absorption by Arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383. https://doi.org/10.2307/1940891
Krupa SV (2003) Effects of atmospheric ammonia (NH3) on terrestrial vegetation: a review. Environ Pollut 124:179–221. https://doi.org/10.1016/S0269-7491(02)00434-7
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379. https://doi.org/10.1890/06-2057.1
Lipson D, Näsholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128:305–316. https://doi.org/10.1007/s004420100693
Liu Y, van Kleunen M (2017) Responses of common and rare aliens and natives to nutrient availability and fluctuations. J Ecol 105:1111–1122. https://doi.org/10.1111/1365-2745.12733
Liu Y, van Kleunen M (2019) Nitrogen acquisition of Central European herbaceous plants that differ in their global naturalization success. Funct Ecol 33:566–575. https://doi.org/10.1111/1365-2435.13288
Liu X, Xu W, Du E, Pan Y, Goulding K (2016a) Reduced nitrogen dominated nitrogen deposition in the United States, but its contribution to nitrogen deposition in China decreased. PNAS 113:E3590–E3591. https://doi.org/10.1073/pnas.1607507113
Liu Y, Dawson W, Prati D, Haeuser E, Feng Y, van Kleunen M (2016b) Does greater specific leaf area plasticity help plants to maintain a high performance when shaded? Ann Bot 118:1329–1336. https://doi.org/10.1093/aob/mcw180
Liu M, Li C, Xu X, Wanek W, Jiang N, Wang H, Yang X (2017a) Organic and inorganic nitrogen uptake by 21 dominant tree species in temperate and tropical forests. Tree Physiol 37:1515–1526. https://doi.org/10.1093/treephys/tpx046
Liu Y, Oduor AM, Zhang Z, Manea A, Tooth IM, Leishman MR, Xu X, van Kleunen M (2017b) Do invasive alien plants benefit more from global environmental change than native plants? Global Change Biol 23:3363–3370. https://doi.org/10.1111/gcb.13579
Liu Y, Zhang X, van Kleunen M (2018) Increases and fluctuations in nutrient availability do not promote dominance of alien plants in synthetic communities of common natives. Funct Ecol 32:2594–2604. https://doi.org/10.1111/1365-2435.13199
Liu Q, Wang H, Xu X (2020) Root nitrogen acquisition strategy of trees and understory species in a subtropical pine plantation in southern China. Eur J Forest Res 139:791–804. https://doi.org/10.1007/s10342-020-01284-6
Liu Y, Oduor AM, Dai Z, Gao F, Li J, Zhang X, Yu FH (2021) Suppression of a plant hormone gibberellin reduces growth of invasive plants more than native plants. Oikos 130:781–789. https://doi.org/10.1111/oik.07819
McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71. https://doi.org/10.1038/415068a
Muff S, Nilsen EB, O’Hara RB, Nater CR (2022) Rewriting results sections in the language of evidence. Trends Ecol Evol 37:203–210. https://doi.org/10.1016/j.tree.2021.10.009
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48. https://doi.org/10.1111/j.1469-8137.2008.02751.x
Pagad S, Bisset S, Genovesi P, Groom Q, Hirsch T, Jetz W, Ranipeta A, Schigel D, Sica YV, McGeoch MA (2022) Country compendium of the global register of introduced and invasive species. Sci Data 9:391. https://doi.org/10.1038/s41597-022-01514-z
Parepa M, Schaffner U, Bossdorf O (2013) Help from under ground: soil biota facilitate knotweed invasion. Ecosphere 4:1–11. https://doi.org/10.1890/ES13-00011.1
Persson J, Näsholm T (2001) Amino acid uptake: a widespread ability among boreal forest plants. Ecol Lett 4:434–438. https://doi.org/10.1046/j.1461-0248.2001.00260.x
Pinheiro J, Bates D, R Core Team (2011) nlme: linear and nonlinear mixed effects models. R package version 3.1–98. https://CRAN.R-project.org/package=nlme
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50. https://doi.org/10.1111/j.1469-8137.2011.03952.x
Primack RB, Miao SL (1992) Dispersal can limit local plant distribution. Conserv Biol 6:513–519. https://doi.org/10.1046/j.1523-1739.1992.06040513.x
Pyšek P, Richardson DM, Williamson M (2004) Predicting and explaining plant invasions through analysis of source area floras: some critical considerations. Divers Distrib 10:179–187. https://doi.org/10.1111/j.1366-9516.2004.00079.x
Pyšek P, Jarošík V, Pergl J, Randall R, Chytrý M, Kühn I, Tichý L, Danihelka J, Chrtek Jun J, Sádlo J (2009) The global invasion success of Central European plants is related to distribution characteristics in their native range and species traits. Divers Distrib 15:891–903. https://doi.org/10.1111/j.1472-4642.2009.00602.x
Pyšek P, Pergl J, Essl F, Lenzner B, Dawson W, Kreft H, Weigelt P, Winter M, Kartesz J, Nishino M, Antonova LA, Barcelona JF, Cabezas FJ, Cárdenas D, Cárdenas-Toro J, Castaño N, Chacón E, Chatelain C, Dullinger S, Ebel AL, Figureiredo E, Fuentes N, Genovesi P, Groom QJ, Henderson L, Inderjit Kupriyanov A, Masciadri S, Maurel N, Meerman J, Morozova O, Moser D, Nickrent D, Nowak PM, Pagad S, Patzelt A, Pelser PB, Seebens H, Shu W, Thomas J, Velayos M, Weber E, Wieringa J, Baptiste MP, van Kleunen M (2017) Naturalized alien flora of the world: species diversity, taxonomic and phylogenetic patterns, geographic distribution and global hotspots of plant invasion. Preslia 89:203–274. https://doi.org/10.23855/preslia.2017.203
R Core Team (2020) R: a language and environment for statistical computing. http://www.r-project.org/index.html
Ramírez-Rodríguez R, Amich F (2017) Effects of local abundance on pollination and reproduction in Delphinium fissum subsp sordidum (Ranunculaceae). Bot Lett 164:371–383. https://doi.org/10.1080/23818107.2017.1383307
Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993. https://doi.org/10.1111/j.1461-0248.2006.00950.x
Schaffner U, Steinbach S, Sun Y, Skjøth CA, de Weger LA, Lommen ST, Augustinus BA, Bonini M, Karrer G, Šikoparija B, Thibaudon M, Müller-Schärer H (2020) Biological weed control to relieve millions from Ambrosia allergies in Europe. Nat Commun 11:1745. https://doi.org/10.1038/s41467-020-15586-1
Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113. https://doi.org/10.1111/j.2041-210X.2010.00012.x
Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353. https://doi.org/10.1111/j.1469-8137.2010.03402.x
Seabloom EW, Borer ET, Buckley YM, Cleland EE, Davies KF, Firn J, Harpole WS, Hautier Y, Lind EM, MacDougall AS, Orrock JL, Prober SM, Adler PB, Anderson TM, Bakker JD, Biederman LA, Blumenthal DM, Brown CS, Brudvig LA, Cadotte M, Chu C, Cottingham KL, Crawley MJ, Damschen EI, Dantonio CM, DeCrappeo NM, Du G, Fay PA, Frater P, Gruner DS, Hagenah N, Hector A, Hillebrand H, Hofmockel KS, Humphries HC, Jin VL, Kay A, Kirkman KP, Klein JA, Knops JMH, La Pierre KJ, Ladwig L, Lambrinos JG, Li Q, Li W, Marushia R, McCulley RL, Melbourne BA, Mitchell CE, Moore JL, Morgan J, Mortensen B, O’Halloran LR, Pyke DA, Risch AC, Sankaran M, Schuetz M, Simonsen A, Smith MD, Stevens CJ, Sullivan L, Wolkovich E, Wragg PD, Wright J, Yang L (2015) Plant species’ origin predicts dominance and response to nutrient enrichment and herbivores in global grasslands. Nat Commun 6:7710. https://doi.org/10.1038/ncomms8710
Seebens H, Blackburn TM, Dyer EE, Genovesi P, Hulme PE, Jeschke JM, Pagad S, Pyšek P, Winter M, Arianoutsou M, Bacher S, Blasius B, Brundu G, Capinha C, Celesti-Grapow L, Dawson W, Dullinger S, Fuentes N, Jäger H, Kartesz J, Kenis M, Kreft H, Kühn I, Lenzner B, Liebhold A, Mosena A, Moser D, Nishino M, Pearman D, Pergl J, Rabitsch W, Rojas-Sandoval J, Roques A, Rorke S, Rossinelli S, Roy HE, Scalera R, Schindler S, Štajerová K, Tokarska-Guzik B, van Kleunen M, Walker K, Weigelt P, Yamanaka T, Essl F (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8(1):1–9. https://doi.org/10.1038/ncomms14435
Seebens H, Bacher S, Blackburn TM, Capinha C, Dawson W, Dullinger S, Genovesi P, Hulme PE, van Kleunen M, Kühn I (2021) Projecting the continental accumulation of alien species through to 2050. Global Change Biol 27:970–982. https://doi.org/10.1111/gcb.15333
Tian Y, Yu M, Xu F, Ouyang S, Xu X, Gao Q, Li X (2020) Uptake of amino acids and inorganic nitrogen by two dominant temperate grasses. Rhizosphere 14:100199. https://doi.org/10.1016/j.rhisph.2020.100199
van Kleunen M, Johnson SD, Fischer M (2007) Predicting naturalization of southern African Iridaceae in other regions. J Appl Ecol 44:594–603. https://doi.org/10.1111/j.1365-2664.2007.01304.x
van Kleunen M, Dawson W, Schlaepfer D, Jeschke JM, Fischer M (2010) Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol Lett 13:947–958. https://doi.org/10.1111/j.1461-0248.2010.01503.x
van Kleunen M, Dawson W, Bossdorf O, Fischer M (2014) The more the merrier: multi-species experiments in ecology. Basic Appl Ecol 15:1–9. https://doi.org/10.1016/j.baae.2013.10.006
van Kleunen M, Dawson W, Essl F, Pergl J, Winter M, Weber E, Kreft H, Weigelt P, Kartesz J, Nishino M, Antonova LA, Barcelona JF, Cabezas FJ, Cárdenas D, Cárdenas-Toro J, Castaño N, Chacón E, Chatelain C, Ebel AL, Figueiredo E, Fuentes N, Groom QJ, Henderson L, Inderjit KA, Masciadri S, Meerman J, Morozova O, Moser D, Nickrent DL, Patzelt A, Pelser PB, Baptiste MP, Poopath M, Schulze M, Seebens H, Shu WS, Thomas J, Velayos M, Wieringa JJ, Pyšek P (2015) Global exchange and accumulation of non-native plants. Nature 525:100–103. https://doi.org/10.1038/nature14910
van Kleunen M, Pyšek P, Dawson W, Kreft H, Pergl J, Weigelt P, Stein A, Dullinger S, König C, Lenzner B, Maurel N, Moser D, Seebens H, Kartesz J, Nishino M, Aleksanyan A, Ansong M, Antonova LA, Barcelona LA, Breckle SW, Brundu G, Cabezas FJ, Cárdenas D, Cárdenas-Toro J, Castaño N, Chacón E, Chatelain C, Conn B, de Sá Dechoum M, Dufour-Dror JM, Ebel AL, Figueiredo E, Fragman-Sapir O, Fuentes N, Groom QJ, Henderson L, Inderjit JN, Krestov P, Kupriyanov A, Masciadri S, Meerman J, Morozova J, Nickrent D, Nowak A, Patzelt A, Pelser PB, Shu WS, Thomas J, Uludag A, Velayos M, Verkhosina A, Villaseñor JL, Weber E, Wieringa JJ, Yazlık A, Zeddam A, Zykova E, Winter M (2019) The global naturalized alien Flora (GloNAF) database. Ecology 100: e02542. https://hdl.handle.net/20.500.12008/31840
Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708. https://doi.org/10.1111/j.1461-0248.2011.01628.x
Warren CR (2013) Quaternary ammonium compounds can be abundant in some soils and are taken up as intact molecules by plants. New Phytol 198:476–485. https://doi.org/10.1111/nph.12171
Xu X, Ouyang H, Kuzyakov Y, Richter A, Wanek W (2006) Significance of organic nitrogen acquisition for dominant plant species in an alpine meadow on the Tibet plateau, China. Plant Soil 285:221–231
Xu X, Stange CF, Richter A, Wanek W, Kuzyakov Y (2008) Light affects competition for inorganic and organic nitrogen between maize and rhizosphere microorganisms. Plant Soil 304:59–72
Zhang Z, Liu Y, Brunel C, van Kleunen M (2020) Evidence for Elton’s diversity-invasibility hypothesis from belowground. Ecology 101:e03187. https://doi.org/10.1002/ecy.3187
Zhang Z, Liu Y, Brunel C, van Kleunen M (2020) Soil-microorganism-mediated invasional meltdown in plants. Nat Ecol Evol 4:1612–1621. https://doi.org/10.1038/s41559-020-01311-0
Acknowledgements
We thank Otmar Ficht, Maximilian Fuchs, Duo Chen, Guanwen Wei and Beate Rüter for pracical assistance.
Funding
Open Access funding enabled and organized by Projekt DEAL. J.Z thanks the funding from China Scholarship Council (201908360251) and National Natural Science Foundation of China (31760123). Y.L acknowledges funding from Chinese Academy of Sciences (Y9B7041001).
Author information
Authors and Affiliations
Contributions
MK conceived the idea, MK, JZ and YL designed the experiment. JZ performed the experiment and collected the data. JZ, MK and YL analyzed the data and wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Zeng, J., Liu, Y. & van Kleunen, M. Widely naturalized species are not more promiscuous to different nitrogen forms, but benefit more from inorganic nitrogen. Biol Invasions 25, 3917–3930 (2023). https://doi.org/10.1007/s10530-023-03148-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-023-03148-7