Introduction

Alien plant invasions cause great damage to the integrity and biodiversity of natural ecosystems and have become a major environmental problem1,2. Identifying the factors that contribute to the success of invasive plants is very important for predicting and controlling such potential species. Invasive species are often distributed sparsely in their native ranges, but frequently form dense mono-dominant stands in their invasive ranges3. This may be due to differences in species composition between the two ranges, since plant interactions are important drivers in structuring plant communities4,5,6,7. The magnitude of plant interactions are related to the identity of neighbors8,9.

The coevolution histories of neighboring plants and the invasive plant are longer in native range than in invasive range. Neighboring plants from native range may be more adapted to competitive strategy of the invasive plant than those from invasive range3,10. Competitive ability may also be different between neighboring plants from native range and those from invasive range11. Moreover, different species composition induces different plant-soil fauna interactions12. All these factors might lead to different performances and distribution patterns for the invasive plant in native and invasive ranges.

Chromolaena odorata (L.) R. M. King and H. Robinson (Asteraceae) is a noxious invasive perennial herb/subshrub in much of the world’s tropical and subtropical regions. It is native to North, Central, and South America, and was introduced to other tropical regions in the mid-19th century. C. odorata distributes sparsely in its native range. However, in invasive range, it usually forms dense monoculture3, and causes severely economic and environmental problems in in invaded areas13. Different neighbor competitors indicate different competitive ability, interactions and adaptive ability with the invader, which might contribute to different distribution patterns of C. odorata between native and invasive ranges. To investigate this, we constructed a series of artificial garden communities, with C. odorata grown in conjunction with three dominant native species from its native range in Mexico or three dominant native species from its invasive range in China at two different levels of density. We hypothesized that the performance of C. odorata would be more suppressed when grown with high-density native plants from Mexico than when grown with them at lower density. We also hypothesized that this pattern would not be in evidence when C. odorata was grown with native species from China.

Results

When C. odorata grown together with native species, density and species had significant effects on aboveground biomass, while category had no but category × density interaction had significant effect on the aboveground biomass (Table 1). Chromolaena odorata produced lower biomass when grown with native species from Mexico than when grown with species from its invasive range in China (Fig. 1), while native species from Mexico produced more biomass than native species from China when grown with C. odorata (Fig. 1). For each category, aboveground biomass at low density was significantly higher than at high density.

Table 1 Differences in biomass and changes in biomass among categories when grown under low and high densities according to the results of linear mixed-effect models. Category, density and their interaction are treated as fixed factors, species nested within category is treated as a random factor.
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Figure 1
figure 1

Individual aboveground biomass of each species. Narrow bars indicate the mean value of individual aboveground biomass for each species when they grown together; four thicker bars in the center depict the mean value for four categories: C. odorara (co-grown with species from Mexico), native species from Mexico, C. odorara (co-grown with species from China), native species from China. *(P < 0.05) indicates there are significant differences between high and low densities for each category; different letters indicate significant differences among categories (P < 0.05). Data was log(x) transformed before the analysis. T. t, C. l, E. l, A. i, B. b and A. m. is the abbreviations of Tithonia tubiformis, Chrysanthemum Leucanthemum, Eupatorium ligustrinum, Abutilon indicum, Bidens biternata, Artemisia Myrianth respectively.

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Category and density had no significant effects on change in biomass, while the effect of their interaction and the effect of species were significant (Table 1). When C. odorata was grown with native species from Mexico, the decrease in its biomass was greater in high-density communities than in low-density communities (Fig. 2). However, this was not the case when C. odorata was grown with native species from China (Fig. 2). For native species from Mexico and China, there were no significant differences for change in biomass between high and low density communities (Fig. 2). The decrease of biomass of C. odorata was higher when it grown with native species from Mexico than when it grown with native species from China (Fig. 2).

Figure 2
figure 2

Change in biomass of Chromolaena odorata and co-grown plant species from its native range in Mexico and invasive range in China. *(P < 0.05) indicates there are significant differences between high and low densities for each category, different letters indicate significant differences among categories (P < 0.05). T. t, C. l, E. l, A. i, B. b and A. m. is the abbreviations of Tithonia tubiformis, Chrysanthemum Leucanthemum, Eupatorium ligustrinum, Abutilon indicum, Bidens biternata, Artemisia Myrianth respectively.

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Discussion

The biomass of C. odorata grown with native species from Mexico was affected to a greater extent at high density than at low density (Fig. 2). This pattern was not in evidence when it was grown with species from its invasive range in China (Fig. 2). This is consistent with our original hypothesis.

Evolutionary responses to plant-plant interactions play a large role in shaping plant communities14. The different coevolutionary histories of C. odorata and native species from Mexico and those from China might explain these findings. In Mexico, Tithonia tubiformis, Chrysanthemum leucanthemum, and Eupatorium ligustrinum have longer coevolution history with C. odorata, and have adapted its’ competitive strategies (growth rate, canopy shape, resource use, etc) accordingly. Further, as these three species are dominant species in Mexico, they may have evolved a stronger ability than C. odorata to cope with high-density conditions15,16,17. Therefore, when grown in high density with C. odorata, they may give a greater effect on C. odorata than in low density condition.

Meanwhile, C. odorata was introduced to China in 1930s, and the coevolution history between native species from China and C. odorata has occurred for a comparatively very short time. Though Abutilon indicum, Bidens biternate, and Artemisia myriantha are dominant species, C. odorata might not be sensitive to their competitive strategies. Furthermore, some invasive species have “novel weapons”, and native species from the invasive range are usually more vulnerable to these “weapons” owing to short coevolution history10,18,19. C. odorata produces odoratin (Eupatorium) (C19H20O6), a potential novel allelochemical3. In a previous study, we found that seedlings from China are more vulnerable to this allelochemical than seedlings from Mexico3. This might contribute to the successful invasion of C. odorata.

Previous studies also revealed invader-neighbor interactions differ between the native range and invasive range. In the native range, the impact of invasive Centaurea stoebe is mainly driven by competition for the same limiting resources between the invader and neighbors, whereas in the invasive range, other factors play an important role11,20. These factors include soil biota, exploitation of resources that are not used by neighbors, and special traits of the invasive species that directly interfere with competitors11,20. Different invader-neighbor interactions could also explain the inconsistent patterns in this study. Native species from Mexico are more competitive than native species from China (Fig. 1). When they grow together with C. odorata, the competition will begin earlier at high density than at low density. This will increase the advantage of native species and the disadvantage of C. odorata, which leads to greater decrease of biomass for C. odorata at high density than at low density. However, when C. odorata competes with native species from China, in addition to direct growth competition, novel weapon3, soil biota21, and herbivores22 all influence the competition, which leads to the mixed results (Fig. 2).

In this study, all native species are common, dominant and have sympatric distirbution with C. odorata in each site, which made our results more plausible in understanding the mechanisms of invasion success of C. odorata. However, the results might also due to sampling effect (such as rapid growth rate, early establishment, etc) for only three species were used within each range. More species should be examined in future studies.

In conclusion, native-range species at high density negatively affected C. odorata to a greater extent than those at low density. This pattern was not observed when C. odorata was grown with species from its invasive range in China. Different species composition and geographical differences in coevolutionary histories between native-range plants and invasive-range plants might explain these results.

Methods

Seed collection

In 2012, we collected seeds of C. odorata and three native species from China (Abutilon indicum, Bidens biternata, and Artemisia myriantha) in Xishuangbanna and Puer (Table 2). Seeds of three native species from Mexico (Tithonia tubiformis, Chrysanthemum leucanthemum, and Eupatorium ligustrinum) were collected in 2011 in Morelos and Veracruz (Table 2). All these native species are common and dominant species in each site, and they can form dense stands in some patches. For each species, seeds were collected from more than 10 individuals growing at least 20 m apart, then mixed uniformly in paper bags. Seeds were germinated in a seedbed in April 2013 and transplanted to a common garden in June. In late 2013/early 2014, newly produced seeds of each species were collected from these next-generation plants in order to exclude maternal effect.

Table 2 Background information on seeds and collecting sites.
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Common garden experiments

Common gardens were constructed in Xishuangbanna Tropical Botanical Garden (21°6′N, 101°15′E, 560 m above sea level), Yunnan Province, southwest China. Here the mean annual temperature is 21.7 °C, the mean temperature in July (the hottest month) is 25.3 °C, and that in January (the coolest month) is 15.6 °C. The average annual precipitation is 1557 mm with a dry period lasting from November to April. The soil is latosol, and total nitrogen, phosphorus and potassium contents were 1.07 g/kg, 0.44 g/kg and 13.48 g/kg, respectively. Twenty-six 2 × 2 m artificial communities were constructed in early 2015 in each common garden, with each community 1 m apart from its neighbors. Three replicate common gardens were constructed. In March 2015, seeds of each species were sown separately into greenhouse seed beds. In the following June, similarly-sized seedlings were transplanted into artificial communities, consisting of monoculture of each species, either C. odorata + native range species or C. odorata + invasive range species, at either of two growing densities: high (36 individuals per plot) or low (8 individuals per plot) (Fig. 3). These densities were set according to our field observation. One of each type of artificial community was constructed in each of the three common gardens. At the first month, a few seedlings died and we substituted them with seedlings of similar size immediately.

Figure 3
figure 3

The design of planting combinations and growing densities.

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In December 2015, the aboveground parts of all plants were harvested, oven-dried at 80 °C for 72 h, and weighed. The magnitude of the neighbor effect was evaluated in terms of the change in biomass, which was calculated as follows:

$${\rm{Change}}\,{\rm{in}}\,{\rm{biomass}}=({{\rm{Biomass}}}_{{\rm{together}}}-{{\rm{Biomass}}}_{{\rm{monoculture}}})/({{\rm{Biomass}}}_{{\rm{monoculture}}}),$$

where Biomasstogether represents the mean value of individual aboveground biomass for each species when grown together with other species, and Biomassmonoculture represents the mean value of individual aboveground biomass for this species when grown in monoculture.

Statistical analysis

The following four categories were defined: C. odorata co-grown with species from Mexico, native species from Mexico, C. odorata co-grown with species from China, and native species from China. When C. odorata was grown together with other species, differences in aboveground biomass and change in biomass among categories were determined by a linear mixed-effects model. Category, density and their interaction were treated as fixed factors. Species nested within category was treated as a random factor. A tukey HSD test was used to compare the differences of neighbor effects between high- and low-density communities. Duncan test was used to compare the differences of biomass among categories. We make a log transformation for aboveground biomass to suitable for the equality of error variances. All analyses were conducted using SPSS 18.0.

Data availability

The data generated during this study are available from the corresponding atuthor on reasonable request.