Alien woody plant invasions in natural forests across China

Abstract

Aims

Alien plant invasion has become a major global environmental issue, causing severe economic and ecological damages. Severe invasions have been reported in some regions of China. However, most studies have been conducted at local and provincial levels, and the overall degree of invasion in natural forests across China remains unclear. Here, we explored the biogeographic patterns and their environmental and socioeconomic controls of the invaded alien woody plants in natural forests across the country.

Methods

We compiled the data of 3573 natural forest plots across the mainland China and mapped spatial distribution of alien woody plant invasion. We also used logistic regression models to identify the key socioeconomic and environmental factors that were associated with the observed invasion patterns.

Important Findings

We found that only 271 plots among 3573 natural forest plots were invaded by alien woody plants, accounting for 7.58% of all plots. Among all 2825 woody plant species across all plots surveyed, only 5 alien species (0.177%) were found. Both human activities and climate factors were related to the observed invasion patterns. Since China’s natural forests are mostly located in remote mountainous areas with limited human disturbance, alien woody plant invasions are less than those reported in North America and Europe. However, with the development of transportation and increased economic activities in mountainous areas, more invasions by alien plants may be expected in the future. Therefore, proactive management and policy making are desired to prevent or slow down the invasion processes.

摘要

外来木本植物在我国天然林中的入侵

外来植物入侵已经成为一个主要的全球性环境问题，造成了严重的经济和生态破坏。中国区域内部分地区已有关于严重入侵情况的报道，但是大多是小尺度上的研究，全国范围天然林中的外来植物入侵情况仍不清楚。本文基于全国天然林的3573个样方数据，绘制了外来木本植物入侵在我国各地天然林中的空间分布格局，探究了可能的环境和社会经济控制因素。研究结果显示，只有271个样方被外来木本植物入侵，占样方总数的7.58%；在所有调查的2825种木本植物中，只有5个外来物种(占比0.177%)。人类活动和气候因素都对入侵格局产生影响。由于我国天然林多位于偏远山区，人为干扰较轻，外来木本植物入侵的报道少于北美森林和欧洲林地。然而，随着交通运输的发展和山区经济活动的增加，在不久的将来可能会有更多。因此，需要积极的管理和政策制定来防止或减缓入侵进程，降低人类活动的干扰，监测外来物种的入侵情况并及时做出应对。

INTRODUCTION

With the development of international trade and traffic, plant invasion has become an important global ecological issue (Early et al. 2016; Turbelin et al. 2017), which could cause severe environmental damage and economic loss (Fei et al. 2014; Hulme et al. 2009). Forests are essential parts of terrestrial ecosystems, providing various ecosystem services. According to the 9th national forest inventory, forests coverage has increased substantially from about 1200 million ha in 1949 to approximately 2204 million ha in China (22.96% of the land surface). Invasions of alien plants have been reported in both local and provincial studies (Yan et al. 2014b, 2017). Region-wide studies also exist but mainly based on field data and anecdotal reports (Feng and Zhu 2010; Ma and Li 2018). However, a nationwide, field-based study is still lacking, but which is essential for obtaining a comprehensive assessment of the degree of alien woody plant invasion in natural forests across China.

In the US and European countries that have complete forest inventory systems, invasive plants in forests and their associated environmental drivers have been broadly reported. Researchers from the US Forest Service Forest Inventory and Analysis Program (FIA) mapped the number of invasive alien plants within the contiguous 48 states of the USA and found that there were more than 150 alien invasive plant species (Iannone et al. 2015; Oswalt et al. 2015). In addition, data from the Delivering Alien Invasive Species in Europe (DAISIE) project showed that there were over 600 alien plant species in European woodlands and forests (Lambdon et al. 2008). One important characteristic of heavily invaded habitats is intense human disturbance (Keller et al. 2011). In contrast, regions with relatively limited human activities showed lower degrees of invasion (Chytrý et al. 2009) and undisturbed forests tended to have better resistance to plant invasions (Martin et al. 2009).

Despite the fact that no province in China was spared from invasion by alien plants, the degree of invasion varies among regions (Zhou et al. 2020). In general, invasive species are believed to be most concentrated in the southwestern and eastern coastal regions with intense population and economic activities (Weber et al. 2008; Yan et al. 2014a). However, previous research was conducted at the provincial level and was based on data from the literature, specimen and/or local reports (Liu et al. 2005; Weber et al. 2008), while field-based studies were mainly carried out at local to landscape scales (Li et al. 2019; Xu et al. 2016). So far, no one has conducted a field-based inventory on plant invasion patterns across China.

Here, we compiled a species list based on field data collected from 3573 plots in natural forests across China. We then compared the species list against the list of China’s invasive alien species and mapped the invasion patterns of alien woody plants in natural forests across the country, and explored possible environmental and socioeconomic factors associated with the observed invasion patterns.

DATA AND METHODS

Field data

Data from 3573 natural forest plots were compiled to map the invasion distributions of alien woody plants (Fig. 1). Most of the plots sampled were in the natural forests with no significant human activities (e.g. thinning or harvesting) and natural disturbances (e.g. fire or storm). Notably, our sites do not include managed forests. Field surveys were carried out during the mid-1990s to 2018, strictly followed the protocol for the survey plan for plant species diversity of China’s mountains (Fang et al. 2004). We focused on these mountain sites because there were no invasion data reported from these sites. The size of forest plots is 600 m² (20 m × 30 m; 100, 400 or 1000 m² in few cases), no plot was resampled over this period. The database was comprised of the species composition and geographic information, such as latitude, longitude and elevation at each plot. These plots covered all biogeographical regions, climatic zones and vegetation zones in China (Fang et al. 2012), and thus they are representative of the vegetation composition in China’s natural forests. Given that not all plots were surveyed for nonwoody plant species, we only included the tree layer and shrub layer data in this study.

Invasive plant list

According to the checklist of China’s invasive alien species (Xu and Qiang 2018), an invasive alien species was defined as an alien species that has the ability to self-reproduce in the local natural or semi-natural ecosystem, and is or may be harmful to the ecological environment and human activities. Information such as species name, life form, habitat, morphological characteristics, time and place of introduction can be found from the checklist. The checklist of the alien flora of China contains a total of 347 species of invasive terrestrial plants that are known to exist in China, including 61 woody species. We compared our plot-based species list against the invasive species list to identify alien woody species on our plots.

Environmental and socioeconomic factors

To explore factors associated with invasion patterns, two environmental variables, annual mean precipitation (Precip) and annual mean temperature (Temp), and four socioeconomic factors, gross domestic product (GDP), population (POP), travel time to cities (TrvlTime) and distance to nearest roads (DistRoad), were compiled for each plot in our database. Precipitation and temperature data were downloaded from WorldClim (http://www.worldclim.org/) with the resolution of 1 km. GDP data were obtained from Gridded global datasets for the 2015 Gross Domestic Product and Human Development Index (Kummu et al. 2018), while 2015 population data were obtained from the 1 km population grid product published by the European Union (Schiavina et al. 2019). The global map of travel time to cities in 2015 (Weiss et al. 2018) was chosen as the data source to describe plot accessibility. We used the global roads data for 2010 (Center for International Earth Science Information Network - CIESIN - Columbia University, and Information Technology Outreach Services - ITOS - University of Georgia 2013) to calculate the distance to the nearest road of each plot.

Data analysis

We first extract climatic and socioeconomic data in the geographic information system ArcGIS 10.4 (ESRI, USA), and then conducted a principal component analysis (PCA) with varimax rotation to attain principal components of the six environmental and socioeconomic variables to reduce the influence of multicollinearity. Since the invasion status of plots is dichotomous (invaded or not invaded), we then conducted binary logistic regression, with the main components as independent variables and invasion status as the dependent variable. The invaded status was defined as ‘1’ and the noninvaded status as ‘0’. A positive logistic regression coefficient indicates a positive correlation with invasion, while a negative coefficient represents a negative correlation. In addition, the 28-year span of the data collection may cause some uncertainty to the invasion patterns. To see if there existed a significant time trend in the invasion ratio and eliminate the effect of sampling years, we illustrated the yearly proportion of invaded plots in the total number of plots surveyed that year. All analyses were carried out in SPSS 24.

RESULTS

Overall, the degree of invasion by alien woody plants was relatively low on the plots surveyed (Fig. 2). Among the 3573 plots surveyed, 271 plots (7.58%) were found to be invaded by at least 1 alien woody species, which mostly occurred in east China. A total of 2825 woody species were identified on these plots; while only 5 species were invasive woody plants: Robinia pseudoacacia, Amorpha fruticosa, Rhus typhina, Solanum pseudocapsicum and Leucaena leucocephala, which made up 0.18% of all woody plant species found across plots.

Among all the 271 invaded plots, 14 plots contained 2 invasive species while others contained only one. Robinia pseudoacacia was the most widely distributed species among the five invasive species, which was present in 84.13% of the invaded plots. The second most frequent invader was A. fruticosa, which was recorded in 18.82% of the invaded plots. Invasions caused by the L. leucocephala, S. pseudocapsicum or R. typhina were relatively rare, with one, one and four plots being invaded by these species, respectively (Table 1). According to Xu and Qiang (2018), all these alien woody plants were introduced intentionally into China within the last century, and then spread into local ecosystems (Supplementary Tables S1 and S2).

The three main components derived from PCA (Table 2) explained a total of 67.1% of the variation in the data. The first component (PC1) was most related to precipitation and temperature, representing climate factors; the second component (PC2) was primarily related to population density and the intensity of economic activities, which could be regarded as the representation of human activity intensity; and the third component (PC3) was related to accessibility, indicating propagule pressure. Component scores of all three main components were then used as independent variables in the logistic regression. Results indicated that climate factors (warmer and wetter climate), the intensity of human activity (higher population density and economic activities), propagule pressure (shorter travel time and distance to population centers) were positively correlated to the successful invasion of alien woody species (Table 3), respectively, with the β value of 0.222, 0.301 and −0.939. All coefficients were statistically significant at P < 0.001. In addition, as indicated in Supplementary Fig. S1, no significant time trend was found in the invasion ratio although our data collection spanned a period of 28 years. A maximum ratio of invaded plots was observed in 2014.

A t-test comparison of environmental and socioeconomic factors between the USA and China indicated that natural forests in China had fewer economic activities, lower population density and longer travel time to cities and longer distance to the nearest road than those in the USA (Table 4). In addition, temperature and precipitation in China’s natural forests appeared to be lower.

DISCUSSION

Invasion patterns and possible causes

Our study found that invasion by alien woody species in natural forests across China was relatively low and mainly concentrated in the eastern part of China. All invaded plots were distributed in the area south of the 400 mm isohyet, and nearly all within the eastern monsoon region. Having broadly distributed mountains and deserts, the climate of the nonmonsoon region is typically continental, with less than 400 mm annual precipitation (Yang et al. 2018). Low precipitation and low temperature in winter may jointly prevent the invasion of alien plants (Wu et al. 2006; Yan et al. 2014a).

Human activity is an important factor associated with the spread of invasive plants (van Kleunen et al. 2018; Liu et al. 2005). As an essential infrastructure in human activities, roads promote species invasion (Riitters et al. 2018). The nonmonsoon region is a geographical area in China i.e. less disturbed by human activities, with a poor transportation network that potentially served as obstacles to the invasion of alien plants. Meanwhile, in the east monsoon region, favorable climate condition, intense human activities and frequent population movement and trade may have reduced forests’ resistance to alien plant invasions.

Biotic factors also play an important in plant invasion. Invasion may depend on plant growth forms (Nunez-Mir et al. 2019), competition abilities (Golivets and Wallin 2018) and intrinsic growth rate (Zhang and van Kleunen 2019). According to the invasion list in China (Xu and Qiang 2018), these five invasive woody plant species showed strong adaptability to the local environments, among which S. pseudocapsicum has become a dominant tree species in northern China. The strong competitive ability of alien plants may give them an advantage in interspecific competition, and promote their invasion into native communities.

Comparison with other regions

Compared with forests in Europe and the USA, China’s natural forests had less severe invasions by alien woody plants. In a study in European native woodlands, 159 alien woody plant species were found in these woodlands (Wagner et al. 2017). Research focusing on region-specific patterns and drivers of macroscale invasions found 47 invasive woody plant species in the US forests (Iannone et al. 2015).

The relatively low disturbed natural forests of China may have resulted in stronger resistance to alien woody plants compared with those in the USA (Table 4). Additionally, China’s forests appeared to be colder and drier, which could serve as another barrier for the establishment and dispersal of alien plants (Pan et al. 2015; Zhou et al. 2020). For both human and climatic reasons, China’s natural forests represented relatively stronger resistance to alien woody plants. However, caution is needed as these studies are not really directly comparable. For example, the study done on the US forests by Iannone et al. (2015) includes all forested plots (natural, managed or plantation forest). It has been shown that invasion by alien species were less abundant in more remote regions than in highly disturbed landscapes (Ward et al. 2020).

This study provides an important basis for making policy decisions around alien invasive prevention and management in China, calling for more attention to the impact of human activities. However, future surveys can improve upon the extent of this quantitative analysis for increased conservation value. Compared with the sample density in Europe and USA, the sample density in this study is relatively lower and a greater number of plots may result in the identification of additional alien invasive species, especially in the more populated regions in the eastern and southeastern China. Moreover, some of data used here were obtained from field surveys conducted over 20 years ago. Results indicate that the relatively natural state may have prevented China’s natural forests from severe invasion over time, but recent data may bring more information. With the advance of additional future field surveys, more plots can be added for analysis in future research, and the database can be constantly updated. In the future, herbaceous layer data should also be included to map the spatial patterns of herbaceous invasive plants in China. Finally, our quantitative analysis of invasive plants in China should be expanded to even further reveal the factors associated with invasion for future policy making in areas undergoing rapid human growth.

CONCLUSIONS

According to the current data, jointly influenced by the climate and human activities, China’s natural forests have not suffered from severe invasion by alien woody plants, and invasion mainly occurred in easily accessible regions with relatively strong human interference. Differing from most province-level research based on literature, our field-based research is more detailed, but potentially suffered with low sampling density. Nevertheless, our invasion map of alien woody plants in natural forest plots across China gave detailed information on invaded regions and the most frequent species, offering a baseline for future studies. With the ongoing development of the economy and road infrastructures, the degree of invasion will unavoidably increase in the future. Therefore, proactive management practices and policies are desired to prevent or detect the invasion process.

Supplementary Material

Supplementary material is available at Journal of Plant Ecology online.

Table S1: List of invaded plots.

Table S2: List of invasive woody plant species.

Figure S1: Proportion of invaded plots by year.

Funding

This research was supported by the National Natural Science Foundation of China (31988102).

Acknowledgements

We thank Dr. Elizabeth LaRue from Purdue University for her valuable comments on the manuscript.

Conflict of interest statement. The authors declare that they have no conflict of interest.

REFERENCES