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China has shown a rapid economic development in recent decades, and several drivers of this change are known to enhance biological invasions, a major cause of biodiversity loss. Here we review the current state of research on plant invasions in China by analyzing papers referenced in the ISI Web of Knowledge. Since 2001, the number of papers has increased exponentially, indicating that plant invasions in China are an emerging hot topic in invasion science. The analyzed papers cover a broad range of methodological approaches and research topics. While more that 250 invasive plant species with negative impacts have been reported from China, only a few species have been considered in more than a handful of papers (in order of decreasing number of references: Spartina alterniflora, Ageratina adenophora, Mikania micrantha, Alternanthera philoxeroides, Solidago canadensis, Eichhornia crassipes). Yet this selection might rather reflect the location of research teams than the most invasive plant species in China. Considering the previous achievements in China found in our analysis research in plant invasions could be expanded by (1) compiling comprehensive lists of non-native plant species at the provincial and national scales and to include species that are native to one part of China but non-native to others in these lists; (2) strengthening pathways studies (primary introduction to the country, secondary releases within the country) to enhance prevention and management; and (3) assessing impacts of invasive species at different spatial scales (habitats, regions) and in relation to conservation resources.
Alien invasive species, biodiversity conservation, control, flora, ecological impact, management
Biological invasions are a major driver of biodiversity loss worldwide (
China is a vast country with rich biodiversity and a long history of species introductions (
In the face of an accelerating pace of environmental change, the awareness of environmental problems associated with plant invasions has grown significantly in China during the last ten years (
The last decade yielded an increasing number of invasion studies in China.
Here we review recent studies and research trends related to plant invasions in China, based on an analysis of papers referenced in the ISI Web of Knowledge. In particular, we were interested in the prevailing types of research (experiments, field investigations, modeling studies, reviews, or integrative analyses), the most studied species and the research topics covered by recent studies. For the latter, we screened for papers that addressed either biological features of introduced species, mechanisms, or impacts associated with plant invasions or control options. By analyzing the research trends and gaps, we also aimed to sketch future perspectives of studies on plant invasions in China.
We screened the Web of Knowledge (ISI) for all papers published between 1945 and 2010 that are related to plant invasions in China. We used “all databases” including (1) Web of Science (1945–2010), (2) Current Contents Connect (1998–2010), (3) MEDLINE (1950–2010), and (4) Journal Citation Reports and analyzed all records published through the end of 2010. We found 643 papers when searching for the terms [plant* or weed*] and [invasion* or invasive* or introduced* or non-native* or neophyte*] and [China] in topic; 329 papers when searching for [invasive species] and [China]; and 143 papers when searching for [plant invasion in China]. Combining these approaches yielded matches of a total of 1, 115 papers. By reading the abstracts of these papers, 187 papers were identified as addressing plant invasions in China. In the discussion of the results we also refer to some recently published papers. We are aware of some caveats in this approach since books on plant invasions are generally not recorded in ISI nor are some papers in non ISI-listed journals (e.g.,
We classified the obtained selection of 187 relevant papers according to the publication year, research type, research topic, and studied species. We differentiated the following research types: experimental studies, field investigations, modeling studies, reviews, and integrative analyses (Table 1). Experimental studies included papers based on experiments, usually done in lab or greenhouse, or manipulative field experiments. Field investigations included studies mainly based on analyses in the field, e.g. of distribution patterns of a single species or changes in community composition due to the naturalization of introduced species. We considered studies to be integrative analyses if they were based on databases of large numbers of species at the regional or national scales (> 300 km2), usually aiming to reveal patterns in species traits or environmental factors related to plant invasions. In addition, we differentiated papers that provided reviews or used modeling approaches.
Classifications of 187 papers on plant invasions in China, published in the period 2001–2010 and referenced in the ISI Web of Knowledge, according to research types and research topics: A – biological features of non-native plants; B – impacts of plant invasions; C – control approaches; D – invasibility or environmental factors related to plant invasions; E – mechanisms of plant invasions; F – predictions of the distribution of non-native plants. Some papers have been attributed to more than one category.
Research types | Research topics | ||||||
---|---|---|---|---|---|---|---|
All | A Traits | B Impacts | C Control | D Invasibility | E Mechanisms | F Predictions | |
Field investigations | 91 | 35 | 33 | 14 | 8 | 6 | 1 |
Experimental studies | 48 | 20 | 12 | 10 | 3 | 6 | 0 |
Integrative analyses | 20 | 5 | 5 | 3 | 11 | 4 | 2 |
Reviews | 19 | 11 | 6 | 9 | 1 | 1 | 1 |
Modeling studies | 9 | 1 | 1 | 0 | 0 | 0 | 7 |
Total | 187 | 72 | 57 | 36 | 23 | 17 | 11 |
In a second step, we analyzed whether the papers addressed one or more of the following research topics: biological features of non-native plant species (e.g., morphological and physiological characters, clonal and propagation characteristics, genetic variation); mechanism of plant invasions (competition and other biotic interactions, human interference, enemy release, ecological, economic, or health impacts of plant invasions) and management approaches (mechanical, chemical, and biological methods). Some papers have been attributed to more than one category. For example, analyses of traits belong to the topic biological features, but when the paper demonstrated plant traits to facilitate invasions it had also been assigned to the research topic of mechanisms of invasions.
The research in ISI revealed an increasing number of studies on plant invasions in China in the last decade, with an exponentially growing number of papers since 2005 (Figure 1). The review by
Cumulative numbers of papers on plant invasions in China based on a screening of the Web of Knowledge (1945–2010), see methods for details.
Most (89%) of the analyzed 187 papers addressed one or several non-native species studied by either field investigations (49%), experimental approaches (26%), modelling approaches (5%), or reviewed the existing knowledge on the species (10%; Table 1). Few papers (11%) offered integrative analyses some of which provided several lists of invasive plants in China at the national scale (
The majority of the most-studied invasive plant species (Table 2) are herbaceous, and all are native to the Americas which generally comprise the most important donor regions for plants introduced to China (
Most-studied alien plant species in China and related research topics (number of studies referenced in the ISI Web of Knowledge, 2001–2010). The native range and life form of the species are also shown. PG – perennial grass; BS – broadleaf shrub; PV – perennial vine; H – perennial herb; APH – aquatic perennial herb. The codes for the research topics A–F are the same as in Table 1.
Species | Life. Form | Native range | All | A Traits | B Impacts | C Control | D Mechanisms | E Invasibility | F Predictions |
---|---|---|---|---|---|---|---|---|---|
Spartina alterniflora | PG | America | 47 | 9 | 30 | 8 | 3 | 3 | 1 |
Ageratina adenophora | BS | North America | 27 | 12 | 5 | 4 | 3 | 5 | 1 |
Mikania micrantha | PV | America | 19 | 8 | 4 | 7 | 1 | 0 | 0 |
Alternanthera philoxeroides | PH | South America | 12 | 9 | 0 | 4 | 4 | 1 | 0 |
Solidago canadensis | PH | North America | 10 | 4 | 2 | 1 | 2 | 1 | 2 |
Eichhornia crassipes | APH | South America | 7 | 3 | 0 | 4 | 0 | 0 | 0 |
Total | - | - | 122 | 45 | 41 | 28 | 13 | 10 | 4 |
The current focus on a rather small group of invasive plant species must not necessarily reflect the importance of a given non-native species in terms of ecological or economic impacts but might be considerably affected by the location and scientific background of research teams. Yet the much higher number of 265 invasive plant species (
Usually, papers on invasive plant species address species that are non-native to the total area of China. Species that are native to a region in China but non-native to one or more others are rarely studied. One example is Syzygium jambos (L.) Alston, which is native to some provinces of China but has been reported as an invasive plant species in Hong Kong (
In 72 papers, the biological features of plant species non-native to China were analyzed, mostly by field studies and experimental approaches (Table 1). More than 20 papers addressed physiology, genetics, or regeneration patterns of introduced species. Fewer papers are related to morphological features and seed ecology.
Some studies illustrated physiological characters of introduced species that contribute to their invasion success. For example,
Studies on the genetic variation or diversity of non-native plants revealed a very low genetic diversity in most clonal invasive plants such as Alternanthera philoxeroides and Eichhornia crassipes (Mart.) Solms (e.g.,
The exploration of larger databases revealed that nearly half of 126 invasive species are clonals, and these are more frequent than other non-native plant species (
Several studies analyzed the germination and seed banking of invasive species. Seed bank studies illustrated the role of sexual regeneration in the range expansion of clonal plants such as the highly invasive Ageratina adenophora and Spartina alterniflora (
There were 57 papers related to impacts of plant invasions in China (Table 1), affecting native plants, birds and other animals, soil biota, climate and economy. Several papers revealed negative effects of Spartina alterniflora on native plants, birds, and macrobenthic invertebrate communities (reviews by
Ageratina adenophora was found to inhibit native species by altering soil microbial communities (
Rather few papers addressed economically relevant invasion impacts. The review by
To our surprise no paper particularly addressed human health, although some books recorded the harmful impacts of invasive plants on human health, in particular of allergenic plants (Ageratina adenophora, Ambrosia species,
Most papers on control or management of plant invasions addressed biological control (Table 1). Several papers explored approaches of using the native parasite Cuscuta campestris Yunck. to restrain the non-native Mikania micrantha (e.g.,
While most studies on biological control focus on invasive plants as target species, some ecologists have begun to study the restoration of native plant communities after performing control. For example, field studies found that native Cuscuta campestris could not only restrain the non-native Mikania micrantha but might also contribute to the recovery of native communities by enhancing the availability of soil resources for native species (
Mechanical control approaches were studied in a few papers. The main target species were Spartina alterniflora (
Policies related to the management of invasive plants were covered by a small selection of papers, and most of them were reviews. As control approaches are usually costly, an economically beneficial use of the harvested biomass could increase the efficiency and sustainability of control measures.
A couple of papers considered mechanisms underlying plant invasions in China (Table 1). Many of these were studies addressing the competition between introduced and native plant species. For example, Spartina alterniflora was found to have a competitive advantage over native plant species (
Some studies tested the EICA hypothesis. For example,
Biotic interactions other than competition have been studied to a lesser extent in China. Some papers studied the role of soil biota (e.g.,
A few papers, mostly integrative data analyses, addressed ways of human interference to invasion processes. The fast growing economy of China has been often suggested to accelerate plant invasions through an enhanced international trade and associated species introductions (
The example of Parthenium hysterophorus illustrates with evidence from nuclear and chloroplast DNA that multiple introductions were responsible for subsequent invasions in China (
Some studies related environmental factors to plant invasions. The decreasing number of invasive plant species from the south to the north of China could be related to climatic factors (
Only a few papers modelled the potential distribution of non-native species (Table 1), based on current environmental factors and biological features of the species, while no paper addresses the potential abundance of non-native plants in China. For example, ecological niche modelling was used to predict the invasion potential of Ageratina adenophora on the basis of occurrence points within colonized areas (
The exponentially increasing number of papers on plant invasions in China in the last decade (Figure 1) suggests plant invasions in China to be an emerging hot topic in invasion science. The analyzed papers cover a broad range of methodological approaches and research topics and clearly enhanced the understanding of plant invasions in China, in particular by compiling species lists, analyzing taxonomic and geographical patterns, and studying species- and environment-related mechanisms that might shape plant invasions and their associated impacts. Although plant invasions have been acknowledged as an important environmental risk to China, only six invasive species have been studied in detail thus far (Table 2). This sharply contrasts to a much higher number of invasive species (
We argue for an additional reason for encouraging further studies on plant invasions in China. This country has undergone far-reaching socio-economic changes in a relatively short period of about 30 years, and several drivers of this change are well known to enhance biological invasions (
Although some lists of naturalized plants in China have recently been compiled (
There is growing evidence that the time since the first introduction of a species to new range matters in terms of habitat occupation, impacts and response to climate (
Human-mediated dispersal is a key process in plant invasions, and identifying and assessing the strength of dispersal vectors helps to set priorities in prevention and management (
The recent economic growth of China is associated with an increasing development of road systems, the linking of watersheds by canals, and a powerful growth of cities. The huge project of water transfer from the southern part of China to the northern part (namely the South-to-North Water Transfer Project of China), which will deliver about 45 billion m3 of water annually from the Yangtze River to the north of China (
Risk assessment and management of invasive plants are essential approaches to prevent potentially harmful new introductions or mitigate negative impacts of already introduced species. While classifications of species as “invasive, ” i.e., problematic, in other regions might be helpful in early warning systems (“invades elsewhere” criterion;
We thank Professor Shili Miao, Ingolf Kühn and two anonymous reviewers for comments on earlier versions of the paper and Kelaine Vargas for improving our English. Jian Liu was financially supported by the Key Science and Technology Project of Shandong Province (No. 2011GGH21605) and the China Scholarship Council for a research stay at Technische Universität Berlin.