Invasive alien species (IAS) are considered one of the key pressures on world’s biodiversity (Leprieur et al. 2008; Butchart et al. 2010; Rands et al. 2010), alter ecosystem services and processes (Hulme et al. 2009; Vilà et al. 2010, 2011), reduce native species abundance and richness (Cohen and Carlton 1998; Blackburn et al. 2004; Gaertner et al. 2009; Hejda et al. 2009), decrease genetic diversity of resident species (Ellstrand and Schierenbeck 2000; Daehler and Carino 2001), and cause substantial economic losses (Pimentel et al. 2005; Xu et al. 2006; Kettunen et al. 2009). Responding to this threat is therefore particularly urgent (Lambertini et al. 2011). In October 2010, world leaders adopted the Strategic Plan for Biodiversity (2011-2020) under the Convention on Biological Diversity (CBD), including the Aichi Target 9 (Secretariat of the Convention on Biological Diversity 2010) calling to identify IAS and pathways, control and eradicate priority species, and to manage pathways in order to prevent further invasions. In order to evaluate achievements of the Aichi Targets, baseline data are needed. However, a global baseline of IAS is unavailable (Butchart et al. 2010; McGeoch et al. 2010), and national/regional data sets suitable for analysis of temporal patterns of biological invasions are rare for developing countries of the world, resulting a pattern that reflects geographical biases in information on invasion patterns (Pyšek et al. 2008; Nuñez and Pauchard 2010).

China is the world’s most populous country with 1.34 billion people and one of the largest territories (Liu and Diamond 2005). China is also one of the mega-diversity countries, with half of its species found nowhere else (Liu et al. 2003; Xu et al. 2008). Its economy, ranked second, is growing at a very fast rate. The extraordinary biogeographic and economic characteristics of China make it ideal for understanding how biological invasions currently affect, and will affect in the future, the fastest growing economies in the world. Here, we present a comprehensive inventory of IAS in China, and analyze the temporal trends of biological invasions in the country in order to identify priority responses to the growing threat from biological invasions.

According to the CBD and IUCN definition, invasive alien species (IAS) are those alien species that became established in natural or semi-natural ecosystems or habitats, are an agent of change, and threaten native biological diversity (IUCN 2000; Shine et al. 2000; McNeely et al. 2001). Alien species refers to a species, subspecies or lower taxon occurring outside its natural, past or present range and dispersal potential (i.e. outside the range it occupies naturally or in a range it could not occupy without direct or indirect introduction by humans) and includes any part, gametes, or propagules (IUCN 2000). Only species with evidence of their impact on biodiversity, human activities or economy were considered in the present assessment. We included IAS that established populations in terrestrial habitats, inland waters or marine ecosystems of China.

We identified IAS and pathways of their introductions based on available literature (Ding and Wang 1998; Xie et al. 2000; Li and Xie 2002; Xiang et al. 2002; Xu and Qiang 2004; Liu et al. 2005; Wan et al. 2005, 2008, 2009; Weber et al. 2008; Xie 2008 ; Zhang et al. 2008; Wu et al. 2010; Huang et al. 2012), including Flora of China (126 volumes edited by the Editoral Committee of Flora Sinica, Chinese Academy of Sciences and published by Science Press in Beijing, China), and Fauna of China (100 volumes edited by the Editoral Committee of Fauna Sinica, Chinese Academy of Sciences, and published by Science Press in Beijing, China), and on field work carried out in most provinces of China. All recorded IAS with evidence of negative impacts on biodiversity, human livelihood or economy were included in the inventory, with information on their presence or absence in particular provinces or autonomous regions. A preliminary inventory of IAS was first drafted, and subsequently verified through many internal reviews and field surveys. The year or period of the first detection of a species in China was recorded, providing information on the minimum residence time (Rejmánek 2000; Pyšek and Jarošík 2005); this information was available for 396 species.

The inventory included 488 IAS in China’s terrestrial habitats, inland waters and marine ecosystems. Of particular taxa, there are 171 animals, 265 plants, 26 fungi, 3 protists, 11 procaryots, and 12 viruses (Appendix). Terrestrial plants account for 51.6% of the total number of IAS, and terrestrial invertebrates (104 species) for 21.3% (Table 1). Intentional introductions accounted for 67.9% of plant IAS and 34.8% of animal IAS (Table 2), such as tropic ageratum (Ageratum conyzoides), common pokeweed (Phytolacca americana), and red-eared slider (Trachemys scripta elegans) introduced as ornamental species. Very few animal and plant species invaded via natural spread (such as Ageratina adenophora and Ondatra zibethicus). All other taxa were introduced unintentionally (Table 2), such as the oriental wood borer (Heterobostrychus aequalis), and the tropical fire ant (Solenopsis geminate) that invaded with trade products. In terms of habitats, 64.3% of IAS occur on farmlands, 13.9% in forests, 8.4% in marine ecosystems, 7.3% in inland waters, and 6.1% in residential areas. Half of all IAS (51.1%) originate from North and South America, 18.3% from Europe, 17.3% from Asia not including China, 7.2% from Africa, 1.8% from Oceania, and the origin of the remaining 4.3% IAS is unknown.

The distribution of IAS can be divided into three zones. Most IAS are distributed in coastal provinces and the Yunnan province; provinces in Middle China have fewer IAS, and most provinces in West China have the least number of IAS (Fig. 1). Jimsonweed (Datura stramonium), cotton whitefly (Bemisia tabaci), two-spotted spider mite (Tetranychus urticae), American cockroach (Periplaneta americana), house mouse (Mus musculus), and brown rat (Rattus norvegicus norvegicus) occur in all provinces. Seventy IAS are distributed in more than half the number of provinces, and 105 IAS in more than one third of the provinces. Sites where IAS were first detected are mainly distributed in the coastal region, the Yunnan Province and the Xinjiang Uyghur Autonomous Region (Fig. 2), but there was a shift towards northern areas that became the main points of entry of IAS into China during the last two decades (Table 3).

Figure 1.

Regional distribution of IAS in China.Note that most IAS are distributed in coastal provinces and the Yunnan province.

Figure 2.

The distribution of first detections of IAS. First detections are concentrated in the coastal region, the Yunnan Province and the Xinjiang Uyghur Autonomous Region.

Only 33 IAS invaded China before 1850, including spiny amaranth (Amaranthus spinosus), wattle (Acacia farnesiana) and common lantana (Lantana camara). The number of newly emerged IAS has been increasing since 1850 (Fig. 3). Two hundred and twelve new IAS (53.5% of IAS with known year or period of first detection) occurred since 1950, for example pine bast scale (Matsucoccus matsumurae), common cordgrass (Spartina anglica), and erythrina gall wasp (Quadrastichus erythrinae). The cumulative number of IAS grew exponentially (Fig. 3). It could be partially due to increased surveillance, but our figure is based on best estimates of species arrival dates.

Figure 3.

Temporal trends of invasions. Cumulative numbers of firstly detected IAS in China (exponential growth: R²=0.981, P<0.001; N=396 IAS with known year or period of first detection in China) were analyzed. Only 33 IAS occurred in China before 1850, and 53.5% of the IAS were recorded after 1950.

The present study is, to our knowledge, the most up-to-date dataset of invasive species for China. However, we have to acknowledge biases that are inherent in the making of the inventory. For example, there are more plants than any other taxa, probably because plants are most numerous and easier to record. There may be biases in the timing of IAS discovery, as changes in resource allocation over time resulted in increasing opportunities for a more rigorous scientific research. It is likely that the survey pressure is not the same in all parts of China, depending on the staff numbers, among other parameters.

The cumulative number of IAS grew exponentially in China. Similar trends in historical accumulation of invasive forest insect pests and diseases have recently been reported from the United States (Aukema et al. 2010). An analysis of alien species in Europe has shown that human activity plays a key role in biological invasions (Pyšek et al. 2010, Jeschke and Genovesi 2011) and that the full effects of current socioeconomic patterns on the numbers of alien species can be delayed by several decades, resulting in what has been called an “invasion debt” (Essl et al. 2010). Our result shows that China is severely affected by invasions, with a pace of increase higher than that recorded in Europe (DAISIE 2009). Considering the fast economic growth of China, and the rapidly increasing levels of trade, tourism and transport, it is very likely that the country will face huge problems from invasive species in the future, and has already accumulated an invasion debt. For example, Europe – with a total surface similar to that of China (10 vs. 9.6 million km²), but with about half the population of China (750 vs. 1340 million inhabitants) – hosts almost three times more IAS with ecological and/or economic impact than China (1347 species [Vilà et al. 2010] compared to the 488 reported in this paper). However, the number of IAS in China could be an underestimate due to the lower research intensity and limited monitoring activities. Nevertheless, the data from Europe and China, and taking into account China’s rapidly increasing economy suggest that the same trends will occur in other countries with fast growing economies where the levels of invasions are likely to increase as a result of economic activities. This imposes severe threats to global biodiversity and the ecosystem services of the concerned countries.