Invasions by alien plant species of the agro-pastoral ecotone in northern China: Species-specific and environmental determinants

Accepted Manuscript Title: Invasions by alien plant species of the agro-pastoral ecotone in northern China: Species-specific and environmental determinants Author: Chao Chen Ding Huang Qinghai Wang Juying Wu Kun Wang PII: DOI: Reference:

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Invasions by alien plant species of the agro-pastoral ecotone in northern China: species-specific and environmental determinants

Chao Chena, Ding Huangb, Qinghai Wanga, Juying Wua, d, 1, Kun Wangb, c *

a

Beijing Research & Development Center for Grass and Environment, Beijing 100097, China

b

Department of Grassland Science, China Agricultural University, Beijing 100193, China

c

National Field Station for Grassland Ecosystem, Guyuan 076550, China

d

Key Laboratory of Urban Agriculture (North), Ministry of Agriculture, Beijing 100097, China

*

Corresponding author: Kun Wang, E-mail address: [email protected];

1 Equal contribution as corresponding author, Juying Wu, E-mail address: [email protected].

Abstract The establishment, reproduction, dispersal, and distribution of alien plants are affected by various factors during the transition from being newly introduced in a habitat to being invasive. In the agro-pastoral ecotone of northern China, comprising farmlands and natural grasslands, the biological characteristics of alien plant species were the key intrinsic factors (propagation characteristics and competitive ability), followed by such extrinsic factors as human interference and environmental heterogeneity. Among biological characteristics, the life form may be an important 1

and useful indicator of the invasive ability of a species, and the risk of invasion is greater from alien species that are poisonous, inedible, and have traits that facilitate wide dispersal. Farmlands may serve as initial shelters for alien species, from which they spread into neighbouring habitats, whereas natural grassland may act as a barrier to plant invasions. Management practices detrimental to grasslands, including overgrazing, reclamation, and road construction, often facilitate the invasions; therefore, counter measures such as reseeding and a ban on grazing need special attention. Environmental factors including precipitation, nutrients, prevailing winds, fires, and topography may be other factors that promote or block the process of invasion. In studying ways of preventing or controlling such invasions, alien plants with short life cycle, prolific seed production, and strong competitiveness, deserve particular attention and so do human activities that may damage the environment and fragile habitats.

Keywords: alien plant species; biological invasions; grassland restoration; life form; overgrazing; prevailing wind

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1. Introduction As a consequence of globalization, the original flora of a region is often disturbed due to human interference (Elton, 1958; Calvao et al., 2013; Auffret et al., 2014) and also changes gradually because of climate change (Bradley et al., 2009; Walther et al., 2009). Many alien plant species brought into new regions, intentionally or unintentionally, have made a significant impact on their new habitats (Wolf et al., 2004; Batten et al., 2006; Wu, 2011; Gooden & French, 2014; Michael et al., 2016). Plant invasions have profoundly influenced biodiversity, economy, farming, and animal husbandry worldwide and drawn the attention of researchers, policymakers, and even of ordinary people (Lonsdale, 1999; Pimentel et al., 2000, 2005; Meyerson & Mooney, 2007). As in China, such invasions have also irreversibly influenced different ecosystems, especially those related to farming, forestry, and animal husbandry (Wan et al., 2009). In China, farmlands and forests are mainly in the south and the east, whereas grasslands have flourished in the north and the west. Consistently, agroforestry has faced a greater risk of plant invasions than animal husbandry (Wan et al., 2009). Although environmental factors associated with human activities have played an important part in the process of plant invasion, the effect of human interference and environmental factors on a regional scale has not been studied systematically. In China, the ecotone that serves as a meeting point of farmland and grassland (Han et al., 2004) is a sensitive terrestrial ecosystem vulnerable to human disturbance and climate change, and has been the subject of many studies on how it has been affected by climate change, land-use pattern, and policies on spatial changes 3

in the boundaries of grasslands and farmlands (Liu & Gao, 2008a, 2008b). However, such aspects as predicting which species are likely to be more invasive and how a region can be protected from them have received little attention. Earlier studies showed that alien species, especially plants, have had a major impact on farmlands, forests, and grasslands (Wan et al., 2009). At present, the research on plant invasions in China concentrates more on agroforestry (Yan & Zhou, 2004; Wan et al., 2005, 2009), little on animal husbandry (Wang et al., 2007), and even less on the ecotone (Chen et al., 2014). However, only a few, if any, of these studies covered an ecotone, or a region that is an interlaced zone of two kinds of ecosystems. The present study focused on the agro-pastoral ecotone of northern China (APENC), which covers both farmlands and grasslands in the region. Over extensive areas of this ecotone, the vegetation changes from moist forest to desert grassland; the ecotone thus offers a variety of habitats suitable for studying the dispersal and distribution of alien plant species. These species may have been introduced on the farmlands by human carriers and may have spread to neighbouring habitats as a result of intentional or unintentional human activities or natural forces. Therefore, the biological characteristics of the alien species and factors that affect plant invasions in the agro-pastoral ecotone are analyzed and discussed here with the hope that such a discussion would serve as a guide to or a source of advice on dealing with plant invasions. Biological characteristics of alien species are important in invasion success, but other factors affect the final distribution and range. Because animals can move or be 4

moved sometimes over large distances, they are less constrained by geography, which is why at times people and animals play a more important role in the invasions of alien plant species than the species themselves (Elton, 1958; Mack et al., 2000). People are critical to plant dispersal not only because they act as carriers but also because they modify the environment or ecosystems in ways that favor invasions (Mack & Lonsdale, 2001; Lee & Chown, 2009; Ware et al., 2011). The movement of people and of agricultural products can serve as a source of alien plant species and help them in invading fresh territories (Craig et al., 2010). In addition, some environmental factors may also either facilitate or hinder such invasions (Bradley et al., 2009; Hulme, 2009). Alien plants have not caused very serious harm to the APENC region so far although many different species of such plants – including some invasive species – already exist in the ecotone (Chen et al., 2012). However, the risk of invasion is bound to increase in the coming years given the increase in international trade, economic globalization, and climate change. In the APENC, farmlands were reclaimed from grasslands during the 1950s. After these farmlands became less fertile because the stock of nutrients was depleted, more grasslands were converted into fresh farmlands, while the earlier ones turned into wastelands. This degradation and desertification of grasslands poses a serious challenge to researchers and policymakers in China. Such degraded grasslands extend over 1.38 × 106 km² at present, and continue to spread by 1.9% annually, claiming the area from the existing 2.74 × 106 km² of fertile grasslands in China (Li, 1997). In response, some 5

countermeasures have been developed, including reseeding the grasslands (Li et al., 2014) and a ban on grazing (Zhou et al., 2012). All human activity including the above measures may affect the invasion by alien species. Roads and vehicles, which are essential to economic development, also play an important role in the process (Schmidt, 1989; Lonsdale & Lane, 1994; Greenberg et al., 1997; Trombulak & Frissell, 2000; Gelbard & Belnap, 2003; Bradley & Mustard, 2006). The present study analysed the factors that may affect the invasions and also tried to find feasible and effective measures to control or to prevent such invasions in future.

2. Materials and methods 2.1 Description of study site The northern ecotone is in the middle of a transition zone in which a monsoonal climate changes to a continental climate (Box 1 & Figure 1). The elevation ranges from 50 m to 1400 m; the average annual precipitation is 300–450 mm, the annual mean temperature ranges from 2 °C to 8 °C, and strong winds blow from the north-west in winter and early spring. The farmland in the study area was reclaimed from grassland, and the main crops are naked oat [Avena chinensis (Fisch. ex Roem. et Schult.) Metzg.], flax (Linum usitatissimum L.), potato (Solanum tuberosum L.), maize (Zea mays L.), wheat (Triticum aestivum L.), foxtail millet [Setaria italica (L.) Beauv.], and buckwheat (Fagopyrum esculentum Moench). In the original grassland, the dominant gramineous plant species were Chinese leymus [Leymus chinensis (Trin.) Tzvel.] and creased wheatgrass [Agropyron cristatum (L.) Gaertn.], which are 6

perennial, and the main auxiliary species included short subulated barley [Hordeum brevisubulatum (Trin.) Link], lanceleaf thermopsis (Thermopsis lanceolata R. Br.), runcinate saussurea (Saussurea runcinata DC.), silverweed clinquefoil (Potentilla anserina L.), and longleaf halerpestes [Halerpestes ruthenica (Jacq.) Ovcz.]. Vegetation cover ranged from 30% in the overgrazed grasslands to 85% in the meadow grasslands. 2.2 Data collection and analysis The data were collected based on a field survey of alien plant species and their distribution conducted during 2009–2013 and supplemented with a database of published

literature

(http://cnki.agrilib.ac.cn/kns55/;

http://apps.webofknowledge.com/_2016-08-01), books published up to 2016, and summarized data on soil nutrition and nitrogen-fixing plants from the data of Ecological System Positioning Observation and Research (2002–2008) in China. Box 1 Profiles on the agro-pastoral ecotone of northern China

The agro-pastoral ecotone of northern China (APENC) is mainly distributed in the northern parts of China, covering over eight provinces, and stretches from the eastern Inner Mongolia to Qinghai in the western region. It serves as a transition zone in the central, in its east it is agricultural region with a large area of farmland, while it extends into relative natural grassland in the west. Thus, it is ideal for the study on invasion of alien plants on the interfaces of farmland-grassland system under human interferences and natural forces.

The alien plant species were divided into invasive and naturalized: invasive were those that had been labeled as such in at least one of the published sources, and naturalized were those alien or non-native species that had spread into the wild whose rate of reproduction was just enough to maintain their population. However, those 7

introduced alien plants that are found only in cultivation were not included in the study. When a plant species becomes naturalized in a new area, it can be either a ‘good’ thing or a ‘bad’ thing depending on subjective opinion, no matter how the naturalized plants were regarded in their earlier native habitat. To the field survey, we found and compiled 20 alien plants naturalized and presenting harmful invasions in the ecotone, while the other 17 alien plants were found merely established in the region (Appendix 1). For these alien plants, life form was classified as annual, biennial, perennial, climber, shrub, tree, and others (including free floating aquatic, succulent plants). Moreover, based on the published literature, we compared proportions of different life forms and major malignant alien plants (Appendix 2) in the ecotone and other provinces or regions in China. Certain some other factors like origin, introduction way, introduction time and distribution ranges in China, were however presented as references in Appendix 1, and are not discussed further in the study.

3. Results and discussion 3.1 Biological characteristics 3.1.1 Life form Life form is an integrated biological characteristic of a plant species and may be a good indicator of whether the species in question will prove invasive in its new habitat or ecosystem. The research so far indicates that throughout China, the number of alien species tends to decrease from the south to the north and from the east to the 8

west (Qi et al., 2004), and that the number of invasive alien species shares that pattern (Weber et al., 2008). In the agro-pastoral ecotone of northern China, annuals comprise the highest percentage of the alien plants; whereas it is also relatively higher in the northern parts of China, including Inner Mongolia (Soyol et al., 2007), Hebei (Long et al., 2008), and the northeast (Gao & Cao, 2010). The proportion of annual alien invasive plants is lower in China’s southern province as in Hainan (Shan et al., 2006), Guangdong (Wang et al., 2009), Guangxi (Tang et al., 2008), Yunnan (Ding et al., 2006), and Fujian (Yang & Chen, 2009), followed by the central provinces of Hubei (Liu & Qin, 2004) and Chongqing (Shi et al., 2004). On the other hand, species other than annuals increase from the north to the south, being from 5.3% in the APENC to 33.3% in Hainan for perennials, from absence to 7.2% for climbers, 16.3% for woody shrubs, and 7.8% for trees (Table 1). However, more than two-fifths of the alien plant species in China are annuals (43.8% of the naturalized alien species and 43.0% of the invasive alien species); the corresponding figures for the perennials are 20.4% and 30.4% (Weber et al., 2008; Jiang et al., 2011). Life form of an organism reflects the ecological environment of a habitat or an ecosystem, which is related to temperature and moisture—in China, both decreases from the south to the north and from the east to the west (Chen et al., unpublished data). Plants that share the same life form behave similarly in a biological ecosystem and occupy the same or similar biological niche (Raunkiaer, 1934). Among introduced alien species, only those with a suitable life form can establish themselves in new habitats. Many native perennials flourished in the grasslands of northern China. As in 9

steppes, perennial grasses were the dominant plants, including Chinese leymus, which can produce more than 1500 tillers in 1 m2 of land (Wang et al., 2004), and these grasses form tall bunds or embankments in the grassland (Dalgleish & Hartnett, 2009). This process is difficult and needs longer life cycles on part of the perennials, whereas annuals with shorter life cycles have a greater chance to occupy the spare niches in a grassland ecosystem. Earlier studies showed that annuals had invaded the eastern Mojave Desert in USA (Craig et al., 2010). Weeds that are annual grasses not only have lower farm productivity but also have an adverse impact on the functioning of natural grassland ecosystems (Tozer et al., 2008). The agro-pastoral ecotone of northern China has been invaded by at least fourteen species of annuals including bear grass (Cenchrus caliculatus Cav. Poaceae), which proved particularly harmful to both farmlands and grasslands (Wang, 2009). Therefore, annual and biennial grasses introduced from other regions deserve more attention as future invaders in grasslands and even in deserts; other perennials, shrubs, and even trees may not be as successful in establishing themselves in these regions. 3.1.2 Poisonous or and inedible plants, special or those possessing suitable accessory structures for self-protection or dispersal Plants native to the ecotone, such as Stellera chamaejasme L. (Thymelaeaceae), Achnatherum inebrians (Hance) Keng (Poaceae), Oxytropis ochrantha Turcz. (Fabaceae), and Thermopsis lanceolata R. Br. (Fabaceae) are poisonous and harmful to animals and therefore flourished in overgrazed grasslands. According to Zhao et al., (2004), as herds in mountain grasslands became larger, so did populations of S. 10

chamaejasme in the vegetation dominated by Stipa sareptana Becker var. krylovii (Roshev.) P. C. Kuo et Y. H. Sun (Poaceae) and Agropyron cristatum (L.) Gaertn. (Poaceae). Some native plant species with barbs, thorns, and spikes, which are not conducive to livestock feed, such as Caragna spp. (Fabaceae), also flourish, in terms of coverage and biomass, in plots subjected to overgrazing (Xiong et al., 2003; Zhao et al., 2014). Plants alien to the APENC may reap similar benefits if they too have such features. For example, coastal plain yellowtop [Flaveria bidentis (L.) Kuntze] is inedible, and it has already invaded farmlands and spread into natural ecosystems in northern China (Gao et al., 2004; Chen et al., 2012). Sweet clovers [Melilotus albus Medic. ex Desr. & M. officinalis (L.) Pall.] are not favorable for feeding livestock and cause poisoning in view of Bishydroxycoumarin it contains, though they are originally planted as leguminous forage (Yan et al., 1986). Bear grass and foxtail barley (Hordeum jubatum L.) have special accessory structures that deter grazing or facilitate long-distance dispersal: bear grass has burrs on the caryopsis so that it easily adheres to the skin of grazing animals, items of clothing, or even to automobile tyres (Xu et al., 2012), and foxtail barley can travel far because of the three long awns on each seed, which facilitate dispersal by wind (Violett, 2012). These alien species, which are inedible or deter grazing, if introduced into grasslands, may pose a greater threat as invaders (Table 2). To the related study on risk assessment, all of these five alien invasive plants had relatively higher risk (> 20 points, 3~39 points, WG-WRA; -6~55 points, WRA) under two risk assessment protocols (Chen et al., 2014). Thus, such biological characteristics are worthy of attention, and need more studies and 11

surveys in the field. 3.1.3 Greater competitiveness Alien species that are highly competitive may prove highly invasive once they are naturalized. Some leguminous N-fixing plants, such as yellow sweet clover and white sweet clover, are such ‘champion’ aliens in the region which may change the whole nutrient regime of the invaded area and have profound negative effects on the native flora. Generally, native leguminous N-fixing plants are relatively scarce among the plants recorded in the grasslands and deserts of northern China (Table 3). Thus, local plants (or vegetation) will therefore face little competition in the ecotone with introduced alien N-fixing plants. Sweet clovers, which can grow up to 1 m or sometimes up to 2 m in the second year, can literally overshadow most native plants in the grasslands and produce seeds in abundance, which are easily carried from farmlands to grasslands or the other way round (Chen et al., 2013). Moreover, this region is generally poor in plant nutrients (Table 4), and plants that can utilize resources more efficiently will be at an advantage. Bear grass can grow well despite droughts and can flourish even in deserts and sandy areas (Xu et al., 2012). In addition, some alien plant species, such as coastal plain yellowtops, can inhibit native plants through allelopathy: they can change the nutrient content of soils and enzyme activity in the rhizosphere of the invaded habitats and thereby establish themselves easily and spread further (Zhang et al., 2010). This species was successively found in Hebei and Tianjin in 2001, and had distributed over 7 cities and 54 counties in Hebei by 2006 (Li et al., 2006), and spread rapidly into Shandong and Henan province 12

(Zhang et al., 2016). In the mountain grasslands of New Zealand, hawkweed (Hieracium spp.) can establish itself on bare land and poses a threat to other native species already under stress as a result of land degradation and depletion of the semi-native tussock grasslands by overgrazing in an arid environment (Rose et al., 1998). As a whole, these successful invaders are competitively superior over native species. It is therefore necessary to predict which of the alien species pose potential threats for preventing and controlling such invasions. Some intrinsic characteristics of the species itself are thus important to its success as an invader, but such invasions are also affected by the environmental factors. It has been suggested that the success of invaders is not solely due to their biological features but facilitated to some extent by environmental changes that favour them over native species (MacDougall & Turkington, 2005), and further studies on the characteristics of the alien plants and the local environment are necessary to study the phenomenon of plant invasion.

3.2 Human interventions 3.2.1 Farmlands and reclaimed grasslands Land-use patterns that affect local vegetation to a large extent may facilitate or hinder invasions by alien plant species. In general, such invasions are more likely on farmlands than on natural grasslands in the region: the invasions typically begin on farmlands and then spread to grasslands in the farmland–grassland ecosystems of

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northern China. For example, a survey of sweet clovers along roadsides showed that these two invasive plant species were growing at much higher densities on sites adjacent to farmlands than on those adjacent to grasslands (Chen et al., 2014). Regular ploughing of farmlands may hinder invasions by plants like yellow sweet clover and white sweet clover, which are biennials in this region. The survey showed the stands of annual sweet clovers to be slightly denser and their above-ground biomass to be slightly greater on farmlands than on free-grazing grasslands, but on farmlands the biennial plants withered away after ploughing in the spring of the second year (Chen et al., 2013). Some other alien perennials, such as alfalfa, also disappeared as a result of ploughing. If alien species are to be naturalized or become invasive on farmlands, those species should complete their life cycle before the harvest of crops; if they do not, they fail to become invasive. Wild oat, for example, could invade flax, wheat, maize, and naked oat fields successfully because it matures and scatters its seeds in the unattended farmlands in early August, while the crops are harvested in the late August or early September (Zhang, 2004). Therefore, alien annuals with a shorter life cycle are more likely than biennials or perennials to invade farmlands in the region and, once naturalized on farmlands, to spread to grasslands close to the farmlands. However, if those grasslands have a high diversity of native perennials and are rich in biodiversity, they will offer greater resistance to the establishment or invasion of non-native species (Kennedy et al., 2002). For example, the free-grazing grasslands in the ecotone have successfully prevented perennial alfalfa from being an invader for over dozens of years (Li & Shao, 2005). On the other hand, grasslands that are used 14

for hay production failed to check the advance of alien species such as sweet clovers, which recorded a much higher density (41.0 ± 4.7/50 m²) in such grasslands compared to that in free-grazing grassland (0.4 ± 0.0/50 m²) (Chen et al., 2013). Thus the land-use pattern affects the degree of plant invasion in this region: grasslands – except those set aside for special purposes such as hay making – offered stronger resistance to such invasions than farmlands, and farmlands that had been reclaimed from natural grasslands were more likely to be invaded (Chen et al., 2014). 3.2.2 Overgrazing on grasslands Grazing is one of the important factors that influence the persistence of grassland ecosystems and is also a management tool to preserve diversity and persistence of native grasses in grasslands (Collins et al., 1998; Knapp et al., 1999; Grime, 2001). Grazing causes community-level changes, and grazing by the vertebrates may enhance grassland diversity by lowering the intensity of competition, or by increasing microhabitat heterogeneity and the number of colonization gaps (McNaughton, 1983; Collins et al., 1998; Olff & Ritchie, 1998). Yet, grazing may not only increase the richness of subordinate or rare native species but also facilitate the establishment of alien species (Hobbs & Huenneke, 1992). A related study found that invasions by alien plant species present a threat to grazed vegetation and that the number of alien species was greater in habitats that were intermediate in fertility, which were also richer in indigenous species (Enrique et al., 2002). However, the current situation in the studied region may be different from what can be expected in light of the above remarks. Plant invasions, for example, the harm 15

and number of alien plants, have not been as serious an issue in the region, especially in free-grazing grasslands. A properly controlled grazing intensity maintains a good balance between native species and non-native species such as sweet clovers, which are less well established in free-grazing grasslands (Chen et al., 2013), and overgrazing may constrain both native and alien plant species. At present, 90% of the grasslands in China are degraded to varying degrees (Li, 1997; Schonbach et al., 2011). Overgrazing has changed the structure of grassland ecosystems, stripped the land of its vegetation cover, lowered microhabitat heterogeneity, and also restricted the invasions to some extent. However, things may be very different if grazing is reduced or banned. It was this very situation that prompted and shaped the policy on overgrazing that sought to protect China’s grassland resources (Zhou et al., 2012). The reseeding undertaken as one of the management measures to recover the grasslands may introduce some alien plant species (of which the seeds used for reseeding are often contaminated with alien species; and sometimes, seeds of alien plants, such as alfalfa and sweet clover, are sowed on the routine), which may occupy any relatively empty ecological niches in a timely manner. It is important to bear in mind that it was neither uncontrolled free grazing nor a total ban on grazing that affected plant invasions—it was the intensity of grazing that has led to the present situations related to plant invasions in the region (Meng et al. 2009; Zhang et al., 2012; Li et al., 2014; Lv et al., 2016). Reduced intensity of grazing, associated with alien plants introduction from reseeding, contributed to the recovery of grassland vegetation under intermediate disturbance, which facilitated the establishment and invasion of pioneer 16

plant species (Wang et al., 1995). However, plant invasion was rarely reported in free grazing (mostly, it was over-grazing in the region) grassland, mostly in the interface of farmland–grassland ecosystem (Chen et al., 2012). 3.2.3 Construction of roads Construction of roads invariably disturbs habitats, and also introduces alien species into new habitats either intentionally or unintentionally. Movement of vehicles and the material used as road-fill introduce seeds of alien species into new habitats, and operations related to road construction and maintenance facilitate the germination of those seeds and the subsequent establishment of alien species (Schmidt, 1989; Lonsdale & Lane, 1994; Greenberg et al., 1997; Trombulak & Frissell, 2000). Removal of original vegetation and deep excavation also provide conditions that favour alien species (Frenkel, 1970; Trombulak & Frissell, 2000). A positive correlation has been reported between roads and the presence of alien species (Gelbard & Belnap, 2003; Bradley & Mustard, 2006). In the U.S.A. the number of alien species declined with the distance from roads in the Glacier National Park, Montana (Tyser & Worley, 1992), in California (Frenkel, 1970; Gelbard & Harrison, 2003), and in the Mojave Desert (Johnson et al., 1975). In the central highlands of India, non-native species also spread along the roads into the interiors of forests (Sharma & Raghubanshi, 2009). A related study in the southern mountainous regions of China reported that roads had played an important part in the dispersal and distribution of seven alien plant species: they were the most abundant within 4 m of the roads, and their numbers decreased beyond that distance towards the interiors 17

(Zhao et al., 2008). Roads are important to the dispersal of alien plant species (US Bureau of Land Management 1999; Gelbard & Belnap, 2003). In arid and semi-arid regions, moisture is a major limiting factor for the growth and reproduction of plants, and factors that influence moisture content also influence the establishment of alien species. For example, low angle slopes favour plants by accumulating rainwater (Starr & Mefford, 2002), and the higher moisture content at the verges that border the roads facilitated the establishment of plants. In the ecotone of northern China, the numbers of sweet clover plants declined significantly from the roadsides to the nearby habitats in relatively homogeneous habitats (Chen et al., 2014). However, soil moisture may not be the only factor, and the disturbances to the soil increased the rate at which soil resources were utilized (Hulme, 2009). In the southern parts of Yunnan, for example, although annual precipitation exceeds 1000 mm, which is suitable for the growth of most plants, the number of alien plants decreased from the roadsides to the nearby habitats (Zhao et al., 2008): in this case, more than moisture, the disturbances to soil and the movement of vehicles proved more important—if they had not brought the seeds or propagules of the alien species in the first place, everything else would have been irrelevant. Thus, the environment may only provide the opportunity: the success of invasions lies in the characteristics of the introduced species, whether they are native weeds or non-native species, and also in their relationship with the local environment. Once the roads are built, they are widely used in the ecotone; as vehicular movement increases, so do the chances of alien seeds or propagules being introduced 18

into new habitats. One study estimated the number of viable seeds carried on footwear alone at 3.9 ± 0.8 for every traveller to the Arctic (Ware et al., 2011). Once introduced, these alien species establish themselves in suitable habitats and spread to nearby habitats. However, some other causes may also disturb the original habitat, such as it being a tourist attraction, a choice for pipelines (Xiao et al., 2016) and settlements, or a site for wind turbines, and thus serve to introduce alien species and provide opportunities for them to prosper (Hobbs & Huenneke, 1992). Roads may also form ‘corridor pathways’ that act as conduits for the invasive species to reach both fragmented (With, 2002) and undisturbed natural landscapes (Hulme et al., 2008). Thus, roads play an important part in the invasion by alien plant species not only directly as means of transport but also indirectly by changing the environment as a result of road building. 3.3 Environmental factors 3.3.1 Precipitation and soil nutrients Precipitation limits plant growth in most parts of the APENC because the precipitation is very unevenly distributed through the year. In the middle part of Inner Mongolia, which forms the main part of the APENC, annual precipitation is 300–450 mm although fluctuations in total precipitation have decreased during the last 50 years (Liu & Wang, 2012) and the overall amount has been decreasing at the rate of 1.5 mm each decade (Zhu & Meng, 2010). Lack of rainfall and fluctuations in total precipitation affect both local and alien species. Changes in precipitation during

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specific seasons seemed especially important in predicting plant invasions based on both field observations (Bradley, 2009) and modelling (Bradley et al., 2009). Summer rainfall is highly variable in the APENC (Gong & Shi, 2001), and the variability in soil moisture in reclaimed grasslands adds to that variability (Liu et al., 2009). Is plant invasion favoured by precipitation together with seasonal fluctuation or deterred by it? The question is yet to be answered, and more research is needed in the form of case studies as well as systematic analysis. Organic matter, nitrogen (N), phosphorus (P), and potassium (K) are the most important elements of plant nutrition and contribute to the maintenance of ecosystem. The agro-pastoral ecotone is low in soil nutrients (Table 4), and most plant species grow poorly. Increased availability of soil N (Perry et al., 2010) and N deposition (Sharma et al., 2010) may facilitate invasive species. As can be seen from Table 4 (from left to right), the amount of soil nutrients decreased from the meadow grassland in the east to sandy areas or deserts in the west. Therefore, alien species that can fix N, including some legumes such as sweet clovers, may alter the soil characteristics of the invaded habitats and facilitate further invasions (Wolf et al., 2004). Some alien species may use up some elements crucial to the native species. Sweet clovers, for example, utilize P quickly, which is not abundant in this region (Table 4). Part of the ecotone comprises farmland that was once natural grassland, and fertilizer application may also have changed the soil characteristics. All such changes may help the establishment of alien plant species. 3.3.2 Prevailing winds 20

Although the effect of wind on invasions by alien plants in the past has received some attention (Lv & Ma, 2004), such studies of the agro-pastoral ecotone are rare. Strong prevailing winds may facilitate the dispersal and distribution of alien species in the farmland–grassland ecosystem of northern China (Chen et al., 2013). For sweet clovers and foxtail barley, which produce light and buoyant seeds, wind was an important environmental factor that promoted their dispersal and distribution. Sweet clovers produce copious seeds, which are also very light: a thousand seeds weigh only 2.65 g on average. This is why sweet clovers are more abundant downwind, and their density decreases from the interface between farmlands and grasslands to the nearby grasslands (Chen et al., 2013). In the case of foxtail barley, the three long awns on seeds enhance their dispersal by wind. The variation range of wind speed in the ecotone is 1.5–5.5 m/s, and the average number of occasions in one year on which the speed exceeds 5 m/s is 85; strong winds are especially common in spring, from March to May (Chen & Zhao, 2005). The steppes are fairly flat over most of the region, and weed seeds are easily dispersed by strong winds with little obstruction from standing plants: overgrazing having reduced such cover to the minimum. Thus, prevailing winds are an important environmental factor that to be considered in studying spread of alien species, especially those with light and buoyant seeds. 3.3.3 Fire Natural fires can be important and necessary for maintaining the structure and function of certain communities and ecosystems, but it can also be an important factor in plant invasions (Grace et al., 2002; Davies et al., 2008; Cavallero & Raffaele, 21

2010). As in mesic African savannah, frequent burning experiment promoted invasions by alien plant species (Masocha et al., 2011; Te Beest et al., 2011), and Keeley et al., (2012) considered shrub lands in the Mediterranean basin to be resilient to frequent fires and resistant to invasion by alien species. In the grasslands of northern China, fire is a missing factor in overgrazed grasslands: only 4.4% of the total area under grasslands was placed in the ‘very high’ risk category with reference to fire; 9.6% was in ‘high’ risk category; 60.9%, in the ‘low’ category; and 5.9% in the ‘very low’ category (Liu et al., 2012). Most grasslands in China are overgrazed and contain little standing litter that can lead to a fire. Because forage is scarce, people are also careful of fires in the dry season and take a series of measures to prevent fires. Thus, fire is largely neglected as a factor in studying invasions by alien plant species in the APENC. However, the policy of grassland restoration in recent years may change that: in blocks of grassland fenced off and banned for grazing as part of that policy, fire may prove an important factor once such blocks have recovered from the earlier overgrazing and may promote the establishment and reproduction of alien plant species. 3.3.4 Sunlight Availability of sunlight affected the dispersal of alien plant species, and the establishment of the more sun-loving among them suffers in shaded habitats (Parendes & Jones, 2000; Zhao et al., 2008). Sweet clovers, for example, are suppressed by native plants in terms of density, during vegetative and reproductive growth, among the shaded shrubs along roadsides in the agro-pastoral ecotone of 22

northern China (Chen et al., 2014). Other alien plants in the region, such as foxtail barley, bear grass, and coastal plain yellowtops, also developed well in the open sites. However, shade-tolerant plants may thrive in shaded habitats as in closed-canopy forests (Martin et al., 2009). Generally, alien plant species are sun-loving, and shaded habitats may block most of the invasions by such plants whereas open and sunny habitats are more prone to being invaded (Pauchard & Alaback, 2004; Martin et al., 2009). 3.3.5 Slope and topography Only a few studies have considered the effect of slope and topography on plant invasions. Blumenthal et al., (2012) found that Linaria dalmatica selectively invaded south-facing slopes in the grasslands of mixed-grass prairie in North America. Such studies are rare in the APENC. On steep slopes, it is possible that plant invasions are affected more by sunlight or soil moisture content than by the topography, whereas on gentle slopes, prevailing wind may play a more important role in dispersal of the invaders. Thus, it may not be the slope or the topography that affects invasions, but changes in soil moisture brought about by slope or topography (He et al., 2008). Factors that influence plant invasions may change with time depending on changes in the external environment ushered in by the process of invasion (Strayer et al., 2006). In the pampas, for example, environmental fluctuations and physical disturbances such as large floods may constrain rather than encourage exotic species in grazed grasslands (Enrique et al., 2002). However, some other environmental factors, such as global warming and the rising CO2 concentrations in the atmosphere 23

associated with climate change, also facilitate or hinder plant invasions (Smith et al., 2000; Bradley et al., 2009; Walther et al., 2009).

4. Conclusion So far, alien plant species have not seriously harmed the APENC. However, future changes in the environment are bound to affect agriculture, and it is wiser to take some protective measures based on the experiences in grasslands or ecosystems elsewhere. Life form may be a good indicator of the success or otherwise of an alien plant species as an invader. For the control and prevention of such invasions of the farmland–grassland ecosystems in northern China, annuals and biennials among the alien species deserve special attention, as well as some N-fixing plants such as sweet clovers, which are more efficient in tapping soil resources – a feature helpful to the invaders. Other species may have an advantage over native plants because the alien species are more competitive or may have special structures that facilitate their dispersal over long distances. Besides the features inherent in the species, land-use patterns also influence the establishment and dispersal of alien plants. A meeting point between farmland and grassland may be more prone to invasions. Compared to farmlands, grasslands offer a stronger barrier to invasions because grasslands have greater biodiversity and because of the presence of grazing animals. However, farmlands may serve as the first home of the alien species, from which they can spread to nearby habitats or ecosystems.

24

Roads play an important part in the dispersal of alien species: roads not only serve as the means of transport but also facilitate establishment because road construction disturbs habitats and the disturbance usually favours the invaders. In addition to these factors, policies and local laws on land use may also facilitate or hinder invasions. In general, characteristics of the alien species and of the habitat – in particular, those that make a habitat easy to invade – are the most common factors that influence the current status of plant invasions. The research so far shows that plant invasions in this particular region, and probably over the entire farmland–grassland ecosystem of China, need to be studied in greater detail in future. More studies on plant invasions in the farmland–grassland ecosystems are needed, particularly those that focus on how the harmful alien plant species are introduced into new habitats and how they are dispersed and spread. Once the alien species establish themselves in a new habitat or ecosystem, it is very difficult to remove them—we should either prevent them from getting a foothold or learn to live with them.

Acknowledgments The authors sincerely thank the workers at the National Field Station for Grassland Ecosystem of China Agricultural University and at local governmental grassland stations in Hebei province for their support. This study was partly supported by the Special Fund for Agro-scientific Research in Public Interest (201203062 & 200903060). The authors also thank Kesi Liu for the suggestions on improving the manuscript. 25

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39

Figure 1 Sketch map of the agro-pastoral ecotone in northern China (delineated in blue)

40

Table 1 Proportion of life forms of invasive alien plant species in provinces/regions of China

Provinces/Regions

Life forms (%)

Total number

Annual

A or B*

Biennial

Perennial

Climber

Shrub

Tree

Others*

APENC* (2012)

73.7

0.0

10.5

5.3

5.3

0.0

5.3

0.0

19

Inner Mongolia (2007)

72.7

0.0

4.6

22.7

0.0

0.0

0.0

0.0

22

Northeast (2010)

61.5

7.7

6.2

20.0

0.0

1.5

3.1

0.0

66

Hebei (2008)

61.9

12.7

3.2

15.9

1.6

1.6

1.6

1.6

63

Hubei (2004)

58.9

16.1

3.6

14.3

0.0

1.8

1.8

3.6

56

Chongqing (2004)

51.1

15.6

2.2

17.8

2.2

6.7

0.0

4.4

46

Yunnan (2006)

45.0

7.0

0.8

25.6

4.7

12.4

3.1

1.6

129

Guangxi (2008)

40.5

9.5

1.4

28.4

4.1

13.5

0.0

2.7

74

Fujian (2009)

39.7

12.3

1.4

30.1

4.1

9.6

0.0

2.7

73

Guangdong (2009)

41.9

6.5

1.1

32.3

5.4

9.7

1.1

2.2

93

Hainan (2006)

32.0

2.0

0.0

33.3

7.2

16.3

7.8

1.3

153

China (2008)

43.0

4.4

4.1

30.4

4.8

5.9

3.7

3.6

270 b

China (2011)

43.8

4.5

4.5

20.4

7.9

6.9

6.2

5.9

861 a

Note:

*

APENC presents agro-pastoral ecotone of northern China, A = Annual, B = Biennial; Others

include free floating aquatic, succulent; a means naturalized alien plants in China, while b means alien invasive plants in China.

41

Table 2 Risk assessment and undesirable traits of naturalized alien plants in the agro-pastoral ecotone in northern China

TAXA

WG-WRA*

WRA*

Undesirable traits

Cenchrus caliculatus

29

28

Melilotus spp.

29

25

Flaveria bidentis

25

28

Hordeum jubatum

28

21

Galinsoga parviflora

25

19

inedible, easy to disperse with buoyant pappus

Amaranthus retroflexus

22

22

edible

Datura stramonium

22

18

poisonous, with thorns and spines on capsule

Amaranthus caudatus

24

15

edible, high feed value

Ipomoea purpurea

24

14

low feed value

Cosmos bipinnata

22

15

inedible

Medicago sativa

24

12

high feed value, good palatability

Avena fatua

21

15

edible, caryopsis with awns

Abutilon theophrasti

22

14

moderate feed value

Eleusine indica

19

16

edible

Hibiscus trionum

18

15

low feed value

Eruca vesicaria subsp. sativa

17

15

moderate feed value

Cannabis sativa

19

13

low feed value

Rhus typhina

20

10

tree

Parthenocissus quinquefolia

19

11

vine, climbers

disperses

easily

with

barbs

and

burrs,

unconducive to livestock feed at maturity easy to disperse with light seeds, feed value drops after flowering easy to disperse, inedible, allelopathy disperses easily with long awns, feed value drops at maturity

*Introduced and compiled from Chen et al., 2014.

42

Table 3 Nitrogen-fixing native plants in different land types of northern China

Frequency Land type

Recorded plant species

of

occurrence

of

N-fixing plant species N-fixing plants (%) a

Meadow grassland

997

63

10.8

APENC *

248

23

7.0

Alpine meadow

74

5

9.6

Steppe grassland

57

7

6.8

Sandy areas

42

5

12.7

Desert

10

0

——

* APENC stands for the agro-pastoral ecotone of northern China; a means the frequency of occurrence of N-fixing plants in quadrat sampling.

43

Table 4 Nutrients in different types of grasslands in northern China Haibei

Hulun Buir

Naiman1

Erdos

Naiman2

Guyuan

Shapotou

Fukang

Celle

(Qinghai)

(I. Mongolia)

(I. Mongolia)

(I. Mongolia)

(I. Mongolia)

(Hebei)

(Ningxia)

(Xinjiang)

(Xinjiang)

Soil nutrients*

Organic matter

0～10 cm

_

65.45±10.24

5.62±0.50

3.26±1.21

1.54±0.41

33.95±3.89

2.56±0.59

3.06±0.34

1.69±0.37

(g/kg)

10～20 cm

70.21±11.30

41.39±9.29

3.36±0.72

2.34±0.92

1.05±0.24

32.09±2.50

2.07±0.12

1.81±0.33

1.62±0.71

Total nitrogen

0～10 cm

6.24±0.78

2.70±0.32

0.43±0.17

0.09±0.04

0.16±0.04

2.31±0.20

0.22±0.04

0.18±0.04

0.17±0.04

(g/kg)

10～20 cm

3.62±0.42

1.84±0.33

0.30±0.05

0.08±0.04

0.10±0.04

2.02±0.16

0.25±0.04

0.11±0.04

0.18±0.08

Total phosphorus

0～10 cm

0.93±0.13

0.18±0.00

0.60±0.04

0.52±0.04

0.27±0.02

0.52±0.05

0.56±0.03

16.6±0.00

13.73±0.93

14.92±1.86

33.2±0.00

14.04±0.81

13.77±2.05

0.33 _

(g/kg)

10～20 cm

0.88±0.10

Total potassium

0～10 cm

22.33±8.16

10～20 cm

N available

0～10 cm

0.62±0.34

0.34

0.09

27.50 _

(g/kg)

0.15 _

22.68±7.27

27.50 _

14.42±1.15

27.50

26.70

293.41±22.54

23.53±3.31

16.19±6.17

8.78±1.50

133.30±13.23

2.73±0.45

14.64±3.55

22.16±5.59

185.59±46.58

15.70±4.63

17.77±12.87

6.66±1.21

_

2.02±0.52

9.86±5.49

32.92±8.88

_ (mg/kg)

10～20 cm

P available

0～10 cm

8.05±2.36

4.55±1.02

9.78±3.15

2.55±0.82

9.23±4.01

7.97±1.60

170.15±29.34

6.15±2.03

5.32±2.77

(mg/kg)

10～20 cm

3.38±1.08

2.34±0.31

5.28±1.43

1.37±0.38

7.03±2.63

_

298.8±46.95

4.05±1.17

5.22±2.14

K available

0～10 cm

431.5±38.85

383.01±191.01

149.70±30.73

64.21±20.56

76.20±23.65

231.07±28.27

410.00±0.00

246.20±52.64

125.43±13.87

(mg/kg)

10～20 cm

231.76±66.84

153.72±57.55

84.12±17.07

50.36±18.42

63.20±23.44

_

640.00±56.57

260.72±47.81

124.20±17.46

*Synthesized from data set of Ecological System Positioning Observation and Research in China (2002-2008).

44

Appendix 1 List of alien plant species in the agro-pastoral ecotone of northern China (APENC) Species

Family

Life form

Origin

Recorded time in

Distribution (number of

China (year)

provinces)

Introduction way

Abutilon theophrasti

Malvaceae

annual

North America

Introduced as fiber plants

659

12

Agrostemma githago

Caryophyllaceae

annual/biennial

Mediterranean

Introduced unintentionally

1800 s

6

Amaranthus blitoides

Amaranthaceae

annual

North America

Introduced unintentionally

1875

4

Amaranthus caudatus

Amaranthaceae

annual

Tropical American

Introduced as vegetables

< 1840

28

Amaranthus retroflexus

Amaranthaceae

annual

Tropical American

Introduced as vegetables

1850 s

28

Avena fatua

Poaceae

annual

Mediterranean

Introduced unintentionally

1850 s

28

Cannabis sativa

Cannabaceae

annual

Central Asia

Introduced as fiber plants

> 1840

28

Cenchrus caliculatus

Poaceae

annual

Asian subtropical

Introduced unintentionally

1985

3

Chenopodium hybridum

Chenopodiaceae

annual

Europe, West Asia

Introduced unintentionally

1864

20

Conyza canadensis

Asteraceae

annual

North America

Introduced unintentionally

1860

26

Cosmos bipinnata

Asteraceae

annual

Mexico

Introduced as gardening flowers

< 1919

5

Datura stramonium*

Solanaceae

annual

Mexico

Introduced as medicinal plants

< 1405

28

Daucus carota

Apiaceae

biennial

Europe

Introduced unintentionally

~ 1300 s

14

Eleusine indica

Poaceae

annual

India

Introduced unintentionally

1760

27

Erigeron annuus

Asteraceae

annual/biennial

North America Mexico

Introduced unintentionally

1886

17

Eruca sativa

Brassicaceae

annual

southern Europe

Introduced unintentionally

——

12

Flaveria bidentis*

Asteraceae

annual

South America

Introduced unintentionally

2001

4

Galinsona parviflora

Asteraceae

annual

South America

Introduced unintentionally

1915

17

Hibiscus trionum

Malvaceae

annual

Central African

Introduced unintentionally

1406

28

Hordeum jubatum

Poaceae

biennial

North America, Asia, Europe

Introduced unintentionally

——

3

Lepidium virginicum

Brassicaceae

annual/biennial

North America

Introduced unintentionally

1933

17

Lolium temulentum

Poaceae

annual/biennial

Mediterranean

Introduced unintentionally

1954

32

45

Melilotus albus

Fabaceae

biennial

West of Eurasian

Introduced as forge

1922

16

Melilotus officinalis

Fabaceae

biennial

Europe

Introduced as forge

——

20

Medicago sativa

Fabaceae

perennial

West Asia

Introduced as forge

B. C. 139

15

Oenothera biennis

Onagraceae

perennial

North America

Introduced as gardening flowers

——

10

Parthenocissus quinquefolia

Vitaceae

vine

North America

Introduced as green plants

1980

7

Pharbitis purpurea

Convolvulaceae

annual

Tropical American

Introduced as gardening flowers

1890

8

Phleum pratense

Poaceae

perennial

Europe, West Asia

Introduced as forage

< 1919

9

Pseudosorghum fasciculare

Poaceae

perennial

Mediterranean

Introduced unintentionally

1900 s

16

Rhus typhina

Anacardiaceae

tree

North America

Introduced as shade tree

1959

5

Ricinus communis

Euphorbiaceae

annual

Northeast of Africa

Introduced as oil plants

659

16

Senecio dubitabilis

Asteraceae

annual

Europe

Introduced unintentionally

——

16

Solanum rostratum

Solanaceae

annual

North America

Introduced unintentionally

1982

6

Sonchus oleraceus

Asteraceae

annual/biennial

Europe

Introduced unintentionally

> 1840

28

Trifolium repens

Fabaceae

perennial

Europe

Introduced as forage or turfgrass

1800 s

21

Vaccaria hispanica

Caryophyllaceae

annual/biennial

Europe

Introduced unintentionally

> 1840

15

Note: Invasive alien species given in bold text; Poisonous or inedible plants labeled with *.

46

Appendix 2 Major alien invasive plants species in some provinces or regions in China Provinces/Regions

Species

APENC* (2012)

Cenchrus caliculatus Cav.; Flaveria bidentis (L.) Kuntze.; Galinsoga parviflora Cav.; Melilotus albus Medik.; Melilotus officinalis (L.) Pall.

Inner Mongolia (2007)

Agrostemma githago L.; Cenchrus caliculatus Cav.; Flaveria bidentis (L.) Kuntze.; Galinsoga parviflora Cav. Agrostemma githago L.; Amaranthus albus L.; Amaranthus lividus L.; Amaranthus retroflexus L.; Amaranthus tricolor L.; Amaranthus viridis

Northeast (2010)

L.; Ambrosia artemisiifolia L.; Chenopodium hybridum L.; Conyza canadensis (L.) Cronq.; Datura stramonium Linn.; Erigeron annuus (L.) Pers.; Galinsoga parviflora Cav.; Lepidium densiflorum Schrad.; Medicago sativa L.; Pharbitis purpurea (L.) Voisgt; Trifolium repens L. Ambrosia artemisiifolia L.; Ambrosia trifida L.; Avena fatua L.; Conyza canadensis (L.) Cronq.; Conyza bonariensis (L.) Cronq.; Eichhornia

Hebei (2008) crassipes (Mart.) Solms; Flaveria bidentis B.L.Rob.; Galinsoga parviflora Cav.; Sorghum halepense (L.) Pers., Spartina anglica Hubb. Alternanthera philoxeroides (Mart.) Griseb.; Amaranthus spinosus L.; Amaranthus tricolor L.; Amaranthus viridis L.; Avena fatua L.; Bidens Hubei (2004)

pilosa L.; Daucus carota L.; Datura stramonium L.; Eleusine indica (L.) Gaertn.; Erigeron annuus (L.) Pers.; Euphorbia helioscopia L.; Lepidium virginicum L.; Pharbitis nil (L.) Choisy; Pharbitis purpurea (L.) Voisgt; Phytolacca americana L.; Ricinus communis L. Alternanthera philoxeroides (Mart.) Griseb; Anredera cordifolia (Tenore) Steenis; Avena fatua L.; Bidens pilosa L.; Conyza canadensis (L.)

Chongqing (2004) Cronq.; Daucus carota L.; Eichhornia crassipes (Mart) Solms; Galinsoga parviflora Cav.; Oxalis corymbosa DC. Acacia mearnsii De Will; Amaranthus tricolor L.; Anredera cordifolia (Tenore) Steenis; Brachiaria eruciformis (Sm.) Griseb.; Bryophyllum pinnatum (L. f.) Oken; Cannabis sativa L.; Capsicum frutescens L.; Cassia sophera L.; Cassia tora L.; Erigeron annuus (L.) Pers.; Euphorbia Yunnan (2006) helioscopia L.; Hibiscus trionum L.; Lolium temulentum L.; Melilotus albus Medic. ex Desr; Mimosa pudica L.; Solanum khasianum C. B. Clarke; Sonchus oleraceus L.; Veronica didyma Tenore Alternanthera philoxeroides (Mart.) Griseb.; Bidens pilosa L.; Borreria latifolia (Aubl.) K. Schum.; Conyza canadensis(L.) Cronq.; Eichhornia crassipes (Mart.) Solms; Eupatorium adenophora Spreng.; Eupatorium odoratum L.; Ipomoea cairica (L.) Sweet; Lantana camara L.; Guangxi (2008) Parthenium hysterophorus L.; Pharbitis purpurea (L.) Voisgt; Solanum torvum Swartz; Sorghum halepense (L.) Pers.; Spartina anglica Hubb.; Tithonia diversifolia A. Gray

47

Amaranthus spinosus L.; Anredera cordifolia (Tenore) Steenis.; Avena fatua L.; Ageratum conyzoides (L.) L.; Bidens pilosa L.; Conyza canadensis (L.) Cronquist; Conyza sumatrensis (Retz.) Walker; Crassocephalum crepidioides (Benth.) S.Moore; Datura stramonium L.; Fujian (2009)

Euphorbia hirta L.; Euphorbia maculata L.; Erigeron annuus (L.) Pers.; Eichhornia crassipes (Mart.) Solms; Galinsoga parviflora Cav.; Lantana camara L.; Lepidium virginicum L.; Mirabilis jalapa L.; Oxalis corymbosa DC.; Pharbitis purpurea (L.) Voisgt; Ricinus communis L.; Solanum capsicoides All.; Scoparia dulcis L.; Soliva anthemifolia (Juss.) Sweet; Sphagneticola trilobata (L.) Pruski; Veronica polita Fr. Alternanthera philoxeroides (Mart.) Griseb.; Ageratum conyzoides L.; Aster subulatus Michx.; Bidens pilosa L.; Conyza canadensis (L.) Cronq.; Erigeron annuus (L.) Pers.; Eupatorium odoratum L.; Galinsoga parviflora Cav.; Ipomoea cairica (L.) Sweet; Mikania micrantha Kunth;

Guangdong (2009) Merremia boisiana (Gagnep.) Ooststr.; Mimosa sepiaria Benth.; Oxalis corymbosa DC.; Pharbitis purpurea (L.) Voisgt; Panicum maximum Jacq.; Rhynchelytrum repens (Willd.) Hubb; Scoparia dulcis L. Amaranthus spinosus L.; Amaranthus viridis L.; Aeschynomene americana L.; Borreria latifolia (Aubl.) K. Schum.; Celosia argentea L.; Chenopodium ambrosioides L.; Cassia occidentalis L.; Cassia mimosoides L.; Cassia tora L.; Euphorbia cyathophora Murr.; Euphorbia hirta Hainan (2006) L.; Gomphrena celosioides Mart.; Mimosa invisa Colla; Opuntia dillenii (Ker Gawl.) Haw.; Pilea microphylla (L.) Liebm.; Phyllanthus niruri L.; Ricinus communis L.; Sesbania cannabina (Retz.) Poir.

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