Water lettuce ( Pistia stratiotes L.) (Araceae) in China: distribution, introduction pathway, and impacts

Non-native aquatic species have caused profound ecological and physical impacts in many waterbodies, and in China many non-native species are known for their ecological displacements and the changes they have induced in a diversity of wetland categories. Water lettuce ( Pistia stratiotes ), a free-floating aquatic vascular plant native to South America, is a highly invasive species that has been introduced in Europe, North America, Africa, Asia, Central America and the Caribbean. This species was brought to China over 500 years ago


Introduction
Non-native species are significant biological factors that negatively influence the environment and ecosystem health (Simberloff et al. 2013), and they are among the primary threats to global biodiversity, ecosystem functions, economic sustainability, sustainable development, and even human health (Molnar et al. 2008;Courchamp et al. 2017).Freshwater ecosystems are considered more vulnerable to invasion by non-native species than terrestrial and marine ecosystems (Vilà et al. 2010;Dudgeon 2019).Non-native aquatic plants are recognized as implementors of ecological engineering, and they influence biodiversity and habitat through both abiotic and biotic factors (Schultz and Dibble 2012;Hussner et al. 2021).The control and management of nuisance non-native plants has become an important issue for local governments and environmental conservation organizations (Hussner 2012;Wang et al. 2016).
China is the country most severely threatened by non-native aquatic species because of the large number of non-native aquatic species that were introduced in China for use in aquaculture, the aquarium trade, ecological restoration and for other purposes (Xiong et al. 2015(Xiong et al. , 2017(Xiong et al. , 2023a;;Wang et al. 2016).Many non-native aquatic plants have escaped and established feral populations in rivers, lakes, ponds, reservoirs, channels and a variety of other wetland habitats (Wang et al. 2016(Wang et al. , 2021)), causing significant negative ecological and economic impacts (Wang et al. 2016).Most recent studies have focused on non-native aquatic plants introduced in China as aquarium species, such as delta arrowhead (Sagittaria platyphylla), parrot's feather (Myriophyllum aquaticum), fanwort (Cabomba caroliniana) and yellow bur-head (Limnocharis flava) (Wang et al. 2020;Xiong et al. 2023b).There has been relatively little research focused on non-native aquatic plants like water lettuce (Pistia stratiotes) that are widely used for forage in rural regions and have widespread feral populations.
Water lettuce, Pistia stratiotes L., is a free-floating perennial monocotyledonous aquatic vascular plant of the Araceae family.Although there are some differences in opinion (Renner and Zhang 2004), most researchers suggest that this species is South American in origin (Holm et al. 1977).Water lettuce has been introduced in North America, Europe, Asia, Africa, and Oceania (Madeira et al. 2022).The first record of this species in China indicates that it appeared at the end of the 17 th century (Li 1758).In the 1950s the use of water lettuce was encouraged, and it was cultivated as swine feed between the 1950s and 1970s (Gu and Hu 2020).It has expanded its range rapidly and it was included in the List of Invasive Alien Species in Chinese Natural Ecosystems (Second Batch) (MEE 2010).Despite its notoriety as an invasive, there has been little detailed information about its occurrence in China (Wang et al. 2016).There has been concern expressed that further development of water conveyance projects such as China's South to North Water Diversion could cause further spread of water lettuce and many other non-native species (Liu et al. 2017).
In this study, we describe the introduction pathway, biological traits, current distribution, and the ongoing and potential future impacts of water lettuce in China.We hope that this study provides useful information and recommendations for aquatic ecologists and environmental managers.

Information collection
We searched the Web of Science (ISI, http://www.isiknowledge.com) and CNKI (http://www.cnki.net)databases for titles, abstracts, and reports that included the keywords Pistia stratiotes, water lettuce and China.Information was also gathered from Chinese books (such as Illustrations of Alien Invasive plants in China) and the invasive species database NSII -China National Specimens (http://www.nsii.org.cn/node/824,accessed 19 April 2021).The species profiles in the CABI Invasive Species Compendium and the Global Invasive Species Database (2023) were also reviewed.Detailed species descriptions of Pistia stratiotes are found in the Flora of China (http://www.iplant.cn/info/Pistia%20stratiotes?t=foc, accessed 18 March 2023) and The Jepson eFlora (https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi/wwwtax.cgi,accessed 18 March 2023).The assessment and characterization of water lettuce are found in a diversity of agency brochures and other references, including sites such as those linked to the United States Department of Agriculture.

Field investigation
Between 2003 and 2020, we conducted over 50 botanical surveys that included all provincial-level administrative regions of China using the sampling methodology described by Fang et al. (2009).We recorded geographic information (longitude, latitude, and elevation), waterbody data (water depth and temperature), and plant community inventories.The geographic and other data are presented in Supplementary material Table S1.

Introduction pathway
The exact date of the introduction of water lettuce in China is not known, but the first record of this species in China appears in a famous traditional Chinese medicine book (Li 1578).Initially, water lettuce was used as a medicinal herb to cure colds, swelling, edema, rheumatism, urinary tract infections and other sicknesses (Li 1578;Fern 2014).It was originally planted at sites like Guangdong and Fujian in South China.This species has been promoted and planted in most provinces of South China as a medicinal herb.In the 1950s the Chinese central and local governments planted water lettuce in large areas as pig fodder in all Provinces, Autonomous Regions, and in many municipalities.This species is rich in nutrients (protein, fat, and carbohydrates and starch account for about 1.25%, 0.75%, and 9% of total plant weight, respectively), and its yield is very high.An individual plant can clonally produce seven or eight independent plants in ten days and when propagated up to sixty individuals can be generated by a single parent plant in a month during the summer.Plants can produce up to 15000 kg daily in a hectare of water surface (Website of Flora of China 2023).This species is a widely used and easily propagated pig fodder and it significantly contributed to the rapid increase of pig rearing in China.Many farmers cook water lettuce and feed it to chickens, ducks, geese and other birds.Water lettuce has been broadly introduced and is farmed in rural areas throughout China (Chen et al. 2015).
China's water bodies are among the most seriously compromised by eutrophication in the world (Qin et al. 2013).A great number of constructed wetlands have been built in the past thirty years to absorb nutrients and control harmful algae (Zhang et al. 2012).Water lettuce has been widely planted in many constructed wetlands in China because of its ability to absorb nutrients and its anti-cyanobacterial capability (Wu et al. 2015).Water lettuce has readily escaped from constructed wetland sites and has established feral populations from that source in many areas (Figure 1).

Current distribution
Based on our field investigations and a review of the literature, feral populations of water lettuce are established in a diversity of habitats and have a wide distribution throughout South China (Figure 1) including 21 Provinces, Autonomous Regions or Municipalities (i.e., Fujian, Guangdong, Guangxi, Guizhou, Hainan, Hubei, Hunan, Jiangsu, Jiangxi, Chongqing, Anhui, Henan, Liaoning, Shandong, Sichuan, Tianjin, Yunnan, Zhejiang, Hongkong, Macau and Taiwan; Figure 1).We observed that water lettuce has a broad range of aquatic habitats in which it occurs, including slow-moving rivers, ponds, reservoirs, lakes and paddy fields (Figure 2).Its optimal growth temperatures are between 22 and 30 °C (Henry-Silva et al. 2008).Because of its ability to rapidly propagate clonally and its tolerance of a wide range of temperature and other environmental characteristics, this species has established a broad distribution throughout South China (including Hainan, Guangdong, Guangxi, Yunnan, and Guizhou).It can survive and develop in temperatures as low as 10 °C (Pieterse et al. 1981;Hussner 2014).Nonetheless, it is very susceptible to temperatures below that, and in the presence of frost and snow, plantlets atrophy when the water surface is frozen or air temperature approaches 0 °C (MacIsaac et al. 2016).In the early period after its introduction, water lettuce only occurred in South China and it did not appear to survive or overwinter successfully in North China.However, in recent years it has been increasing reported in North China because of global warming and the expansion of artificial farming environments (Wang et al. 2012).Water lettuce has well-established feral populations in North China (Henan, Beijing, and Liaoning) and in some high latitude areas (such as Yunnan, Sichuan, and Chongqing) (Figure 1).

Ecological and economic impacts
Water lettuce grows very rapidly, and in the summer months with sunny days and high temperatures (from April to October), one water lettuce plant can proliferate into 7 or 8 new individuals in 10 days and over 60 new plants in 30 days in East China (Editorial Committee of the Flora of China, Chinese Academy of Sciences 2005).This species easily forms dense monospecific stands in most regions of China and reduces native submerged plants by blocking light and oxygen exchange (EPPO 2017).In our field studies we observed that water lettuce forms dense monospecific stands at most invaded sites and that these areas lack native species otherwise associated with them (Table 1).Some native submerged plants, such as Ottelia and Nuphar species, have been displaced by water lettuce in some regions of China.This phenomenon accelerates the decrease of native freshwater biodiversity (Fang et al. 2006).
South China and the middle and lower areas of the Yangtze River basin are very important agricultural regions in China (Wang et al. 2020), and they are the areas with the most serious colonization by water lettuce (Figure 1).Some invasive aquatic plants flourish in these regions that are heavily influenced by an increased water evaporation and by irrigation pumping (Wang et al. 2020;Xiong et al. 2021).Water lettuce is abundant in agricultural irrigation channels and drainage ditches, and thus has become a potential threat to food production (Tan 2017).
The primary area of water lettuce's distribution in China is also the region that supports the highest human population and most rapidly growing economy (Wang et al. 2020;Xiong et al. 2022).The demand on the area's water supply and quality is increasing rapidly.Unfortunately, water lettuce in some waterbodies has decreased both the quantity of water available for potable human use (its large mats increase water evaporation and hampers water pumping) and the water quality (it increases detrital deposits and mortality among native species, producing both a decline in water quality and a decrease in overall biodiversity).Water lettuce has also become a significant threat to the safety and security of drinking water, as well as its use for other human domestic purposes.It can form mats of over 300 hectares of monospecific populations so dense that they can decrease ship speed, reduce fisheries catch, as well as the quality of drinking water (Wanfenghu Lake, the fifth largest freshwater lake in China, is an example of a site experiencing these impacts) (Wang and Fu 2005).Water lettuce has become a notorious weed in many reservoirs, such as the Three Gorges Reservoirs, and administrative departments spend millions of dollars annually to manage and remove this problematic non-native species (Xiong et al. 2018).
The dense monospecific populations of some aquatic plants provide suitable habitats for disease-carrying mosquitos (Xiong et al. 2021).Extensive mats of water lettuce provide suitable oviposition habitats and shelter for mosquitos and also decrease the effectiveness of fish predation upon them (Lounibos and Dewald 1989).Thus, water lettuce can increase the risk of infectious mosquito-borne diseases.Especially in tropical and subtropical regions (such as Hainan, Guangdong, Guangxi, Hongkong and Macau), yellow fever, dysentery and dengue are high risk mosquito-borne infectious diseases.

Management and control
Due to its invasiveness and its significant ecological and economic impacts, water lettuce appears in the Second List of Invasive Alien Species in China (MEE 2010).To avoid the contamination of aquatic habitats, herbicides are not recommended to control water lettuce.Hand removal or temporary drainage of a waterway are the primary methods used to manage and eliminate this species (MEE 2010).Manual eradication is labor-intensive, expensive, and slow because of the density of stands and the large size of the plants needing removal (we observed individual plants of over 25 cm high).Some local governments purchase special plant removal boats specifically designed to remove water lettuce (Website 2021).Although some researchers recommend biological control to manage invasive aquatic plants (Day et al. 2020), no suitable biological agents have been observed that might be useful for water lettuce control in China.Thus, water lettuce has flourishing wild populations in most regions and has become a significant and problematic invasive species in China (MEE 2010).
The regions that suffer most from water lettuce invasion support over 70% of China's agricultural food production (National Bureau of Statistics 2021).The spread of feral water lettuce is a serious threat to native aquatic biodiversity, to the availability of drinking water, agricultural production, and to the control of mosquito-borne diseases.More monitoring and research in needed on water lettuce in China.

Figure 2 .
Figure 2. A monospecific stand of water lettuce (Pistia stratiotes) in Hainan wetland of China.Photo by Keyan Xiao.