Coverage of Native Plants Is Key Factor Influencing the Invasibility of Freshwater Ecosystems by Exotic Plants in China.

Understanding the biotic and abiotic factors that influence the susceptibility of a community to invasion is beneficial for the prediction and management of invasive species and the conservation of native biodiversity. However, the relationships between factors and invasibility of a community have not been fully confirmed, and the factors most associated with the susceptibility of a community to invasion have rarely been identified. In this study, we investigated the species richness patterns in aquatic exotic and native plants and the relationships of exotic species richness with habitat and water environment factors in 262 aquatic plant communities in China. A total of 11 exotic plant species were recorded in our field survey, and we found neither a negative nor a positive relationship between aquatic exotic and native plant species richness. The aquatic exotic plant species richness is negatively correlated with the relative coverage and biomass of native plants but positively correlated with the total nitrogen (TN), total phosphorus (TP), and chemical oxygen demand (COD) concentrations in the water. The native plant species richness, native species' relative coverage, and native species' biomass were positively related to each other, whereas the TP, TN, and COD were also positively related to each other. The native plant species richness, native species' relative coverage, and native species biomass were each negatively correlated with the TP, TN, and COD. In addition, biotic rather than abiotic predictors accounted for most of the variation in exotic plant richness. Our results suggest that improving the vegetation coverage and the biodiversity of native plants is the most effective approach for preventing alien plant invasions and minimizing their impacts on freshwater ecosystems.

Introduction

Plant invasions reduce biodiversity and alter the species composition, structures, processes, and functions of invaded ecosystems (Vitousek, 1990; D’Antonio and Kark, 2002; Vilà et al., 2011). Moreover, invasions are considered one of the main causes of species extinctions (Clavero and García-Berthou, 2005). Understanding the mechanism of invasion can help control biological invasions and is also beneficial to biodiversity conservation. Some biotic and abiotic factors influence the susceptibility of a community to invasion; however, the relationships between these factors and the invasibility of a community have not been fully confirmed. In addition, identifying the factors most closely associated with the susceptibility of a community to invasion has rarely been investigated.

Communities with high biodiversity are considered more capable of resisting invasions (Elton, 1958; Kennedy et al., 2002) because more species produce stronger competition pressure and more fully occupy the available niche space, thereby limiting the opportunities for additional species to establish and survive (Elton, 1958; Levine and D’Antonio, 1999; Shea and Chesson, 2002). Previous studies have found the existence of negative correlations between native species richness and invasive richness at fine scales (n class="Chemical">Naeem et al., 2000; Kenpan>nedy et al., 2002; Gilbert anpan>d Lechowicz, 2005). Inpan> conpan>trast, rich native areas support manpan>y more invasive species thanpan> areas with relatively few native species at the lanpan>dscape or regionpan>al scales (Lonpan>sdale, 1999; Fridley et al., 2007). Habitat heterogenpan>eity or the spatial variability of resources or conpan>ditionpan>s at large scales promotes the coexistenpan>ce of native anpan>d exotic species. Moreover, sites with favorable growing conpan>ditionpan>s genpan>erate high richnpan>ess in both native anpan>d exotic species (Stohlgrenpan> et al., 2006; Fridley et al., 2007). Previous studies have also reported that native anpan>d exotic species richnpan>ess values are positively related at both the local anpan>d the lanpan>dscape scales (Davies et al., 2007; Souza et al., 2011), although no relationpan>ship betweenpan> native anpan>d invasive species richnpan>ess has beenpan> founpan>d (Capers et al., 2007).

Resource availability is a key factor that determines the susceptibility of a community to invasion by exotic species. The fluctuating resources hypothesis states that a plant community becomes more susceptible to invasion whenever there is an increase in the amount of unused resources (Davis et al., 2000). Invasive plants can oun class="Chemical">tperform native planpan>ts inpan> resource-rich enpan>vironpan>menpan>ts (Daehler, 2003; Burnpan>s, 2004; Blumenpan>thal, 2005; Fanpan> et al., 2013). However, inpan>vasive planpan>ts canpan> exhibit greater performanpan>ce, resource-use efficienpan>cy, anpan>d phenpan>otypic plasticity thanpan> native planpan>ts inpan> resource-limited enpan>vironpan>menpan>ts (Funpan>k anpan>d Vitousek, 2007; Funpan>k, 2008; Matzek, 2011). Other elemenpan>ts of global chanpan>ge canpan> also affect the success of biological inpan>vasionpan> (Dukes anpan>d Moonpan>ey, 1999), but whether these elemenpan>ts facilitate or inpan>hibit the inpan>vasionpan> of planpan>ts still needs to be clarified. For inpan>stanpan>ce, inpan>creased atmospheric pan> class="Chemical">CO2 concentrations can positively or negatively impact invasive plants (Dukes and Mooney, 1999), and warmer climate can also have diametrically opposite effects on the potential ranges of invasive plants (Merow et al., 2017).

Freshn class="Chemical">water ecosystems are particularly vulnpan>erable to inpan>vasionpan> (Shea anpan>d Chessonpan>, 2002). Greater rates of commerce lead to high propagule pressure inpan> freshpan> class="Chemical">water ecosystems, and propagules also spread rapidly in connected water systems. Furthermore, freshwater ecosystems are one of the most severely altered ecosystems due to human activity. During the past 30 years in China, rapid urbanization, gross domestic product (GDP) increases, vast population growth, and living standard improvements have all produced domestic and industrial wastewater. Moreover, due to insufficient sewage treatment capacities, some of this wastewater is discharged without treatment directly into rivers and lakes (Shao et al., 2006; Yang and Pang, 2006; Le et al., 2010), which causes high levels of organic compounds and nutrients (nitrogen and phosphorus) in rivers and lakes and thus the organic pollution and eutrophication of many water bodies. Recently, 73% of the major lakes in China have undergone severe eutrophication, and the area of eutrophication amounts to 15,000 km2 (Jin et al., 2005; Li, 2006). Land-use and land-cover changes, environmental pollution, overexploitation, and large hydroelectric projects have severely reduced lake sizes, increased habitat fragmentation, decreased both richness and coverage of aquatic vascular plants, altered the species composition of aquatic plant communities, and reduced the population size and individual body size of some species in the freshwater ecosystems of China (Fang et al., 2006). These changes may affect the invasion of exotic aquatic plants. In this study, we investigated the relationships among native plant richness, native vegetation coverage, native vegetation biomass, water nutrition [total nitrogen (TN) and total phosphorus (TP) concentrations], pollution level [chemical oxygen demand (COD)], habitat size, latitude, and exotic plant richness, and determined the correlations among these factors in the freshwater ecosystems of China. We also identified the explanatory power of these factors for the richness of exotic plant species in communities.

Materials and Methods

Field Surveys

From June to October in 2014, 2015, and 2016, we surveyed 594 aquatic plant communities in various natural freshn class="Chemical">water ecosystems (including brackish lakes) throughout China. The survey area included northeast China, northwest China, westernpan> China, easternpan> China, northernpan> China, cenpan>tral China, southernpan> China, southwest China, Hainanpan> Islanpan>d, anpan>d Qinghai Tibet Plateau (Figure ). Inpan> high latitude anpan>d altitude regionpan>s (northeast China, northwest China, northernpan> China, Qinghai Tibet Plateau), planpan>t communpan>ities were surveyed from Junpan>e to August. Inpan> the middle anpan>d low latitude anpan>d altitude regionpan>s (easternpan> China, northernpan> China, cenpan>tral China, southernpan> China, southwest China, Hainanpan> Islanpan>d), planpan>t communpan>ities were surveyed from August to October. After selecting a communpan>ity, we first recorded the habitat informationpan>: locationpan> (GPS), habitat type (lake, river, canpan>al, marsh, ponpan>d, or reservoir), anpan>d habitat size (the width of river anpan>d canpan>al or the shortest distanpan>ce betweenpan> the two banpan>ks). We thenpan> placed 9–20 quadranpan>ts (1 m × 1 m) alonpan>g three-to-six tranpan>sects, anpan>d more quadranpan>ts anpan>d tranpan>sects were placed in large or complicated communpan>ities. Inpan> large, simple communpan>ities, the distanpan>ces betweenpan> two adjacenpan>t quadranpan>ts anpan>d tranpan>sects were large (30, 50, 100, anpan>d 200 m), whereas the distanpan>ces betweenpan> two adjacenpan>t quadranpan>ts anpan>d tranpan>sects in complicated communpan>ities were smaller (5, 10, anpan>d 20 m). Briefly, the quadranpan>ts in a communpan>ity were selected to represenpan>t the actual communpan>ity structure. For each quadranpan>t, the relative coverage of the native planpan>ts (C) was determined by visual estimationpan>, anpan>d all native planpan>ts (including emergenpan>t anpan>d submerged parts anpan>d roots) anpan>d vegetative propagules in the quadranpan>ts were collected, washed, anpan>d dried at 70°C for >48 h to determine the total biomass (M). The meanpan> relative coverage of native planpan>ts in the communpan>ity (Cn) was calculated as follows:

Geographical locations of the sampling sites (red circles show the communities in which at least one exotic plant was present and black circles show the communities that did not have exotic plants).

where i is the number of quadrants in the community.

The mean biomass of the native plants in the community (Mn) was calculated as follows:

where i is the number of quadrants in the community.

We recorded all exotic and native plants in the community, including species that were not present in the quadrants. A n class="Chemical">water sample was collected inpan> the cenpan>ter of the communpan>ity, anpan>d the Tpan> class="Chemical">N and TP concentrations as well as the COD in the water were determined with a Palintest 7500 Photometer (Palintest, United Kingdom).

Data Analyses

A total of 594 aquatic plant communities and 5583 quadrants were surveyed in various natural freshn class="Chemical">water ecosystems throughout Chinpan>a. However, onpan>ly 262 communpan>ities inpan> the mainpan> distributionpan> area of exotic planpan>ts were anpan>alyzed. We applied simple linpan>ear regressionpan>s to determinpan>e the patternpan>s of exotic planpan>t richnpan>ess alonpan>g enpan>vironpan>menpan>tal anpan>d biological gradienpan>ts, inpan>cludinpan>g the richnpan>ess, relative coverage anpan>d biomass of native planpan>ts, latitude, habitat size, anpan>d Tpan> class="Chemical">N, TP, and COD contents of the water bodies. In addition, simple linear regressions were performed among these environmental and biological factors. To identify which biotic or abiotic factors are most associated with exotic plant richness, we employed hierarchical partitioning to analyze the independent explanatory power (I) of these factors for the richness of exotic plant species. The statistical significance of each I was determined by randomizing the data matrix 100 times (Mac Nally, 2002). The results of the significance tests are expressed as Z-scores. The linear regressions were performed using SPSS 13.0 (SPSS Inc., Chicago, IL, United States). The hierarchical partitioning was performed using the hier.part package (Walsh and Mac Nally, 2013) in R v3.4.2 (R Development Core Team, 2017).

Results

There were 222 communities in which at least one exotic plant was present and 372 communities where no exotic plants were present. In the main distribution area of exotic plants (eastern China, central China, southern China, southwest China, and Hainan Island), only 40 communities did not have exotic plants. In the 262 communities in the main distribution area of exotic plants, a total of 11 exotic plant species were recorded: n class="Species">Alternanthera philoxeroides, pan> class="Species">Eichhornia crassipes, Pistia stratiotes, Myriophyllum aquaticum, Hydrocotyle vulgaris, Egeria densa, Elodea nuttallii, Cabomba caroliniana, Echinodorus sp., Nuphar sp., and Azolla filiculoides. The richness of exotic plant species in the 262 communities ranged from 0 to 4 species, and the richness of the native plant species in the 262 communities ranged from 1 to 27 species.

There was no relationship between the richness of exotic and native plant species (r = 0.074, P > 0.05) (Figure ), but the exotic plant species richness was negatively related to both the biomass (r = 0.358, P < 0.001) and the relative coverage (r = 0.401, P < 0.001) (Figures ) of native plants. The exotic plant species richness was positively related to the n class="Chemical">TP (r = 0.251, P < 0.001) (Figure ), Tpan> class="Chemical">N (r = 0.220, P < 0.001) (Figure ), and COD (r = 0.185, P < 0.005) (Figure ) of the water. Neither latitude nor habitat size impacted the exotic plant species richness (Figures ). However, latitude was negatively related to exotic plant species richness when the analysis was limited to the communities where exotic species were recorded (r = 0.151, P < 0.05).

Relationships of invasive plant richness with native plant richness (A), mean biomass of native plants (B), relative coverage of native plants (C), n class="Chemical">TP (D), Tpan> class="Chemical">N (E), COD (F), latitude (G), and habitat size (H).

Many of the factors were correlated. The native plant species richness, the relative coverage of native plants, and the biomass of native plants were positively related to each other (Table ), and the n class="Chemical">TP, Tpan> class="Chemical">N, and COD of the water were also positively related to each other (Table ). The native plant species richness, the relative coverage of native plants, and the biomass of native plants were each negatively correlated with the TP, TN, and COD (Table ). Habitat size had a negative relationship with TN, but positive relationships with native plant species richness, the relative coverage of native plants, the biomass of native plants, and latitude were observed (Table ). The relative coverage of native plants had the highest independent correlations with the exotic plant species richness, and its independent explanatory power for the richness of exotic plant species was 40.67%. The independent explanatory powers of the biomass and the richness of native plants species on the richness of exotic plant species were 23.77 and 16.90%, respectively. The influences of the water body’s nutrient level and COD on the richness of exotic plant species were weaker than the effects of native plants. The independent explanatory power of TP, TN, and COD on the richness of exotic plant species was 9.43, 3.23, and 4.74%, respectively. The independent explanatory power of latitude and habitat size on the richness of exotic plant species was the lowest, only 0.86 and 0.40%, respectively (Figure ).

Correlation coefficients (r-values) of simple regressions among n class="Chemical">TP, Tpan> class="Chemical">N, COD, richness of native plants, coverage of native plants, biomass of native plants, and habitat size.

Percent independent explanatory power (I) of biotic and abiotic factors of exotic plant richness. The Z-scores were 14.21 (native plant richness), 15.42 (native plant biomass), 31.91 (native plant coverage), 3.61 (n class="Chemical">TP), 1.72 (Tpan> class="Chemical">N), 1.92 (COD), 0.35 (latitude), and 0.14 (habitat size). ∗The Z-score is considered significant at P ≤ 0.05 (Z ≥ 1.65).

Discussion

Impacts of Native Plants on the Richness of Exotic Plant Species

There is doubt concerning which characteristics of resident plants can resist invasions. Some researchers believe that abundant native plants can reduce the susceptibility of resident communities to invasion, but this depends on the spatial scale (Fridley et al., 2007). Local or fine scales are considered at a resolution of 10 m2 or less (Fridley et al., 2007), and the community sizes in our study ranged from 50 to 100,000 m2; therefore, the scale of our study was coarse (broad). We found that native plant species richness was neither positively nor negatively correlated with exotic plant species richness. In freshn class="Chemical">water ecosystems, the likelihood of the occurrenpan>ce of some exotic planpan>ts was positively affected by macrophyte richnpan>ess, but some were negatively affected by macrophyte richnpan>ess, anpan>d some planpan>ts had no relationpan>ship with native species richnpan>ess (Thomaz et al., 2009; Thomaz anpan>d Michelanpan>, 2011; Fleming et al., 2015). Capers et al. (2007) reported that invasive species richnpan>ess at a fine scale is positively or negatively correlated with native species richnpan>ess in some lakes but that invasive species richnpan>ess in most lakes is not correlated with native species richnpan>ess. Similar to our results, these authors also reported no correlationpan> betweenpan> native anpan>d exotic species richnpan>ess at larger spatial scales. Therefore, there is no conpan>stanpan>t native species–exotic species richnpan>ess relationpan>ship onpan> either fine or large scales.

There are fewer exotic plant species in communities where biomass or relative coverage of native plants is high. Indeed, the vacant niche hypothesis, the biotic resistance hypothesis, and the resource fluctuation hypothesis all assert that a sufficient amount of resident plants can occupy all niches and sequester available resources and can thus competitively exclude invaders (Elton, 1958; Davis et al., 2000). Higher biomass and relative coverage of native plants use more space, nutrition, and light. n class="Chemical">Native species may resist inpan>vasionpan> inpan> communpan>ities onpan>ly if the denpan>sity or productivity is high (Capers et al., 2007; Davies et al., 2007). Evenpan> whenpan> the productivity of communpan>ities is low, more native species will accompanpan>y more exotic species (Davies et al., 2007). A previous study founpan>d that the denpan>sities anpan>d growth rates of native macrophytes play evenpan> more importanpan>t roles inpan> decreasinpan>g the inpan>vasibility of pan> class="Species">Urochloa arrecta than does native species richness (Michelan et al., 2013). Therefore, our results suggested that the abundance and biomass of native plant communities are more resistant to invaders than the richness of native plant species. However, biodiversity conservation is still a realistic and significant method for controlling invasive plants. Whether in an ecosystem or a plant community, higher species richness can increase the productivity and total cover of plants (Tilman et al., 1997; Waide et al., 1999; Balvanera et al., 2006). Higher plant species richness can utilize the spatial and temporal niches adequately, which results in higher functional diversity and can contribute to the higher productivity of the ecosystem (Tilman et al., 1997). In our study, both the relative coverage and the biomass of native plants were positively related to plant species richness, which suggests that plant species richness may affect invasive plants by altering ecosystem processes.

Impacts of Eutrophication and Pollution on the Richness of Exotic Plants

The fluctuating resource hypothesis states that a plant community becomes more susceptible to invasion when the amount of unused resources increases (Davis et al., 2000). Increased nutrition will produce new niches and cause more exotic plants to invade communities. The competitive ability and fitness of exotic plants are promoted in a higher nutrient environment; therefore, increased nutrition could promote the probability of invasion success by exotic aquatic plants. The relative growth rates, photosynthetic rates, leaf n class="Chemical">nitrogen conpan>tenpan>ts, anpan>d photosynpan>thetic pan> class="Chemical">nitrogen-use efficiencies of aquatic exotic plants increase more intensively with increasing nutrients than do those of native species (Xie et al., 2010; Fan et al., 2013). Compared with native species, exotic aquatic plants exhibited improved reproductive rates and survival rates under conditions of high nutrient availability (Xie et al., 2010), and in warm temperate zones, eutrophication in water increased the overwintering survival rate of the aquatic invasive plant E. crassipes (Dong and Fan, unpublished data). In addition, enemy release favors exotics over natives in high-resource environments (Blumenthal, 2005, 2006).

Excessive increases in nutrients and sewage discharge also constitute a type of disturbance that markedly alters the species composition and often decreases the biological diversity in aquatic ecosystems (Balls et al., 1989; Hough et al., 1989; Hautier et al., 2009). n class="Chemical">Water eutrophicationpan> canpan> lead to the rapid productionpan> of phytoplanpan>ktonpan> anpan>d other micro-organpan>isms; denpan>se phytoplanpan>ktonpan> populationpan>s kill the submerged planpan>ts by competinpan>g with submerged planpan>ts for ecological resources, such as nutrienpan>ts, light, pan> class="Chemical">oxygen, and living space (Balls et al., 1989; Le et al., 2010). Our study found that increased TN, TP, and COD were all associated with reduced richness, biomass, or relative coverage of the native plant communities; therefore, water pollution and eutrophication can reduce the resistance of resident communities to invaders, likely favoring invaders directly. In addition, eutrophication is the consequence of human activities (Carpenter et al., 1998). Frequent human activities bring greater propagule pressure, leading to the invasion of resident communities by more exotic species (Vitousek et al., 1997; Lockwood et al., 2005).

Impacts of Habitat Size on the Richness of Exotic Plants

Larger areas have more native and invasive species (Lonsdale, 1999) because of their higher spatial heterogeneity. In our study, the number of native species increased with an increase in habitat size, but there was no relationship between exotic species richness and habitat size. In our study, some plants, such as n class="Species">A. philoxeroides, pan> class="Species">M. aquaticum, E. crassipes, and P. stratiotes, have consistent life forms, morphologies, and niches. Higher morphological plasticity enables invasive plants to live in a variety of environments (Richards et al., 2006; Davidson et al., 2011). Therefore, some exotic aquatic plants can coexist in small habitats. We also found that habitat size had positive relationships with richness, relative coverage, and biomass of native plants but were negatively correlated with TN in the water. This result suggested that large habitats are more tolerant to disturbance than small habitats.

Native Plant Species Are More Likely to Predict the Richness of Exotic Plant Species Than Other Factors

The identification of which factors are of greatest importance for predicting the invasion of exotic plants can help us prevent exotic species invasion and minimize their impacts (Gosper et al., 2015). Souza et al. (2011) found that native species richness rather than abiotic predictors (road density, soil moisture, and light availability) accounted for most of the variation in exotic plant richness at the landscape scale. However, at the local scale, native plant richness, light availability, road density, field density, and soil clay accounted for similar amounts of variation in exotic plant species richness. Another study also found that the independent explanatory powers of 12 predictors of the presence of alien species were similar (Gosper et al., 2015). Our study found that the independent explanatory power of native plant coverage of the exotic plant species richness was highest. Overall, biotic predictors (richness, coverage, and biomass of native plants) rather than abiotic predictors (Tn class="Chemical">N, pan> class="Chemical">TP, and COD in water, latitude, and habitat size) accounted for more of the variation in exotic plant species richness, consistent with the results of Souza et al. (2011). Our study implied that improving the vegetation coverage and biodiversity is the most effective approach for preventing alien plant invasions and minimizing their impacts in freshwater ecosystems. The reduction of industrial and domestic wastewater discharge and hydroelectric projects, the prohibition of aquaculture, sand excavation and mining, wetland and lake corrosion, the improvement of environmental awareness, and ecological restoration will improve the vegetation coverage (Fang et al., 2006; Xu et al., 2006).

Although the coverage of native plants is the most significant factor influencing richness of exotic plant species in communities, the factors for different exotic aquatic plants were different. Increases in the n class="Chemical">water pan> class="Chemical">N and P concentrations were the main reason for the successful colonization of free-floating exotic plants, whereas richer nutrients in sediments enhance the chances of colonization and successful invasion of rooted macrophytes (Thomaz et al., 2015). Even though E. crassipes, P. stratiotes, and Salvinia molesta are all free-floating exotic plants, their response to the rise in nutrition was different (Henry-Silva et al., 2008). Warming can increase the survival percentage, regrowth, and clonal propagation of E. crassipes (You et al., 2013), but it did not influence the abundance or growth rate of E. nuttallii (Mckee et al., 2002). Aquatic vegetation loss and eutrophication in global freshwater ecosystems is becoming increasingly serious. In future research, we plan to focus on the establishment and colonization mechanisms of exotic aquatic plants in an environment of increasing nutrition and on investigating the synergistic effects of eutrophication and vegetation loss on aquatic plant invasion.

Conclusion

Researchers pay substantial attention to studying the relationships between native and exotic species richness to assess the susceptibility of resident communities to invasion. However, our study found that the richness of native plant species cannot directly predict the number of exotic plant species in aquatic plant communities. n class="Chemical">Native aquatic pan> class="Disease">vegetation loss, eutrophication, and water pollution are important factors that cause the invasion of exotic aquatic plants in freshwater ecosystems in China. China is still a developing country, and its freshwater ecosystems are under substantial strain. Strengthening the protection and restoration of fragile freshwater ecosystems is beneficial to controlling invasive species and conserving the native biodiversity.

Author Contributions

SF and CL designed and executed the research project. HY, SF, and LW collected the field data. HY led the reflectance data analysis and drafted the manuscript with the assistance of SF. All the co-authors commented on and approved the final manuscript.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Table 1

Correlation coefficients (r-values) of simple regressions among TP, TN, COD, richness of native plants, coverage of native plants, biomass of native plants, and habitat size.

	TP	TN	COD	Richness of	Coverage of	Biomass of
				native plants	native plants	native plants
TN	0.683***
COD	0.245***	0.336***
Richness of native plants	-0.149*	-0.177*	-0.207***
Coverage of native plants	-0.147*	-0.136*	-0.307***	0.410***
Biomass of native plants	-0.206***	-0.126*	-0.218***	0.303***	0.650***
Habitat size	-0.088	-0.125*	0.035	0.160**	0.177**	0.213***