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All issues No 422 (2021) Knowl. Manag. Aquat. Ecosyst., 422 (2021) 11 Full HTML
Open Access
Issue
Knowl. Manag. Aquat. Ecosyst.
Number 422, 2021
Article Number 11
Number of page(s) 8
DOI https://doi.org/10.1051/kmae/2021012
Published online 18 March 2021

© X. Huang et al., Published by EDP Sciences 2021

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (https://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

1 Introduction

With the development of economic globalisation, exchanges among different countries and regions have become more frequent, and an increasing number of introduced species have been intentionally or unintentionally brought into new areas (Xu et al., 2006; Hussner et al., 2017; Wu and Ding, 2019). Successful invasive species constitute a minority of introduced species (Nentwig, 2008). However, they have resulted in reduced abundance and diversity of native species in invaded natural habitats and cause harm to human society (Lowe et al., 2000; Goodenough, 2010; Vilà et al., 2011; Reshi et al., 2013). Invasive aquatic plants are strong competitors (Lacoul and Freedman, 2006). The successful invasion of an invasive species depends on its specific traits (for instance, functional traits), and successful invaders may have advantageous traits over native species. This thought dates back to The Genetics of Colonizing Species by Baker, who is a pioneer in invasion biology (Baker and Stebbins, 1965). Invasive species, normally prone to exhibiting advantageous functional traits over native species, can change the native plant structure and reduce diversity via out competing these plants and/or interfering in competition to exclude native species in biological communities (Hamilton et al., 2005; van Kleunen et al., 2010a; Caplan and Yeakley, 2013; Mathakutha et al., 2019). van Kleunen et al. (2010b) also showed that invasive plant species have significantly higher trait values than non-invasive species in a meta-analysis study. In freshwater ecosystems, invasive aquatic plants cause the extinction of native aquatic plants, loss of fish abundance and reduction of benthos, which significantly change freshwater ecosystems (Gallardo et al., 2016; Michelan et al., 2018; Wu and Ding, 2019). Nearly 24% of the plants listed in the 100 of the World's Worst Invasive Alien Species by the International Union for Conservation of Nature (IUCN) were aquatic plants, which is disproportionate to the area of freshwater habitats (less than 6%) on the earth (Zedler and Kercher, 2004).

By the end of 2016, more than 600 invasive species had been found in China, including nearly 50 of the species identified in the above list (Zhan et al., 2017). The flourishing breeding industries for red swamp crayfishes (Procambarus clarkia) and hairy crabs (Eriocheir sinensis) have introduced a large number of highly palatable plants, many of which are invasive (Jiang et al., 2011). Additionally, with the increasing prosperity of the aquarium market, a variety of ornamental aquatic plants have been introduced into China (Wang et al., 2016; Yu et al., 2018). Among these, the invasive plant Carolina fanwort (Cabomba caroliniana) has been a dominant submerged plant in some areas of the Lake Taihu basin (LTB) (Huang et al., 2020). This plant has only recently been included in the List of Invasive Species in China (Ministry of Ecology and Environment (MEE), 2016). Before being listed, it was widely used as a garden wetland plant in ecological restoration, especially in the area downstream of the LTB. Its invasiveness has gained considerable attention; however, it seems there is no conclusion regarding how this invasive plant is successfully invading China.

To our knowledge, no previous competitiveness comparisons have been conducted among C. caroliniana and co-occurring native plants. In this study, the morphological traits (total dry mass, shoot/root (S/R) ratio, relative growth rate (RGR) and competitive ability index log response ratio (ln RR)) of C. caroliniana and two co-occurring species (water thyme (Hydrilla verticillata) and Eurasian watermilfoil (Myriophyllum spicatum)), were evaluated in a mesocosm experiment. As competition will hamper the biomass and growth of plants, comparisons of these associated traits will reflect the relationship among plants (Grotkopp et al., 2002; Wang et al., 2008b; Dawson et al., 2012; Shen et al., 2019). Two questions were posed: (1) Does C. caroliniana have more advantageous traits than native species? (2) Can C. caroliniana out compete native counterparts within the invaded area?

2 Materials and methods

2.1 Study area

The mesocosm experiment was conducted in the Taihu Laboratory for Lake Ecosystem Research (TLLER) (31.4198°N, 120.2159°E), which is one of the national field stations of the Chinese National Ecosystem Research Network (CNERN) in Wuxi City, Jiangsu Province. Downstream of the Yangtze River, the LTB is one of the most prosperous areas in China. It contains 1/22 of the total population but contributed nearly 1/10 of the gross domestic product (GDP) of China in 2018 (Taihu Basin Authority (TBA), 2019).

2.2 Plant materials

Three commonly co-occurring submerged plants in the LTB, the native H. verticillata, M. spicatum, and the invasive C. caroliniana, were used in this study. Before the experiment began, we conducted an aquatic plant field reconnaissance investigation in the LTB. Sampling quadrats with an area of 1 × 1 m2 were randomly selected. The plant coverage was calculated as the species coverage/all species coverage ratio in a sampling quadrat. The results showed that within 1 × 1 m2 mature mono-species community quadrats, when the plant coverage was 95% (in freshwater ecosystems, it is rare for plants to show 100% coverage, as gaps among species always exist), the average density of H. verticillata was 42/m2 (estimated density was 44/m2 for 100% coverage), the average density of M. spicatum was 32/m2 (estimated density was 34 for 100% coverage), and the average density of C. caroliniana was 35/m2 (estimated density was 37/m2 for 100% coverage). The same plant density was used as high-density treatment (H2M2C2) accordingly to the experiment bucket (basal area = 0.16 m2 and h = 0.76 m) in the experiment (Tab. 1). Half of the high densities were used as medium-density treatment (HIM1C1) (Tab. 1). In the mono-species treatments (H1, M1 and C1), one shoot of each species was cultivated individually, and for low-density treatment, one shoot of these species was cultivated together (Tab. 1).

Table 1

Plant density calculation for the mesocosm experiment.

2.3 Experimental design

Young shoots of the three species were collected and cultivated at the TLLER for one month. The experiment began on June 20th, 2018. Two factors were set in the experiment: the plant species and density. At the beginning of the experiment, 20 cm of lake sediment from the Lake Taihu was collected, mixed, and then added to each bucket. The lake water was filtered with a sieve and then poured into the buckets to 40 cm (measured from the bottom of the bucket). The lake water parameters were total dissolved nitrogen (TDN) = 0.71 ± 0.11, total dissolved phosphorus (TDP) = 0.052 ± 0.007, dissolved oxygen (DO) = 4.26 ± 0.67 mg/L, conductivity = 395 ± 46 µS/cm and pH = 7.93 ± 1.6 (mean ±S.D.) during the experimental period. The TDN and TDP were measured once aweek, and the other parameters were measured twice a week. Young shoots measuring 20–25 cm from the three species were selected and planted in the buckets (Tab. 1). Each treatment had five replicates (n = 5), and 40 buckets were used. After one week, all the plants survived, and appeared to have acclimated to the new environment (Li et al., 2015; Li et al., 2016; Huang et al., 2018). The water level in each bucket was then increased to 75 cm (measured from the bottom of the bucket). The plants were harvested when flower buds of M. spicatum and H. verticillata appeared, which indicated that they had reached the end of vegetative growth on August 4th, 2018.

The plant shoot/root (S/R) biomass ratio was calculated as follows:

S/R ratio = shoot biomass/root biomass;

The relative growth rate (RGR) was calculated as follows (Gillard et al., 2017):

RGR (mg · g−1 · d−1) = (lnr2 − lnr1)/(t2 − t1);

where r1 is the initial dry plant biomass at initial time t1 ; and r2 is the dry plant biomass at harvest time t2 . In this study, t2 − t1 = 45 d.

The competition index log response ratio (ln RR) was calculated as follows (Goldberg et al., 1999; Hedges et al., 1999; Weigelt and Jolliffe, 2003):

ln RR = ln (rmono/rmix)

where rmono represents the total dry mass of a single plant in a bucket (in the absence of competition, namely, H1, M1 and M1 in this study) and rmix represents the average total dry mass of a plant in a bucket containing more than one plant. A higher ln RR indicates more intraspecific and/or interspecific competition intensity.

2.4 Data analysis

A two-way ANOVA was applied with plant species and density as the primary factors to test their effects on plant traits in the competition experiment. When a significant treatment effect was detected, post hoc pairwise comparisons of the means were performed to examine the differences between treatments using Duncan's multiple range test for multiple comparisons.

3 Results

The three species, H. verticillata, M. spicatum, and C. caroliniana, exhibited significant differences (P< 0.05) in the plant total dry mass, S/R ratio, RGR and ln RR, which indicates the occurrence of significant differences among these plant species (Tab. 2). The plant density had a significant influence (P< 0.05) on all the plant trait values except for the S/R ratio (Tab. 2), and the interaction between the plant species and density was significant for all the measured plant trait values except for the total dry mass (Tab. 2).

Table 2

Two-way ANOVA results regarding the plant species and density for the plant total biomass, shoot/root (S/R) ratio, relative growth rate (RGR), and competition index ln RR during the experiment.

3.1 Morphological traits

The native plant M. spicatum showed a relatively higher total dry mass in the mono-species treatment M1 and low-density treatment H1M1C1 compared with the other treatments. The total dry mass for the native plant H.verticillata did not show significant differences, but a decreasingtrend was detected for the invasive plant C. caroliniana (Fig. 1).

The highest S/R ratio was obtained for the no competition treatment C1, namely, the treatment that involves one C. caroliniana plant, and it decreased with an increase in the plant density (Fig. 2). Conversely, the S/R ratio increased with an increase in plant density for H. verticillata, and M. spicatum showed a relatively stable fluctuation (Fig. 2).

Myriophyllum spicatum had the highest RGR among all the treatments, followed by H. verticillata, while C. caroliniana showed a decreasing trend with increasing plant density (Fig. 3).

thumbnail Fig. 1

The plant trait total dry mass of different treatments of Hydrilla verticillata, Myriophyllum spicatum, and Cabomba caroliniana in the experiment. The values are the means ± SE. Different lowercase letters indicate significant differences among treatments.
thumbnail Fig. 2

The Plant trait shoot/root (S/R) ratio of different treatments of Hydrilla verticillata, Myriophyllum spicatum, and Cabomba caroliniana in the experiment. The values are the means ± SE. Different lowercase letters indicate significant differences among treatments.
thumbnail Fig. 3

The plant trait relative growth rate (RGR) of different treatments of Hydrilla verticillata, Myriophyllum spicatum, and Cabomba caroliniana in the experiment. The values are means ± SE. Different lowercase letters indicate significant differences among treatments.

3.2 Competition intensity

The competition intensity, as measured by the competition index ln RR, showed a similar trend among the three plant species (Fig. 4). Cabomba caroliniana, as well as the other two plant species had the highest value for the high-density treatment H2M2C2, followed by the medium-density treatments M2C2 and H2C2, while the value for the low-density treatment H1M1C1 was the lowest (Fig. 4).

thumbnail Fig. 4

The plant trait competition index log response ratio (ln RR) of different treatments of Hydrilla verticillata, Myriophyllum spicatum, and Cabomba caroliniana in the experiment. The values are the means ± SE. Different lowercase letters indicate significant differences among treatments.

4 Discussion

4.1 The successful invasion of C. caroliniana may not be caused by outcompeting native species

In this study, we found that invasive C. caroliniana did not show more advantageous traits or a lower competition index than those of the native H. verticillata or M. spicatum of the same life-form. The three submerged species can coexist at low density, but high density will lead to competition and result in the inhibition of C. caroliniana. This result contradicted previous findings showing that invasive species had more advantageous traits or a higher competitive ability than native species.

As primary producers, biomass accumulation is perhaps the most important manifestation of biological vegetative growth of aquatic plants (Fan et al., 2015; Dalla Vecchia et al., 2020). In this study, C. caroliniana did not show a higher total dry mass and a decreasing trend when the density of its native counterparts M. spicatum or H. verticillata increased, which indicates that the plant may not win competition by showing high biomass production.Biomass allocation is an adaptive strategy developed by plants in response to ecological factors (Barrat-Segretain, 2001; Wang et al., 2008b). Although C. caroliniana have the highest S/R ratio in mono-species treatment C1 (Fig. 2), it shows a decreasing trend when plant density increases, which may indicate that the shoot growth of the plant is suppressed by the two other species while the root is less affected.

Competition is the most common negative interaction among different plants; it is a mutual relationship between two or more plants when the required environmental resources or space are relatively insufficient (Goldberg et al., 1999). Some plants are more efficient in obtaining resources or can occupy more space, thus limiting the survival of other plants (Weigelt and Jolliffe, 2003). Normally, invasive plants are believed to have a higher RGR (Richards et al., 2006; Dawson et al., 2011). A recent study also showed that intrinsic growth rates (similar to RGR) are more important than competitive ability, as introduced plants were shown to have higher intrinsic growth rates than those of native plants (Zhang and van Kleunen, 2019). However, we did not record this tendency in C. caroliniana (Fig. 4). The less advantageous traits of C. caroliniana may indicate that the successful invasion of this plant was not supported by directly outcompeting native plants. This result emphasised its weak competitive ability in invaded habitats, which indicates that other factors, biotic or abiotic factors, affecting the successful invasion of this species should be considered.

4.2 Implications for the control of invasive submerged plants

Submerged plants are probably the most important group of aquatic plants, as they provide the fundamental functions and structures of freshwater ecosystems (Scheffer, 2004; Lacoul and Freedman, 2006). As C. caroliniana has been a successful invader in China, it has caused serious and widespread effects (Liu et al., 2018). It seems that no successful removal measures have been identified for the plant, and the only proven successful method is manual removal; during this process, the plant is easily broken into fragments and washed away with the water flow (Fig. 5). Under certain conditions, new populations can be colonized, which may lead to new populations (Ørgaard, 1991; Schooler et al., 2006; Jacobs and Macisaac, 2009; Lima et al., 2014; Bickel, 2015, 2017; Scheers et al., 2019). A realistic and feasible control method for this plant seems difficult.

Myriophyllum spicatum is the most studied aquatic plant species in the scientific literature (Dalla Vecchia et al., 2020). It is a native plant in China but an invasive plant in other countries, especially North America (Gassmann et al., 2006; Li et al., 2016; Hussner et al., 2017; Smith et al., 2021). A large ecological amplitude,low palatability, high nutrient-capturing ability and diverse mechanisms of propagation (seed, rhizome production, and stem segment) enable colonization by this species (Wang et al., 2008a; Bosch et al., 2009; Li et al., 2015; Yu et al., 2016; Son et al., 2017). In this study, we showed that M. spicatum has relatively higher values for certain traits and competitive abilities than C. caroliniana which may indicate that it is an already quite aggressive species. Other traits of this species and their responses to environmental factors, as well as those of other plant species and herbivores remain to be investigated.

Hydrilla verticillata is native to Asia and is a successful invasive submerged plant throughout the world (Bellinger and Davis, 2017). This plant is adapted to various environmental conditions and has a unique C4 photosynthesis mechanism and a broad ecological amplitude, which causes the suppression of the native aquatic plant community (Bowes et al., 2002; Sousa, 2011). It has been attempted but found to be ineffective as a biological control method for C. caroliniana (Schooler et al., 2012). Thus, conducting common-garden experiments with the three plants in invaded and non-invaded areas may be helpful for understandingthe invasion and control of these plants.

thumbnail Fig. 5

The manual removal of Cabomba caroliniana in a river channel (31.4224°N, 120.2165°E) near TLLER in the Lake Taihu Basin. The removal process can produce plant stem fragments (image in the top left corner). Both photographs were taken by the first author.

5 Conclusions

In this study, we conducted a mesocosm experiment to evaluate the morphological traits and competitive ability of the invasive plant C. caroliniana and two of its commonly co-occurring native submerged plants H. verticillata and M. spicatum. In total, C. carolinianadid not show more advantageous traits. Thus, we provide a counterexample in which the successful invasion of a submerged species may not be explained by successful competition over native plants. Other biotic or abiotic factors should be explored to explain the widespread distribution of this invasive species.

Acknowledgments

The authors acknowledge funding support from the National Science Foundation of China (NSFC) (31930074 and 32001157), the Science and Technology Service Network Initiative (KFJ-STS-QYZD-156) of the Chinese Academy of Sciences (CAS), and National Science and Technology Fundamental Resources Investigation Program of China (2019FY100600).

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Cite this article as: Huang X, Yu J, Liu S, Xie H, He H, Li K. 2021. Plant morphological traits and competition index comparisons of three invasive and native submerged plants. Knowl. Manag. Aquat. Ecosyst., 422, 11.

All Tables

Table 1

Plant density calculation for the mesocosm experiment.

In the text
Table 2

Two-way ANOVA results regarding the plant species and density for the plant total biomass, shoot/root (S/R) ratio, relative growth rate (RGR), and competition index ln RR during the experiment.

In the text

All Figures

thumbnail Fig. 1

The plant trait total dry mass of different treatments of Hydrilla verticillata, Myriophyllum spicatum, and Cabomba caroliniana in the experiment. The values are the means ± SE. Different lowercase letters indicate significant differences among treatments.
In the text
thumbnail Fig. 2

The Plant trait shoot/root (S/R) ratio of different treatments of Hydrilla verticillata, Myriophyllum spicatum, and Cabomba caroliniana in the experiment. The values are the means ± SE. Different lowercase letters indicate significant differences among treatments.
In the text
thumbnail Fig. 3

The plant trait relative growth rate (RGR) of different treatments of Hydrilla verticillata, Myriophyllum spicatum, and Cabomba caroliniana in the experiment. The values are means ± SE. Different lowercase letters indicate significant differences among treatments.
In the text
thumbnail Fig. 4

The plant trait competition index log response ratio (ln RR) of different treatments of Hydrilla verticillata, Myriophyllum spicatum, and Cabomba caroliniana in the experiment. The values are the means ± SE. Different lowercase letters indicate significant differences among treatments.
In the text
thumbnail Fig. 5

The manual removal of Cabomba caroliniana in a river channel (31.4224°N, 120.2165°E) near TLLER in the Lake Taihu Basin. The removal process can produce plant stem fragments (image in the top left corner). Both photographs were taken by the first author.
In the text

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