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Mowing plus shading as an effective method to control the invasive plant Spartina alterniflora
Flora 257 (2019) 151408
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Mowing plus shading as an effective method to control the invasive plant Spartina alterniflora
T
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Caiyun Zhao, Junsheng Li , Xiangjian Zhao Chinese Research Academy of Environmental Sciences, Beijing, 100012, China
A R T I C LE I N FO
A B S T R A C T
Edited by Fei-Hai Yu
Plant invasions greatly threaten native biodiversity and ecosystem health, and measures to effectively control and eradicate invasive plants are urgently needed. Spartina alterniflora has invaded large areas of coastal China as well as many other countries, and caused tremendous ecological and economic problems. To develop measures for effectively controlling the invasion of this species, a field experiment was conducted to test the effectiveness of two methods, i.e. mowing alone, and mowing + shading, on suppressing the growth and reproduction of S. alterniflora, with no shading and mowing as the control. The treatments were applied at five different times, i.e. in May, July, August, October, and November of 2013, and measurements were done at the end of the growing season in both 2013 and 2014. Overall, mowing alone could not effectively suppress S. alterniflora at the end of the second growing season (in 2014); instead, this method promoted both the sexual and asexual reproduction of this invasive plant. The mowing + shading treatment, however, highly effectively suppressed the growth and reproduction of S. alterniflora, and no asexual individuals (ramets) or seedlings were observed at the end of the second growing season. The effectiveness of both methods for controlling S. alterniflora was independent of the timing of the treatments in the long term. We propose the use of mowing + shading to effectively eradicate S. alterniflora in China and possibly also in other counties in future, and the selection of the timing for the treatment according to the cost and convenience.
Keywords: Invasion control Invasive plant Physical control Mowing alone Smooth cord-grass Treatment timing
1. Introduction Plant invasions are considered a global problem and have produced tremendous economic and ecological impacts (Theoharides and Dukes, 2007; Naidoo and Naidoo, 2018; Paolacci et al., 2018; Wang et al., 2017; Chen et al., 2019). In the past, scientists and managers have proposed different measures to control the spread of invasive plants (Hedge et al., 2003; Yuan et al., 2011; Hussner et al., 2017; Byun et al., 2018). While some measures are effective for controlling a particular invasive plant, they may not useful for others as many measures are species-specific (Grevstad et al., 2003). Thus, more measures need to be evaluated in order to effectively control the invasion of some invasive plants (Jardine and Sanchirico, 2018). Spartina alterniflora Loisel. (Poaceae) is native in the Atlantic and Gulf coasts of the United States (Simenstad and Thom, 1995). This species has been introduced into many estuarine regions around the world as it can reduce tidal wave energy, mitigate erosion and trap sediments (Balletto et al., 2005; Weishar et al., 2005). Since its introduction, S. alterniflora has successfully invaded coastal saltmarsh worldwide, and has produced tremendous negative impacts on native
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ecosystems (An et al., 2007; Ainouche and Gray, 2016). This species is now listed as one of the most problematic invasive plants in the world (Weber, 2003; Li et al., 2009). Spartina alterniflora was introduced in China in 1979 (Chung, 1993; Deng et al., 2006). Since then, it has rapidly spread with an annual expansion rate of 20.4% (Zhang et al., 2017), and has occupied almost all coastal areas of China (Zhao et al., 2015a,b,c; Zhang et al., 2017). Many studies have showed that S. alterniflora could outcompete native species such as Phragmites australis (Li et al., 2009), Scirpus mariqueter (Chen et al., 2004, 2005a), and mangroves (Zhang et al., 2018). Moreover, the invasion by S. alterniflora has greatly altered the community composition and species diversity of macro-invertebrates (Chen et al., 2005b; Wang et al., 2010, 2014; Zhao et al., 2014a, 2014b, Zhao et al., 2015a,b,c). In 2003, S. alterniflora was listed as one of the 16 most invasive species in China because of its negative effects (Chen et al., 2004; An et al., 2007). Many measures have been proposed to control S. alterniflora, including chemical controls (Kilbride et al., 1995; Liu et al., 2004), biological controls (Wu et al., 1999; Grevstadet al., 2003) and physical controls (Frid et al., 1999). Herbicides have been used to suppress the
Corresponding author. E-mail address: [email protected] (J. Li).
https://doi.org/10.1016/j.flora.2019.05.007 Received 28 February 2019; Received in revised form 17 May 2019; Accepted 23 May 2019 Available online 28 May 2019 0367-2530/ © 2019 Elsevier GmbH. All rights reserved.
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Fig. 1. The location of the study site (Qingshantou) and the experimental layout. The treatments were applied in May, July, August, October and November 2013, respectively. M represents mowing Spartina alterniflora alone, MS represents mowing plus shading S. alterniflora, and C represent the control (no mowing or shading).
whether the timing of the treatments played a role. Therefore, we conducted a field experiment in southern China, and applied the treatments of mowing alone and mowing + shading on S. alterniflora at five different times (in May, July, August, October, and November in 2013), with no mowing and shading as the control. We aim at addressing the following questions. (1) Can mowing + shading effectively suppress the growth and reproduction of S. alterniflora? (2) Is this method more effective at controlling S. alterniflora than mowing alone? (3) Does the timing of the treatments influence the effectiveness on controlling S. alterniflora?
aboveground growth of S. alterniflora (Liu et al., 2004). However, herbicides have not been widely used in field applications due to their potential impacts on native species. In Qi’ao Island, China, the use of Sonneratia apetala as an alternative plant species to replace S. alterniflora was shown to be effective (Tang et al., 2007). An introduced insect, Prokelisia marginata, was also released to suppress the growth of S. alterniflora in Willapa Bay, Washington, U.S. (Grevstad et al., 2003). However, it was argued that such intentionally introduced exotic species may lead to a potential issue of new invasion (Li and Zhang, 2008). Physical methods, including clipping/mowing, burning, pruning, excavating, dredging, flooding/draining and reaping young ramets, were previously used to control this species (Hedge et al., 2003). The mowing method was demonstrated to be more efficient than other physical methods (Hedge et al., 2003; Li and Zhang, 2008). Studies have shown that repeated mowing may effectively suppress the growth of S. alterniflora, but mowing alone may not (Hedge et al., 2003; Wang et al., 2006; Simmons et al., 2007). However, repeated mowing requires a large investment of human resources, which is not cost-effective and thus difficult to be supported by local governments. Shading alone could effectively suppress the growth of S. alterniflora if the degree of shading is high (Gu et al., 2010), but this method is difficult to apply in the field as this species can be very tall (up to 1.92 m; Zhao et al., 2015a,b,c) and shading material (e.g. shading nets) can be easily moved away by tides. Combined measures have been proposed (Hammond and Cooper, 2002; Major et al., 2003; Li and Zhang, 2008), including the method of mowing + waterlogging, which was demonstrated to be able to successfully eradicate this plant (Yuan et al., 2011). However, the establishment of the waterlogging regime is costly. Thus, a simple, effective method to control S. alterniflora is still lacking. In this study, we tested the effect of another combined measure, i.e., mowing + shading, on the effectiveness of controlling S. alterniflora, and compared it with the effect of mowing alone. We also tested
2. Methods and materials 2.1. Study site This study was conducted at Qingshantou (21°28′N, 109°47′E) in the Beihai Estuary, Beibu Gulf in Guangxi Province, China. This region is also one of the most concentrated distribution areas for mangroves in China (Wu et al., 2013). Spartina alerniflora was first introduced to the area in 1979 for the purpose of reducing tidal waves (Tan et al., 2010). Since then, this invasive plant has rapidly spread along the coastline of the Beihai estuary, forming a mono-dominant community. It competes with Kandelia candel which is an important mangrove species native to this region. The average height of S. alterniflora is 93.3 cm and the average density is 255 ramets m−2 (Zhao et al., 2015a,b,c). The mean annual precipitation is 1500–1700 mm, and the mean temperature is 23.4 °C. Tidal fluctuation in this area is irregular. Diurnal tides occur in 60% of the days within a year and semi-diurnal tides occur in the remaining 40% of the days, with an average tidal height of 2.31–2.59 m. The salinity of the seawater is 20‰–23‰, and pH is 7.60–7.80 (Zhao et al., 2015a,b,c). 2
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Table 1 Two-way ANOVA of the effects of the control method (mowing vs. mowing + shading) and the initial treatment time on the control efficiency on Spartina alterniflora at the end of the 1st growing season and at the beginning and end of the 2nd growing season after treatments. (A) At the end of the 1st growing season
(B) At the beginning of the 2nd growing season
(C) At the end of the 2nd growing season
Effect
df
P
df
F
P
df
F
P
Control efficiency Control method Treatment time Interaction
based on ramet density 1 728.3 3 130.7 3 181.1
< 0.001 < 0.001 < 0.001
1 4 4
984.2 1.5 2.1
< 0.001 0.197 0.085
1 4 4
750.1 4.2 4.2
< 0.001 0.004 0.004
Control efficiency Control method Treatment time Interaction
based on ramet height 1 2759.2 3 428.7 3 883.3
< 0.001 < 0.001 < 0.001
1 4 4
326.9 0.3 0.9
< 0.001 0.854 0.468
1 4 4
759.5 3.9 3.9
< 0.001 0.006 0.006
Control efficiency Control method Treatment time Interaction
based on aboveground biomass 1 1032.9 < 0.001 3 25.6 < 0.001 3 190.7 < 0.001
1 4 4
904.5 0.5 1.6
< 0.001 0.715 0.179
1 4 4
667.5 3.2 3.2
< 0.001 0.017 0.017
Control efficiency Control method Treatment time Interaction
based on seedling density 1 594.7 < 0.001 3 54.7 < 0.001 3 82.4 < 0.001
1 4 4
1139.3 0.6 0.6
< 0.001 0.653 0.653
1 4 4
675.6 3.5 3.5
< 0.001 0.011 0.011
Control efficiency Control method Treatment time Interaction
based on flowering ramet density 1 225.1 < 0.001 3 67.7 < 0.001 3 67.7 < 0.001
– –
– – –
– – –
1 4 4
363.5 1.4 1.4
< 0.001 0.232 0.232
F
–
Degree of freedom for the error term is 64 at the end of the 1 st growing season and 80 on the 2nd growing season.
each of the performance variables, i.e. aboveground biomass, ramet density, mean ramet height, seedling density and flowering ramet density, if available. No ramet flowered at the beginning of the second growing season so that CE of flowering ramet density was not available at this harvest. A greater value of CE reflects a lower level of the control efficiency.
2.2. Experimental design The experiment consisted of three levels of controlling methods (control, mowing alone, and mowing + shading) and five levels of initial treatment time (treatments started on May 24, July 2, August 28, October 20, and November 20, 2013, respectively), resulting in a total of 15 treatments. There were three blocks and each block was an area of 5 m × 125 m which was randomly positioned in the S. alterniflora stands. With each block, plots (3 m × 6 m) were established and randomly assigned to the treatments (Fig. 1). In the control treatment, no mowing and shading was applied. In the mowing treatment (M), aboveground shoots of S. alterniflora were cut at the ground level and subsequently removed. In the mowing + shading treatment (MS), aboveground shoots of S. alterniflora were cut off and removed, and then covered by one layer of black shading nets. The sharing nets were composed of a high-density polyethylene filament, which has a light transmission rate of only 10–20%. The light transmission rate was calculated based on the data of light intensity measured between 10:00 am and 11:00 am. The shading nets were fixed by bamboo sticks that were firmly inserted into the sediment.
2.4. Data analysis Two-way ANOVAs were used to test the effects of the control method (mowing vs. mowing + shading), the initial treatment time and their interaction on CE based on each of the growth and reproduction variables of S. alterniflora at the end of the first growing season (on November 20, 2013) and at the beginning (on May 24, 2014) and end (on November 26, 2014) of the second growing season. All data were transformed to log(x+1) to increase normality and homogeneity of variance. IBM SPSS version 19.0 (IBM Corporation, USA) was used for all analyses. 3. Results At the end of the first growing season, there was highly significant effect of the control method, treatment time and their interaction on the control efficiency (CE) based each of the five growth and reproduction traits of S. alterniflora (Table 1A: all P < 0.001). Overall, CE of four traits (aboveground biomass, ramet density, ramet height and flowering ramet density) was smaller than 100% when mowing alone was used (Fig. 2). Also, CE of the four traits was much smaller when mowing alone was done in May and July than when it was done in August and October (P < 0.001; Fig. 2A-C, E). The exception was CE of seeding density, which did not differ among the for initial treatment times of mowing alone (Fig. 2D). CE of all five traits was much smaller when mowing + shading was used than when mowing alone was used in May and July (Fig. 2). Furthermore, CE of four traits (biomass, ramet density, ramet height and seedling density) was smaller when the treatment of mowing + shading was done in May and July than when it was done in August and October (P < 0.05; Fig. 2A–D). At the beginning of the second growing season, the control method
2.3. Measurements and calculations In each plot, three quadrats (0.5 m × 0.5 m) were randomly located and the growth and reproduction traits of S. alterniflora were measured. In each quadrat, we measured total number of ramets, number of seedlings and number of flowering ramets. We also randomly selected ten ramets and measured their height in each quadrat. Then, aboveground parts of these ten ramets in each quadrat were harvested and dried in an oven at 80 °C for 48 h to obtain constant mass. We carried out the measurements at the end of the first growing season (on November 20, 2013) and also at the beginning and end of the second growing season (on May 24 and November 26, 2014, respectively). We calculated the control efficiency (CE) of the treatment as CE = PT/PC × 100%, where PT represents a performance variable of S. alterniflora in the mowing treatment or the mowing + shading treatment (Tang et al., 2009), and PC represents the performance variable in the control. We calculated CE in each of the sampling times based on 3
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Fig. 2. Effects of mowing alone vs. mowing + shading at different times on the control efficiency (CE) on Spartina alterniflora at the end of the first growing season after the treatments. Bars represent mean and SE.
4. Discussion
had a highly significant effect on CE of all four growth traits (Table 1B: all P < 0.001). At this time, CE of aboveground biomass, ramet density and seedling density was close to zero and that of ramet height was less than 20% when the treatment of mowing + shading was applied (Fig. 3). However, when mowing alone was conducted, CE of aboveground biomass and ramet height were 60.9%–110.9%, and 64.1%–83.5%, respectively (Fig. 3A, C), and CE of ramet density and seedling density was much larger than 100% (Fig. 3B, D). The pattern of CE at the end of the second growing season was similar to that at the end of the first growing season, except for flowering ramet density (Table 1C, Fig. 4). The control method had a highly significant effect on CE of all five growth and reproduction traits (Table 1C: all P < 0.001). CE of all five traits in the treatment of mowing + shading was zero, while CE in the treatment of mowing alone was larger than 100% in many cases (Fig. 4). CE of the four traits (aboveground biomass, ramet density, ramet height and seedling density) was much smaller when mowing alone was done in May and July than when it was done in the other two treatment times (P < 0.05; Fig. 4 A–D).
4.1. Effects of the control method Our results clearly demonstrated that the method of mowing + shading was much more effective than the method of mowing alone in controlling and eradicating S. alterniflora. During two growing seasons, mowing alone only slightly suppressed aboveground biomass and ramet height of S. alterniflora (CE was not much smaller than 100%), but boosted ramet density, seedling density and flowering ramet density in many cases (CE was much larger than 100%; Figs. 3 and 4). These results suggest that mowing alone cannot effectively control and remove S. alterniflora, and instead is likely to promote the spread of this invasive plant. The removal of aboveground plant parts may reduce the energy allocated to the belowground structures of the plant (Haferkamp and Karl, 2007; Reeder and Hacker, 2004; Darby et al., 2008; Negrin et al., 2012b), such that the growth of S. alterniflora was somewhat suppressed after mowing. However, the removal of aboveground parts released the apical dominance of the plant and benefited its seed germination. As a
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Fig. 3. Effects of mowing alone vs. mowing + shading at different times on the control efficiency (CE) on Spartina alterniflora at the beginning of the second growing season after the treatments. CE of flower ramet density was not available as no ramet flowered at this time. Bars represent mean and SE.
result, ramet density, seedling density and flowering ramet density all increased rapidly after the treatment of mowing alone in the second growing season (Figs. 3 and 4). These results imply that mowing alone can promote population maintenance and regeneration, which was consistent with results of many previous studies (Feldman et al., 2004; Wang et al., 2006; Li and Zhang, 2008; Gao et al., 2009; Tang et al., 2009). The results suggest that mowing alone is not an effective method to control the spread of S. alterniflora and should not be considered in the future. In contrast, the mowing + shading treatment effectively eradicated S. alterniflora within only two growing seasons. Already at the end of the first growing season, no ramets of S. alterniflora came out when the mowing + shading treatment was applied on May 24 or July 2, i.e. about 6 or 5 months after the treatment was done (Fig. 2). While some ramets still came out when the mowing + shading treatment was applied on August 28 and October 20, i.e. about 3 or 1 month after the treatment was done, their biomass and height were greatly reduced and their ramet density were much smaller (Fig. 2). At the end of the second growing season, no ramets of S. alterniflora were found in the plots subjected to the mowing + shading treatment. Spartina alterniflora is a C4 plant (Long et al., 1975; Wan et al., 2008). This character imparts a comparative advantage for photosynthesis, and contributes to its successful invasion (Baruch et al., 1985; Feldman et al., 2004; Zhao et al., 2005). After most of aboveground structures of S. alterniflora was removed by mowing, shading that reduces light quantity (Li et al., 2001; He et al., 2015) was further used to restrict the photosynthesis and compensatory growth of S. alterniflora (Xiao et al., 2005). This combined method greatly reduced the regrowth capacity of S. alterniflora so that no living aboveground parts of S. alterniflora were observed at the end of the second growing season. Our results are in agreement with findings of a previous study demonstrating that plant height, biomass and photosynthetic ability of S. alterniflora were associated with light intensity (Gu et al., 2010; Zhang, 2016). Also, on Qi’ao Island, China, S. alterniflora was successfully controlled primarily because of the reduced light availability caused by the growth of Sonneratia apetala (Tang et al., 2007; Zhou et al., 2015c). Overall, our results indicate that we can rapidly remove S. alterniflora using the combined method of mowing + shading. However, our
observations were only for two growing seasons. Additional observations should be conducted to examine the long-term effect of this method. Also, we need to monitor the growth of S. alterniflora when the treatment is stopped, such that we can find the most cost-effective way to apply such a method. Future studies could be conducted to address these questions. 4.2. Effects of the control timing Considering the overall control efficiency, the timing for the treatments seems of little importance in the long run, especially for the mowing + shading method (Figs. 1–3). While at the end of the first growing season the impacts of both control methods seemed stronger when the treatments were applied earlier (in May and July) than when they were conducted later (in August and October), this was likely because the treatments themselves were still not long enough (as the measurements were done in November of the same year). We should notice that the timing of mowing could affect the effects of mowing on each of the growth and reproduction traits of S. alterniflora (Fig. 4). For instance, at the end of the second growth season, ramet density and seedling density were higher when the mowing treatment was done in November (winter) than when it was done in May and July (Fig. 4B, D). Such a timing effect of mowing may be related to the growth characteristics of the species (Gao et al., 2009). Spartina alterniflora began to store resources in the roots and rhizomes over the winter season (Hopkinson and Schubauer, 1984; White and Howes, 1994). In autumn, the energy storage of S. alterniflora reached a maximum (Negrin et al., 2012a) and CO2 assimilatory activity and photosynthesis sharply declined (Morash et al., 2007). Thus, mowing late may allow more energy to be transferred to belowground parts of the plant (Tang et al., 2009). Therefore, the growth of S. alterniflora could be over compensated when mowing is done late (Belsky, 2002; Maschinski and Whitham, 1989; Yuan et al., 2000), as shown in this study. Despite this difference, the effect of timing on the effectiveness of controlling S. alterniflora was little when all the five growth and reproduction traits were considered when the measurements were conducted at the end of the second year. This is especially true for the mowing + shading treatment, in which no any living aboveground 5
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Fig. 4. Effects of mowing alone vs. mowing + shading at different times on the control efficiency (CE) on Spartina alterniflora at the end of the second growing season after the treatments. Bars represent mean and SE.
the effectiveness of this method on controlling S. alterniflora is not determined by the timing of its application in the long term, we propose to select the timing of the treatment according to the cost and convenience.
parts of S. alterniflora was observed. For mowing alone, while it reduced plant height and ramet density when the mowing treatment was done in July, it greatly increased seedling density and flowering ramet density (Fig. 4). Also, no matter when mowing alone was applied, it stimulated the production of seedlings and flowering ramets at the end of the second growing season (Fig. 4). Thus, for controlling S. alterniflora, mowing alone is not effective at all no matter when it is applied. Our results suggest that when we applied the treatment to control S. alterniflora the timing is not necessary to be considered regarding its controlling effectiveness in the long run.
Acknowledgments We appreciate Dr. Fengchun Zhang for his help with editing of the entire manuscript. We thank Qingfu Zeng and Hongyu Sun from the Beihai Environmental Protection Bureau, and Zhenzhen Deng, Yongchao Jin, Xiaoyan Liu and Fengchun Lü from our laboratory for their assistance in collecting field data. This work was supported by the National Key Research and Development Program of China (grant numbers 2017YFC0506200 and 2016YFC1201100) and the program fund of the Ministry of Environmental Protection of China.
4.3. Conclusions By comparing the control efficiency of two simple methods used in two growing seasons, we showed that the mowing + shading treatment was a highly effective method to control S. alterniflora, while mowing alone was not. Thus, in the future this simple method of mowing + shading is encouraged to apply in order to control the invasion by S. alterniflora in China and possibly also in other counties. As
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Effect of sun-shade on the growth of Spartina alterniflora. Forest Pest Dis. 3, 34–39. Haferkamp, M.R., Karl, M.G., 2007. Clipping effects on growth dynamics of Japanese brome. J. Range Manage. 52, 339–345. https://doi.org/10.2307/4003543. Hammond, M.E.R., Cooper, A., 2002. Spartina anglica eradication and intertidal recovery in Northern Ireland estuaries. In: Veitch, C.R., Clout, M.N. (Eds.), The Eradication of Invasive Species. IUCN SSC Invasive Species Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 124–131. He, Y.L., Liu, H.X., Li, X.Z., Guo, W.Y., Tang, Y.Y., Xin, Z.J., 2015. Response of plant distribution to photon flux density in salt marsh of Dongtan wetlands in Yangze river estuary. Resour. Environ. Yangtze Basin 24, 640–646. Hedge, P., Kriwoken, L.K., Patten, K., 2003. A review of Spartina management in Washington State, US. J. Aquat. Plant Manage. 41, 82–90. Hopkinson, C.S., Schubauer, J.P., 1984. Static and dynamic aspects of nitrogen cycling in the salt marsh graminoid Spartina alterniflora. Ecology 65, 961–969. https://doi.org/ 10.2307/1938068. Hussner, A., Stiers, I., Verhofstad, M.J.J.M., Bakker, E.S., Grutters, B.M.C., Haury, J., van Valkenburg, J.L.C.H., Brundu, G., Newman, J., Clayton, J.S., Anderson, L.W.J., Hofstra, D., 2017. Management and control methods of invasive alien freshwater aquatic plants: a review. Aquat. Bot. 136, 112–137. https://doi.org/10.1016/j. aquabot.2016.08.002. Jardine, S.L., Sanchirico, J.N., 2018. Estimating the cost of invasive species control. J. Environ. Econ. Manage. 87, 242–257. https://doi.org/10.1016/j.jeem.2017.07.004. Kilbride, K.M., Paveglio, F.L., Grue, C.E., 1995. Control of smooth cordgrass with Rodeo in southwestern Washington estuary. Wildlife Soc. B 23, 520–524. https://www.jstor. org/stable/3782964. 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autonomous region. Soc. Wetl. Sci. Bull. 12, 733–739. Zhao, C.Y., Bai, J.D., Liu, X.Y., Li, J.S., 2015a. Impact of Spartina alterniflora on benthic macro-invertebrate communities in Beihai’s cosatal flat, Guangxi zhuang autonomous region. Res. Envir. Sci. 28, 377–383. Zhao, G.Q., Zhang, L.Q., Liang, X., 2005. A comparison of photosynthetic characteristics between an invasive plant Spartina alterniflora and an indigenous plant Phragmites australis. Acta Ecol. Sin. 25, 1604–1610. Zhao, X.J., Zhao, C.Y., Liu, X.Y., Gong, L., Deng, Z.Z., Li, J.S., 2015b. Growth characteristics and adaptability of Spartina alterniflora in different latitude areas along China coast. Ecol. Sci. 34, 119–128. Zhou, T., Liu, S.C., Feng, Z.L., Liu, G., Gan, Q., Peng, S.L., 2015c. Use of exotic plants to control Spartina alterniflora invasion and promote mangrove restoration. Sci. Rep. 5, 1–13. https://doi.org/10.1038/srep12980.
Zhang, D.H., Hu, Y.M., Liu, M., Chang, Y., Yan, X.L., Bu, R.C., Zhao, D.D., Li, Z.M., 2017. Introduction and spread of an exotic plant, Spartina alterniflora, along coastal marshes of China. Wetlands 37, 1181–1193. https://doi.org/10.1007/s13157-017-0950-0. Zhang, J.S., 2016. Effect of different coverage measures on physiological characteristics and growth of Spartina alterniflora. J. Fujian Forestry Sci. Tech. 43, 72–75. Zhang, Y.H., Meng, H.Y., Wang, Y., He, Q., 2018. Herbivory enhances the resistance of mangrove forest to cordgrass invasion. Ecology 99, 1382–1390. https://doi.org/10. 1002/ecy.2233. Zhao, C.Y., Liu, X.Y., Bai, J.D., Lu, F.C., Li, J.S., 2014a. Impact of Spartina alterniflora on benthic macro-invertebrates communities on mangrove wetland in Xicungang Estuary, Guangxi. Biodivers. Sci. 22, 630–639. Zhao, C.Y., Li, J.S., Gong, L., Luo, J.W., 2014b. Effect on benthic macro-invertebrates of Spartina alterniflora invasion in coastal wetlands of Beihai, Guangxi zhuang
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Mowing plus shading as an effective method to control the invasive plant Spartina alterniflora
T
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Caiyun Zhao, Junsheng Li , Xiangjian Zhao Chinese Research Academy of Environmental Sciences, Beijing, 100012, China
A R T I C LE I N FO
A B S T R A C T
Edited by Fei-Hai Yu
Plant invasions greatly threaten native biodiversity and ecosystem health, and measures to effectively control and eradicate invasive plants are urgently needed. Spartina alterniflora has invaded large areas of coastal China as well as many other countries, and caused tremendous ecological and economic problems. To develop measures for effectively controlling the invasion of this species, a field experiment was conducted to test the effectiveness of two methods, i.e. mowing alone, and mowing + shading, on suppressing the growth and reproduction of S. alterniflora, with no shading and mowing as the control. The treatments were applied at five different times, i.e. in May, July, August, October, and November of 2013, and measurements were done at the end of the growing season in both 2013 and 2014. Overall, mowing alone could not effectively suppress S. alterniflora at the end of the second growing season (in 2014); instead, this method promoted both the sexual and asexual reproduction of this invasive plant. The mowing + shading treatment, however, highly effectively suppressed the growth and reproduction of S. alterniflora, and no asexual individuals (ramets) or seedlings were observed at the end of the second growing season. The effectiveness of both methods for controlling S. alterniflora was independent of the timing of the treatments in the long term. We propose the use of mowing + shading to effectively eradicate S. alterniflora in China and possibly also in other counties in future, and the selection of the timing for the treatment according to the cost and convenience.
Keywords: Invasion control Invasive plant Physical control Mowing alone Smooth cord-grass Treatment timing
1. Introduction Plant invasions are considered a global problem and have produced tremendous economic and ecological impacts (Theoharides and Dukes, 2007; Naidoo and Naidoo, 2018; Paolacci et al., 2018; Wang et al., 2017; Chen et al., 2019). In the past, scientists and managers have proposed different measures to control the spread of invasive plants (Hedge et al., 2003; Yuan et al., 2011; Hussner et al., 2017; Byun et al., 2018). While some measures are effective for controlling a particular invasive plant, they may not useful for others as many measures are species-specific (Grevstad et al., 2003). Thus, more measures need to be evaluated in order to effectively control the invasion of some invasive plants (Jardine and Sanchirico, 2018). Spartina alterniflora Loisel. (Poaceae) is native in the Atlantic and Gulf coasts of the United States (Simenstad and Thom, 1995). This species has been introduced into many estuarine regions around the world as it can reduce tidal wave energy, mitigate erosion and trap sediments (Balletto et al., 2005; Weishar et al., 2005). Since its introduction, S. alterniflora has successfully invaded coastal saltmarsh worldwide, and has produced tremendous negative impacts on native
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ecosystems (An et al., 2007; Ainouche and Gray, 2016). This species is now listed as one of the most problematic invasive plants in the world (Weber, 2003; Li et al., 2009). Spartina alterniflora was introduced in China in 1979 (Chung, 1993; Deng et al., 2006). Since then, it has rapidly spread with an annual expansion rate of 20.4% (Zhang et al., 2017), and has occupied almost all coastal areas of China (Zhao et al., 2015a,b,c; Zhang et al., 2017). Many studies have showed that S. alterniflora could outcompete native species such as Phragmites australis (Li et al., 2009), Scirpus mariqueter (Chen et al., 2004, 2005a), and mangroves (Zhang et al., 2018). Moreover, the invasion by S. alterniflora has greatly altered the community composition and species diversity of macro-invertebrates (Chen et al., 2005b; Wang et al., 2010, 2014; Zhao et al., 2014a, 2014b, Zhao et al., 2015a,b,c). In 2003, S. alterniflora was listed as one of the 16 most invasive species in China because of its negative effects (Chen et al., 2004; An et al., 2007). Many measures have been proposed to control S. alterniflora, including chemical controls (Kilbride et al., 1995; Liu et al., 2004), biological controls (Wu et al., 1999; Grevstadet al., 2003) and physical controls (Frid et al., 1999). Herbicides have been used to suppress the
Corresponding author. E-mail address: [email protected] (J. Li).
https://doi.org/10.1016/j.flora.2019.05.007 Received 28 February 2019; Received in revised form 17 May 2019; Accepted 23 May 2019 Available online 28 May 2019 0367-2530/ © 2019 Elsevier GmbH. All rights reserved.
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Fig. 1. The location of the study site (Qingshantou) and the experimental layout. The treatments were applied in May, July, August, October and November 2013, respectively. M represents mowing Spartina alterniflora alone, MS represents mowing plus shading S. alterniflora, and C represent the control (no mowing or shading).
whether the timing of the treatments played a role. Therefore, we conducted a field experiment in southern China, and applied the treatments of mowing alone and mowing + shading on S. alterniflora at five different times (in May, July, August, October, and November in 2013), with no mowing and shading as the control. We aim at addressing the following questions. (1) Can mowing + shading effectively suppress the growth and reproduction of S. alterniflora? (2) Is this method more effective at controlling S. alterniflora than mowing alone? (3) Does the timing of the treatments influence the effectiveness on controlling S. alterniflora?
aboveground growth of S. alterniflora (Liu et al., 2004). However, herbicides have not been widely used in field applications due to their potential impacts on native species. In Qi’ao Island, China, the use of Sonneratia apetala as an alternative plant species to replace S. alterniflora was shown to be effective (Tang et al., 2007). An introduced insect, Prokelisia marginata, was also released to suppress the growth of S. alterniflora in Willapa Bay, Washington, U.S. (Grevstad et al., 2003). However, it was argued that such intentionally introduced exotic species may lead to a potential issue of new invasion (Li and Zhang, 2008). Physical methods, including clipping/mowing, burning, pruning, excavating, dredging, flooding/draining and reaping young ramets, were previously used to control this species (Hedge et al., 2003). The mowing method was demonstrated to be more efficient than other physical methods (Hedge et al., 2003; Li and Zhang, 2008). Studies have shown that repeated mowing may effectively suppress the growth of S. alterniflora, but mowing alone may not (Hedge et al., 2003; Wang et al., 2006; Simmons et al., 2007). However, repeated mowing requires a large investment of human resources, which is not cost-effective and thus difficult to be supported by local governments. Shading alone could effectively suppress the growth of S. alterniflora if the degree of shading is high (Gu et al., 2010), but this method is difficult to apply in the field as this species can be very tall (up to 1.92 m; Zhao et al., 2015a,b,c) and shading material (e.g. shading nets) can be easily moved away by tides. Combined measures have been proposed (Hammond and Cooper, 2002; Major et al., 2003; Li and Zhang, 2008), including the method of mowing + waterlogging, which was demonstrated to be able to successfully eradicate this plant (Yuan et al., 2011). However, the establishment of the waterlogging regime is costly. Thus, a simple, effective method to control S. alterniflora is still lacking. In this study, we tested the effect of another combined measure, i.e., mowing + shading, on the effectiveness of controlling S. alterniflora, and compared it with the effect of mowing alone. We also tested
2. Methods and materials 2.1. Study site This study was conducted at Qingshantou (21°28′N, 109°47′E) in the Beihai Estuary, Beibu Gulf in Guangxi Province, China. This region is also one of the most concentrated distribution areas for mangroves in China (Wu et al., 2013). Spartina alerniflora was first introduced to the area in 1979 for the purpose of reducing tidal waves (Tan et al., 2010). Since then, this invasive plant has rapidly spread along the coastline of the Beihai estuary, forming a mono-dominant community. It competes with Kandelia candel which is an important mangrove species native to this region. The average height of S. alterniflora is 93.3 cm and the average density is 255 ramets m−2 (Zhao et al., 2015a,b,c). The mean annual precipitation is 1500–1700 mm, and the mean temperature is 23.4 °C. Tidal fluctuation in this area is irregular. Diurnal tides occur in 60% of the days within a year and semi-diurnal tides occur in the remaining 40% of the days, with an average tidal height of 2.31–2.59 m. The salinity of the seawater is 20‰–23‰, and pH is 7.60–7.80 (Zhao et al., 2015a,b,c). 2
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Table 1 Two-way ANOVA of the effects of the control method (mowing vs. mowing + shading) and the initial treatment time on the control efficiency on Spartina alterniflora at the end of the 1st growing season and at the beginning and end of the 2nd growing season after treatments. (A) At the end of the 1st growing season
(B) At the beginning of the 2nd growing season
(C) At the end of the 2nd growing season
Effect
df
P
df
F
P
df
F
P
Control efficiency Control method Treatment time Interaction
based on ramet density 1 728.3 3 130.7 3 181.1
< 0.001 < 0.001 < 0.001
1 4 4
984.2 1.5 2.1
< 0.001 0.197 0.085
1 4 4
750.1 4.2 4.2
< 0.001 0.004 0.004
Control efficiency Control method Treatment time Interaction
based on ramet height 1 2759.2 3 428.7 3 883.3
< 0.001 < 0.001 < 0.001
1 4 4
326.9 0.3 0.9
< 0.001 0.854 0.468
1 4 4
759.5 3.9 3.9
< 0.001 0.006 0.006
Control efficiency Control method Treatment time Interaction
based on aboveground biomass 1 1032.9 < 0.001 3 25.6 < 0.001 3 190.7 < 0.001
1 4 4
904.5 0.5 1.6
< 0.001 0.715 0.179
1 4 4
667.5 3.2 3.2
< 0.001 0.017 0.017
Control efficiency Control method Treatment time Interaction
based on seedling density 1 594.7 < 0.001 3 54.7 < 0.001 3 82.4 < 0.001
1 4 4
1139.3 0.6 0.6
< 0.001 0.653 0.653
1 4 4
675.6 3.5 3.5
< 0.001 0.011 0.011
Control efficiency Control method Treatment time Interaction
based on flowering ramet density 1 225.1 < 0.001 3 67.7 < 0.001 3 67.7 < 0.001
– –
– – –
– – –
1 4 4
363.5 1.4 1.4
< 0.001 0.232 0.232
F
–
Degree of freedom for the error term is 64 at the end of the 1 st growing season and 80 on the 2nd growing season.
each of the performance variables, i.e. aboveground biomass, ramet density, mean ramet height, seedling density and flowering ramet density, if available. No ramet flowered at the beginning of the second growing season so that CE of flowering ramet density was not available at this harvest. A greater value of CE reflects a lower level of the control efficiency.
2.2. Experimental design The experiment consisted of three levels of controlling methods (control, mowing alone, and mowing + shading) and five levels of initial treatment time (treatments started on May 24, July 2, August 28, October 20, and November 20, 2013, respectively), resulting in a total of 15 treatments. There were three blocks and each block was an area of 5 m × 125 m which was randomly positioned in the S. alterniflora stands. With each block, plots (3 m × 6 m) were established and randomly assigned to the treatments (Fig. 1). In the control treatment, no mowing and shading was applied. In the mowing treatment (M), aboveground shoots of S. alterniflora were cut at the ground level and subsequently removed. In the mowing + shading treatment (MS), aboveground shoots of S. alterniflora were cut off and removed, and then covered by one layer of black shading nets. The sharing nets were composed of a high-density polyethylene filament, which has a light transmission rate of only 10–20%. The light transmission rate was calculated based on the data of light intensity measured between 10:00 am and 11:00 am. The shading nets were fixed by bamboo sticks that were firmly inserted into the sediment.
2.4. Data analysis Two-way ANOVAs were used to test the effects of the control method (mowing vs. mowing + shading), the initial treatment time and their interaction on CE based on each of the growth and reproduction variables of S. alterniflora at the end of the first growing season (on November 20, 2013) and at the beginning (on May 24, 2014) and end (on November 26, 2014) of the second growing season. All data were transformed to log(x+1) to increase normality and homogeneity of variance. IBM SPSS version 19.0 (IBM Corporation, USA) was used for all analyses. 3. Results At the end of the first growing season, there was highly significant effect of the control method, treatment time and their interaction on the control efficiency (CE) based each of the five growth and reproduction traits of S. alterniflora (Table 1A: all P < 0.001). Overall, CE of four traits (aboveground biomass, ramet density, ramet height and flowering ramet density) was smaller than 100% when mowing alone was used (Fig. 2). Also, CE of the four traits was much smaller when mowing alone was done in May and July than when it was done in August and October (P < 0.001; Fig. 2A-C, E). The exception was CE of seeding density, which did not differ among the for initial treatment times of mowing alone (Fig. 2D). CE of all five traits was much smaller when mowing + shading was used than when mowing alone was used in May and July (Fig. 2). Furthermore, CE of four traits (biomass, ramet density, ramet height and seedling density) was smaller when the treatment of mowing + shading was done in May and July than when it was done in August and October (P < 0.05; Fig. 2A–D). At the beginning of the second growing season, the control method
2.3. Measurements and calculations In each plot, three quadrats (0.5 m × 0.5 m) were randomly located and the growth and reproduction traits of S. alterniflora were measured. In each quadrat, we measured total number of ramets, number of seedlings and number of flowering ramets. We also randomly selected ten ramets and measured their height in each quadrat. Then, aboveground parts of these ten ramets in each quadrat were harvested and dried in an oven at 80 °C for 48 h to obtain constant mass. We carried out the measurements at the end of the first growing season (on November 20, 2013) and also at the beginning and end of the second growing season (on May 24 and November 26, 2014, respectively). We calculated the control efficiency (CE) of the treatment as CE = PT/PC × 100%, where PT represents a performance variable of S. alterniflora in the mowing treatment or the mowing + shading treatment (Tang et al., 2009), and PC represents the performance variable in the control. We calculated CE in each of the sampling times based on 3
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Fig. 2. Effects of mowing alone vs. mowing + shading at different times on the control efficiency (CE) on Spartina alterniflora at the end of the first growing season after the treatments. Bars represent mean and SE.
4. Discussion
had a highly significant effect on CE of all four growth traits (Table 1B: all P < 0.001). At this time, CE of aboveground biomass, ramet density and seedling density was close to zero and that of ramet height was less than 20% when the treatment of mowing + shading was applied (Fig. 3). However, when mowing alone was conducted, CE of aboveground biomass and ramet height were 60.9%–110.9%, and 64.1%–83.5%, respectively (Fig. 3A, C), and CE of ramet density and seedling density was much larger than 100% (Fig. 3B, D). The pattern of CE at the end of the second growing season was similar to that at the end of the first growing season, except for flowering ramet density (Table 1C, Fig. 4). The control method had a highly significant effect on CE of all five growth and reproduction traits (Table 1C: all P < 0.001). CE of all five traits in the treatment of mowing + shading was zero, while CE in the treatment of mowing alone was larger than 100% in many cases (Fig. 4). CE of the four traits (aboveground biomass, ramet density, ramet height and seedling density) was much smaller when mowing alone was done in May and July than when it was done in the other two treatment times (P < 0.05; Fig. 4 A–D).
4.1. Effects of the control method Our results clearly demonstrated that the method of mowing + shading was much more effective than the method of mowing alone in controlling and eradicating S. alterniflora. During two growing seasons, mowing alone only slightly suppressed aboveground biomass and ramet height of S. alterniflora (CE was not much smaller than 100%), but boosted ramet density, seedling density and flowering ramet density in many cases (CE was much larger than 100%; Figs. 3 and 4). These results suggest that mowing alone cannot effectively control and remove S. alterniflora, and instead is likely to promote the spread of this invasive plant. The removal of aboveground plant parts may reduce the energy allocated to the belowground structures of the plant (Haferkamp and Karl, 2007; Reeder and Hacker, 2004; Darby et al., 2008; Negrin et al., 2012b), such that the growth of S. alterniflora was somewhat suppressed after mowing. However, the removal of aboveground parts released the apical dominance of the plant and benefited its seed germination. As a
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Fig. 3. Effects of mowing alone vs. mowing + shading at different times on the control efficiency (CE) on Spartina alterniflora at the beginning of the second growing season after the treatments. CE of flower ramet density was not available as no ramet flowered at this time. Bars represent mean and SE.
result, ramet density, seedling density and flowering ramet density all increased rapidly after the treatment of mowing alone in the second growing season (Figs. 3 and 4). These results imply that mowing alone can promote population maintenance and regeneration, which was consistent with results of many previous studies (Feldman et al., 2004; Wang et al., 2006; Li and Zhang, 2008; Gao et al., 2009; Tang et al., 2009). The results suggest that mowing alone is not an effective method to control the spread of S. alterniflora and should not be considered in the future. In contrast, the mowing + shading treatment effectively eradicated S. alterniflora within only two growing seasons. Already at the end of the first growing season, no ramets of S. alterniflora came out when the mowing + shading treatment was applied on May 24 or July 2, i.e. about 6 or 5 months after the treatment was done (Fig. 2). While some ramets still came out when the mowing + shading treatment was applied on August 28 and October 20, i.e. about 3 or 1 month after the treatment was done, their biomass and height were greatly reduced and their ramet density were much smaller (Fig. 2). At the end of the second growing season, no ramets of S. alterniflora were found in the plots subjected to the mowing + shading treatment. Spartina alterniflora is a C4 plant (Long et al., 1975; Wan et al., 2008). This character imparts a comparative advantage for photosynthesis, and contributes to its successful invasion (Baruch et al., 1985; Feldman et al., 2004; Zhao et al., 2005). After most of aboveground structures of S. alterniflora was removed by mowing, shading that reduces light quantity (Li et al., 2001; He et al., 2015) was further used to restrict the photosynthesis and compensatory growth of S. alterniflora (Xiao et al., 2005). This combined method greatly reduced the regrowth capacity of S. alterniflora so that no living aboveground parts of S. alterniflora were observed at the end of the second growing season. Our results are in agreement with findings of a previous study demonstrating that plant height, biomass and photosynthetic ability of S. alterniflora were associated with light intensity (Gu et al., 2010; Zhang, 2016). Also, on Qi’ao Island, China, S. alterniflora was successfully controlled primarily because of the reduced light availability caused by the growth of Sonneratia apetala (Tang et al., 2007; Zhou et al., 2015c). Overall, our results indicate that we can rapidly remove S. alterniflora using the combined method of mowing + shading. However, our
observations were only for two growing seasons. Additional observations should be conducted to examine the long-term effect of this method. Also, we need to monitor the growth of S. alterniflora when the treatment is stopped, such that we can find the most cost-effective way to apply such a method. Future studies could be conducted to address these questions. 4.2. Effects of the control timing Considering the overall control efficiency, the timing for the treatments seems of little importance in the long run, especially for the mowing + shading method (Figs. 1–3). While at the end of the first growing season the impacts of both control methods seemed stronger when the treatments were applied earlier (in May and July) than when they were conducted later (in August and October), this was likely because the treatments themselves were still not long enough (as the measurements were done in November of the same year). We should notice that the timing of mowing could affect the effects of mowing on each of the growth and reproduction traits of S. alterniflora (Fig. 4). For instance, at the end of the second growth season, ramet density and seedling density were higher when the mowing treatment was done in November (winter) than when it was done in May and July (Fig. 4B, D). Such a timing effect of mowing may be related to the growth characteristics of the species (Gao et al., 2009). Spartina alterniflora began to store resources in the roots and rhizomes over the winter season (Hopkinson and Schubauer, 1984; White and Howes, 1994). In autumn, the energy storage of S. alterniflora reached a maximum (Negrin et al., 2012a) and CO2 assimilatory activity and photosynthesis sharply declined (Morash et al., 2007). Thus, mowing late may allow more energy to be transferred to belowground parts of the plant (Tang et al., 2009). Therefore, the growth of S. alterniflora could be over compensated when mowing is done late (Belsky, 2002; Maschinski and Whitham, 1989; Yuan et al., 2000), as shown in this study. Despite this difference, the effect of timing on the effectiveness of controlling S. alterniflora was little when all the five growth and reproduction traits were considered when the measurements were conducted at the end of the second year. This is especially true for the mowing + shading treatment, in which no any living aboveground 5
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Fig. 4. Effects of mowing alone vs. mowing + shading at different times on the control efficiency (CE) on Spartina alterniflora at the end of the second growing season after the treatments. Bars represent mean and SE.
the effectiveness of this method on controlling S. alterniflora is not determined by the timing of its application in the long term, we propose to select the timing of the treatment according to the cost and convenience.
parts of S. alterniflora was observed. For mowing alone, while it reduced plant height and ramet density when the mowing treatment was done in July, it greatly increased seedling density and flowering ramet density (Fig. 4). Also, no matter when mowing alone was applied, it stimulated the production of seedlings and flowering ramets at the end of the second growing season (Fig. 4). Thus, for controlling S. alterniflora, mowing alone is not effective at all no matter when it is applied. Our results suggest that when we applied the treatment to control S. alterniflora the timing is not necessary to be considered regarding its controlling effectiveness in the long run.
Acknowledgments We appreciate Dr. Fengchun Zhang for his help with editing of the entire manuscript. We thank Qingfu Zeng and Hongyu Sun from the Beihai Environmental Protection Bureau, and Zhenzhen Deng, Yongchao Jin, Xiaoyan Liu and Fengchun Lü from our laboratory for their assistance in collecting field data. This work was supported by the National Key Research and Development Program of China (grant numbers 2017YFC0506200 and 2016YFC1201100) and the program fund of the Ministry of Environmental Protection of China.
4.3. Conclusions By comparing the control efficiency of two simple methods used in two growing seasons, we showed that the mowing + shading treatment was a highly effective method to control S. alterniflora, while mowing alone was not. Thus, in the future this simple method of mowing + shading is encouraged to apply in order to control the invasion by S. alterniflora in China and possibly also in other counties. As
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