Ecological Engineering 73 (2014) 367–372 Contents lists available at ScienceDirect Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng Eradicating invasive Spartina alterniflora with alien Sonneratia apetala and its implications for invasion controls a,c,1, b,1, b a,d a,e Huai Chen *, Baowen Liao **, Bin’er Liu , Changhui Peng , Yao Zhang , b a a Wei Guan , Qiu’an Zhu , Gang Yang a State Key Laboratory of Soil Erosion and Dryland Farming, College of Forestry, Northwest A&F University, Yangling 712100, China b Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou 510520, China c Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China d Institut des Sciences de l’Environnement, Université du Québec à Montréal (UQAM), 201 Président-Kennedy, Montréal, H2X3Y7, Canada e Department of Microbiology and Plant Biology, Center for Spatial Analysis, University of Oklahoma, Norman, OK 73019, USA A R T I C L E I N F O A B S T R A C T Article history: The smooth cordgrass (Spartina alterniflora) has invaded coastal areas throughout the world, including Received 9 July 2014 China, in the past decades. Scientists of China and other countries are trying all means to control its Received in revised form 4 September 2014 invasion, including physical removal, chemicals, and biological control by herbivores. The present Accepted 26 September 2014 research chose a small island (the Qi’ao Island) to study biocontrol of S.alterniflora with mangroves. In Available online xxx 1999, we began to introduce fast-growing mangroves (mainly an alien species, Sonneratia apetala) to control S. alterniflora invasion. In 2011, we eventually eradicated S. alterniflora (only 0.63 ha remained for Keywords: experimental purpose) through expanding mangroves up to 300 ha. The dozen-year monitoring showed Coastal ecosystems that S. apetala did not invade in native mangroves. The isolated island in the present study makes an Biocontrol fi Biodiversity experiment platform for scientists to nd a strategy to check one invasive plant with another alien plant Mangroves but not introducing new invasions. ã Biological invasions 2014 Elsevier B.V. All rights reserved. 1. Introduction Eradication of invasive alien species is acknowledged as a key management for mitigating invasion-caused impacts. However, Alien plants have been increasing in floras around the world, regarding invasive alien plants, it appears that only some very with invasive aliens considered as a global threat to biodiversity localized removals have been completed (Capdevila-Argüelles and ecosystem functioning (Bax et al., 2003; Bjerknes et al., 2007; et al., 2005). Biological control is an effective and valuable tool to Knapp and Kühn, 2012). Such invasive aliens usually cause negative control invasion through releasing natural enemies or competitors economic impacts and costs in the recipient regions (Vilà et al., from the invader’s native range (Hoddle, 2004; Messing and 2010). With intensified anthropogenic activities, new invasion of Wright, 2006), though usually with risk of negative impacts of the alien species continues all over the world, especially in regions introduced biological control agents on local ecosystems (Henne- with rapidly developing trade and economics, e.g. China (Kowarik, man and Memmott, 2001; Messing and Wright, 2006). 2003; Lin et al., 2007; Liu et al., 2005). Moreover, global warming The smooth cordgrass (Spartina alterniflora, Fig. 1) is a perennial enables alien species to expand into regions where they previously C4 grass native to upper intertidal salt marshes across the Atlantic could not survive and reproduce (Walther et al., 2009). Therefore, and Gulf coasts of North America. It was firstly introduced as continuous strengthened efforts should be made in controls of ecological engineering species to prevent shoreline erosion, but invasive aliens, with early detection and rapid response (Huang quickly invaded the coastal ecosystems (Wan et al., 2009). Now it is et al., 2012). found in coastal marshes almost all over the world. In 1979 S. alterniflora was introduced to China from the United States, also for ecological engineering purposes including reducing tidal wave energy, mitigating erosion, trapping sediments, reclaiming tidal * Corresponding author. Tel.: +86 28 8289 0543; fax: +86 28 8289 0536. flats and protecting dike (An et al., 2007; Chung, 2006). With ** Corresponding author. Tel.:+ 86 20 87028494; fax: +86 20 87031622. anthropogenic transplanting, natural dispersing and hybridizing E-mail addresses: [email protected], [email protected] (H. Chen), with native species, S. alterniflora successfully invaded in nine of [email protected] (B. Liao). 1 Both authors equally contribute to this work. the fourteen coastal provinces of China (Wan et al., 2009), forming http://dx.doi.org/10.1016/j.ecoleng.2014.09.096 0925-8574/ã 2014 Elsevier B.V. All rights reserved. 368 H. Chen et al. / Ecological Engineering 73 (2014) 367–372 monocultures and expanding its coverage to more than 112 000 ha case of biocontrol (almost complete eradiation) of S. alterniflora by 2000 (An et al., 2007). For its great negative effects on with an alien plant (Sonneratia apetala) in an island of China. biodiversity and other ecosystem services, S. alterniflora is now regarded as one of the top 16 most harmful exotic plants in China 2. Methods and materials (Wang et al., 2008). Several control methods have been used to prevent and mitigate the spread of S. alterniflora, including 2.1. Ethics Statement burning, harvesting, grazing by snails, herbicide application (not permitted now for health consideration), freshwater irrigation, and Our field studies were approved by the Bureau of Qi’ao some combined methods, e.g. substituted by Phragmites australis Mangrove Wetland Natural Reserve. The study was observational, after hydrology changing, but all with unclear effectiveness (An involving no cruelty to animals, no damage to habitats and no harm et al., 2007; Silliman and Zieman, 2001; Wan et al., 2009). to endangered plants, therefore no review from the ethnic Therefore, as an invasive plant, S. alterniflora is thought to be hard committee was required in China. All the work was carried out to eradicate (Qin and Chung, 1992). This paper reports a successful under the Wildlife Protection Law of the People’s Republic of China. Fig. 1. Location of the Qi’ao Island. Spartina alterniflora distributes along the coast of China from Tianjin to Guangxi, marked in purple. Dark blue dots represent Sonneratia apetala’s distribution in the south part of China coast. Four pictures from up to down in the right show the S. alterniflora monoculture, artificial clearance of S. alterniflora, biocontrol of S. alterniflora by S. apetala, and eradication of S. alterniflora followed by S. apetala plantation. H. Chen et al. / Ecological Engineering 73 (2014) 367–372 369 Table 1 2.2. Experiment site and S. apetala Influence of shading on the growth of Spartina alterniflora. ’ The Qi ao Island in Zhuhai City, Guangdong Province has a total Shade Light Height Quantity of 2 treatment transmittance (cm) tillerings area of 24 km , with vast mudflat along the coast. The Qi’ao Mangrove Wetland Natural Reserve is located in the northwest of No shade 100%a 42 Æ 0.5a 12 Æ 1a 0 0 0 0 One-layer 65.8%b 38 Æ 0.4a 10 Æ 1a the island (113 36 –113 39 E, 22 23 –22 27 N). The climate in the shade Qi’ao Island is sub-tropical maritime climate, with an average Two-layer 32.5%c 25 Æ 0.5b 4 Æ 1b annual temperature of 22.4 C. The lowest average temperature shade (15.3 C) appears in January, with the historically lowest tempera- Three-layer 15.2%d 0c 0c ture 2.5 C. The mean annual precipitation is 1964.4 mm. Its tide is shade irregular semidiurnal tide; the mean high water level is 0.17 m, and Different letters mean significant differences (P < 0.05) among the À the mean low water level 0.14 m. Southeast wind blows in shade treatments. summer while northeast wind blows in winter. The annual mean m salinity of the sea water is 18.2 . Its soil is coastal saline meadow Maximum Likelihood to perform the supervised classification. m – marsh soil, with salinity about 20.8 in the surface (0 13 cm). Training areas were selected using high-resolution SPOT 5 image. The 15 true mangrove species in this island belong to 10 families The result was in agreement with history records. and 13 genus, with S. apetala plantation the main mangrove now. S. apetala (Fig. 1) is naturally distributed and serves as a very 2.4. Shading experiments important restoration species in South Asia including India, Bangladesh and Myanmar (Mitra et al., 2012). It was originally To test the effect of mangrove shades on the growth of S. introduced in 1985 to the Dong Zhaigang Mangrove Nature Reserve alterniflora, shading experiments were done in Research Institute of of China for mangrove restoration from Sundarban, southwestern Tropical Forestry, Chinese Academy of Forestry, Guangzhou, from Bangladesh (Liao et al., 2004). After 10-year restoration of April 15 to July 15, 2009. Shade nets were used to simulate shadiness mangroves, due to high adaptability and tolerance to salinity of mangroves. Three treatments (one layer, two layers and three (Chen et al., 2000), S. apetala occupied about 95% of the restored layers ofshade nets)andonecontrol(no shade)wereset up. Foreach mangroves (Liao et al., 2004). Currently covering 2300 ha, S. apetala treatment, we set up triplicates for each of the eight pots of S. is also listed as a leading restoration species in China (Ren et al., alterniflora incorporated. During the three-month experiment, we 2009).