Eradicating Invasive Spartina Alterniflora with Alien Sonneratia

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

State Key Laboratory of Soil Erosion and Dryland Farming, College of Forestry, Northwest A&F University, Yangling 712100, China

Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou 510520, China

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

Institut des Sciences de l’Environnement, Université du Québec à Montréal (UQAM), 201 Président-Kennedy, Montréal, H2X3Y7, Canada

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.

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).

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

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 0.5a 12 1a

0 0 0 0

One-layer 65.8%b 38 0.4a 10 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 0.5b 4 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

the mean low water level 0.14 m. Southeast wind blows in shade treatments.

summer while northeast wind blows in winter. The annual mean

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). With some individuals of S. apetala occurring in native semimonthlymeasuredtheheightandtillernumberofS.alterniﬂora.

ecosystems of southern coastal China, Chinese scientists began to

discuss its invasive potential (Ren et al., 2009; Tang, 2009). Some 2.5. Monitoring controlling effects of different mangroves species on S.

even listed S. apetala as an invasive species and tried to remove it alterniﬂora

(Tang, 2009; Wang et al., 2004). There existed no S. apetala on the

’

Qi ao island before we introduced it in 1999. Since 1999, we cut S. alterniﬂora to form ridge belts and planted

on them ﬁve kinds of mangrove with nutrition bags: Kandelia

ﬂ

2.3. Monitoring dynamics of S. alterni ora and S. apetala by remote candel, Bruguiera gymnorrhiza, Rhizophora stylosa,Sonneratia case-

sensing olaris, and S. apetala. The plantation density was 0.3 m 0.3 m for

K. candel, B. gymnorrhiza, R. stylosa, and 1 m 1 m for S. caseolaris

We used Landsat TM/ETM+ image dating from 1990 to and S. apetala. After 3 years, we set 3 quadrats (1 m 1 m) in each

2011 from the US Geological Survey (USGS) archive. Eight images plantation and in the S. alterniﬂora stand to measure the growth of

were selected between November to January for little cloud cover S. alterniﬂora. We recorded the biomass, plant height, the quantity

ﬂ

and large contrast between mangrove and S. alterni ora. For each of tillerings and ground diameter of S. alterniﬂora.

image we used 10 ground control points and controlled the root

mean square error (RMSE) below 0.5 pixel. We used the 2.6. Monitoring S. alterniﬂora retreat and S. apetala growth

In 2005, we chose three S. apetala plantations with different

ages (2-year, 3-year and 4-year) to monitor S. alterniﬂora retreat

and S. apetala growth. For each plantation, we set up a typical plot

(300 m ). In each plot, we set up three large quadrats (10 m 10 m)

to record the height, diameter at breast height (DBH), crown range

Table 2

Controlling effects of different mangroves on growth indices of Spartina alterniﬂora.

Mangrove Quadrate (m ) Growth index of S. alterniﬂora under

species mangroves

Biomass (g Tillering Height (m) Ground m2) number diameter

(cm)

S.apetala 1 20.5 4.5a 2.6 0.4a 0.82 0.07a 0.43 0.11a

S.caseolaris 1 4.1 0.8a 5.0 2.1a 0.49 0.15a 0.29 0.06a

K.candel 1 1788.8 265.7b 220.6 39ba 1.66 0.32b 0.48 0.08b

B. gymnorrhiza 1

1749.0 247.3b 202.5 36b 1.59 0.30b 0.48 0.08b

R.stylosa 1 1929.9 350.0b 215.1 39b 1.68 0.25b 0.46 0.11b

Control 1 1987.5 179.0b 228.6 27b 1.63 0.20b 0.47 0.10b

Fig. 2. Area of Spartina alterniﬂora Loisel and mangroves in the Qi’ao Island from

1990 to 2011. The three pictures from remote sensing data show the condition of Different letters mean signiﬁcant differences (P < 0.05) among the mangrove

1995, 1999 and 2009. treatments.

370 H. Chen et al. / Ecological Engineering 73 (2014) 367–372

Table 3

Characteristics of S. apetala plantations of different ages and the growth index of S. alterniﬂora under such plantations in the year 2005.

S. apetala Plantation Characteristics of plantation Growth index of S. alterniﬂora

Height (m) Crown density Crown range (m ) DBH (cm) Height (m) Coverage Biomass 2

(%) (kg m )

2-year 2.5 0.1a 0.60–0.70 3.0 0.1a 4.9 0.5a 0.76 0.24a 100a 0.51 0.07a

3-year 3.7 0.1b 0.60–0.75 3.3 0.2ab 4.6 0.1a 0.60 0.15a 16b 0.05 0.01b

4-year 6.1 0.2c 0.65–0.80 3.5 0.2a 6.9 0.2b 0b 0c 0c

Different letters mean signiﬁcant differences (P < 0.05) among the mangrove treatments.

and crown density of S. apetala, and three small quadrats for P < 0.05. The above analyses were performed with SPSS 11.5 for

(1 m 1 m) to record the height, frequency, biomass and coverage Windows.

of S. alterniﬂora.

3. Results and discussion

2.7. Long-term monitoring of S. alterniﬂora plantations

3.1. S. alterniﬂora vs S. apetala on the Qi’ao Island

In 2011, we set up 8 quadrats of 3-year, 5 quadrats of 6-year,

4 quadrats of 9-year, and 3 quadrats of 12-year S. apetala. At the In the early 1990s, S. alterniﬂora began to invade in the salty

opposite angles of the quadrat, 2 small quadrats of 4 m 4 m were marshes, gaps of natural mangroves and barren ﬂats of the Qi’ao

set up for the seedlings (shorter than 30 cm). Around each small Island (Fig. 1), with fast invasion pattern similar with other coastal

quadrat, there were 12 sub-small quadrats of 1 m 1 m. We regions in China (An and others 2007). After only ﬁve years, the

recorded the height, DBH, basal diameter, crown size, clump invasive fast-growing S. alterniﬂora had formed monocultures and

number (arbor and herbaceous). We calculated the frequency, expanded its coverage up to 227 ha by 1995. Then during

plant density, clump density and basal area. construction of ﬁsh or shrimp ponds, some of S. alterniﬂora was

removed. However, S. alterniﬂora was still dominant in the coastal

2.8. Monitoring mangrove seedlings in different habitats ﬂat of this island, about 59 ha in 1999 (Fig. 2).

We realized the serious invasion of S. alterniﬂora and began to

In 2004, we recorded the density, height and age of seedlings of control it around this island in 1999. Through our three-month

different species with 2 m 2 m quadrates inside a four-year experiments, we found that increases in shadiness signiﬁcantly

plantation (n = 8), on its edge (n = 24), in a ditch around the reduced the height and number of tillers of S. alterniﬂora (Table 1).

plantation (n = 40), a S. alterniﬂora stand (n = 16) and a section of Therefore, we considered that the dense canopy of fast-growing

bare beach (n = 9). In the four-year S. apetala plantation, we mangroves might be an effective way to control the notorious

randomly chose 6 individuals of S. apetala to harvest seeds from weed. We began to introduce four native mangroves (K. candel, B.

three big twigs (with diameter larger than 2.5 cm) and three small gymnorrhiza, R. stylosa, S. caseolaris) and S. apetala after clearing the

ones (with diameter smaller than 2.5 cm) for each tree to calculate aboveground part of S. alterniﬂora in 1999, hoping it could be

seed harvest per tree. substituted by the mangroves. Three years after the initial

introduction, three of the four native species had no signiﬁcant

2.9. Statistical analysis control on S. alterniﬂora regrowth, while only the native S.

caseolaris and the alien S. apetala succeeded in forming dense

Mean values of factors were calculated by averaging the canopy to control the regrowth of S. alterniﬂora (Table 2).

replicates for each treatment. Analyses of variance (ANOVA) were Thereafter, we collaborated with the local government to afforest

performed using such means to test the difference of factors. The these two mangrove species to substitute S. alterniﬂora.

effect of a certain variable was considered statistically signiﬁcant

e 15000 0

Height of S. apetala S. apeta la (alien)

Crown density 100000 e A. ilicifolius (native)

1.0

20 A. carniculatum (native) ) -1

(m) d 5000 0 d 15

S. apetala e d 400 0 b 10 0.5 c

b Crown density Seedling density (N ha density Seedling d

Height of 200 0 5 a b b c a b

0 0.0 0

3-year 6-year 9-year 12-year In the S.apetala forest S.apetala forest edge Ditch S. al terniflora stand Bare beach

S. apetala Plantations Habitat s

Fig. 3. Height and crown density of S. apetala plantations of different ages in the Fig. 4. Seedling density of the alien species (S. apetala) and native species (A.

Qi’ao Island. Different letters mean signiﬁcant differences (P < 0.05) of the height ilicifolius and A. carniculatum) in different habitats in a typical landscape of a 4-year

among the plantations of different ages. S. apetala plantation, bare beach, ditch and a S. alterniﬂora stand.

H. Chen et al. / Ecological Engineering 73 (2014) 367–372 371

recorded a small amount of K. candel (about 67 individuals per ha),

which is the dominant species of a native mangrove forest on the

island. Though S. apetala was found in laboratory to release some

chemicals to suppress other plants, the above-mentioned obser-

vations in plantations of different ages showed that S. apetala did

not exclude native species but rather enhanced the settlement of

shade-tolerant native species. Similar with our results, in a 14-year

S. apetala plantation in Dongzhaigang of Hainan Island, two native

mangrove species (A. carniculatum and K. candel) were found to

dominate the understory of the stand (Wang et al., 2011). However,

in Leizhou Bay of southern China, native species were only

observed in young plantations (less than 10 years) and disappeared

in plantations older than 10 years (Ren et al., 2008). This was

probably due to the limited seed source and low seedling quantity

in the region. Therefore, given plentiful seeds and seedlings of

native species, natural regeneration of native mangroves should

gradually occur in S. apetala plantations after 10 years or so.

Fig. 5. Dieback of S.caseolaris and reinvasion of S. alterniﬂora after the ice storm in

Furthermore, we found that there was a higher density of A.

2008. This photo was taken by Baowen Liao.

carniculatum in the edge of plantations than that inside the

plantation, which indicated that increasing the range of edges

Since our annual afforestation of S. caseolaris and S. apetala, S.

through circled or striped plantation would accelerate natural

alterniﬂora coverage continually decreased and at the same time

regeneration of native mangroves (Ren et al., 2008).

mangroves expanded their coverage up to 223 ha by 2007, mainly

As mentioned above, S. apetala has sometimes been regarded as

through S. apetala afforestation. In 2008, the large-scale ice storm

an invasive species due to sporadic natural regeneration in native

in Southern China attacked this island, resulting in dying of most S.

ecosystems in southern China (Ren et al., 2008). In our study, we

caseolaris individuals, which explained the decline of mangroves

found three-year old individuals could blossom and bear fruit,

and a slight increase of S. alterniﬂora in 2009. Then we replaced the

producing more than 2700 berries per tree with 30 to 50 seeds per

degraded S. caseolaris plantation with S. apetala, which was more

berry. Therefore, there were enough seed sources for S. apetala

tolerant of cold. To 2011, we eventually eradicated S. alterniﬂora

regeneration and “invasion”. However, after 17 years of S. apetala

(only 0.63 ha remained for experimental purposes) through

introduction to Dongzhaigang, there were only 64 matured

expanding mangroves up to 300 ha.

individuals and 6 small ones along the edges of two rivers there

(Liao et al., 2004), which indicated that S. apetala “invaded” very

3.2. Monitoring the eradication progress and aftermaths slowly, if they ever did. We investigated S. apetala seedlings in

different habitats on the Qi’ao Island and observed a lowest density

In a dozen of years, the fast-growing S. apetala successfully of S. apetala seedlings inside the 4-year S. apetala plantation

controlled S. alterniﬂora, with its plantations of different age (Fig. 4). These seedlings were youngest, only three or four months

dominating the coastal line of the Qi’ao Island. Since the very old among different habitats. There are several reasons for this.

beginning of our biocontrol of S. alterniﬂora, we had monitored the First, the natural germination rate of S. apetala was very low, which

dynamics of S. apetala, S. alterniﬂora and the native mangrove is limited by tides, salinity and sediments, etc. Second, S. apetala

species. In 2005, we noted that a two-year S. apetala plantation had seedlings were shade-intolerant and hard to survive under the

already formed a dense mangrove forest with a canopy about dense mangroves (Liao et al., 2004). Comparing with S. apetala, we

60%–70% (Table 3). With time, S. apetala plantations greatly found more native species seedlings in almost all kinds of habitats

increased in height, crown range and DBH (Table 3). One exception on this island except for the edge of its plantation and bare beaches

was the crown density, which, after getting to its peak (100%) in the (Fig. 4). Moreover, the ratio of native seedlings to S. apetala

6-year plantation, decreased to 90% and 80% in the 9-year and seedlings was much higher in older S. apetala plantations than in

12-year ones, respectively (Fig. 3), probably due to the self- young ones. Based on these results, we do not think S. apetala can

thinning effect. Furthermore, the biomass accumulation and soil “invade” in native mangroves at the present status.

organic carbon (SOC) under S. apetala plantations were found to

increase with time, e.g. in the 10-year plantation the total forest 3.3. Replacing S. apetala plantation with native mangroves or not?

1 1

and SOC were up to 108.1 Mg ha and 35.0 Mg ha , respectively

(Ren et al., 2010). Simultaneous with the general increase of height, Some scholars regarded S. apetala as a nurse plant to facilitate

crown density, biomass accumulation and SOC of S. apetala on the settlement of native mangroves species at early stages, then

Qi’ao Island, signiﬁcant reduction was found in the height, biomass compete with these seedlings, and later suppress the natural

and coverage of S. alterniﬂora (Table 3). In the 4-year plantation regeneration of native mangroves. Therefore, they suggested

only three individuals of S. alterniﬂora were found in a 300 m plot removing S. apetala in order to approach native mangroves (Ren

and no one was found in the 12-year plantation. et al., 2008). In Hong Kong, a few scientists already tried all means

With the retreat of S. alterniﬂora, some kinds of native species to eradicate such a fast-growing exotic species (Tang, 2009).

(especially shrubs and herbs, such as Acanthus ilicifolius, Aegiceras However, although S.apetala plantations seem to be in the

carniculatum, Acrostichum aureurm, etc.) encroached in the successive progress to native mangroves on the island and at

understory of young S. apetala plantations. In 2005, we observed some other sites (Wang et al., 2011), such progresses will take a

several native species and their seedlings under a 2-year long time with many uncertainties. Direct removals of S.apetala

plantation. Dense aerial roots of S. apetala provided more support may not be a wise way to approach native mangroves. Our study

for seedlings and further enhanced the settlement of shrubs, herbs was a good example, in which S. apetala did a good job in effectively

and seedling of native mangroves. In 2011, we found that A. controlling S. alterniﬂora. The ice storm of 2008 proved it a right

ilicifolius and their seedlings almost dominated the understory of decision not to remove S. apetala to approach native mangroves. If

the 9-year and 12-year plantations. In the 12-year plantation, we we had done so, it could have resulted in reinvasion of S.

372 H. Chen et al. / Ecological Engineering 73 (2014) 367–372

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