Effects of spatial expansion between Phragmites australis and Cyperus malaccensis on variations of arsenic and heavy metals in decomposing litters in a typical subtropical estuary (Min River), China

Chemosphere 240 (2020) 124965

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Effects of spatial expansion between Phragmites australis and Cyperus malaccensis on variations of arsenic and heavy metals in decomposing litters in a typical subtropical estuary (Min River), China Xiao Li a, b, Zhigao Sun a, b, c, *, Liping Tian a, b, Tao He a, b, Jing Li a, b, Jie Wang a, b, Hua Wang a, b, Bingbing Chen a, b a b c

Institute of Geography, Fujian Normal University, Fuzhou, 350007, PR China Key Laboratory of Humid Subtropical Eco-geographical Process (Fujian Normal University), Ministry of Education, Fuzhou, 350007, PR China Fujian Provincial Key Laboratory for Subtropical Resources and Environment, Fujian Normal University, Fuzhou, 350007, PR China

h i g h l i g h t s

g r a p h i c a l a b s t r a c t


Spatial expansion altered the decomposition rates of different litters in ecotone.
Levels of Pb, Cu, Zn, Ni, Cd and As in litters generally showed increasing tendency.
Both physicochemical sorption and substrate quality affected As/metals variation.
Exposure risk of Zn, Ni, Cd and Cr in ecotone increased during spatial expansion.
Variation of decay rate and increased exposure risk in ecotone should be emphasized.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 30 October 2018 Received in revised form 13 September 2019 Accepted 23 September 2019 Available online 25 September 2019

To investigate the effects of spatial expansion between native invasive species (Phragmites australis) and commom native species (Cyperus malaccensis) on variations of micro-elements (Pb, Cr, Cu, Zn, Ni, Cd and As) in decomposing litters in the Min River estuary, in situ filed decomposition experiment was conducted in P. australis (PA) community (before expansion, BE), C. malaccensis (CM) community (before expansion, BE) and P. australis-C. malaccensis (PA0 -CM’) community (during expansion, DE) from February 2016 to February 2017 by space-for- time substitution method. Results showed that the decomposition of C. malaccensis were faster than those of P. australis whether at BE stage or at DE stage. The decomposition rate of PA’ increased by 24.40% compared to PA whereas the value of CM’ decreased by 15.67% compared with CM. The concentrations of Pb, Cu, Zn, Ni, Cd and As in decomposing litters of P. australis (PA and PA’) and C. malaccensis (CM and CM’) generally showed increasing tendency and the values in the former were significantly lower than those in the latter (p < 0.05). The physicochemical sorption onto recalcitrant organic fractions and the substrate quality (C/N and M/C ratios) of decomposing litters were two important factors affecting the differences in As/metals variations between species. The levels of Cr in decaying litters increased initially and decreased afterward, and the values in P. australis were significantly higher than those in C. malaccensis (p < 0.05). Whether at BE stage or at DE stage, stocks of As/

Handling Editor: Martine Leermakers Keywords: Arsenic Heavy metals Decomposition Spatial expansion Min river estuary

* Corresponding author. Institute of Geography, Fujian Normal University, Fuzhou, 350007, PR China. E-mail address: [email protected] (Z. Sun). https://doi.org/10.1016/j.chemosphere.2019.124965 0045-6535/© 2019 Elsevier Ltd. All rights reserved.

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X. Li et al. / Chemosphere 240 (2020) 124965

metals in decomposing litters of P. australis (PA and PA’) were generally higher than those of C. malaccensis (CM and CM’). The lower stocks of As/metals in CM or CM’ might be more dependent on its lower mass remaining. Compared with PA at BE stage, the accumulation of As/metals in decomposing litters of PA’ at DE stage decreased greatly, which might be ascribed to the lower precipitation of metal sulfides in PA’. Stocks of Zn, Ni, Cd and Cr in CM’ and stocks of Cr in PA’ generally evidenced the export of metals from decomposing litter to environment, indicating that the potential exposure risk of Zn, Ni, Cd and Cr might be increased as CM was invading by PA. This study found that the spatial expansion between P. australis and C. malaccensis not only altered the stocks of As/metals in decomposing litters but also increased the exposure risk of Zn, Ni, Cd and Cr in ecotone. In future, as the ecological functions of ecotone was precisely evaluated during the expansion of the two plants in the Min River estuary, the alterations of litter decomposition rates and the exposure risks of Zn, Ni and Cd caused by CM’ should be emphasized. © 2019 Elsevier Ltd. All rights reserved.

1. Introduction Heavy metals are critical global pollutants and can cause a variety of environmental problems due to their toxicity, persistence and bio-accumulation in natural conditions. Estuarine marshes are crucial ecosystems in which the material-energy exchanges between continental river water and marine salt water occur. With the rapid industrialization and economic development in coastal zone, large quantities of pollutants containing heavy metals are imported into estuary, which produces great effect on the habitation of flora and fauna in estuarine marsh (Duarte et al., 2010). Marsh plants generally absorb the metals into their aerial and belowground organs from external environment (Wang et al., 2015a, 2015b; Zhang et al., 2018). Once plants biomass started to degrade and tissues enter the litter layer and being decayed, increasing metal concentrations can be observed (Windham et al., 2004). Decomposing plant tissues can act as a sink if, during decomposition, heavy metals are bound to litter by passive sorption or by physiological mechanisms of microbial colonizers. Plant detritus can also act as a metal source when microbial activity mobilizes metals or when it becomes available to deposit feeders (Duarte et al., 2010; Sun et al., 2016a). Thus, the accumulation and release of metals in decomposing litters can directly or indirectly influence their bioavailability, mobility and toxicity to wild animals or human through exposure from the food chains. In the past two decades, considerable efforts have been conducted to study the litter decomposition in different coastal marshes (Anesio et al., 2003; Janousek et al., 2017; Duan et al., 2018). Most of these research focus on investigating litter decomposition rates and macro-nutrient [carbon (C), nitrogen (N) and phosphorus (P)] variations in decomposing litters (Harmon et al., 1990; Keuskamp et al., 2015; Grasset et al., 2017; Hu et al., 2019) and the roles of abiotic (e.g., temperature, moisture, salinity, sedimentation, tide inundation and duration) and biotic factors (e.g., benthonic animals, fungi, meiofauna, free and attached microorganisms) (Lopes et al., 2011; Gingerich et al., 2014; Janousek et al., 2017) on decomposition, whereas information on variations of micro-elements (e.g., As and heavy metals) in decomposing litters is still lacking. Particularly, the comparative study on heavy metal dynamics or stocks in different decomposing litters remains scarce. In China, the related studies have also been carried out in different coastal marshes such as the salt marshes in the Yellow River estuary (Sun et al., 2016a; Sun and Mou, 2016), the Min River estuary (Tong and Liu, 2009; Zhang et al., 2014; Hu et al., 2019) and the Yangtze River estuary (Duan et al., 2018), and the mangrove swamps in the Southeast China (Zhang et al., 2019). Generally, present studies also concentrate on exploring litter decomposition rates and nutrient dynamics in decomposing litters and the key roles of biotic and

abiotic variables during decaying process (Zhang et al., 2014; Wang et al., 2015a, 2015b; Sun et al., 2016b), while information on variations of As and heavy metals in plant detritus is still very limited. The Min River estuary, located in the transition between central and southern subtropical climatic zones, is one of the most typical estuaries in Southeast China. As the biggest river flowing into the East China Sea in the Fujian Province of Southeast China, the Min River plays a very important role in guaranteeing the ecological security of the Min River basin. In recent years, the loadings of total pollutants from industrial and urban sewage and mining enterprises in the Min River basin always maintained a high level (8.6e12.9  105 tons). Every year, approximately 0.6e2.4  103 tons of heavy metals and about 40e130 tons of As were discharged into estuary through rivers, runoff and land-based point sources (China Oceanic Information Network, 2017). Large amounts of pollutants (especially As and heavy metals) imported into Min River may have significantly toxic effects on flora and fauna in estuarine marsh and even threaten the ecological health of estuary (Sun et al., 2017). The marshes in the Min River estuary generally distribute along the riverbank and start from Zhuqi in the west and ends in Chuanshi Island in the east, with a total area of 980.6 km2 (Liu et al., 2006). Shanyutan, the largest marsh in the Min River estuary, colonized by the most common native plants: Scirpus triqueter, Phragmites australis, Cyperus malaccensis and Cyperus compressus. Among them, P. australis and C. malaccensis, are two dominant communities and widely distribute in intertidal zone. P. australis is a native invasive species, which first colonized the middle-west area of Shanyutan at about 30e40 years ago (presumably by dispersal from middle and upper reaches of the Min River) (Tong et al., 2011). Since then, the marsh originally dominated by C. malaccensis were gradually expanded by P. australis at spatial scale, resulting in which became a single dominant community or even formed an ecotonal community with C. malaccensis (100e150 m-wide). In fact, the spatial expansion between P. australis and C. malaccensis mainly referred to the competitions of the two species for environmental resources such as light, water, and nutrient (Qin et al., 2010; Wang et al., 2019). Before spatial expansion, the highest population height of P. australis and C. malaccensis was about 2 m and 1.5 m, the density was about 100 ind m2 and 1500 ind m2, and the biomass was about 2400 g m2 and 2000 g m2, respectively (Wang et al., 2015a, 2015b; He et al., 2018), but during their expansion, the height and biomass of P. australis and the density and biomass of C. malaccensis decreased significantly, whereas the density of P. australis and the height of C. malaccensis increased obviously (He et al., 2018; Wang et al., 2019). He et al. (2018) further indicated that the spatial expansion between P. australis and C. malaccensis significantly altered the sedimentary environment in ecotone and the composition of silt and clay in surface sediment, which might greatly

X. Li et al. / Chemosphere 240 (2020) 124965

affect the decomposition rates of litters via a number of direct and indirect mechanisms, such as alteration of ambient water chemistry, compaction of detritus, reduction of gas exchange between the detrital layer and the surrounding water, and suppression of bacterial and fungal breakdown of detritus (Tong et al., 2011). In addition, the spatial expansion between P. australis and C. malaccensis also greatly altered the stoichiometries of plants and litters (Tong et al., 2011; Wang et al., 2015a, 2015b; Mi et al., 2018), which, to some extents, might influence the decomposition rates of litters and the release or accumulation of metals in detritus. Although many studies on litter decomposition have been conducted in the Min River estuary, most of them focus on nutrient dynamics and the related affecting factors such as tidal flooding, salinity gradient and typhoon intensity (Tong and Liu, 2009; Zhang et al., 2014; Wang et al., 2016), while information on micro-element (e.g., As and heavy metals) variations in decomposing litters remains scarce. Especially, the effects of spatial expansion between native invasive species (P. australis) and common native species (C. malaccensis) on variations of As and heavy metal in decomposing litters are still poorly documented. Understanding the differences in As/metals variations in decomposing litters of P. australis and C. malaccensis in different expansion stages is beneficial to reveal the alteration of As/metal stocks and their exposure risks of common native species as it is invaded or invading by native invasive species. In this paper, the influences of spatial expansion between native invasive species (P. australis) and common native species (C. malaccensis) on variations of As and heavy metals in decomposing litters were investigated by space-for-time substitution method. The decomposition of different litters was studied by litterbag technique and the levels of As/metals (Pb, Cr, Cu, Zn, Ni, Cd) in decomposing litters were determined by ICP-MS analysis. Objectives of this study were: і) to explore the differences in decomposition rates of P. australis and C. malaccensis litters at different expansion stages; іі) to determine the variations of As/ metal concentrations in decomposing litters during the expansion of the two plants; and ііі) to investigate the dynamics of As/metal stocks in decomposing litters and evaluate their exposure risks in different expansion stages. 2. Materials and methods 2.1. Study region This study was conducted in intertidal zone of the northwest Shanyutan (26 000 3600 N-26 030 4200 N; 119 3401200 E119 400 4000 E), which is located in the south of the Min River estuary (Fig. 1a). Shanyutan is the largest marsh in the Min River estuary, with an area of 893 hm2 (Liu et al., 2006). The climate in the study region is warm and wet; with a mean annul temperature of 19.6  C and a mean annual precipitation of 1350 mm (Wang et al., 2015a, 2015b). The tide in intertidal zone is typical semi-diurnal tide and the marsh in intertidal zone is generally submerged for 3e3.5 h during each tidal inundation. The marsh soil is dominated by saline soil and the main native species include Phragmites australis, Cyperus malaccensis, Scirpus triqueter and Cyperus compressus. 2.2. Study methods 2.2.1. Experimental design The space-for-time substitution method was used to investigate the effects of spatial expansion between native invasive species (P. australis) and commom native species (C. malaccensis) on the variations of As/metals in decomposing litters. Three experimental plots (50 m  50 m) were randomly laid in intertidal zone of the

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northwest Shanyutan (Fig. 1b). At each plot, three subplots (20 m  20 m) were laid in P. australis (PA) community (before expansion, BE), P. australis-C. malaccensis (PA0 -CM’) community (during expansion, DE) and C. malaccensis (CM) community (before expansion, BE), respectively (Fig. 1b and c). Litter decomposition was studied by litterbag technique from February 2016 to February 2017. On 10 February 2016, the standing litters of P. australis (PA and PA’) and C. malaccensis (CM and CM’) were collected from above-mentioned subplots. The litters were washed in deionized water, cut into 10 cm segments and ovendried for constant weight. Each 20 cm  20 cm litterbag was made of nylon netting (0.5 mm mesh) and was filled with 15 g (oven-dried weight) litter. On 19 February 2016, the litterbags were randomly placed in the corresponding subplots and were labeled by different marks (avoid confusion). In order to prevent the litterbag from being carried away by the tide, the litterbags were attached to the PPR pipe (1.5 m, approximately 1.0 m was embedded into sediment) with nylon cord. In order to prevent the litterbags from being affected by sedimentation caused by tide during decomposition, each sub-plot was tightly enclosed by nylon netting (0.2 mm mesh, approximately 1.5 m height). The substrate quality of P. australis (PA and PA’) and C. malaccensis (CM and CM’) litters used in this study were shown in Table 1. 2.2.2. Sample collection The decomposition experiment included 13 sampling times with different intervals [2016-3-4 (15 d), 2016-3-19 (30 d), 2016-420 (62 d), 2016-5-22 (94 d), 2016-6-20 (123 d), 2016-7-20 (153 d), 2016-8-20 (184 d), 2016-9-22 (217 d), 2016-10-20 (245 d), 2016-1120 (276 d), 2016-12-20 (306 d), 2017-1-17 (334 d), 2017-2-27 (375 d)], and, at each sampling time, three or four litterbags were retrieved from each subplot. After retrieval, these litterbags were immediately transferred to the laboratory and the adhering sediments and macro-invertebrates in remaining litters were removed. All litterbags were further cleaned carefully in de-ionized water and weighed after being dried to a constant weight. 2.2.3. Sample analysis The samples of decomposing litters were ground and determined the total carbon (TC), total nitrogen (TN) and total sulfur (TS) contents by an element analyzer (Elementar Vario Micro, German). A 0.0500 (±0.0005) g homogenized sample was digested with 2 ml HNO3 (70%) and 2 ml H2O2 (30%) at 180  C for 15 h. The residue was diluted to 40 ml with deionized water for analyzing As and heavy metal levels. The concentrations of As/metals (Pb, Cr, Cu, Zn, Ni and Cd) in all samples were determined by ICP-MS (XSeriesII, Thermo Company, USA). Quality assurance and quality control were assessed using duplicates (three replications), method blanks and certified reference materials (GBW10020) from the National Research Center for Standards in China with each batch of samples (two blank and one standard for each 30 samples). The recoveries of samples spiked with standards ranged from 82.7% to 103.6%. 2.2.4. Determinations of environmental variables Sediment temperature was measured in each subplot on sampling date. Sediment pH and electrical conductivity (EC) in 0e10 cm depths were determined in situ by portable pH meter (HACHPHW37-SS, USA) and Soil & Solution EC meter (EC Testr11 þ Multi Range), respectively. Sediment moisture in 0e10 cm depths was measured by high-precision moisture measuring instrument (TZS1). 2.2.5. Calculations The percentage of dry mass remaining (R, %) and decomposition rates (d1) were calculated by the following equations:

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X. Li et al. / Chemosphere 240 (2020) 124965

a

Phragmites australis (PA)

P. australis-Cyperus malaccensis (PA'-CM')

C. malaccensis (CM)

c

Fig. 1. Sketch of the study region (a), the experimental plots (b), and the Phragmites australis, Cyperus malaccensis and P. australis-C. malaccensis communities (c).


R ¼ ðLt =L0  100%
ln ðLt =L0 ¼  kt where Lt is the remaining dry mass at time “t”, L0 is the original dry mass, k is the coefficient of decomposition rate and t (d) is the decomposition in days. The accumulation index of the “i” element (As, Pb, Cr, Cu, Zn, Ni and Cd) (AIi) was used to describe the accumulation or release status during decomposition, which could be calculated by the following equation (Sun et al., 2017):

AIi ¼

Lj ,Cj  100% Lo ,Co

where L0 is the original dry mass, C0 is the original element levels in

decaying litters, Lj is the remaining dry mass at time “j”, and Cj is the element levels in decomposing litters at time “j”. The metal/carbon ratio (Mt/Ct) was calculated by the concentrations of As/metals and carbon at time “t” (Sun et al., 2016a). 2.2.6. Statistical analyses Data analysis was performed by SPSS 20.0 statistical software and figures were drawn by Origin 8.0 software. The results were presented as means over the replications, with standard deviation (S.D). The analysis of variance (ANOVA) tests was employed to determine if environmental variables among marshes and dry mass remaining, environment variables, As/metal levels and stocks among decomposing litters differed significantly (p < 0.05). If ANOVA showed significant differences, multiple comparison of means was undertaken by Tukey’s test with a significance level of p ¼ 0.05. Pearson correlation analyses were used to investigate the relationships between dry mass remaining and environmental

37.62 ± 2.54 26.81 ± 2.07b 38.12 ± 0.09a 29.40 ± 0.49b 2.72 ± 0.44 3.44 ± 0.23ab 2.50 ± 0.28ac 2.61 ± 0.23a 11.24 ± 0.66 15.71 ± 1.15a 13.22 ± 0.29b 13.22 ± 0.29a 42.20 ± 0.36 41.99 ± 0.17a 39.45 ± 0.04b 38.88 ± 0.22b PA PA’ CM’ CM

Notes: PA, Phragmites australis; CM, Cyperus malaccensis; PA’, P. australis in P. australis-C. malaccensis community; and CM’, C. malaccensis in P. australis-C. malaccensis community. Different letters within the same column indicate significant differences at p < 0.05.

0.38 ± 0.07a 0.79 ± 0.16b 1.30 ± 0.28c 0.88 ± 0.07bd 0.03 ± 0.00 0.05 ± 0.02ac 0.12 ± 0.03b 0.04 ± 0.00ac 4.19 ± 1.49 6.74 ± 2.13ab 9.00 ± 3.82b 2.74 ± 0.07c 19.94 ± 0.64 30.00 ± 7.59ab 31.87 ± 9.95b 15.95 ± 0.64c 3.02 ± 0.70 4.73 ± 1.53ac 8.49 ± 2.80b 5.74 ± 2.79ac 1.16 ± 0.30 2.78 ± 1.07ab 5.25 ± 1.71bc 2.42 ± 0.01ab

34.13 ± 15.55 52.52 ± 7.44a 39.62 ± 31.25ab 18.78 ± 4.00bc

Cd (mg kg1)

a ac

Ni (mg kg1) Zn (mg kg1) Cu (mg kg1)

ac a a

TS (mg g1) TN (mg g1)

a

TC (%) Litters

Table 1 Substrate quality of the litters used in this study.

c

C/N

a

Pb (mg kg1)

Cr (mg kg1)

ab

a

As (mg kg1)

X. Li et al. / Chemosphere 240 (2020) 124965

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factors, and between As/metal levels and substrate quality (C/N or M/C ratios). Stepwise linear regression analyses were conducted to best predict the variations of dry mass remaining of different litters based on environmental variables and substrate quality. In all tests, differences were considered significantly only if p＜0.05. 3. Results 3.1. Mass remaining and decomposition rate of litters The percentage of dry mass remaining of different litters generally decreased and the values of P. australis (PA and PA’) were significantly higher than those of C. malaccensis (CM and CM’) (p < 0.01) (Fig. 2). After 375 days of decomposition, approximately 64.13% (PA), 61.33% (PA’), 90.43% (CM’) and 93% (CM) of dry mass were lost, respectively. The decomposition rates of the four litters followed the sequence of CM (0.007292 d1) > CM’ (0.006150 d1) > PA’ (0.003243 d1) > PA (0.002607 d1), indicating that the decomposition of C. malaccensis were faster than those of P. australis whether at BE stage or at DE stage. Significantly higher t0.95 (time needed for 95% of dry mass decomposed) were observed for P. australis (PA, 3.16yr; PA’, 2.61yr) compared to C. malaccensis (CM, 1.05yr; CM’, 1.30yr). The decomposition rate of PA’ increased by 24.40% compared to PA whereas the value of CM’ decreased by 15.67% compared with CM. 3.2. Carbon and metal concentrations in decomposing litters Carbon concentrations varied between 29.91% and 42.20% in PA, between 29.28% and 41.99% in PA’, from 29.05% to 44.05% in CM’ and from 28.65% to 42.59% in CM, respectively, but no statistical differences were observed among the four decomposing litters (p > 0.05). With a few exceptions, Pb, Cu, Zn, Ni, Cd and As levels showed increasing tendency during decomposition (Fig. 3). The concentrations of Cr in P. australis (PA and PA’) were significantly higher than those in C. malaccensis (CM and CM’) (p < 0.05), while the levels of Pb, Cu, Zn, Ni, Cd and As in P. australis (PA and PA’) were significantly lower than those in C. malaccensis (CM and CM’) in most sampling times (p < 0.05) (Fig. 3). Similar variations of the levels of As/metals in decomposing litters of PA and PA’ were observed (p > 0.05). The levels of Zn, Ni and Cd in decomposing litters of CM’ were significantly lower than those in CM (p < 0.05) (Fig. 3), indicating that, as CM was invading by PA, the concentrations of Zn, Ni and Cd in litters of CM’ decreased obviously. 3.3. Metal stocks in different decomposing litters Stocks of Pb, Cu and As in the four decomposing litters showed accumulation in most periods, but only the values in PA and PA’ showed statistical difference (p < 0.01). With a few exceptions, higher stocks of Pb, Cu and As were observed in PA/or CM compared to PA’/or CM’, implying that the accumulation of the three metals decreased from BE stage to DE stage. Except for the releasing of Cr in decomposing litters of PA’, CM’ and CM at the end of experiment, Cr stocks in the three litters in other periods and those in PA throughout the experiment demonstrated net accumulation. Stocks of Zn, Ni and Cd in CM’ generally evidenced the export from litters to surroundings, while those in CM, PA and PA’ generally showed incorporation, comparatively, the accumulation of Zn, Ni and Cd in PA were significantly higher than those in PA’ (p < 0.01) (Fig. 4). Whether at BE stage or at DE stage, stocks of As/metals in the four litters generally showed PA > CM/or PA’ > CM’. Compared with PA at BE stage, the accumulation of As/metals in decomposing litters of PA’ at DE stage decreased greatly. Stocks of Zn, Ni and Cd in CM and CM’ varied significantly (p < 0.01), which generally shifted from

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X. Li et al. / Chemosphere 240 (2020) 124965

120

PA

PA'

CM'

CM

Mass remaining (%)

100

80

60

40

a a

20

0

b b 0

15

30

62

94

123 153 184 217 245 276 306 334 375

Decomposition time (days) Fig. 2. Dry mass remaining of P. australis (PA and PA’) and C. malaccensis (CM and CM’) litters during decomposition. Different letters indicate significant differences at the level of p < 0.05.

Fig. 3. Variations of As/metals concentrations in decomposing litters of P. australis (PA and PA’) and C. malaccensis (CM and CM’). Different letters indicate significant differences at the level of p < 0.05.

X. Li et al. / Chemosphere 240 (2020) 124965 Pb

PA

PA'

CM '

CM

700

AICr

AIPb

a

1500 1000

500

800

400 300

b b b 0

a ab b ab

100 0

15 32 62 94 123 153 184 217 245 276 306 334 375

Decomposition time (days)

Zn

500

600

b

400

200

500

a

1000

500

2000

Cu

1200

600

2500

0

1400

Cr

AICu

3000

7

0

Ni

bc c

200 0

15 32 62 94 123 153 184 217 245 276 306 334 375

0

Decomposition time (days)

1000

15 32 62 94 123 153 184 217 245 276 306 334 375

Decomposition time (days)

Cd

400

100

b

0

a

bd c 0

15 32 62 94 123 153 184 217 245 276 306 334 375

400

200 100 0

b

b b

200

c 0

Decomposition time (days) 2000

600

AICd

200

a

800

300

a

AINi

AIZn

400 300

0

15 32 62 94 123 153 184 217 245 276 306 334 375

b c 0

15 32 62 94 123 153 184 217 245 276 306 334 375

Decomposition time (days)

Decomposition time (days)

As

1600

a

AIAs

1200 800

b

400 0

c c 0

15 32 62 94 123 153 184 217 245 276 306 334 375

Decomposition time (days)

Fig. 4. Variations of Pb, Cr, Cu, Zn, Ni, Cd and As stocks in decomposing litters of P. australis (PA and PA’) and C. malaccensis (CM and CM’). Different letters indicate significant differences at the level of p < 0.05.

4. Discussion 4.1. Effects of spatial expansion on decomposition rates of different litters This study indicated that the decomposition of C. malaccensis (CM and CM’) were faster than those of P. australis (PA and PA’) whether at BE stage or at DE stage, which was probably dependent on their litter qualities and the alterations of nutrients during decomposition. Present studies have found that litter quality was the determining factors affecting the decomposition rate and the C/ N ratio was an effective index in representing decomposition rate; a high C/N ratio generally resulted in a slow decomposition rate (Harmon et al., 1990; Sun et al., 2012). In this paper, whether at BE stage or at DE stage, significantly higher C/N ratios in P. australis (PA and PA’) were observed compared to C. malaccensis (CM and CM’) (Fig. 5), which could be ascribed to the fact that P. australis was an herb with higher lignin and cellulose contents (p < 0.05) (Gessner, 2000). This could partly explain the lower decomposition rate of P. australis and the higher decomposition rates of C. malaccensis. Moreover, compared with P. australis community, C. malaccensis community was more adjacent to the sea and this increased the chance of nutrient (e.g., N) in seawater immobilized by microbes, which, to some extent, could better explain the lower C/N ratios in decomposing litters and the higher decomposition rates of C. malaccensis. Similar result was drawn by Deng and Bai (2012) who found that frequently tidal flooding might promote the decomposition of Suaeda salsa litters.

This study also found that the lower C/N ratios were observed in PA’/or CM compared to PA/or CM’ (Fig. 5), and, compared to the litters at BE stage (PA and CM), the decomposition rate of PA’ increased whereas the value of CM’ decreased. Present studies have indicated that the initial N concentration of litters clearly affected the decay rate, the lower the initial C/N ratio, the higher the decomposition rate (Sun et al., 2012), and this was tested by the paper (Table 1). Compared with the litters at BE stage (PA and CM),

PA

PA'

CM '

CM

50

a

40

C/N

accumulation to release as the CM was invading by PA.

b

30

c

cd

20

0

15

30

62

94

123 153 184 217 245 276 306 334 375

Decomposition time (days) Fig. 5. Variations of C/N ratios in P. australis (PA and PA’) and C. malaccensis (CM and CM’) litters during decomposition. Different letters indicate significant differences at the level of p < 0.05.

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X. Li et al. / Chemosphere 240 (2020) 124965

Table 2 Stepwise linear regression equations between residual rates of decomposing litters and physicochemical factors. Litters

Stepwise regression equations

R2

p

PA PA’ CM’ CM

y ¼ 48.362e10.903x1þ1.167x3 y ¼ 39.684e21.076x1þ18.033x2þ0.965x3 y ¼ 13.831e11.813x1þ2.984x3 y ¼ 58.704 þ 4.073x3

0.468 0.664 0.800 0.776

0.005 0.045 0.000 0.000

Notes: x1, EC; x2, pH; and x3, C/N.

the initial C/N ratios of PA’ decreased whereas those of CM’ increased, which could be attributed to the great variations of ecological traits of the two plants as the CM was invading by PA. There were two possible reasons. For one thing, under the conditions of nutrient limiting, the ecological adaptation strategies of plants generally presented as slow growth rates and high capacity to retain nutrients in the biomass associated with high capacity to resorb nutrients (Gonz
alez et al., 2010; Wang et al., 2015a, 2015b). He et al. (2018) indicated that, as the CM was invading by PA in the Min River estuary, the two plants generally adopted different strategies to adapt the competitive environment. Thus, in this paper, the variations of nutrient-use and ecological adaption strategies of the two plants might greatly impact upon the initial C/N ratios of the two decaying litters (PA’ and CM’) at DE stage. For another, compared to the plants (PA and CM) at BE stage, the capacity of intercepting suspended particulate matter (especially fine particles) in seawater by the plants at DE stage (PA’ and CM’) enhanced greatly and the total contents of clay and silt in surface sediment of ecotone increased by 11.8e29.1% (He et al., 2018). Simultaneously, the nutrient contained in fine particles was imported into the ecotone, which might also influence on the ecological traits and nutrients absorption of the two plants (PA’ and CM’), and, ultimately, affect the initial substrate quality (e.g., C/N ratio) of the two decaying litters. In this paper, no significant differences in sediment EC, pH, moisture and temperature were observed among the three marshes (p > 0.05), implying that these variables might be less important in contributing to the observed differences in decomposition rates of the decaying litters. Thus, the differences in decomposition rates of the four litters might be more dependent on the above mentioned factors, namely initial C/N ratios and the C/N ratios during decomposition, and this was tested by the Pearson correlation analyses which found that significantly positive correlations were observed between C/N ratios and dry mass remaining (PA, r1 ¼ 0.564, p ¼ 0.002; PA’, r2 ¼ 0.551, p ¼ 0.002; CM, r3 ¼ 0.822, p ¼ 0.000; CM’, r4 ¼ 0.885, p ¼ 0.000). EC was also a crucial variable affecting the decomposition rates of the four litters and significantly negative correlations occurred between sediment EC and mass remaining (PA, r1 ¼ 0.570, p ¼ 0.002; PA’, r2 ¼ 0.729, p ¼ 0.000; CM, r3 ¼ 0.528, p ¼ 0.004; CM’, r4 ¼ 0.571, p ¼ 0.002), implying that the higher the salinity, the faster the decay rates.

Stepwise linear regression analyses further indicated that the variations of mass remaining of PA, PA’ and CM’ could be better explained by C/N ratios and sediment EC, while those of CM could be better explained by C/N ratios (Table 2). In this paper, the positive effects of salinity on decomposition of the four litters were very likely mediated by microorganisms and macro-invertebrates (e.g., Eriocheir sinensis; Scylla serrate and Exopalaemon carinicauda) adapted to hyper saline conditions. Similar reasons were reported by some previous studies (Lopes et al., 2011; Sun et al., 2016a; Stagg et al., 2017). 4.2. Effects of spatial expansion on As/metals concentrations and stocks in decomposing litters This study found that, with a few exceptions, Pb, Cu, Zn, Ni, Cd and As levels in decomposing litters generally showed increasing tendency during decomposition, and the values in P. australis (PA and PA’) were significantly lower than those in C. malaccensis (CM and CM’) whether at BE stage or at DE stage (p < 0.05) (Fig. 3). Similar results have been reported by some previous studies. Du Laing et al. (2006) indicated increasing metal levels (Cu, Cr, Ni, Pb and Zn) in leaf blades, sheaths and stems of P. australis during decomposition. Sun et al. (2016a) showed increasing Cu and Zn concentrations in three typical halophyte litters (P. australis, Suaeda salsa and Suaeda glauca) during decomposition in the Yellow River estuary. Increase of metal levels could be ascribed to some direct and indirect mechanisms such as contamination by sediment particles, passive sorption onto recalcitrant organic fractions and active metabolism of microbiota (Weis and Weis, 2004; Du Laing et al., 2006). In this study, compared to P. australis community, the surface sediments in C. malaccensis community could be more easily resuspended by tidal wave action and this increased the chance of physicochemical sorption of metals in fine particles onto the remaining recalcitrant tissues (Du Laing et al., 2006; Sun et al., 2016a, 2017). It was also reported that Pb, Cu, Zn, Cd and As levels showed significant positive correlations with the ratio of Cl/  SO2 4 (Bai et al., 2019). He et al. (2018) found that the ratio of Cl / 2 SO4 in surface sediment of C. malaccensis community was much higher than that of P. australis community due to the higher duration and frequency of tidal inundation, which, to some extents, might increase the levels of these metals in decomposing litters by passive sorption. Present studies also reported that C/N ratio was an effective index in representing decomposition rate and microbial activity (Hobbie, 1996; Sun et al., 2017). In this paper, the C/N ratio of P. australis (PA and PA’) and C. malaccensis (CM and CM’) generally decreased during decomposition (Fig. 5), indicating that the microbial activities in decomposing litters might be enhanced simultaneously. Pearson correlation analyses further showed that significantly negative correlations occurred between Pb (Cu, Zn, Ni, Cd or As) levels and C/N ratios in the four decomposing litters (Table 3). As mentioned previously, whether at BE stage or at DE

Table 3 Correlation coefficients between As/metal levels and carbon/nitrogen (C/N) ratios or metal/carbon (M/C) ratios. Litters

Ratios

Pb

Cr

Cu

Zn

Ni

Cd

As

PA

C/N M/C C/N M/C C/N M/C C/N M/C

0.644** 0.990** 0.658** 0.984** 0.745** 0.971** 0.797** 0.987**

0.232 0.989** 0.181 0.983** 0.238 0.961** 0.194 0.977**

0.720** 0.992** 0.703** 0.983** 0.703** 0.968** 0.810** 0.987**

0.548** 0.984** 0.577** 0.976** 0.702** 0.975** 0.802** 0.981**

0.620** 0.987** 0.606** 0.980** 0.749** 0.970** 0.778** 0.986**

0.682** 0.991** 0.682** 0.989** 0.708** 0.962** 0.802** 0.985**

0.580** 0.992** 0.691** 0.987** 0.648** 0.977** 0.725** 0.991**

PA’ CM’ CM

Notes: PA, Phragmites australis; CM, Cyperus malaccensis; PA’, P. australis in P. australis-C. malaccensis community; and CM’, Cyperus malaccensis in P. australis-C. malaccensis community. * Correlation is significant at the 0.05 level; and ** Correlation is significant at the 0.01 level.

X. Li et al. / Chemosphere 240 (2020) 124965

stage, significantly higher C/N ratios in P. australis (PA and PA’) were observed compared to C. malaccensis (CM and CM’) (Fig. 5), which might induce the relatively low levels of As/metals (Pb, Cu, Zn, Ni and Cd) in P. australis (PA and PA’). This was reminiscent of the findings of Du Laing et al. (2006) who found significantly positive correlations between fungal biomass and metal levels in tissues, implying that fungal activity might be important in immobilizing metals in decomposing tissues. This study also found that, similar variations of the concentrations of As/metals in decaying litters of PA and PA’ were observed (p > 0.05), but significant differences in levels of Zn, Ni and Cd occurred between CM and CM’ (p < 0.05), implying that the variations of As/metals in P. australis (PA and PA’) and C. malaccensis (CM and CM’) not only depended on microbial activities affected by C/N ratios but also rested with the M/C ratios in decomposing litters. Present studies have reported that once carbon was the primary constituent of decaying litter, metal levels could be normalized to carbon content to better interpret the variation of metal concentrations as litter decomposed (Pereira et al., 2007; Sun and Mou, 2016). In this paper, significantly positive correlations were observed between As/metal levels (Pb, Cr, Cu, Zn, Ni and Cd) and M/ C ratios (p < 0.01) (Table 3), implying that M/C ratios, to a great extent, might influence the As/metal variations in P. australis (PA and PA’) and C. malaccensis (CM and CM’) during decomposition. Compared to CM, significantly lower levels of Zn, Ni and Cd in decomposing litters of CM’ (Fig. 3) might be related to the sulfate dissimilation and the reactions between sulfides and metal ions. Wang et al. (2019) reported that the spatial expansion between PA and CM significantly decreased the contents of acid volatile sulfide in sediments of ecotone, which might induce the metal sulfides formed in CM’ to be declined compared to CM. As a result, the levels of some metals (e.g., Zn, Ni and Cd) in decomposing litter (CM’) at DE stage decreased greatly. In contrast with Pb, Cu, Zn, Ni, Cd and As, Cr concentrations in the four decomposing litters increased firstly and decreased afterward (Fig. 3). The increase of Cr levels in decaying litters at early stage might be more dependent on the sorption of Cr by the iron plaque in decomposing litters (Xu, 2018). Previous studies have reported that Cr behavior was greatly affected by iron cycling and organic matter degradation. The oxidation of organic matter might lead to the use of Fe- and Croxides as electron acceptor and the reduced Fe and Cr forms might leach from decomposing litters (Sun et al., 2017). It was reported that, in the Min River estuary, the levels of Fe in sediments of P. australis community, C. malaccensis community and P. australis-C. malaccensis community were very high, and the values varied from 44.11 to 44.36 g kg1, from 42.61 to 42.82 g kg1 and from 42.97 to 46.35 g kg1, respectively (Mi et al., 2018), implying that Fe and Cr leaching from the four decomposing litters might be enhanced as Fe- and Cr-oxides were reduced. Comparatively, the lowest value occurred in C. malaccensis marsh, indicating that Fe and Cr leaching from C. malaccensis litters (CM and CM’) might be lower than those from P. australis litters (PA and PA’), and this was tested in Fig. 3. This paper indicated that, stocks of Pb, Cu and As in the four decomposing litters showed accumulation in most periods, implying that, the release of Pb, Cu and As from the four litters was not counterbalanced the incorporation by microbiota and passive sorption onto recalcitrant organic fractions. Whether at BE stage or at DE stage, the litters might act as cation exchanger absorbing ions from sediments or seawater and the strong affinity of Pb, Cu and As to organic matter might promote this sorption (Weis and Weis, 2004; Sun et al., 2016a). Moreover, Pb, Cu and As were sulfur affinity elements, which mainly existed in the form of sulfides and sulfate minerals and could be adsorbed and complexed by the decomposing litters. Stocks of Zn, Ni and Cd in PA and PA’, and Cr stocks in PA were generally positive, evidencing incorporation of

9

them in most sampling periods. However, stocks of Zn, Ni, Cd and Cr in CM’ and stocks of Cr in PA’ generally evidenced the export of metals from litter to environment, indicating that the potential exposure risk of Zn, Ni, Cd and Cr might be increased as CM was invading by PA. Whether at BE stage or at DE stage, stocks of As/ metals in the four litters generally showed PA > CM/or PA’ > CM’. Compared to PA or PA’, the lower stocks of As/metals in CM or CM’ might be more dependent on its lower mass remaining although the active accumulation for As/metals occurred in decomposing litters. Moreover, compared with PA at BE stage, the accumulation of As/metals in decomposing litters of PA’ at DE stage decreased greatly. As mentioned previously, the contents of acid volatile sulfide in sediments of ecotone at DE stage decreased significantly, and this reduced the chances of reactions between sulfur ions (S2) and metal ions (e.g., Pb2, Cu2, Zn2, Ni2 and Cd2) simultaneously, resulting in the lower precipitation of metal sulfides in decomposing litters of PA’ (Wang et al., 2015a, 2015b). In addition, as CM was invading by PA, stocks of Zn, Ni and Cd in decomposing litters of C. malaccensis (CM and CM’) generally shifted from incorporation to release, implying that, during the expansion of the two plants, the eco-toxic risk of Zn, Ni and Cd exposure might be increased. The release of Zn and Cd from decomposing litters of C. malaccensis (CM and CM’) might be related to the strong migration of Zn and the actively chemical behaviors of Cd, and, as pH or ionic strength was slightly altered during tidal inundation, their mobility could be enhanced greatly (Tian et al., 2018). In conclusion, the spatial expansion between the two plants not only altered the stocks of As/ metals in decomposing litters but also increased the exposure risk of Zn, Ni, Cd and Cr in ecotone. Particularly, the exposure risk produced in ecotone, to a great extent, rested with the contribution of CM’ litters. Thus, the exposure risks of Zn, Ni and Cd caused by CM’ litters should be emphasized in future as the ecological functions of ecotone was precisely evaluated during the expansion of P. australis and C. malaccensis in the Min River estuary. Acknowledgements This study was financially supported by the National Nature Science Foundation of China (No. 41971128; 41371104), the Award Program for Min River Scholar in Fujian Province (No. Min [2015] 31), and the Key Foundation of Science and Technology Department of Fujian Province (No. 2016R1032-1). References Anesio, A.M., Abreu, P.C., Biddanda, B.A., 2003. The role of free and attached microorganisms in the decomposition of estuarine macrophyte detritus. Estuar. Coast Shelf Sci. 56 (2), 197e201. Bai, J.H., Zhao, Q.Q., Wang, W., Wang, X., Jia, J., Cui, B.S., Liu, X.H., 2019. Arsenic and heavy metals pollution along a salinity gradient in drained coastal wetland soils: depth distributions, sources and toxic risks. Ecol. Indicat. 96, 91e98. China Oceanic Information Network, 2017. Ocean environmental quality communique of China during 2012-2016. http://www.nmdis.org.cn/gongbao/huanjing/ 201704/t20170413_35526.html. Deng, W., Bai, J.H., 2012. Pattern Evolution of Typical Wetland System and Process of Water Ecology-A Case of Huang-Huai-Hai Area. Science Press, Beijing, pp. 223e226. Du Laing, G., Van Ryckegem, G., Tack, F.M.G., Verloo, M.G., 2006. Metal accumulation in intertidal litter through decomposing leaf blades, sheaths and stems of Phragmites australis. Chemosphere 63 (11), 1815e1823. Duan, H., Wang, L., Zhang, Y.N., Fu, X.H., Tsang, Y.F., Wu, J.H., Le, Y.Q., 2018. Variable decomposition of two plant litters and their effects on the carbon sequestration ability of wetland soil in the Yangtze River estuary. Geoderma 319, 230e238. Duarte, B., Caetano, M., Almeida, P.R., Vale, C., Caçador, I., 2010. Accumulation and biological cycling of heavy metal in four salt marsh species, from Tagus estuary (Portugal). Environ. Pollut. 158 (5), 1661e1668. Gessner, M.O., 2000. Breakdown and nutrient dynamics of submerged Phragmites shoots in the littoral zone of a temperate hardwater lake. Aquat. Bot. 66 (1), 9e20. Gingerich, R.T., Merovich, G., Anderson, J.T., 2014. Influence of environmental parameters on litter decomposition in wetlands in West Virginia, USA. J. Freshw.

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