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Dynamics of decomposition and nutrient release of leaf litter in Kandelia obovata mangrove forests with different ages in Jiulongjiang Estuary, China
Ecological Engineering 73 (2014) 454–460
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Dynamics of decomposition and nutrient release of leaf litter in Kandelia obovata mangrove forests with different ages in Jiulongjiang Estuary, China Ting Li a,b , Yong Ye a, * a Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystem, College of the Environment and Ecology, Xiamen University, Xiamen,Fujian, China b South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 June 2014 Received in revised form 12 September 2014 Accepted 29 September 2014 Available online xxx
Rates of in-situ decomposition and nutrient (organic C, N and P) release of leaf litter were seasonally compared among three planted Kandelia obovata mangrove forests (K12, K24 and K48 with forest ages of 12, 24 and 48 years, respectively) and one natural mature K. obovata forest (KM) in Jiulongjiang Estuary, China. The average values of half-time (T50) of leaf litter decomposition in spring, summer, autumn and winter were 29.8, 18.7, 23.9 and 47.4d, respectively. Decomposition rates were lower in the older forests (with T50 values of 30.1 and 31.1d averaged by all seasons in K48 and KM, respectively) than in the younger ones (with T50 values 29.8 and 28.8d averaged by all seasons in K12 and K24, respectively), especially in summer and autumn. The annual mean T50 of nutrient release of leaf litter during decomposition followed an order of KM > K48 > K24 > K12. During leaf litter decomposition, C releases were very similar to dry weight losses, while N releases were slower and P releases were much faster than dry weight losses. With the development of restored mangrove forests, decomposition and nutrient release of leaf litter became slow, which may increase the chance of leaf litter being exported into the surrounding waters. ã 2014 Elsevier B.V. All rights reserved.
Keywords: Mangrove Kandelia obovata Leaf litter Decomposition Nutrient release Forest age
1. Introduction Mangrove forests are extremely open and productive ecosystems providing large amounts of energy and organic matter to estuarine and coastal systems via litter fall and decomposition (Lugo and Snedaker, 1974; Mackey and Smail, 1996; Ye et al., 2011). Litter fall has been estimated to account for 30–60% of total primary production of mangrove forests (Bunt et al., 1979). The high productivity was often attributed to rapid litter decomposition and efficient recycling of nutrient elements in mangrove forests (Bosire et al., 2005). Most of mangrove primary production, mainly consisting of mangrove leaves, becomes available to consumers after senescence and breakdown. Decomposition of litter fall is one of the basic functions of forest ecosystems (Harley, 1971; Ananda et al., 2008). The rate and extent of in situ decomposition governs how much of organic matter and nutrients is recycled within the mangrove forest, and how much is exported to near-shore waters (Boulton and Boon, 1991 Zhou et al., 2010).
* Corresponding author. Tel.: +86 592 2880249; fax: +86 592 2880249. E-mail address: [email protected] (Y. Ye). http://dx.doi.org/10.1016/j.ecoleng.2014.09.102 0925-8574/ ã 2014 Elsevier B.V. All rights reserved.
The importance of mangrove litter fall and its decomposition in the maintenance of debris-based food webs in the coastal waters and their significance for coastal fisheries were indicated (Golley et al., 1962; Odum et al., 1975; Lee, 1995; Ashton et al., 1999). Despite the value and importance of mangrove forests, these ecosystems have been under severe pressure from rapidly increasing human population, large scale deforestation practices and conversion of forests into aquaculture farms (Alongi 2002; Ye et al., 2011; Gross et al., 2014). In order to compensate the losses of mangrove forests and to enhance biological functions of coastal zones, vegetation restoration projects have been carrying out in Jiulongjiang Estuary, China in the past decades (Chen et al., 2007; Chen and Ye, 2011), but to achieve the ultimate goal of ecosystem function restoration there still has a long way to go and the changes in litter decomposition with forest restoration stages should be fully understood. Decomposition of mangrove leaf litter has been studied in numerous subtropical and tropical regions (e.g. Valk and Attiwill, 1984; Woodroffe and Moss, 1984; Benner et al., 1986; Robertson, 1988; Tam et al., 1990; Ananda et al., 2008). Faster decomposition rates result in nutrient retention, while slow decomposition rates increases the chance of leaf litter being exported (Ashton et al.,
T. Li, Y. Ye / Ecological Engineering 73 (2014) 454–460
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respectively (Fig. 1B). In addition, one natural mature K. obovata forest (KM) was also selected as the succession endpoint of restored mangroves (Fig. 1B). The floors of these forests are not inundated during neap tides. Tides are semidiurnal with an average range of 4 m and the mean salinity of open water adjacent to the mangrove forests is about 17.1 psu (Chen et al., 2007). These four forests were subjected to roughly equivalent tidal elevation from field observation and are inundated by high tides for 6–8 days every month. In order to completely represent the litter decomposition condition in these K. obovata forests, mudflat of each forest was divided into three tide stripes, each ranging around 50 m. Sediment and vegetation surveys for these four forests were conducted in each tide strip of each forest in April 2010. One sediment samples (5–25 cm deep) was collected in the middle zone of each stripe to determine moisture, total organic C content, total N content and pH value (Table 2). Density, height and basal diameter of adult trees were recorded within one quadrat of 25 m2 in the middle zone of each stripe (Table 3). Fig. 1. Maps of (A) Caoputou, the study area, and (B) positions of the four studied mangrove forests K48, K24 and K12 for K. obovata forests aged 48, 24 and 12 years, and KM for one natural mature K. obovata forest.
1999 Zhou et al., 2010). Most published information is on genera such as Rhizophora and Avicennia, but data on species such as Kandelia obovata commonly found in subtropical regions are scanty (Tam et al., 1998), and studies associated with the progress of vegetation restoration are even rare. Therefore, the present study focused on the question how decomposition and nutrient dynamics of leaf litter of K. obovata, a species widely distributed and commonly used in mangrove restoration in China, differ among mangrove forests with forest ages. 2. Study area and methods 2.1. Study area From March 2010 to February 2011, field experiments were carried out along the southern coastline of Jiulongjiang Estuary near Caoputou Village (24 24 0 N, 117 55 0 E), Fugong Town, Longhai County, Zhangzhou City, Fujian Province of China (Fig. 1A). The climate of this region is a southern subtropical maritime (Table 1), with annual mean air temperature of 21.0 C. In this region, winter lasts from December to February, and the low air temperatures usually appear in December or January. Spring months (from March to May) are wet season with relatively long rain periods and most of rainfall during hot seasons (summer from June to August or autumn from September to November) is derived from typhoons. To protect the sea bank in this area, several mangrove plantations (mainly the species K. obovata) have been successfully carried out since 1960s so that there are planted K. obovata mangrove forests with different ages. In this study, the selected three K. obovata forests were planted in 1962 (K48), 1986 (K24) and 1998 (K12) with ages of 48, 24 and 12 years (up to the year 2010),
2.2. Leaf litter decomposition experiments Decomposition experiments were seasonally conducted in each of the four chosen K. obovata forests by the litterbag method (Fell et al., 1984) in March 2010, June 2010, September 2010 and February 2011, representing spring, summer, autumn and winter, respectively. In each season, newly fallen leaves with yellow color were randomly picked from each forest. The leaves were washed clean and air-dried for 12 h so that no surface water remained and then about every 20 g leaves were placed into each nylon litter bag (18 25 cm2) with mesh size of 1 mm. The litter bags were securely tied to aerial roots of K. obovata trees so that they were kept to lay on the mud surface during the experiments. Totally 63 bags were prepared for each forest, with 21 bags (7 bags a group fixed on 3 random position) at each tide stripe. Three litter bags were sampled at each tide stripe (one at each position) of each following time, days 0 (not incubated on mud surface), 3, 7, 14, 21, 28 and 35 in spring, summer and autumn, and days 0, 7, 14, 21, 28, 42 and 56 in winter. These samples were brought to the laboratory and gently washed in a sieve to remove sediment. The washed leaf litter was immediately dried at 60 C for 48 h, the final dry weight was recorded, then ground in a mill and passed through the 100-mesh sieve. The powders were stored under desiccant conditions for chemical analyses. 2.3. Chemical analyses Subsamples of leaf litter were digested with sulfuric acid and hydrogen peroxide. N contents were determined by the micro Kjeldahl method and P contents were assayed by the ascorbic acidantimony reducing phosphate colorimetric method. Organic C contents were analyzed by the method from Walkley and Black (1934). The initial dry weight values of leaf litter were converted by the moisture contents and fresh weight of leaf litter in the day 0 bags. All of the chemical analyses were done in laboratory at about 20 C. Three samples were tested for each sampling event at each stripe.
Table 1 Monthly mean climate parameters from December 2009 to November 2010. Parameter
Dec
Jan
Feb
Mar
Apr
May
Jun
Jul
Aug
Sep
Oct
Nov
Temperature ( C) Rainfall(mm)
15.6 29.7
15.1 41.5
16.2 110.3
18.1 18.2
19.6 78.1
24.1 268.9
26.5 119.3
30.1 63.4
29.4 8.2
27.2 157.8
23.8 192.8
19.7 14.5
Data from the local weather bureau of Longhai County about 17 km from the study area.
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T. Li, Y. Ye / Ecological Engineering 73 (2014) 454–460
Table 2 Sediment parameters (5–25 cm deep) in the studied K. obovata forests (mean SE, n = 3). TN (%) and TOC (%) are contents of total nitrogen and total organic carbon in sediments. Forest
pH
TN (%)
TOC (%)
K12 K24 K48 KM
7.05 0.48 6.35 0.48 6.16 0.34 5.50 0.74
0.080 0.011 0.092 0.012 0.101 0.023 0.088 0.025
1.59 0.08 1.73 0.14 1.92 0.21 1.89 0.50
Table 3 Characteristics of plant communities of the studied K. obovata forests (n = 3). Forest
Stem diameter (cm)
Stem height (m)
Tree density (ind hm2)
K12 K24 K48 KM
5.4 0.2 6.7 0.1 9.7 0.4 12.0 1.8
4.5 0.2 5.9 0.4 7.1 0.7 7.0 0.4
10978 1487 15387 12 10233 318 9733 400
2.4. Statistical analysis The relationship between the percentage of initial dry weight remaining in litter bags and sampling time was best fitted by the negative single exponential model (with correction factor): X t ¼ aekt where Xt is the percentage of the initial material remaining after decomposition time (t), a is the correction factor and k is a decomposition coefficient. The times required for the decomposition of the half the initial material (T50) were determined by the equation T50 = ln (a/50)/k. Differences in litter decomposition rates and changes in nutrients (organic C, N, P) among the four forests (K12, K24, K48 and KM) and four seasons (spring, summer, autumn and winter) with decomposition time series of 1, 2, 3, 4 and 5 weeks were tested by repeated measures two-way analysis of variance (ANOVA) with decomposition time as within-subject factor, forest age and season as between-subject factors. One-way ANOVA test was employed to evaluate any difference in T50 among the four forests in each season. The same test was used to assess any difference in litter decomposition rate, initial concentrations of nutrients and nutrient release in leaf litter among the four forests. All analyses were performed by SPSS16.0 and Excel 2003 for Windows.
Table 4 Results of repeated measures ANOVA for dry weight loss during decomposition of leaf litter in the studied K. obovata forests. Source of variation Within-subject Time Time age Time season Time age season Error Between-subject Age Season Age season Error
df
MS
F
p
4 12 12 36 128
0.951 0.004 0.021 0.002 0.000
3017.056 11.358 66.027 7.746
0.000 0.000 0.000 0.000
3 3 9 32
0.009 0.551 0.006 0.001
14.474 902.692 9.876
0.000 0.000 0.000
Within-subject factor is decomposition time; between-subject factors are forest age and season. Decomposition time refers to the number of weeks (1, 2, 3, 4 and 5) leaf litter bags were in the field.
3. Results 3.1. Leaf litter decomposition There were significantly interactive effects of forest age, season and decomposition time on dry weight losses during leaf litter decomposition (Table 4), and the highly significant effect of decomposition time suggests that dry weight loss changed significantly in leaf litter over the incubation period. Decomposition rates varied not only within the incubation period, but also among forests and seasons. Statistical significance of ‘forest by time’ and ‘season by time’ interaction suggest that rate and pattern of decomposition of K. obovata leaf litter were significantly different at harvest times over the total incubation period, when the younger forests compared with the older forests or the hotter seasons compared with the colder seasons. Leaf litter of K. obovata in each forest degraded rapidly in the first 3 weeks, with about 30% of litter dry weight loss from the litter bag (Fig. 2). The decomposition rate of leaf litter reached its maximum within two weeks. At the end of the incubation (5–7 weeks), leaf materials of K. obovata were difficult to be identified and the residues were intermingled with sediment inside the bags, so the field decomposition experiment is hard to proceed any longer with this litter bag method. The decomposition patterns observed in different seasons and different forests were similar, with very rapid early losses. Such decomposition patterns were better described by simple negative exponential 2 Equations than simple linear regression equations as R (coefficient of determination) values of the exponential regression were higher than the linear regression (Tam et al., 1998), so exponential equations were used to create fitting curves of leaf litter decomposition (Table 5). Despite the similarity in litter decomposition pattern among the four K. obovata forests, mean half-time of leaf decomposition (T50) values were significantly different among the four forests in each season except for winter (p < 0.001, F = 20.659 in spring; p = 0.005, F = 9.802 in summer; p = 0.002, F = 13.699 in autumn; p > 0.05 in winter according to one-way ANOVA). Mean T50 was 29.8 d in spring, 18.7d in summer, 23.9 d in autumn and 47.4 d in winter with an order of increasing degradation rate as summer > autumn > spring > winter. There were higher decomposition rates and more significant differences among seasons at the early periods of the experiment than the remaining periods. Decomposition rates were lower in the older forests (with T50 values of 30.1 and 31.1d averaged by all seasons in K48 and KM, respectively) than in the younger ones (with T50 values 29.8 and 28.8d averaged by all seasons in K12 and K24, respectively), especially in summer and autumn. Averaged by all of the forests and seasons, T50 value of dry weight loss during decomposition of leaf litter was 29.9d. 3.2. Nutrient releases The nutrient (organic C, N, P) contents in K. obovata leaf litter were analyzed during the decomposition processes. The initial values of the contents of C, N and P in leaf litter at the beginning of decomposition decreased with the increasing forest age and C:N ratios of younger forests (K12 and K24) were significantly higher than those of older forests (K48 and KM), but there were not significant differences in any of these parameters between K48 and KM (Table 6). There were significant effects of forest age, season and decomposition time on nutrient releases duing leaf litter decomposition (Tables 7–9). Nutrient releases of organic C, N and P during decomposition experiments were closely paralleled with dry weight losses (Figs. 3–5). The loss percentages of C were very similar to those of dry weight losses, while the loss percentages of N were slightly lower and the loss percentages of P were faster than
T. Li, Y. Ye / Ecological Engineering 73 (2014) 454–460
Dry weight loss (%)
80
K12
80 60
60
40
40
20
20
K24
0
0 0
7
14
21
80 Dry weight loss (%)
457
28
35
42
49
56
0
63
7
14
21
80
K48
60
60
40
40
20
20
0
28
35
42
49
56
63
KM
Spring Summer Autumn Winter
0 0
7
14
21
28 35 42 Time (days)
49
56
63
0
7
14
21
28 35 42 Time (days )
49
56
63
Fig. 2. Loss percentages of initial dry weight during decomposition of leaf litter in the studied K. obovata forests (n = 3).
Table 5 Simple negative exponential regression equations (X = aekt) on % of litter mass remaining in litter bags (X) against time (t) during decomposition of leaf litter in the studied K. obovata forests. Season
Forest
R2
k
T50 (n = 3)
Spring
K12 K24 K48 KM K12 K24 K48 KM K12 K24 K48 KM K12 K24 K48 KM
0.969 0.962 0.938 0.993 0.982 0.965 0.969 0.986 0.914 0.944 0.926 0.947 0.901 0.903 0.886 0.934
0.023 0.026 0.023 0.023 0.038 0.031 0.031 0.032 0.025 0.025 0.024 0.023 0.013 0.013 0.013 0.013
32.2 1.27c 26.9 0.69a 29.9 0.41b 30.3 0.71b 16.9 0.72a 18.1 1.19ab 19.1 0.99bc 20.7 0.51c 22.0 1.33a 23.2 0.58ab 24.1 0.51b 26.1 0.52c 47.9 1.32a 46.9 2.52a 47.4 2.90a 47.3 2.76a
Summer
Autumn
Winter
R, coefficient of determination; k, decomposition constant; T50, half life time. Different letters after T50 data in the same season indicate statistically significant differences among forests in each season at the level of 0.05.
Table 6 Initial contents of nutrients in leaf litter at the beginning of decomposition in the studied K. obovata forests. Forest
C (%)
N (%)
P (%)
C:N
K12 K24 K48 KM
45.28 0.84b 44.50 0.65b 43.15 0.51a 43.29 0.17a
1.06 0.02c 0.91 0.03b 0.72 0.04a 0.70 0.05a
0.122 0.003b 0.109 0.003a 0.104 0.003a 0.101 0.009a
42.80 0.29c 49.01 1.41b 60.06 3.46a 61.71 4.26a
Table 7 Results of repeated measures ANOVA for C losses during decomposition of leaf litter in the studied K. obovata forests. Source of variation Within-subject Time Time age Time season Time age season Error Between-subject Age Season Age season Error
df
MS
F
p
4 12 12 36 128
0.934 0.004 0.028 0.002 0.000
4103.597 16.024 122.040 8.452
0.000 0.000 0.000 0.000
3 3 9 32
0.008 0.535 0.010 0.001
8.408 573.446 10.626
0.000 0.000 0.000
Table 8 Results of repeated measures ANOVA for N losses during decomposition of leaf litter in the studied K. obovata forests. Source of variation Within-subject Time Time age Time season Time age season Error Between-subject Age Season Age season Error
df
MS
F
p
4 12 12 36 128
1.057 0.006 0.042 0.003 0.002
557.205 3.208 22.126 1.710
0.000 0.000 0.000 0.016
3 3 9 32
0.179 0.429 0.024
62.354 149.330 8.412
0.000 0.000 0.000
Different letter indicate statistically significant differences among forests at the level of 0.05.
those of dry weight losses. More rapid releasing of organic C, N and P from decomposed leaves were found in summer and autumn than in winter and spring, indicating more nutrients were released and exported to the surrounding waters in hot seasons. For N concentrations in the residual litter materials during decomposition (Fig. 4), there were general increases from the 2nd to the 3rd or the 4th weeks of leaf litter decomposition in Spring, Summer and Autumn. After these periods, the N remaining in litter materials declined steadily. P remaining in the residual litter material rapidly
decreased during the first 3 weeks and then decreased gradually (Fig. 5). After 35 days’ decomposition, the nutrients releases from leaf litter were around 54% for organic C, 50% for N and 66% for P in spring, 68% for C, 62% for N and 76% for P in summer, 57% for C, 53% for N and 68% for P in autumn, and 41% for C, 29% for N and 49% for P in winter. The decomposition patterns of nutrients in K. obovata leaf litter were also described by simple negative exponential 2 Equations
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T. Li, Y. Ye / Ecological Engineering 73 (2014) 454–460
Table 9 Results of repeated measures ANOVA for P losses during decomposition of leaf litter in the studied K. obovata forests. Source of Variation Within-subject Time Time age Time season Time age season Error Between-subject Age Season Age season Error
df
MS
F
p
4 12 12 36 128
1.016 0.004 0.017 0.001 0.002
495.825 1.712 8.097 0.622
0.000 0.071 0.000 0.950
3 3 9 32
0.023 0.559 0.010 0.005
4.859 116.932 2.167
0.007 0.000 0.052
4. Discussion
Within-subject factor is decomposition time; between-subject factors are forest age and season. Decomposition time refers to the number of weeks (1, 2, 3, 4 and 5) leaf litter bags were in the field.
K12 K48
110
K24 KM
% C remaining
90 Spring
70
Mangrove litter has been reported to be quickly decomposed with rapid decreases in dry weight and high leaching rates in the first few weeks of exposure in the field (Valk and Attiwill, 1984; Mfilinge et al., 2005). In the present study, the highest decomposition rate occurred in the 2nd week in winter and in the first week in other seasons, and then followed by slower decreases for the rest of the experiment period. This quick decomposition at early stage might be related to leaching of soluble organic materials and inorganic compounds such as
110 90 S ummer
70
50
50
30
30
10
10 0
10
20
30
40
110 % C remaining
releases during decomposition of leaf litter. Averaged by data in the four forests, T50 values of releases of C, N and P during decomposition of leaf litter were 29.4, 40.4 and 21.2d.
0
10
20
30
40
110
90
Autumn
90
70
70
50
50
30
30
10
Winter
10 0
10
20 Time (days)
30
40
20
0
40
60
Time (days)
Fig. 3. Remaining percentages of organic C during decomposition of leaf litter in the studied K. obovata forests (n = 3).
K12 K48
% N remaining
120
K24 KM
100
S pring
100
80
80
60
60
40
40
S ummer
20
20 0
10
20
30
0
40
120 % N remaining
120
10
20
30
40
120
100
Autumn
100
80
80
60
60
40
40
20
Winter
20 0
10
20 Time (days)
30
40
0
20
40
60
Time (days)
Fig. 4. Remaining percentages of N during decomposition of leaf litter in the studied K. obovata forests (n = 3).
(Table 10). The four forests had significantly different T50 values of releases of C, N and P during decomposition of leaf litter, with larger differences in N releases than those in C and P releases. Generally, T50 values of nutrient releases increased with forest age, indicating that the longer the forest grows, the slower the nutrients
soluble sugars (Steinke et al., 1993). A slower loss of dry weight reflected the loss of more resistant materials (Steinke et al., 1990). The decomposition pattern in the present study was similar to those observed in previous studies (Twilley et al., 1986; Mackey and Smail, 1996; Wafar et al., 1997; Imgraben and Dittmann, 2008).
T. Li, Y. Ye / Ecological Engineering 73 (2014) 454–460
K12 K48
% P remaining
110
K24 KM
90
S pring
90 70
50
50
30
30
10
10 10
20
30
S ummer
0
40
110 % P remaining
110
70
0
459
10
20
30
40
110
90
Autumn
90
70
70
50
50
30
30
10
Winter
10 0
10
20 Time (days)
30
40
0
20
40
60
Time (days)
Fig. 5. Remaining percentages of P during decomposition of leaf litter in the studied K. obovata forests (n = 3).
Leaf litter decomposition can be influenced by not only seasons (Mackey and Smail, 1996) but also spatial scales such as tidal levels (Lee, 1989; Mackey and Smail, 1996; Dick and Osunkoya, 2000; Mfilinge et al., 2002). The decomposition rates in both summer and winter from K. obovata forests in Jiulongjiang Estuary in China in the present study, with T50 of dry weight losses of 18.7 and 47.4d respectively, were much slower than those with corresponding values of 13 and 42d from mangrove forests of the same species in Hong Kong (Tam et al., 1990), about 2 -latitude and 2 C annual mean air temperature less than the area of the present study. The decomposition rates of leaf litter in each of the four mangrove forests in the present study were more rapid in summer than those in winter because activities of microbes increased in hot seasons, as reported in other mangrove forests (Lin, 1999). Earlier studies indicated that initial nutrients level of litter, in particular N content, has a controlling influence on litter decomposition rates (Melillo et al., 1982; Twilley et al., 1997). Decomposition rates generally increase for litter with high leaf N content (Pelegraí et al., 1997). Fenchel et al. (1998) suggested that high initial N content or low C:N ratio in litter would result in high microbial assimilation and mineralization efficiencies, and less immobilization effects, hence accelerate the decomposition of litter fall. Certainly, we observed a steady enrichment of litter N in
Table 10 Simple negative exponential regression equations (X = aekt) on % of annual litter nutrients remaining in litter bags (X) against time (t) during decomposition of leaf litter in the studied K. obovata forests. Nutrient
Forest
R2
k
T50 (n = 3)
C remaining
K12 K24 K48 KM K12 K24 K48 KM K12 K24 K48 KM
0.992 0.985 0.985 0.989 0.988 0.949 0.903 0.979 0.979 0.962 0.964 0.978
0.023 0.022 0.022 0.022 0.022 0.020 0.014 0.017 0.032 0.028 0.028 0.029
28.6 0.57a 28.8 1.09a 29.2 0.63a 30.9 1.02b 32.3 0.68a 36.9 0.84b 51.1 3.24 d 41.1 1.82c 19.4 0.74a 21.3 0.43ab 21.4 1.13ab 22.5 1.60b
N remaining
P remaining
R, coefficient of determination; k, decomposition constant; T50, half life time. Different letters after T50 data for the same nutrient indicate statistically significant differences among forests at the level of 0.05.
the first 3 weeks of decomposition and N quantity declined much slower than organic C and P. This may be due to the rapid releases of soluble forms of P from litter by leaching (Steinke et al., 1993; Tam et al., 1998). The decomposition of leaf litter is greatly associated with the surrounding environment which can be largely changed with the development of a restored forest. At different stages of a restored mangrove ecosystem, many factors such as litter production, microbiological activity, inundation condition, aerobic condition of sediment, faunal communities and litter nutritional values also changed (Clough et al., 2000; Morrisey et al., 2003; Nga et al., 2005; Chen et al., 2007; Ye et al., 2013). The present study showed that initial N and P levels in leaf litter declined as the increase in forest age of K. obovata forests. This is in line with findings from Nga et al. (2005) that mangrove plants in younger forests (7 and 11 years) are able to take up more N and P than those in older forests (17 and 24 years) and the formers produce a large quantity of higher quality litter as input to the aquatic system. Hong and San (1993) concluded that old trees produce much woody materials, such as stems, branches and reproductive parts, while young trees produce more leaves. Clough et al. (2000) even indicated that the leaf area index (LAI) decreased with the increase in mangrove forest age, resulting in more closed canopy in young forests than in old ones. Chen et al. (2007) showed that younger forests (4 and 7 years) generally had more macro-benthic fauna species than older ones (19 and 43 years). In a conclusion, litter decomposition rate is inevitably to show some differences with the development of a restored mangrove forest, as is indicated by the present study that litter decomposition rates are directly correlated to the age of the mangrove forests. We found that leaf litter lose its dry weight and nutrients (organic C, N, P) significantly faster in younger forests (K12, K24) than in older forests (K48, KM), especially during the hotter and wetter seasons (summer and autumn). With the development of restored mangrove forests, slower decomposition and nutrient release of leaf litter may increase the chance of leaf litter being exported into ocean. Acknowledgements The work described in this paper is supported by the grants from National Natural Science Foundation of China (Project no.
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41076049 and 41276077). We thank Baipeng Pang and Yantao Gu for their dedicating work in the field and/or laboratory. Reference Alongi, D.M., 2002. Present state and future of the world’s mangrove forests. Environ. Conserv. 29, 331–349. Ananda, K., Sridhar, K., Raviraja, N., Bärlocher, F., 2008. Breakdown of fresh and dried Rhizophora mucronata leaves in a mangrove of Southwest India. Wetland. Ecol. Manage. 16, 1–9. Ashton, E., Hogarth, P., Ormond, R., 1999. Breakdown of mangrove leaf litter in a managed mangrove forest in Peninsular Malaysia. Hydrobiologia 413, 77–88. Benner, R., Peele, E.R., Hodson, R.E., 1986. Microbial utilization of dissolved organic matter from leaves of the red mangrove Rhizophora mangle, in the Fresh Creek estuary, Bahamas. Est. Coast. Shelf. Sci. 23, 607–619. Bosire, J., Dahdouh-Guebas, F., Kairo, J., Kazungu, J., Dehairs, F., Koedam, N., 2005. Litter degradation and CN dynamics in reforested mangrove plantations at Gazi Bay. Kenya Biol. Conserv. 126, 287–295. Boulton, A., Boon, P., 1991. A review of methodology used to measure leaf litter decomposition in lotic environments: time to turn over an old leaf. Mar. Freshwater Res. 42, 1–43. Bunt, J., Boto, K., Boto, G., 1979. A survey method for estimating potential levels of mangrove forest primary production. Mar. Biol. 52, 123–128. Chen, G.C., Ye, Y., 2011. Restoration of Aegiceras corniculatum mangroves in Jiulongjiang Estuary changed macro-benthic faunal community. Ecol. Eng. 37, 224–228. Chen, G.C., Ye, Y., Lu, C.Y., 2007. Changes of macro-benthic faunal community with stand age of rehabilitated Kandelia candel mangrove in Jiulongjiang Estuary. China. Ecol. Eng. 31, 215–224. Clough, B., Tan, D.T., Phuong, D.X., Buu, D.C., 2000. Canopy leaf area index and litter fall in stands of the mangrove Rhizophora apiculata of different age in the Mekong Delta. Vietnam. Aquat. Bot. 66, 311–320. Dick, T.M., Osunkoya, O.O., 2000. Influence of tidal restriction floodgates on decomposition of mangrove litter. Aquat. Bot. 68, 273–280. Fell, J.W., Master, I.M., Wiegert, R.G., 1984. Litter decomposition and nutrient enrichment. In: Snedaker, S.C., Snedaker, J.G. (Eds.), The Mangrove Ecosystem: Research Methods. Unesco/SCOR, UK, pp. 239–251. Fenchel, T., King, G.M., Blackburn, T.H., 1998. Bacterial Biogeochemistry: the Ecophysiology of Mineral Cycling, second ed. Academic Press, San Diego. Golley, F., Odum, H.T., Wilson, R.F., 1962. The structure and metabolism of a Puerto Rican red mangrove forest in May. Ecology 43, 9–19. Gross, J., Flores, E.E., Schwendenmann, L., 2014. Stand structure and aboveground biomass of a Pelliciera rhizophorae mangrove forest, Gulf of Monitjo Ramsar Site, Pacific Coast, Panama. Wetlands 34, 55–65. Harley, J., 1971. Fungi in ecosystems. J. Ecol. 59, 653–668. Hong, P.N., San, T.H., 1993. Mangroves of Vietnam. IUCN, Bangkok, Tailand. Imgraben, S., Dittmann, S., 2008. Leaf litter dynamics and litter consumption in two temperate South Australian mangrove forests. J. Sea Res. 59, 83–93. Lee, S., 1989. Litter production and turnover of the mangrove Kandelia candel (L.) Druce in a Hong Kong tidal shrimp pond. Est. Coast. Shelf. Sci. 29, 75–87. Lee, S., 1995. Mangrove outwelling: a review. Hydrobiologia 295, 203–212. Lin, P., 1999. Mangrove Ecosystem in China. Scientific Press, Beijing. Lugo, A.E., Snedaker, S.C., 1974. The ecology of mangroves. Annu. Rev. Ecol. Syst. 5, 39–64. Mackey, A., Smail, G., 1996. The decomposition of mangrove litter in a subtropical mangrove forest. Hydrobiologia 332, 93–98.
Melillo, J.M., Aber, J.D., Muratore, J.F., 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63, 621–626. Mfilinge, P., Atta, N., Tsuchiya, M., 2002. Nutrient dynamics and leaf litter decomposition in a subtropical mangrove forest at Oura Bay Okinawa, Japan. Trees-Struct. Funct. 16, 172–180. Mfilinge, P.L., Meziane, T., Bachok, Z., Tsuchiya, M., 2005. Litter dynamics and particulate organic matter outwelling from a subtropical mangrove in Okinawa Island. South Japan. Est. Coast. Shelf. Sci. 63, 301–313. Morrisey, D., Skilleter, G., Ellis, J., Burns, B., Kemp, C., Burt, K., 2003. Differences in benthic fauna and sediment among mangrove (Avicennia marina var: australasica) stands of different ages in New Zealand. Est. Coast. Shelf. Sci. 56, 581–592. Nga, B., Tinh, H., Tam, D., Scheffer, M., Roijackers, R., 2005. Young mangrove stands produce a large and high quality litter input to aquatic systems. Wetland. Ecol. Manag. 13, 569–576. Odum, W., Heald, E., Cronin, L., 1975. The detritus-based food web of an estuarine community. Est. Res. 1, 265. Pelegraí, S.P., Rivera-Monroy, V.H., Twilley, R.R., 1997. A comparison of nitrogen fixation (acetylene reduction) among three species of mangrove litter, sediments, and pneumatophores in south Florida, USA. Hydrobiologia 356, 73–79. Robertson, A., 1988. Decomposition of mangrove leaf litter in tropical Australia. J. Exp. Mar. Biol. Ecol. 116, 235–247. Steinke, T., Barnabas, A., Somaru, R., 1990. Structural changes and associated microbial activity accompanying decomposition of mangrove leaves in Mgeni Estuary. S. Afr. J. Bot. 56, 39–48. Steinke, T., Holland, A., Singh, Y., 1993. Leaching losses during decomposition of mangrove leaf litter. S. Afr. J. Bot. 59, 21–25. Tam, N.F.Y., Vrijmoed, L., Wong, Y.S., 1990. Nutrient dynamics associated with leaf decomposition in a small subtropical mangrove community in Hong Kong. B. Mar. Sci. 47, 68–78. Tam, N.F., Wong, Y.S., Lan, C., Wang, L., 1998. Litter production and decomposition in a subtropical mangrove swamp receiving wastewater. J. Exp. Mar. Biol. Ecol. 226, 1–18. Twilley, R.R., Pozo, M., Garcia, V.H., Rivera-Monroy, V.H., Zambrano, R., Bodero, A., 1997. Litter dynamics in riverine mangrove forests in the Guayas River estuary. Ecuador. Oecologia 111, 109–122. Twilley, R.W., Lugo, A.E., Patterson-Zucca, C., 1986. Litter production and turnover in basin mangrove forests in southwest Florida. Ecology 67, 670–683. Valk, A.G.V., Attiwill, P., 1984. Decomposition of leaf and root litter of Avicennia marina at Westernport Bay Victoria Australia. Aquat. Bot. 18, 205–221. Wafar, S., Untawale, A., Wafar, M., 1997. Litter fall and energy flux in a mangrove ecosystem. Est. Coast. Shelf. Sci. 44, 111–124. Walkley, A., Black, I.A., 1934. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci. 37, 29. Woodroffe, C.D., Moss, T.J., 1984. Litter fall beneath Rhizophora stylosa Griff. Vaitupu, Tuvalu,South Pacific. Aquat. Bot. 18, 249–255. Ye, Y., Pang, B., Chen, G., Chen, Y., 2011. Processes of organic carbon in mangrove ecosystems. Acta Ecol. Sin. 31 (3), 169–173. Ye, Y., Chen, Y.P., Chen, G.C., 2013. Litter production and litter elemental composition in two rehabilitated Kandelia obovata mangrove forests in Jiulongjiang Estuary, China. Mar. Environ. Res. 83, 63–72. Zhou, H.C., Wei, S.D., Zeng, Q., Zhang, L.H., Tam, N.F., Lin, Y.M., 2010. Nutrient and caloric dynamics in Avicennia marina leaves at different developmental and decay stages in Zhangjiang River Estuary. China. Est. Coast. Shelf. Sci. 87, 21–26.
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Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
Dynamics of decomposition and nutrient release of leaf litter in Kandelia obovata mangrove forests with different ages in Jiulongjiang Estuary, China Ting Li a,b , Yong Ye a, * a Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystem, College of the Environment and Ecology, Xiamen University, Xiamen,Fujian, China b South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 June 2014 Received in revised form 12 September 2014 Accepted 29 September 2014 Available online xxx
Rates of in-situ decomposition and nutrient (organic C, N and P) release of leaf litter were seasonally compared among three planted Kandelia obovata mangrove forests (K12, K24 and K48 with forest ages of 12, 24 and 48 years, respectively) and one natural mature K. obovata forest (KM) in Jiulongjiang Estuary, China. The average values of half-time (T50) of leaf litter decomposition in spring, summer, autumn and winter were 29.8, 18.7, 23.9 and 47.4d, respectively. Decomposition rates were lower in the older forests (with T50 values of 30.1 and 31.1d averaged by all seasons in K48 and KM, respectively) than in the younger ones (with T50 values 29.8 and 28.8d averaged by all seasons in K12 and K24, respectively), especially in summer and autumn. The annual mean T50 of nutrient release of leaf litter during decomposition followed an order of KM > K48 > K24 > K12. During leaf litter decomposition, C releases were very similar to dry weight losses, while N releases were slower and P releases were much faster than dry weight losses. With the development of restored mangrove forests, decomposition and nutrient release of leaf litter became slow, which may increase the chance of leaf litter being exported into the surrounding waters. ã 2014 Elsevier B.V. All rights reserved.
Keywords: Mangrove Kandelia obovata Leaf litter Decomposition Nutrient release Forest age
1. Introduction Mangrove forests are extremely open and productive ecosystems providing large amounts of energy and organic matter to estuarine and coastal systems via litter fall and decomposition (Lugo and Snedaker, 1974; Mackey and Smail, 1996; Ye et al., 2011). Litter fall has been estimated to account for 30–60% of total primary production of mangrove forests (Bunt et al., 1979). The high productivity was often attributed to rapid litter decomposition and efficient recycling of nutrient elements in mangrove forests (Bosire et al., 2005). Most of mangrove primary production, mainly consisting of mangrove leaves, becomes available to consumers after senescence and breakdown. Decomposition of litter fall is one of the basic functions of forest ecosystems (Harley, 1971; Ananda et al., 2008). The rate and extent of in situ decomposition governs how much of organic matter and nutrients is recycled within the mangrove forest, and how much is exported to near-shore waters (Boulton and Boon, 1991 Zhou et al., 2010).
* Corresponding author. Tel.: +86 592 2880249; fax: +86 592 2880249. E-mail address: [email protected] (Y. Ye). http://dx.doi.org/10.1016/j.ecoleng.2014.09.102 0925-8574/ ã 2014 Elsevier B.V. All rights reserved.
The importance of mangrove litter fall and its decomposition in the maintenance of debris-based food webs in the coastal waters and their significance for coastal fisheries were indicated (Golley et al., 1962; Odum et al., 1975; Lee, 1995; Ashton et al., 1999). Despite the value and importance of mangrove forests, these ecosystems have been under severe pressure from rapidly increasing human population, large scale deforestation practices and conversion of forests into aquaculture farms (Alongi 2002; Ye et al., 2011; Gross et al., 2014). In order to compensate the losses of mangrove forests and to enhance biological functions of coastal zones, vegetation restoration projects have been carrying out in Jiulongjiang Estuary, China in the past decades (Chen et al., 2007; Chen and Ye, 2011), but to achieve the ultimate goal of ecosystem function restoration there still has a long way to go and the changes in litter decomposition with forest restoration stages should be fully understood. Decomposition of mangrove leaf litter has been studied in numerous subtropical and tropical regions (e.g. Valk and Attiwill, 1984; Woodroffe and Moss, 1984; Benner et al., 1986; Robertson, 1988; Tam et al., 1990; Ananda et al., 2008). Faster decomposition rates result in nutrient retention, while slow decomposition rates increases the chance of leaf litter being exported (Ashton et al.,
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respectively (Fig. 1B). In addition, one natural mature K. obovata forest (KM) was also selected as the succession endpoint of restored mangroves (Fig. 1B). The floors of these forests are not inundated during neap tides. Tides are semidiurnal with an average range of 4 m and the mean salinity of open water adjacent to the mangrove forests is about 17.1 psu (Chen et al., 2007). These four forests were subjected to roughly equivalent tidal elevation from field observation and are inundated by high tides for 6–8 days every month. In order to completely represent the litter decomposition condition in these K. obovata forests, mudflat of each forest was divided into three tide stripes, each ranging around 50 m. Sediment and vegetation surveys for these four forests were conducted in each tide strip of each forest in April 2010. One sediment samples (5–25 cm deep) was collected in the middle zone of each stripe to determine moisture, total organic C content, total N content and pH value (Table 2). Density, height and basal diameter of adult trees were recorded within one quadrat of 25 m2 in the middle zone of each stripe (Table 3). Fig. 1. Maps of (A) Caoputou, the study area, and (B) positions of the four studied mangrove forests K48, K24 and K12 for K. obovata forests aged 48, 24 and 12 years, and KM for one natural mature K. obovata forest.
1999 Zhou et al., 2010). Most published information is on genera such as Rhizophora and Avicennia, but data on species such as Kandelia obovata commonly found in subtropical regions are scanty (Tam et al., 1998), and studies associated with the progress of vegetation restoration are even rare. Therefore, the present study focused on the question how decomposition and nutrient dynamics of leaf litter of K. obovata, a species widely distributed and commonly used in mangrove restoration in China, differ among mangrove forests with forest ages. 2. Study area and methods 2.1. Study area From March 2010 to February 2011, field experiments were carried out along the southern coastline of Jiulongjiang Estuary near Caoputou Village (24 24 0 N, 117 55 0 E), Fugong Town, Longhai County, Zhangzhou City, Fujian Province of China (Fig. 1A). The climate of this region is a southern subtropical maritime (Table 1), with annual mean air temperature of 21.0 C. In this region, winter lasts from December to February, and the low air temperatures usually appear in December or January. Spring months (from March to May) are wet season with relatively long rain periods and most of rainfall during hot seasons (summer from June to August or autumn from September to November) is derived from typhoons. To protect the sea bank in this area, several mangrove plantations (mainly the species K. obovata) have been successfully carried out since 1960s so that there are planted K. obovata mangrove forests with different ages. In this study, the selected three K. obovata forests were planted in 1962 (K48), 1986 (K24) and 1998 (K12) with ages of 48, 24 and 12 years (up to the year 2010),
2.2. Leaf litter decomposition experiments Decomposition experiments were seasonally conducted in each of the four chosen K. obovata forests by the litterbag method (Fell et al., 1984) in March 2010, June 2010, September 2010 and February 2011, representing spring, summer, autumn and winter, respectively. In each season, newly fallen leaves with yellow color were randomly picked from each forest. The leaves were washed clean and air-dried for 12 h so that no surface water remained and then about every 20 g leaves were placed into each nylon litter bag (18 25 cm2) with mesh size of 1 mm. The litter bags were securely tied to aerial roots of K. obovata trees so that they were kept to lay on the mud surface during the experiments. Totally 63 bags were prepared for each forest, with 21 bags (7 bags a group fixed on 3 random position) at each tide stripe. Three litter bags were sampled at each tide stripe (one at each position) of each following time, days 0 (not incubated on mud surface), 3, 7, 14, 21, 28 and 35 in spring, summer and autumn, and days 0, 7, 14, 21, 28, 42 and 56 in winter. These samples were brought to the laboratory and gently washed in a sieve to remove sediment. The washed leaf litter was immediately dried at 60 C for 48 h, the final dry weight was recorded, then ground in a mill and passed through the 100-mesh sieve. The powders were stored under desiccant conditions for chemical analyses. 2.3. Chemical analyses Subsamples of leaf litter were digested with sulfuric acid and hydrogen peroxide. N contents were determined by the micro Kjeldahl method and P contents were assayed by the ascorbic acidantimony reducing phosphate colorimetric method. Organic C contents were analyzed by the method from Walkley and Black (1934). The initial dry weight values of leaf litter were converted by the moisture contents and fresh weight of leaf litter in the day 0 bags. All of the chemical analyses were done in laboratory at about 20 C. Three samples were tested for each sampling event at each stripe.
Table 1 Monthly mean climate parameters from December 2009 to November 2010. Parameter
Dec
Jan
Feb
Mar
Apr
May
Jun
Jul
Aug
Sep
Oct
Nov
Temperature ( C) Rainfall(mm)
15.6 29.7
15.1 41.5
16.2 110.3
18.1 18.2
19.6 78.1
24.1 268.9
26.5 119.3
30.1 63.4
29.4 8.2
27.2 157.8
23.8 192.8
19.7 14.5
Data from the local weather bureau of Longhai County about 17 km from the study area.
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T. Li, Y. Ye / Ecological Engineering 73 (2014) 454–460
Table 2 Sediment parameters (5–25 cm deep) in the studied K. obovata forests (mean SE, n = 3). TN (%) and TOC (%) are contents of total nitrogen and total organic carbon in sediments. Forest
pH
TN (%)
TOC (%)
K12 K24 K48 KM
7.05 0.48 6.35 0.48 6.16 0.34 5.50 0.74
0.080 0.011 0.092 0.012 0.101 0.023 0.088 0.025
1.59 0.08 1.73 0.14 1.92 0.21 1.89 0.50
Table 3 Characteristics of plant communities of the studied K. obovata forests (n = 3). Forest
Stem diameter (cm)
Stem height (m)
Tree density (ind hm2)
K12 K24 K48 KM
5.4 0.2 6.7 0.1 9.7 0.4 12.0 1.8
4.5 0.2 5.9 0.4 7.1 0.7 7.0 0.4
10978 1487 15387 12 10233 318 9733 400
2.4. Statistical analysis The relationship between the percentage of initial dry weight remaining in litter bags and sampling time was best fitted by the negative single exponential model (with correction factor): X t ¼ aekt where Xt is the percentage of the initial material remaining after decomposition time (t), a is the correction factor and k is a decomposition coefficient. The times required for the decomposition of the half the initial material (T50) were determined by the equation T50 = ln (a/50)/k. Differences in litter decomposition rates and changes in nutrients (organic C, N, P) among the four forests (K12, K24, K48 and KM) and four seasons (spring, summer, autumn and winter) with decomposition time series of 1, 2, 3, 4 and 5 weeks were tested by repeated measures two-way analysis of variance (ANOVA) with decomposition time as within-subject factor, forest age and season as between-subject factors. One-way ANOVA test was employed to evaluate any difference in T50 among the four forests in each season. The same test was used to assess any difference in litter decomposition rate, initial concentrations of nutrients and nutrient release in leaf litter among the four forests. All analyses were performed by SPSS16.0 and Excel 2003 for Windows.
Table 4 Results of repeated measures ANOVA for dry weight loss during decomposition of leaf litter in the studied K. obovata forests. Source of variation Within-subject Time Time age Time season Time age season Error Between-subject Age Season Age season Error
df
MS
F
p
4 12 12 36 128
0.951 0.004 0.021 0.002 0.000
3017.056 11.358 66.027 7.746
0.000 0.000 0.000 0.000
3 3 9 32
0.009 0.551 0.006 0.001
14.474 902.692 9.876
0.000 0.000 0.000
Within-subject factor is decomposition time; between-subject factors are forest age and season. Decomposition time refers to the number of weeks (1, 2, 3, 4 and 5) leaf litter bags were in the field.
3. Results 3.1. Leaf litter decomposition There were significantly interactive effects of forest age, season and decomposition time on dry weight losses during leaf litter decomposition (Table 4), and the highly significant effect of decomposition time suggests that dry weight loss changed significantly in leaf litter over the incubation period. Decomposition rates varied not only within the incubation period, but also among forests and seasons. Statistical significance of ‘forest by time’ and ‘season by time’ interaction suggest that rate and pattern of decomposition of K. obovata leaf litter were significantly different at harvest times over the total incubation period, when the younger forests compared with the older forests or the hotter seasons compared with the colder seasons. Leaf litter of K. obovata in each forest degraded rapidly in the first 3 weeks, with about 30% of litter dry weight loss from the litter bag (Fig. 2). The decomposition rate of leaf litter reached its maximum within two weeks. At the end of the incubation (5–7 weeks), leaf materials of K. obovata were difficult to be identified and the residues were intermingled with sediment inside the bags, so the field decomposition experiment is hard to proceed any longer with this litter bag method. The decomposition patterns observed in different seasons and different forests were similar, with very rapid early losses. Such decomposition patterns were better described by simple negative exponential 2 Equations than simple linear regression equations as R (coefficient of determination) values of the exponential regression were higher than the linear regression (Tam et al., 1998), so exponential equations were used to create fitting curves of leaf litter decomposition (Table 5). Despite the similarity in litter decomposition pattern among the four K. obovata forests, mean half-time of leaf decomposition (T50) values were significantly different among the four forests in each season except for winter (p < 0.001, F = 20.659 in spring; p = 0.005, F = 9.802 in summer; p = 0.002, F = 13.699 in autumn; p > 0.05 in winter according to one-way ANOVA). Mean T50 was 29.8 d in spring, 18.7d in summer, 23.9 d in autumn and 47.4 d in winter with an order of increasing degradation rate as summer > autumn > spring > winter. There were higher decomposition rates and more significant differences among seasons at the early periods of the experiment than the remaining periods. Decomposition rates were lower in the older forests (with T50 values of 30.1 and 31.1d averaged by all seasons in K48 and KM, respectively) than in the younger ones (with T50 values 29.8 and 28.8d averaged by all seasons in K12 and K24, respectively), especially in summer and autumn. Averaged by all of the forests and seasons, T50 value of dry weight loss during decomposition of leaf litter was 29.9d. 3.2. Nutrient releases The nutrient (organic C, N, P) contents in K. obovata leaf litter were analyzed during the decomposition processes. The initial values of the contents of C, N and P in leaf litter at the beginning of decomposition decreased with the increasing forest age and C:N ratios of younger forests (K12 and K24) were significantly higher than those of older forests (K48 and KM), but there were not significant differences in any of these parameters between K48 and KM (Table 6). There were significant effects of forest age, season and decomposition time on nutrient releases duing leaf litter decomposition (Tables 7–9). Nutrient releases of organic C, N and P during decomposition experiments were closely paralleled with dry weight losses (Figs. 3–5). The loss percentages of C were very similar to those of dry weight losses, while the loss percentages of N were slightly lower and the loss percentages of P were faster than
T. Li, Y. Ye / Ecological Engineering 73 (2014) 454–460
Dry weight loss (%)
80
K12
80 60
60
40
40
20
20
K24
0
0 0
7
14
21
80 Dry weight loss (%)
457
28
35
42
49
56
0
63
7
14
21
80
K48
60
60
40
40
20
20
0
28
35
42
49
56
63
KM
Spring Summer Autumn Winter
0 0
7
14
21
28 35 42 Time (days)
49
56
63
0
7
14
21
28 35 42 Time (days )
49
56
63
Fig. 2. Loss percentages of initial dry weight during decomposition of leaf litter in the studied K. obovata forests (n = 3).
Table 5 Simple negative exponential regression equations (X = aekt) on % of litter mass remaining in litter bags (X) against time (t) during decomposition of leaf litter in the studied K. obovata forests. Season
Forest
R2
k
T50 (n = 3)
Spring
K12 K24 K48 KM K12 K24 K48 KM K12 K24 K48 KM K12 K24 K48 KM
0.969 0.962 0.938 0.993 0.982 0.965 0.969 0.986 0.914 0.944 0.926 0.947 0.901 0.903 0.886 0.934
0.023 0.026 0.023 0.023 0.038 0.031 0.031 0.032 0.025 0.025 0.024 0.023 0.013 0.013 0.013 0.013
32.2 1.27c 26.9 0.69a 29.9 0.41b 30.3 0.71b 16.9 0.72a 18.1 1.19ab 19.1 0.99bc 20.7 0.51c 22.0 1.33a 23.2 0.58ab 24.1 0.51b 26.1 0.52c 47.9 1.32a 46.9 2.52a 47.4 2.90a 47.3 2.76a
Summer
Autumn
Winter
R, coefficient of determination; k, decomposition constant; T50, half life time. Different letters after T50 data in the same season indicate statistically significant differences among forests in each season at the level of 0.05.
Table 6 Initial contents of nutrients in leaf litter at the beginning of decomposition in the studied K. obovata forests. Forest
C (%)
N (%)
P (%)
C:N
K12 K24 K48 KM
45.28 0.84b 44.50 0.65b 43.15 0.51a 43.29 0.17a
1.06 0.02c 0.91 0.03b 0.72 0.04a 0.70 0.05a
0.122 0.003b 0.109 0.003a 0.104 0.003a 0.101 0.009a
42.80 0.29c 49.01 1.41b 60.06 3.46a 61.71 4.26a
Table 7 Results of repeated measures ANOVA for C losses during decomposition of leaf litter in the studied K. obovata forests. Source of variation Within-subject Time Time age Time season Time age season Error Between-subject Age Season Age season Error
df
MS
F
p
4 12 12 36 128
0.934 0.004 0.028 0.002 0.000
4103.597 16.024 122.040 8.452
0.000 0.000 0.000 0.000
3 3 9 32
0.008 0.535 0.010 0.001
8.408 573.446 10.626
0.000 0.000 0.000
Table 8 Results of repeated measures ANOVA for N losses during decomposition of leaf litter in the studied K. obovata forests. Source of variation Within-subject Time Time age Time season Time age season Error Between-subject Age Season Age season Error
df
MS
F
p
4 12 12 36 128
1.057 0.006 0.042 0.003 0.002
557.205 3.208 22.126 1.710
0.000 0.000 0.000 0.016
3 3 9 32
0.179 0.429 0.024
62.354 149.330 8.412
0.000 0.000 0.000
Different letter indicate statistically significant differences among forests at the level of 0.05.
those of dry weight losses. More rapid releasing of organic C, N and P from decomposed leaves were found in summer and autumn than in winter and spring, indicating more nutrients were released and exported to the surrounding waters in hot seasons. For N concentrations in the residual litter materials during decomposition (Fig. 4), there were general increases from the 2nd to the 3rd or the 4th weeks of leaf litter decomposition in Spring, Summer and Autumn. After these periods, the N remaining in litter materials declined steadily. P remaining in the residual litter material rapidly
decreased during the first 3 weeks and then decreased gradually (Fig. 5). After 35 days’ decomposition, the nutrients releases from leaf litter were around 54% for organic C, 50% for N and 66% for P in spring, 68% for C, 62% for N and 76% for P in summer, 57% for C, 53% for N and 68% for P in autumn, and 41% for C, 29% for N and 49% for P in winter. The decomposition patterns of nutrients in K. obovata leaf litter were also described by simple negative exponential 2 Equations
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Table 9 Results of repeated measures ANOVA for P losses during decomposition of leaf litter in the studied K. obovata forests. Source of Variation Within-subject Time Time age Time season Time age season Error Between-subject Age Season Age season Error
df
MS
F
p
4 12 12 36 128
1.016 0.004 0.017 0.001 0.002
495.825 1.712 8.097 0.622
0.000 0.071 0.000 0.950
3 3 9 32
0.023 0.559 0.010 0.005
4.859 116.932 2.167
0.007 0.000 0.052
4. Discussion
Within-subject factor is decomposition time; between-subject factors are forest age and season. Decomposition time refers to the number of weeks (1, 2, 3, 4 and 5) leaf litter bags were in the field.
K12 K48
110
K24 KM
% C remaining
90 Spring
70
Mangrove litter has been reported to be quickly decomposed with rapid decreases in dry weight and high leaching rates in the first few weeks of exposure in the field (Valk and Attiwill, 1984; Mfilinge et al., 2005). In the present study, the highest decomposition rate occurred in the 2nd week in winter and in the first week in other seasons, and then followed by slower decreases for the rest of the experiment period. This quick decomposition at early stage might be related to leaching of soluble organic materials and inorganic compounds such as
110 90 S ummer
70
50
50
30
30
10
10 0
10
20
30
40
110 % C remaining
releases during decomposition of leaf litter. Averaged by data in the four forests, T50 values of releases of C, N and P during decomposition of leaf litter were 29.4, 40.4 and 21.2d.
0
10
20
30
40
110
90
Autumn
90
70
70
50
50
30
30
10
Winter
10 0
10
20 Time (days)
30
40
20
0
40
60
Time (days)
Fig. 3. Remaining percentages of organic C during decomposition of leaf litter in the studied K. obovata forests (n = 3).
K12 K48
% N remaining
120
K24 KM
100
S pring
100
80
80
60
60
40
40
S ummer
20
20 0
10
20
30
0
40
120 % N remaining
120
10
20
30
40
120
100
Autumn
100
80
80
60
60
40
40
20
Winter
20 0
10
20 Time (days)
30
40
0
20
40
60
Time (days)
Fig. 4. Remaining percentages of N during decomposition of leaf litter in the studied K. obovata forests (n = 3).
(Table 10). The four forests had significantly different T50 values of releases of C, N and P during decomposition of leaf litter, with larger differences in N releases than those in C and P releases. Generally, T50 values of nutrient releases increased with forest age, indicating that the longer the forest grows, the slower the nutrients
soluble sugars (Steinke et al., 1993). A slower loss of dry weight reflected the loss of more resistant materials (Steinke et al., 1990). The decomposition pattern in the present study was similar to those observed in previous studies (Twilley et al., 1986; Mackey and Smail, 1996; Wafar et al., 1997; Imgraben and Dittmann, 2008).
T. Li, Y. Ye / Ecological Engineering 73 (2014) 454–460
K12 K48
% P remaining
110
K24 KM
90
S pring
90 70
50
50
30
30
10
10 10
20
30
S ummer
0
40
110 % P remaining
110
70
0
459
10
20
30
40
110
90
Autumn
90
70
70
50
50
30
30
10
Winter
10 0
10
20 Time (days)
30
40
0
20
40
60
Time (days)
Fig. 5. Remaining percentages of P during decomposition of leaf litter in the studied K. obovata forests (n = 3).
Leaf litter decomposition can be influenced by not only seasons (Mackey and Smail, 1996) but also spatial scales such as tidal levels (Lee, 1989; Mackey and Smail, 1996; Dick and Osunkoya, 2000; Mfilinge et al., 2002). The decomposition rates in both summer and winter from K. obovata forests in Jiulongjiang Estuary in China in the present study, with T50 of dry weight losses of 18.7 and 47.4d respectively, were much slower than those with corresponding values of 13 and 42d from mangrove forests of the same species in Hong Kong (Tam et al., 1990), about 2 -latitude and 2 C annual mean air temperature less than the area of the present study. The decomposition rates of leaf litter in each of the four mangrove forests in the present study were more rapid in summer than those in winter because activities of microbes increased in hot seasons, as reported in other mangrove forests (Lin, 1999). Earlier studies indicated that initial nutrients level of litter, in particular N content, has a controlling influence on litter decomposition rates (Melillo et al., 1982; Twilley et al., 1997). Decomposition rates generally increase for litter with high leaf N content (Pelegraí et al., 1997). Fenchel et al. (1998) suggested that high initial N content or low C:N ratio in litter would result in high microbial assimilation and mineralization efficiencies, and less immobilization effects, hence accelerate the decomposition of litter fall. Certainly, we observed a steady enrichment of litter N in
Table 10 Simple negative exponential regression equations (X = aekt) on % of annual litter nutrients remaining in litter bags (X) against time (t) during decomposition of leaf litter in the studied K. obovata forests. Nutrient
Forest
R2
k
T50 (n = 3)
C remaining
K12 K24 K48 KM K12 K24 K48 KM K12 K24 K48 KM
0.992 0.985 0.985 0.989 0.988 0.949 0.903 0.979 0.979 0.962 0.964 0.978
0.023 0.022 0.022 0.022 0.022 0.020 0.014 0.017 0.032 0.028 0.028 0.029
28.6 0.57a 28.8 1.09a 29.2 0.63a 30.9 1.02b 32.3 0.68a 36.9 0.84b 51.1 3.24 d 41.1 1.82c 19.4 0.74a 21.3 0.43ab 21.4 1.13ab 22.5 1.60b
N remaining
P remaining
R, coefficient of determination; k, decomposition constant; T50, half life time. Different letters after T50 data for the same nutrient indicate statistically significant differences among forests at the level of 0.05.
the first 3 weeks of decomposition and N quantity declined much slower than organic C and P. This may be due to the rapid releases of soluble forms of P from litter by leaching (Steinke et al., 1993; Tam et al., 1998). The decomposition of leaf litter is greatly associated with the surrounding environment which can be largely changed with the development of a restored forest. At different stages of a restored mangrove ecosystem, many factors such as litter production, microbiological activity, inundation condition, aerobic condition of sediment, faunal communities and litter nutritional values also changed (Clough et al., 2000; Morrisey et al., 2003; Nga et al., 2005; Chen et al., 2007; Ye et al., 2013). The present study showed that initial N and P levels in leaf litter declined as the increase in forest age of K. obovata forests. This is in line with findings from Nga et al. (2005) that mangrove plants in younger forests (7 and 11 years) are able to take up more N and P than those in older forests (17 and 24 years) and the formers produce a large quantity of higher quality litter as input to the aquatic system. Hong and San (1993) concluded that old trees produce much woody materials, such as stems, branches and reproductive parts, while young trees produce more leaves. Clough et al. (2000) even indicated that the leaf area index (LAI) decreased with the increase in mangrove forest age, resulting in more closed canopy in young forests than in old ones. Chen et al. (2007) showed that younger forests (4 and 7 years) generally had more macro-benthic fauna species than older ones (19 and 43 years). In a conclusion, litter decomposition rate is inevitably to show some differences with the development of a restored mangrove forest, as is indicated by the present study that litter decomposition rates are directly correlated to the age of the mangrove forests. We found that leaf litter lose its dry weight and nutrients (organic C, N, P) significantly faster in younger forests (K12, K24) than in older forests (K48, KM), especially during the hotter and wetter seasons (summer and autumn). With the development of restored mangrove forests, slower decomposition and nutrient release of leaf litter may increase the chance of leaf litter being exported into ocean. Acknowledgements The work described in this paper is supported by the grants from National Natural Science Foundation of China (Project no.
460
T. Li, Y. Ye / Ecological Engineering 73 (2014) 454–460
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