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Use of degraded coastal wetland in an integrated mangrove–aquaculture system: a case study from the South China Sea
Ocean & Coastal Management 85 (2013) 209e213
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Ocean & Coastal Management journal homepage: www.elsevier.com/locate/ocecoaman
Use of degraded coastal wetland in an integrated mangrovee aquaculture system: a case study from the South China Sea Yisheng Peng a, b,1, Guizhu Chen a,1, Shiyu Li a, b, 2, Yu Liu a, b, 3, John C. Pernetta c, * a School of Environmental Science and Engineering/Research Centre of Wetland Science, Sun Yat-Sen University, 135 West Xingang Road, Guangzhou 510275, Guangdong Province, China b Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, Sun Yat-Sen University, 135 West Xingang Road, Guangzhou 510275, Guangdong Province, China c 35/323 Yingrouwes Niwet, Bangtalad, Pak Kret, Nonthaburi 11120, Thailand
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 16 May 2013
The coastal wetlands of the South China Sea are highly productive and, in 2004, the capture fishery and aquaculture of this area contributed around 8% and 54% of world production, respectively. However, the coastal zone is characterized by high population density and rapid development such that mangrove conversion and reclamation is one of the main threats to coastal wetlands. Globally, about 26% of the mangrove has disappeared since the 1980s much of it being converted to aquaculture ponds. In an attempt to achieve the target of combining mangrove conservation and aquaculture, the Integrated Mangrove Aquaculture System (IMAS) was established in 2002 in southern China. This system was directed towards three goals: mangrove replanting; water purification; and more ecologically friendly aquaculture. Different aquaculture ponds were planted with one of four mangrove species and the aquaculture production, water quality and mangrove growth and survival were compared with control ponds. It has been found that the mangrove species Aegiceras corniculatum is the best for planting in aquaculture ponds given its high tolerance of long-term inundation and its effectiveness in purifying the aquaculture water body in both laboratory and in situ experiments. Following planting with mangrove, the aquaculture ponds can become self-purifying through nutrient uptake by the mangrove. Aquaculture harvests of some mangrove-dependent species, such as red drum (Sciaenops ocellatus), and oyster (Crassostrea rivularis), were increased by over 10% in the presence of mangroves. The food chain, traced by stable isotope analyses, indicates that mangrove litterfall contributes between 1 and 26% of the diet of cultured fishes. The two replicated trials implemented in Shantou and Shenzhen displayed similar results of water purification. Further replication of the use of the IMAS should be attempted at other sites of southern China. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction 1.1. Coastal wetland degradation and its causes in the South China Sea Wetlands are defined as “areas of marsh, peatland or water, whether natural or artificial, permanent or temporary, with water
* Corresponding author. Tel.: þ66 870226996. E-mail addresses: [email protected] (Y. Peng), [email protected] (G. Chen), [email protected] (S. Li), [email protected] (Y. Liu), [email protected], [email protected] (J.C. Pernetta). 1 Tel.: þ86 20 8403 9097. 2 Tel.: þ86 20 8411 4987. 3 Tel.: þ86 20 8411 2293. 0964-5691/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ocecoaman.2013.04.008
that is static or flowing, fresh, brackish or salt, including areas of marine water, the depth of which at low tide does not exceed 6 m” (Ramsar Convention, 1971). Wetlands are one of the most productive and biologically diverse habitats globally covering an estimated 5.7 108 ha (Keddy, 2000). The coastal wetlands of the South China Sea are highly productive. The capture fishery and aquaculture of this area contributed around 8% and 54% of world production in 2004 (UNEP, 2004). Despite the importance of wetlands in terms of biodiversity and resource conservation, however, coastal wetlands have still suffered degradation and loss during the last few decades. This is attributable to rapid population increase and agricultural and urban development. The major threats to coastal wetlands are conversion and reclamation but with overexploitation of biological resources and land-based pollution contributing significantly (Chen et al., 2005).
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1.2. Mangrove degradation and the incompatibility of mangrove protection with aquaculture Mangroves are the unique intertidal plant formations growing in sheltered tropical and subtropical coastal areas. Due to increasing population and economic development, they have been severely damaged over the last several decades and the area of mangrove have declined from 187,940 to 152,310 km2 worldwide (Saenger, 2002). The situation in Asia was comparatively worse with 24.6% of mangroves being lost between 1980 and 2005 (FAO, 2007). In southern China, there have been concomitant declines. In 1956, about 400e420 km2 of mangroves were found in this area but this was reduced to 213 km2 by 1986, following two decades of reclamation for farmland and aquaculture. By the early 1990s, only 151 km2 had survived (Zheng et al., 2003). In the Pearl River Estuary, one of the most urbanized and developed areas of the south China coastline, 33.4% of the mangroves had been removed by 1995 (Li et al., 2006). Reclamation for the purposes of aquaculture was listed as one of the major factors causing the decline of mangroves in southern China (Peng et al., 2008). Mangrove conservation and aquaculture are therefore generally considered to be mutually incompatible in southeast Asia. 1.3. Objectives for establishing Integrated MangroveeAquaculture Systems It is difficult for mangrove conservation and aquaculture development to coexist. It is therefore crucial to resolve the problem of the conflict between mangrove habitat requirements and the suitability of such areas for pond aquaculture. The idea of “mangroves as filters of shrimp pond effluent” was raised almost two decades ago (Robertson and Phillips, 1995). There has been some utilization of this idea to treat aquaculture wastewaters in southeast Asia by circulating aquaculture wastewater through mangroves prior to discharge or reuse (Shimoda et al., 2005). The system entitled ‘Integrated MangroveeAquaculture System (IMAS)’ was established to attempt to bring pond aquaculture more in line with mangrove conservation. The main objectives of using IMAS are: (1) to reverse the trend in mangrove loss and replant mangroves; (2) to achieve environmental-friendly aquaculture models; and (3) to solve the apparent conflict between the sustainable use of mangroves and aquacultural development. In the present study, a demonstration ecosystem based on IMAS was established in the Pearl River Estuary. 2. Materials and methods 2.1. Selection of mangrove species: using adaptation as a criterion In 2007, fifteen abandoned shrimp ponds, previously used for the tiger shrimp (Penaeus monodon) farming, were designated as experimental ponds on the eastern shore of the Pearl River Estuary. Saplings of four native mangrove species, Kandelia candel, Aegiceras corniculatum, Rhizophora stylosa and Bruguiera gymnorrhiza, were planted on the slope of the banks of four sets of ponds at a density of 10,000 saplings per hectare, which had proved to be suitable proportion of planting area during initial research on establishment of IMAS in 2002 (Peng et al., 2009). Three replicates for each species were established. Simultaneously, three control ponds without mangroves were also established to compare water purification effects and aquaculture harvests with and without mangroves (Table 1). These fifteen ponds constituted the first trial (Trial 1) reported in this article. The planting location was permanently inundated over than ten months when the sluice gates were closed, having a water level
Table 1 Characteristics of the fifteen experimental ponds in Trial 1. No.
Mangrove planted
Area (ha)
Salinity
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
Kandelia candel Kandelia candel Kandelia candel Aegiceras corniculatum Aegiceras corniculatum Aegiceras corniculatum Bruguiera gymnorrhiza Bruguiera gymnorrhiza Bruguiera gymnorrhiza Rhizophora stylosa Rhizophora stylosa Rhizophora stylosa No mangrove planted No mangrove planted No mangrove planted
1.33 1.60 1.45 1.67 1.60 1.45 1.47 1.67 1.47 1.67 1.67 1.47 1.33 1.00 1.87
7.9 7.9 7.9 8.0 7.9 8.0 7.9 8.1 8.0 7.9 7.9 7.8 8.4 8.4 8.4
1.9 1.8 1.9 2.0 1.8 1.9 1.8 1.8 1.9 1.9 1.8 1.8 2.1 2.1 2.2
Temp. ( C) 20.1 20.2 20.3 20.2 20.2 20.2 20.1 20.1 20.2 20.3 20.3 20.2 20.2 20.2 20.3
6.3 6.4 6.2 6.2 6.4 6.4 6.2 6.3 6.3 6.1 6.2 6.3 6.2 6.2 6.2
Water level (cm) 9.2 9.5 9.6 9.3 9.0 9.3 9.4 9.2 9.3 9.6 9.0 9.1 9.4 9.5 8.8
0.5 0.4 0.6 0.7 0.5 0.4 0.6 0.7 0.7 0.6 0.9 0.5 0.4 0.6 0.8
from 8.8 to 9.6 cm. This differs considerably from the natural tidal flat habitat, consequently adaptation to inundation was considered the critical factor in the selection of suitable mangrove species for IMAS. Three permanent quadrats were established in each pond to monitor mangrove growth. The sapling height, biomass and mortality were recorded over three years to evaluate their adaptability to the conditions of inundation. 2.2. Evaluation of self-purifying effects within the system Prior to the commencement of the experiment, the ponds were drained and left dry for one month. Mangrove saplings were planted during this period and, at the end of one month, the ponds were filled with seawater. During the whole experimental period, the sluice gates were shut to prevent water exchange between the aquaculture ponds and the adjacent creeks. Water quality was measured in terms of the concentration of two nutrient constituents, namely total nitrogen (TN) and total phosphorus (TP). The constituents were determined by the alkaline potassium persiflage digestion-UV spectrophotometric method and the ammonium molybdate spectrophotometric method, respectively (SOA, 1998). To determine the nutrient removal rate of different mangrove species, a laboratory experiment was also performed in a greenhouse located beside Pond 1. Four mangrove saplings of the same species were planted in plastic tanks with sediments dug and mixed from all of the ponds. Then the plastic tanks were filled with aquaculture water and remained in such an ex situ simulated system for forty-two days. The nutrient removal rate can be calculated by the balance of the nutrient concentrations during this phase. Data were collected in 2010 when the system was at its most stable. The removal rate was calculated as:
ðInitial mass of nutrient Final mass of nutrientÞ 100% Initial mass of nutrient from three ponds with the same mangrove species planted. 2.3. Statistics of the aquaculture harvest From 2008, three mangrove-dependent species were fed in the ponds; i.e., red drum (Sciaenops ocellatus) in 2008; oyster (Crassostrea rivularis) in 2009; and the mud crab (Scylla paramamosain) in 2010. Tilapia (Oreochromis niloticus) fish were also harvested occasionally because of larvae input from the tidal creek. The annual feeding period was from February to December. At the end of each year, the harvest per hectare was calculated to compare the
Y. Peng et al. / Ocean & Coastal Management 85 (2013) 209e213
effectiveness of implementing ecological friendly aquaculture with the control ponds. The same routine management actions were applied to the control ponds and experimental ponds, including feeding, water level control and harvest. In order to assess the contribution of mangroves to the IMAS food chain, stable isotope analysis was carried out to indicate the amount of litterfall transferred to the aquatic animals. Phytoplankton, zooplankton, mangrove litterfall, macrobenthic algae and tissues of aquatic animals were sampled and processed with vacuum freeze drying, then sieved and analyzed with isotope ratio mass spectrometers (Finnigan MAT Delta V advantage, Thermo Scientific, USA). Two natural stable isotope, d13C and d15N were determined and calculations made using the process of the IsoSource software (version 1.3.1) that was recommended by the USEPA (Phillips and Gregg, 2003). The carrying capacity of the aquaculture ponds was also calculated via a mass-balance steady-state model using ECOPATH 5.1 (Christensen et al., 2000; Xu et al., 2011). 2.4. Replication of IMAS in two other areas Two replicate trials were implemented in Shantou and Shenzhen in 2009 and 2010, respectively. Mangrove growth status and water quality were surveyed to test whether the IMAS was effective in these other locations. The details of these two replicates are given in Table 2. These replicates were named as Trials 2 and 3. 2.5. Statistical analysis The data, including mangrove growth, water quality and aquaculture harvest, were analysed using Analysis of Variance (ANOVA) and Duncan’s Multiple Range Test from the SPSS software package (version 16.0, SPSS Inc.). 3. Results 3.1. Tolerance of mangrove species to long-term inundation At the end of the three-year original Trial 1, the four mangroves were found to be quite distinct in terms of their growth and survival. R. stylosa grew the slowest and could not adapt to long-term inundation and low salinity conditions in the aquaculture ponds. Mortality of this species exceeded 80% in the first year and, by the end of the three years, only 5.9% individuals remained alive in the system. B. gymnorrhiza and K. candel grew fast and their height and biomass increases were greater than the other two species. A. corniculatum grew with moderate speed and had the lowest mortality among the four mangrove species. Considering mortality rates, A. corniculatum had the lowest rate followed by B. gymnorrhiza, then K. candel, with R. stylosa, having Table 2 Experimental design of the replicated models in Shantou and Shenzhen. Place
No.
Mangrove planted
Area (ha)
Shantou Trial 2
1
Mixed with K. candel, A. corniculatum, B. gymnorrhiza Mixed with K. candel, A. corniculatum, B. gymnorrhiza Mixed with K. candel, A. corniculatum, B. gymnorrhiza No mangrove planted No mangrove planted No mangrove planted Kandelia candel Aegiceras corniculatum Bruguiera gymnorrhiza No mangrove planted
3.45
2 3
Shenzhen Trial 3
4 5 6 1 2 3 4
3.53 3.54 3.42 3.60 3.55 1.80 1.76 1.65 1.59
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Table 3 Growth and survival (mean SD) of four mangrove species in IMAS Trial 1 from 2008 to 2010. Species
Year
Height (cm)
K. candel
2008 2009 2010 2008 2009 2010 2008 2009 2010 2008 2009 2010
36.8 69.5 91.7 27.2 56.1 78.0 45.8 59.8 64.7 43.3 82.2 110.0
A. corniculatum
R. stylosa
B. gymnorrhiza
2.3 5.0 7.6 1.6 9.2 15.3 3.7 2.2 5.6 0.6 4.2 14.4
Biomass (g m2) 12.2 81.7 205.1 4.2 69.7 137.6 16.9 22.4 31.6 31.9 126.3 257.0
3.4 35.6 89.8 0.7 34.0 38.0 5.0 3.7 8.4 2.4 14.4 45.1
Mortality (%) 24.1 31.5 44.4 9.5 14.3 21.4 82.4 88.2 94.1 20.0 26.7 40.0
1.9 3.4 3.7 1.2 2.6 3.0 7.5 6.9 9.4 2.1 2.9 4.5
the highest mortality. In the case of growth, B. gymnorrhiza had the highest biomass increase followed by K. candel and A. corniculatum with R. stylosa showing the least growth. In terms of height, B. gymnorrhiza showed the greatest increase followed by K. candel, A. corniculatum and R. Stylosa. The values for height and weight in 2010 were significantly different (p < 0.05) when the different mangrove species were compared (Table 3). 3.2. Nutrient removal from the waterbody In terms of their capacity to remove nutrients from the waterbody, the four mangrove species performed with differing effectiveness compared to the controls. A. corniculatum nutrient removal rates were 83.6% for total phosphorus and 85.9% for total nitrogen in the laboratory but slightly less, 68.7% and 77.5%, respectively, in the IMAS. Table 4 presents the mean standard deviation for the percentage rate of nutrient removal by the four mangrove species compared with the control in Trial 1. All four species removed significantly more total nitrogen and total phosphorus from the water column that was lost in the controls. Generally, the nutrient removal rates of mangroves in the IMAS were lower than those in the laboratory experiments. The ability of different mangrove species to remove nutrients from the water column differed from their adaptability. A. corniculatum had the highest nutrient removal rate while B. gymnorrhiza had the lowest removal rates of 34.8% and 55.2% for total phosphorus and total nitrogen respectively. 3.3. Aquaculture harvests and change of fish diets From 2008 to 2010, the average harvest of fish (red drum, S. ocellatus), shellfish (oyster, C. rivularis) in the experimental ponds were higher than those of the control ponds. The difference between the harvests from the IMAS and control ponds were statistically significant (p < 0.05). However, not all the average harvest of crab (mud crab, S. paramamosain) in the experimental ponds were higher than those of the control ponds. Overall, the increase in the fish and crab harvests of ponds planted with A. corniculatum, were significantly greater than those of the ponds planted with K. candel, R. stylosa and B. gymnorrhiza (Fig. 1). Based on the analysis of the stable isotope ratios of fish and the potential food sources, organic detritus, phytoplankton and mangrove litterfall were clearly important food sources in the IMAS. Their contributions in the omnivorous fish, such as tilapias, were 5%e55%, 10%e40% and 15%e26%, respectively. This contrasts with their contributions of 8%e64%, 25%e55% and 1%e12%, respectively, in the control ponds. This clearly demonstrates the importance of mangrove litter in the diet of this species.
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Table 4 Mean and SD of nutrient concentrations (mg L1) and their removal rates (%) from the water column in ex situ laboratory experimental systems and IMAS Trial 1. The different superscript letters in the same row indicate significant differences from all other values in the same row at p 0.05. Nutrient
System
Phase
K. candel
A. corniculatum
R. stylosa
B. gymnorrhiza
Control
TN
ex situ
Feb., 2010 Dec., 2010 Removal rate Feb., 2010 Dec., 2010 Removal rate Feb., 2010 Dec., 2010 Removal rate Feb., 2010 Dec., 2010 Removal rate
3.45 0.91 0.52 0.13d 84.9 3.47 0.86 1.26 0.21b 63.6 1.52 0.13 0.31 0.12c 79.4 1.46 0.25 0.57 0.18c 61.1
3.38 0.76 0.47 0.14e 85.9 3.54 0.65 1.11 0.32c 68.7 1.59 0.16 0.26 0.12d 83.6 1.57 0.23 0.36 0.11d 77.5
3.19 0.70 0.56 0.18c 82.4 3.31 0.72 1.22 0.34b 63.0 1.66 0.15 0.77 0.13a 53.6 1.78 0.18 0.9 0.09b 49.6
3.85 0.75 0.68 0.16b 82.4 3.68 0.81 1.65 0.32a 55.2 1.48 0.20 0.33 0.10bc 77.7 1.73 0.25 1.13 0.20a 34.8
3.70 0.83 0.98 0.20a 73.4
IMAS
TP
ex situ
IMAS
3.4. Mangrove adaptation and water purification in the replicated systems In 2010, two locations along the South China Sea coast at Shantou and Shenzhen were selected as replication demonstration sites. After a one-year experiment, B. gymnorrhiza still recorded the highest growth rate indicated by height and basal area increment. Its mortality was 12.3%, which meant that more than four fifth of the saplings survived in the pond. A. corniculatum had the lowest mortality of 5.0% that was even lower than that in the original trials. K. candel and R. stylosa grew slowly and mortality exceeded 50% (Table 5). Water quality was represented by four variables, DO, COD, DIN and phosphate (see Table 6). The data from control and mangrove ponds showed a significantly higher dissolved oxygen content and significantly lower levels of dissolved organic nitrogen and phosphate than the water from the tidal creek. The control and mangrove ponds showed no significant differences in these indicators. In contrast, the chemical oxygen demand was higher in the creek water than in the control or mangrove ponds although this difference was not significant. 4. Discussion 4.1. Mangrove replanting in the abandoned aquaculture ponds: an opportunity to restore mangroves in southeast Asia In southern China, usually, Avicennia marina and A. corniculatum occupy the seaward tidal flats close to the low-tide zone and are
ND 1.62 0.16 0.39 0.11b 75.9
ND
considered the pioneer species; the mid-tide zone is dominated by K. candel, R. stylosa and A. corniculatum; B. gymnorrhiza and K. candel occur in the landward high-tide zone that is always dominated by the climax species (Lin and Fu, 2000). Thus, their adaptability to inundation is different. The pioneer species always have higher tolerance to inundation and hence hypoxic soil environments than the climax species (Ye et al., 2003). Therefore, in the IMAS, A. corniculatum was the best adapted mangrove species to long-term inundation. This was demonstrated by its having the lowest mortality among the mangroves tested. For the purposes of water body purification, although A. corniculatum did not have highest growth rate and biomass, it demonstrated the highest nutrient removal rate both ex situ and in the field. B. gymnorrhiza exhibited relatively low mortality but its nutrient removal rate was the lowest. Regarding adaptability, both A. corniculatum and B. gymnorrhiza are considered suitable for the IMAS. A. corniculatum was suitable for water body purification whereas B. gymnorrhiza was not. The process of purification is related not only to the mangrove species, but probably also to other factors such as the presence of mycorrhizae; such processes need to be clarified in future experiments. Where aquaculture ponds have been constructed subsequent recovery of natural hydrological condition, such as salinity and natural tidal rhythm, is both important and challenging (Ellison, 2000) if mangroves are to be restored. In cases where restoration of the natural inundation regime is not possible, the inundation adaptability of mangroves is important in the selection of species. On the basis of the present research, A. corniculatum proved to be the most adaptable and stable species during the habitat modification process. This was proved by the stability of the percentage volume of its aerenchyma (VPA) in the roots. VPA is considered an indicator of the adaptability to anoxia of plants. Comparing the individuals grown in IMAS and natural tidal habitats, the VPA range increase of A. corniculatum was most among A. marina, A. corniculatum, B. gymnorrhiza, K. candel and R. stylosa (Wu et al., 2010). Thus, on the basis of its adaptability and purification
Table 5 Mangrove adaptation in the replicated IMAS in Shenzhen Bay in southern China (Values are means SD. The different superscript letters in the second and third column indicate significant differences from all other values in the same column at p 0.05).
Fig. 1. Fishery harvest in IMAS and control ponds from 2008 to 2010.
Species
Height increment (cm)
A. corniculatum B. gymnorrhiza K. candel R. stylosa
24.1 43.6 5.7 3.6
5.8a 10.1b 2.1c 0.9d
Basal area increment (cm2) 2.7 6.8 3.5 0.9
0.9a 1.0b 1.3c 0.2d
Mortality (%) 5.0 12.3 53.3 89.4
1.1 5.4 10.7 14.6
Y. Peng et al. / Ocean & Coastal Management 85 (2013) 209e213 Table 6 Water quality in the replicated IMAS Trials 2 and 3 in Shenzhen Bay and Shantou mg L1 (The different superscript letters in the second and third column indicate significant differences from all other values in the same column at p 0.05). Ponds Tidal creek Control Mangrove
DO
COD a
1.84 0.68 4.00 0.88b 4.32 1.42b
PO3 4
DIN a
4.40 0.98 3.96 1.29a 3.76 1.72ab
a
4.75 0.62 1.29 0.82b 1.03 0.48b
0.67 0.19a 0.16 0.27b 0.12 0.09b
ability, A. corniculatum is highly recommended for the establishment of IMAS along the southern coast of China. 4.2. IMAS: an environmental-friendly aquaculture mode Habitat change, wastewater discharge and salinization of soil and water have been identified as the major environmental impacts of aquaculture (Primavera, 2006). In China, the pollution caused by large-scale and highly-intensive aquaculture is causing deterioration of coastal waters. According to the State Oceanic Administration, between 1989 and 2007, aquaculture was listed as one of the main sources of coastal seawater pollution, together with landbased pollution and oil spills during transportation (SOA, 2012). The traditional method of aquaculture (i.e., pond aquaculture) is unsustainable and competes with mangroves for space in coastal areas. The establishment of IMAS reduced the discharge of aquacultural wastes, especially nutrients. Combined with mangrove replanting, IMAS can partially reverse the trend of mangrove degradation and loss and partially resolve the incompatibility between coastal wetland conservation and the construction of aquaculture ponds. It can also increase fishery harvests and thus could result in improvement of the livelihoods of local communities. The increased harvest may reflect the fact that, following the introduction of mangroves and fishes into the pond system, the ratio of energy flows between detrivory and herbivory food chains reduced from 4.4:1 to 3.9:1. This reduction in the ratio indicates more energy flow from organic detritus through the herbivore food chain (Xu et al., 2010). 5. Conclusions In Asia, there are an estimated total of over 400,000 ha of abandoned aquaculture ponds (Stevenson et al., 1999). The IMAS offers an opportunity to partially restore mangroves in southern China. IMAS can be considered as a more environmentally friendly method of aquaculture than simple unvegetated pond construction. The simple expression “more mangrove, lower nutrient effluent, increased aquacultural production” was the theme of IMAS development to achieve sustainable development and wise use of coastal wetlands. It is concluded that planting mangrove along the margins of aquaculture ponds increases aquaculture production and that of the four species tested A. corniculatum has the greatest effect on water quality and the greatest tolerance of inundation. Acknowledgements This research was supported by the Natural Science Foundation of China (40901278), the UNEP/GEF Medium-Sized
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Project (GF/3010-07-03), UNEP/GEF South China Sea Project (GF/2730-02-4340) 863 and a Project of the Ministry of Science and Technology, China (No. 2007AA091703, 2003AA627030). Thanks go to the persons who assisted us during field sampling and laboratory analyses, especially Mr. Zhongming SHE, Prof. Zhihong YE, Prof. Yaochu LI, Dr. Shannan XU, Dr. Xingwen ZHENG, Dr. Hualin XU, MSc. Kalan WU, Msc. Xulin LI, Msc. Xianmei GE, Mr. Jinzao LIN and Mr. Shenghua PENG. The authors would also like to thank the editors of this special issue for their useful comments on an earlier draft of the paper. References Chen, G.Z., Lan, Z.H., Deng, P.Y., 2005. National Report of China on Wetlands. Sun Yat-Sen University Press, Guangzhou, pp. 78e81. Christensen, V., Walters, C.J., Pauly, D., 2000. ECOPATH with ECOSIM (Version 5). University of British Columbia, Fisheries Centre. Ellison, A.M., 2000. Mangrove restoration: do we know enough? Restoration Ecology 8 (3), 219e229. FAO (Food and Agricultural Organization of the United Nations), 2007. The World’s Mangroves 1980e2005, pp. 1e9. Keddy, P.A., 2000. Wetland Ecology: Principles and Conservation. Cambridge University Press, Cambridge, UK, pp. 1e18. Li, X., Yeh, A., Liu, K., Wang, S.G., 2006. Inventory of mangrove wetlands in the Pearl River Estuary of China using remote sensing. Journal of Geographical Sciences 16 (2), 155e164. Lin, P., Fu, Q., 2000. Environmental Ecology and Economic Utilization of Mangroves in China. Berlin Heidelberg CHEP and Springer Verlag, pp. 1e46. Peng, Y.S., Zhou, Y.W., Chen, G.Z., 2008. The restoration of mangrove wetland: a review. Acta Ecologica Sinica 28 (2), 786e797. Peng, Y.S., Li, X.L., Wu, K.L., Peng, Y.G., Chen, G.Z., 2009. Effect of an integrated mangrove-aquaculture system on aquacultural health. Frontiers of Biology in China 4 (4), 579e584. Phillips, D.L., Gregg, J.W., 2003. Source partitioning using stable isotope: coping with too many sources. Ecologia 136, 261e269. Primavera, J.H., 2006. Overcoming the impacts of aquaculture on the coastal zone. Ocean and Coastal Management 49, 531e545. Ramsar Convention Bureau, 1971. Convention on Wetlands of International Importance Especially as Waterfowl Habitats. Available online: www.ramsar. org/cda/en/ramsar-documents-texts-convention-on/main/ramsar. Robertson, A.I., Phillips, M.J., 1995. Mangroves as filters of shrimp pond effluent: predictions and biogeochemical research needs. Hydrobiologia 295, 311e321. Saenger, P., 2002. Mangrove Ecology, Silviculture and Conservation. Kluwer Academic Publishers, Dodrecht, Netherland, pp. 1e10. Shimoda, T., Fujioka, Y., Srithong, C., Aryuthaka, C., 2005. Phosphorus budget in shrimp aquaculture pond with mangrove enclosure and aquaculture performance. Fisheries Science 71, 1249e1255. SOA (State Oceanic Administration, People’s Republic of China), 1998. Criteria of Marine Monitoring and Determination (GB 17378-1998). Standard Press, Beijing, pp. 176e178. SOA (State Oceanic Administration, People’s Republic of China), 2012. Marine Environmental Quality Bulletin. Available online: www.coi.gov.cn/hygb/hjzl. Stevenson, N.J., Lewis, R.R., Burbridge, P.R., 1999. Disused shrimp ponds and mangrove rehabilitation. In: Streever, W. (Ed.), An International Perspective on Wetland Rehabilitation. Kluwer Academic Publishers, Dodrecht, Netherland, pp. 277e297. UNEP, 2004. Wetlands Bordering the South China Sea. UNEP/GEF/SCS Technical Publication No. 4. Bangkok, Thailand, p. 8. Wu, K.L., Peng, Y.S., Zheng, K.Z., Li, X.L., Chen, G.Z., 2010. Responses of aerenchyma in five mangrove species on artificial-non-tidal habitats. Acta Ecologica Sinica 30 (24), 6927e6934. Xu, S.N., Chen, Z.Z., Huang, H.H., Huang, X.P., Li, S.Y., 2010. Food sources of Oreochromis niloticus in the mangrove and plantation-aquaculture ecological coupling systems. Acta Scientiarum Naturalium Universitatis Sunyatseni 49 (1), 101e106. Xu, S.N., Chen, Z.Z., Li, S.Y., He, P.M., 2011. Modeling trophic structure and energy flows in a coastal artificial ecosystem using mass-balance ecopath model. Estuaries and Coasts 34, 351e363. Ye, Y., Tam, N.F.Y., Wong, Y.S., 2003. Growth and physiological responses of two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to waterlogging. Environmental and Experimental Botany 49, 209e221. Zheng, D.Z., Li, M., Zheng, S.F., Liao, B.W., Chen, Y.J., 2003. Headway of study on mangrove recovery and development in China. Guangdong Forestry Science and Technology 19 (1), 10e14.
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Use of degraded coastal wetland in an integrated mangrovee aquaculture system: a case study from the South China Sea Yisheng Peng a, b,1, Guizhu Chen a,1, Shiyu Li a, b, 2, Yu Liu a, b, 3, John C. Pernetta c, * a School of Environmental Science and Engineering/Research Centre of Wetland Science, Sun Yat-Sen University, 135 West Xingang Road, Guangzhou 510275, Guangdong Province, China b Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, Sun Yat-Sen University, 135 West Xingang Road, Guangzhou 510275, Guangdong Province, China c 35/323 Yingrouwes Niwet, Bangtalad, Pak Kret, Nonthaburi 11120, Thailand
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 16 May 2013
The coastal wetlands of the South China Sea are highly productive and, in 2004, the capture fishery and aquaculture of this area contributed around 8% and 54% of world production, respectively. However, the coastal zone is characterized by high population density and rapid development such that mangrove conversion and reclamation is one of the main threats to coastal wetlands. Globally, about 26% of the mangrove has disappeared since the 1980s much of it being converted to aquaculture ponds. In an attempt to achieve the target of combining mangrove conservation and aquaculture, the Integrated Mangrove Aquaculture System (IMAS) was established in 2002 in southern China. This system was directed towards three goals: mangrove replanting; water purification; and more ecologically friendly aquaculture. Different aquaculture ponds were planted with one of four mangrove species and the aquaculture production, water quality and mangrove growth and survival were compared with control ponds. It has been found that the mangrove species Aegiceras corniculatum is the best for planting in aquaculture ponds given its high tolerance of long-term inundation and its effectiveness in purifying the aquaculture water body in both laboratory and in situ experiments. Following planting with mangrove, the aquaculture ponds can become self-purifying through nutrient uptake by the mangrove. Aquaculture harvests of some mangrove-dependent species, such as red drum (Sciaenops ocellatus), and oyster (Crassostrea rivularis), were increased by over 10% in the presence of mangroves. The food chain, traced by stable isotope analyses, indicates that mangrove litterfall contributes between 1 and 26% of the diet of cultured fishes. The two replicated trials implemented in Shantou and Shenzhen displayed similar results of water purification. Further replication of the use of the IMAS should be attempted at other sites of southern China. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction 1.1. Coastal wetland degradation and its causes in the South China Sea Wetlands are defined as “areas of marsh, peatland or water, whether natural or artificial, permanent or temporary, with water
* Corresponding author. Tel.: þ66 870226996. E-mail addresses: [email protected] (Y. Peng), [email protected] (G. Chen), [email protected] (S. Li), [email protected] (Y. Liu), [email protected], [email protected] (J.C. Pernetta). 1 Tel.: þ86 20 8403 9097. 2 Tel.: þ86 20 8411 4987. 3 Tel.: þ86 20 8411 2293. 0964-5691/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ocecoaman.2013.04.008
that is static or flowing, fresh, brackish or salt, including areas of marine water, the depth of which at low tide does not exceed 6 m” (Ramsar Convention, 1971). Wetlands are one of the most productive and biologically diverse habitats globally covering an estimated 5.7 108 ha (Keddy, 2000). The coastal wetlands of the South China Sea are highly productive. The capture fishery and aquaculture of this area contributed around 8% and 54% of world production in 2004 (UNEP, 2004). Despite the importance of wetlands in terms of biodiversity and resource conservation, however, coastal wetlands have still suffered degradation and loss during the last few decades. This is attributable to rapid population increase and agricultural and urban development. The major threats to coastal wetlands are conversion and reclamation but with overexploitation of biological resources and land-based pollution contributing significantly (Chen et al., 2005).
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1.2. Mangrove degradation and the incompatibility of mangrove protection with aquaculture Mangroves are the unique intertidal plant formations growing in sheltered tropical and subtropical coastal areas. Due to increasing population and economic development, they have been severely damaged over the last several decades and the area of mangrove have declined from 187,940 to 152,310 km2 worldwide (Saenger, 2002). The situation in Asia was comparatively worse with 24.6% of mangroves being lost between 1980 and 2005 (FAO, 2007). In southern China, there have been concomitant declines. In 1956, about 400e420 km2 of mangroves were found in this area but this was reduced to 213 km2 by 1986, following two decades of reclamation for farmland and aquaculture. By the early 1990s, only 151 km2 had survived (Zheng et al., 2003). In the Pearl River Estuary, one of the most urbanized and developed areas of the south China coastline, 33.4% of the mangroves had been removed by 1995 (Li et al., 2006). Reclamation for the purposes of aquaculture was listed as one of the major factors causing the decline of mangroves in southern China (Peng et al., 2008). Mangrove conservation and aquaculture are therefore generally considered to be mutually incompatible in southeast Asia. 1.3. Objectives for establishing Integrated MangroveeAquaculture Systems It is difficult for mangrove conservation and aquaculture development to coexist. It is therefore crucial to resolve the problem of the conflict between mangrove habitat requirements and the suitability of such areas for pond aquaculture. The idea of “mangroves as filters of shrimp pond effluent” was raised almost two decades ago (Robertson and Phillips, 1995). There has been some utilization of this idea to treat aquaculture wastewaters in southeast Asia by circulating aquaculture wastewater through mangroves prior to discharge or reuse (Shimoda et al., 2005). The system entitled ‘Integrated MangroveeAquaculture System (IMAS)’ was established to attempt to bring pond aquaculture more in line with mangrove conservation. The main objectives of using IMAS are: (1) to reverse the trend in mangrove loss and replant mangroves; (2) to achieve environmental-friendly aquaculture models; and (3) to solve the apparent conflict between the sustainable use of mangroves and aquacultural development. In the present study, a demonstration ecosystem based on IMAS was established in the Pearl River Estuary. 2. Materials and methods 2.1. Selection of mangrove species: using adaptation as a criterion In 2007, fifteen abandoned shrimp ponds, previously used for the tiger shrimp (Penaeus monodon) farming, were designated as experimental ponds on the eastern shore of the Pearl River Estuary. Saplings of four native mangrove species, Kandelia candel, Aegiceras corniculatum, Rhizophora stylosa and Bruguiera gymnorrhiza, were planted on the slope of the banks of four sets of ponds at a density of 10,000 saplings per hectare, which had proved to be suitable proportion of planting area during initial research on establishment of IMAS in 2002 (Peng et al., 2009). Three replicates for each species were established. Simultaneously, three control ponds without mangroves were also established to compare water purification effects and aquaculture harvests with and without mangroves (Table 1). These fifteen ponds constituted the first trial (Trial 1) reported in this article. The planting location was permanently inundated over than ten months when the sluice gates were closed, having a water level
Table 1 Characteristics of the fifteen experimental ponds in Trial 1. No.
Mangrove planted
Area (ha)
Salinity
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
Kandelia candel Kandelia candel Kandelia candel Aegiceras corniculatum Aegiceras corniculatum Aegiceras corniculatum Bruguiera gymnorrhiza Bruguiera gymnorrhiza Bruguiera gymnorrhiza Rhizophora stylosa Rhizophora stylosa Rhizophora stylosa No mangrove planted No mangrove planted No mangrove planted
1.33 1.60 1.45 1.67 1.60 1.45 1.47 1.67 1.47 1.67 1.67 1.47 1.33 1.00 1.87
7.9 7.9 7.9 8.0 7.9 8.0 7.9 8.1 8.0 7.9 7.9 7.8 8.4 8.4 8.4
1.9 1.8 1.9 2.0 1.8 1.9 1.8 1.8 1.9 1.9 1.8 1.8 2.1 2.1 2.2
Temp. ( C) 20.1 20.2 20.3 20.2 20.2 20.2 20.1 20.1 20.2 20.3 20.3 20.2 20.2 20.2 20.3
6.3 6.4 6.2 6.2 6.4 6.4 6.2 6.3 6.3 6.1 6.2 6.3 6.2 6.2 6.2
Water level (cm) 9.2 9.5 9.6 9.3 9.0 9.3 9.4 9.2 9.3 9.6 9.0 9.1 9.4 9.5 8.8
0.5 0.4 0.6 0.7 0.5 0.4 0.6 0.7 0.7 0.6 0.9 0.5 0.4 0.6 0.8
from 8.8 to 9.6 cm. This differs considerably from the natural tidal flat habitat, consequently adaptation to inundation was considered the critical factor in the selection of suitable mangrove species for IMAS. Three permanent quadrats were established in each pond to monitor mangrove growth. The sapling height, biomass and mortality were recorded over three years to evaluate their adaptability to the conditions of inundation. 2.2. Evaluation of self-purifying effects within the system Prior to the commencement of the experiment, the ponds were drained and left dry for one month. Mangrove saplings were planted during this period and, at the end of one month, the ponds were filled with seawater. During the whole experimental period, the sluice gates were shut to prevent water exchange between the aquaculture ponds and the adjacent creeks. Water quality was measured in terms of the concentration of two nutrient constituents, namely total nitrogen (TN) and total phosphorus (TP). The constituents were determined by the alkaline potassium persiflage digestion-UV spectrophotometric method and the ammonium molybdate spectrophotometric method, respectively (SOA, 1998). To determine the nutrient removal rate of different mangrove species, a laboratory experiment was also performed in a greenhouse located beside Pond 1. Four mangrove saplings of the same species were planted in plastic tanks with sediments dug and mixed from all of the ponds. Then the plastic tanks were filled with aquaculture water and remained in such an ex situ simulated system for forty-two days. The nutrient removal rate can be calculated by the balance of the nutrient concentrations during this phase. Data were collected in 2010 when the system was at its most stable. The removal rate was calculated as:
ðInitial mass of nutrient Final mass of nutrientÞ 100% Initial mass of nutrient from three ponds with the same mangrove species planted. 2.3. Statistics of the aquaculture harvest From 2008, three mangrove-dependent species were fed in the ponds; i.e., red drum (Sciaenops ocellatus) in 2008; oyster (Crassostrea rivularis) in 2009; and the mud crab (Scylla paramamosain) in 2010. Tilapia (Oreochromis niloticus) fish were also harvested occasionally because of larvae input from the tidal creek. The annual feeding period was from February to December. At the end of each year, the harvest per hectare was calculated to compare the
Y. Peng et al. / Ocean & Coastal Management 85 (2013) 209e213
effectiveness of implementing ecological friendly aquaculture with the control ponds. The same routine management actions were applied to the control ponds and experimental ponds, including feeding, water level control and harvest. In order to assess the contribution of mangroves to the IMAS food chain, stable isotope analysis was carried out to indicate the amount of litterfall transferred to the aquatic animals. Phytoplankton, zooplankton, mangrove litterfall, macrobenthic algae and tissues of aquatic animals were sampled and processed with vacuum freeze drying, then sieved and analyzed with isotope ratio mass spectrometers (Finnigan MAT Delta V advantage, Thermo Scientific, USA). Two natural stable isotope, d13C and d15N were determined and calculations made using the process of the IsoSource software (version 1.3.1) that was recommended by the USEPA (Phillips and Gregg, 2003). The carrying capacity of the aquaculture ponds was also calculated via a mass-balance steady-state model using ECOPATH 5.1 (Christensen et al., 2000; Xu et al., 2011). 2.4. Replication of IMAS in two other areas Two replicate trials were implemented in Shantou and Shenzhen in 2009 and 2010, respectively. Mangrove growth status and water quality were surveyed to test whether the IMAS was effective in these other locations. The details of these two replicates are given in Table 2. These replicates were named as Trials 2 and 3. 2.5. Statistical analysis The data, including mangrove growth, water quality and aquaculture harvest, were analysed using Analysis of Variance (ANOVA) and Duncan’s Multiple Range Test from the SPSS software package (version 16.0, SPSS Inc.). 3. Results 3.1. Tolerance of mangrove species to long-term inundation At the end of the three-year original Trial 1, the four mangroves were found to be quite distinct in terms of their growth and survival. R. stylosa grew the slowest and could not adapt to long-term inundation and low salinity conditions in the aquaculture ponds. Mortality of this species exceeded 80% in the first year and, by the end of the three years, only 5.9% individuals remained alive in the system. B. gymnorrhiza and K. candel grew fast and their height and biomass increases were greater than the other two species. A. corniculatum grew with moderate speed and had the lowest mortality among the four mangrove species. Considering mortality rates, A. corniculatum had the lowest rate followed by B. gymnorrhiza, then K. candel, with R. stylosa, having Table 2 Experimental design of the replicated models in Shantou and Shenzhen. Place
No.
Mangrove planted
Area (ha)
Shantou Trial 2
1
Mixed with K. candel, A. corniculatum, B. gymnorrhiza Mixed with K. candel, A. corniculatum, B. gymnorrhiza Mixed with K. candel, A. corniculatum, B. gymnorrhiza No mangrove planted No mangrove planted No mangrove planted Kandelia candel Aegiceras corniculatum Bruguiera gymnorrhiza No mangrove planted
3.45
2 3
Shenzhen Trial 3
4 5 6 1 2 3 4
3.53 3.54 3.42 3.60 3.55 1.80 1.76 1.65 1.59
211
Table 3 Growth and survival (mean SD) of four mangrove species in IMAS Trial 1 from 2008 to 2010. Species
Year
Height (cm)
K. candel
2008 2009 2010 2008 2009 2010 2008 2009 2010 2008 2009 2010
36.8 69.5 91.7 27.2 56.1 78.0 45.8 59.8 64.7 43.3 82.2 110.0
A. corniculatum
R. stylosa
B. gymnorrhiza
2.3 5.0 7.6 1.6 9.2 15.3 3.7 2.2 5.6 0.6 4.2 14.4
Biomass (g m2) 12.2 81.7 205.1 4.2 69.7 137.6 16.9 22.4 31.6 31.9 126.3 257.0
3.4 35.6 89.8 0.7 34.0 38.0 5.0 3.7 8.4 2.4 14.4 45.1
Mortality (%) 24.1 31.5 44.4 9.5 14.3 21.4 82.4 88.2 94.1 20.0 26.7 40.0
1.9 3.4 3.7 1.2 2.6 3.0 7.5 6.9 9.4 2.1 2.9 4.5
the highest mortality. In the case of growth, B. gymnorrhiza had the highest biomass increase followed by K. candel and A. corniculatum with R. stylosa showing the least growth. In terms of height, B. gymnorrhiza showed the greatest increase followed by K. candel, A. corniculatum and R. Stylosa. The values for height and weight in 2010 were significantly different (p < 0.05) when the different mangrove species were compared (Table 3). 3.2. Nutrient removal from the waterbody In terms of their capacity to remove nutrients from the waterbody, the four mangrove species performed with differing effectiveness compared to the controls. A. corniculatum nutrient removal rates were 83.6% for total phosphorus and 85.9% for total nitrogen in the laboratory but slightly less, 68.7% and 77.5%, respectively, in the IMAS. Table 4 presents the mean standard deviation for the percentage rate of nutrient removal by the four mangrove species compared with the control in Trial 1. All four species removed significantly more total nitrogen and total phosphorus from the water column that was lost in the controls. Generally, the nutrient removal rates of mangroves in the IMAS were lower than those in the laboratory experiments. The ability of different mangrove species to remove nutrients from the water column differed from their adaptability. A. corniculatum had the highest nutrient removal rate while B. gymnorrhiza had the lowest removal rates of 34.8% and 55.2% for total phosphorus and total nitrogen respectively. 3.3. Aquaculture harvests and change of fish diets From 2008 to 2010, the average harvest of fish (red drum, S. ocellatus), shellfish (oyster, C. rivularis) in the experimental ponds were higher than those of the control ponds. The difference between the harvests from the IMAS and control ponds were statistically significant (p < 0.05). However, not all the average harvest of crab (mud crab, S. paramamosain) in the experimental ponds were higher than those of the control ponds. Overall, the increase in the fish and crab harvests of ponds planted with A. corniculatum, were significantly greater than those of the ponds planted with K. candel, R. stylosa and B. gymnorrhiza (Fig. 1). Based on the analysis of the stable isotope ratios of fish and the potential food sources, organic detritus, phytoplankton and mangrove litterfall were clearly important food sources in the IMAS. Their contributions in the omnivorous fish, such as tilapias, were 5%e55%, 10%e40% and 15%e26%, respectively. This contrasts with their contributions of 8%e64%, 25%e55% and 1%e12%, respectively, in the control ponds. This clearly demonstrates the importance of mangrove litter in the diet of this species.
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Table 4 Mean and SD of nutrient concentrations (mg L1) and their removal rates (%) from the water column in ex situ laboratory experimental systems and IMAS Trial 1. The different superscript letters in the same row indicate significant differences from all other values in the same row at p 0.05. Nutrient
System
Phase
K. candel
A. corniculatum
R. stylosa
B. gymnorrhiza
Control
TN
ex situ
Feb., 2010 Dec., 2010 Removal rate Feb., 2010 Dec., 2010 Removal rate Feb., 2010 Dec., 2010 Removal rate Feb., 2010 Dec., 2010 Removal rate
3.45 0.91 0.52 0.13d 84.9 3.47 0.86 1.26 0.21b 63.6 1.52 0.13 0.31 0.12c 79.4 1.46 0.25 0.57 0.18c 61.1
3.38 0.76 0.47 0.14e 85.9 3.54 0.65 1.11 0.32c 68.7 1.59 0.16 0.26 0.12d 83.6 1.57 0.23 0.36 0.11d 77.5
3.19 0.70 0.56 0.18c 82.4 3.31 0.72 1.22 0.34b 63.0 1.66 0.15 0.77 0.13a 53.6 1.78 0.18 0.9 0.09b 49.6
3.85 0.75 0.68 0.16b 82.4 3.68 0.81 1.65 0.32a 55.2 1.48 0.20 0.33 0.10bc 77.7 1.73 0.25 1.13 0.20a 34.8
3.70 0.83 0.98 0.20a 73.4
IMAS
TP
ex situ
IMAS
3.4. Mangrove adaptation and water purification in the replicated systems In 2010, two locations along the South China Sea coast at Shantou and Shenzhen were selected as replication demonstration sites. After a one-year experiment, B. gymnorrhiza still recorded the highest growth rate indicated by height and basal area increment. Its mortality was 12.3%, which meant that more than four fifth of the saplings survived in the pond. A. corniculatum had the lowest mortality of 5.0% that was even lower than that in the original trials. K. candel and R. stylosa grew slowly and mortality exceeded 50% (Table 5). Water quality was represented by four variables, DO, COD, DIN and phosphate (see Table 6). The data from control and mangrove ponds showed a significantly higher dissolved oxygen content and significantly lower levels of dissolved organic nitrogen and phosphate than the water from the tidal creek. The control and mangrove ponds showed no significant differences in these indicators. In contrast, the chemical oxygen demand was higher in the creek water than in the control or mangrove ponds although this difference was not significant. 4. Discussion 4.1. Mangrove replanting in the abandoned aquaculture ponds: an opportunity to restore mangroves in southeast Asia In southern China, usually, Avicennia marina and A. corniculatum occupy the seaward tidal flats close to the low-tide zone and are
ND 1.62 0.16 0.39 0.11b 75.9
ND
considered the pioneer species; the mid-tide zone is dominated by K. candel, R. stylosa and A. corniculatum; B. gymnorrhiza and K. candel occur in the landward high-tide zone that is always dominated by the climax species (Lin and Fu, 2000). Thus, their adaptability to inundation is different. The pioneer species always have higher tolerance to inundation and hence hypoxic soil environments than the climax species (Ye et al., 2003). Therefore, in the IMAS, A. corniculatum was the best adapted mangrove species to long-term inundation. This was demonstrated by its having the lowest mortality among the mangroves tested. For the purposes of water body purification, although A. corniculatum did not have highest growth rate and biomass, it demonstrated the highest nutrient removal rate both ex situ and in the field. B. gymnorrhiza exhibited relatively low mortality but its nutrient removal rate was the lowest. Regarding adaptability, both A. corniculatum and B. gymnorrhiza are considered suitable for the IMAS. A. corniculatum was suitable for water body purification whereas B. gymnorrhiza was not. The process of purification is related not only to the mangrove species, but probably also to other factors such as the presence of mycorrhizae; such processes need to be clarified in future experiments. Where aquaculture ponds have been constructed subsequent recovery of natural hydrological condition, such as salinity and natural tidal rhythm, is both important and challenging (Ellison, 2000) if mangroves are to be restored. In cases where restoration of the natural inundation regime is not possible, the inundation adaptability of mangroves is important in the selection of species. On the basis of the present research, A. corniculatum proved to be the most adaptable and stable species during the habitat modification process. This was proved by the stability of the percentage volume of its aerenchyma (VPA) in the roots. VPA is considered an indicator of the adaptability to anoxia of plants. Comparing the individuals grown in IMAS and natural tidal habitats, the VPA range increase of A. corniculatum was most among A. marina, A. corniculatum, B. gymnorrhiza, K. candel and R. stylosa (Wu et al., 2010). Thus, on the basis of its adaptability and purification
Table 5 Mangrove adaptation in the replicated IMAS in Shenzhen Bay in southern China (Values are means SD. The different superscript letters in the second and third column indicate significant differences from all other values in the same column at p 0.05).
Fig. 1. Fishery harvest in IMAS and control ponds from 2008 to 2010.
Species
Height increment (cm)
A. corniculatum B. gymnorrhiza K. candel R. stylosa
24.1 43.6 5.7 3.6
5.8a 10.1b 2.1c 0.9d
Basal area increment (cm2) 2.7 6.8 3.5 0.9
0.9a 1.0b 1.3c 0.2d
Mortality (%) 5.0 12.3 53.3 89.4
1.1 5.4 10.7 14.6
Y. Peng et al. / Ocean & Coastal Management 85 (2013) 209e213 Table 6 Water quality in the replicated IMAS Trials 2 and 3 in Shenzhen Bay and Shantou mg L1 (The different superscript letters in the second and third column indicate significant differences from all other values in the same column at p 0.05). Ponds Tidal creek Control Mangrove
DO
COD a
1.84 0.68 4.00 0.88b 4.32 1.42b
PO3 4
DIN a
4.40 0.98 3.96 1.29a 3.76 1.72ab
a
4.75 0.62 1.29 0.82b 1.03 0.48b
0.67 0.19a 0.16 0.27b 0.12 0.09b
ability, A. corniculatum is highly recommended for the establishment of IMAS along the southern coast of China. 4.2. IMAS: an environmental-friendly aquaculture mode Habitat change, wastewater discharge and salinization of soil and water have been identified as the major environmental impacts of aquaculture (Primavera, 2006). In China, the pollution caused by large-scale and highly-intensive aquaculture is causing deterioration of coastal waters. According to the State Oceanic Administration, between 1989 and 2007, aquaculture was listed as one of the main sources of coastal seawater pollution, together with landbased pollution and oil spills during transportation (SOA, 2012). The traditional method of aquaculture (i.e., pond aquaculture) is unsustainable and competes with mangroves for space in coastal areas. The establishment of IMAS reduced the discharge of aquacultural wastes, especially nutrients. Combined with mangrove replanting, IMAS can partially reverse the trend of mangrove degradation and loss and partially resolve the incompatibility between coastal wetland conservation and the construction of aquaculture ponds. It can also increase fishery harvests and thus could result in improvement of the livelihoods of local communities. The increased harvest may reflect the fact that, following the introduction of mangroves and fishes into the pond system, the ratio of energy flows between detrivory and herbivory food chains reduced from 4.4:1 to 3.9:1. This reduction in the ratio indicates more energy flow from organic detritus through the herbivore food chain (Xu et al., 2010). 5. Conclusions In Asia, there are an estimated total of over 400,000 ha of abandoned aquaculture ponds (Stevenson et al., 1999). The IMAS offers an opportunity to partially restore mangroves in southern China. IMAS can be considered as a more environmentally friendly method of aquaculture than simple unvegetated pond construction. The simple expression “more mangrove, lower nutrient effluent, increased aquacultural production” was the theme of IMAS development to achieve sustainable development and wise use of coastal wetlands. It is concluded that planting mangrove along the margins of aquaculture ponds increases aquaculture production and that of the four species tested A. corniculatum has the greatest effect on water quality and the greatest tolerance of inundation. Acknowledgements This research was supported by the Natural Science Foundation of China (40901278), the UNEP/GEF Medium-Sized
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Project (GF/3010-07-03), UNEP/GEF South China Sea Project (GF/2730-02-4340) 863 and a Project of the Ministry of Science and Technology, China (No. 2007AA091703, 2003AA627030). Thanks go to the persons who assisted us during field sampling and laboratory analyses, especially Mr. Zhongming SHE, Prof. Zhihong YE, Prof. Yaochu LI, Dr. Shannan XU, Dr. Xingwen ZHENG, Dr. Hualin XU, MSc. Kalan WU, Msc. Xulin LI, Msc. Xianmei GE, Mr. Jinzao LIN and Mr. Shenghua PENG. The authors would also like to thank the editors of this special issue for their useful comments on an earlier draft of the paper. References Chen, G.Z., Lan, Z.H., Deng, P.Y., 2005. National Report of China on Wetlands. Sun Yat-Sen University Press, Guangzhou, pp. 78e81. Christensen, V., Walters, C.J., Pauly, D., 2000. ECOPATH with ECOSIM (Version 5). University of British Columbia, Fisheries Centre. Ellison, A.M., 2000. Mangrove restoration: do we know enough? Restoration Ecology 8 (3), 219e229. FAO (Food and Agricultural Organization of the United Nations), 2007. The World’s Mangroves 1980e2005, pp. 1e9. Keddy, P.A., 2000. Wetland Ecology: Principles and Conservation. Cambridge University Press, Cambridge, UK, pp. 1e18. Li, X., Yeh, A., Liu, K., Wang, S.G., 2006. Inventory of mangrove wetlands in the Pearl River Estuary of China using remote sensing. Journal of Geographical Sciences 16 (2), 155e164. Lin, P., Fu, Q., 2000. Environmental Ecology and Economic Utilization of Mangroves in China. Berlin Heidelberg CHEP and Springer Verlag, pp. 1e46. Peng, Y.S., Zhou, Y.W., Chen, G.Z., 2008. The restoration of mangrove wetland: a review. Acta Ecologica Sinica 28 (2), 786e797. Peng, Y.S., Li, X.L., Wu, K.L., Peng, Y.G., Chen, G.Z., 2009. Effect of an integrated mangrove-aquaculture system on aquacultural health. Frontiers of Biology in China 4 (4), 579e584. Phillips, D.L., Gregg, J.W., 2003. Source partitioning using stable isotope: coping with too many sources. Ecologia 136, 261e269. Primavera, J.H., 2006. Overcoming the impacts of aquaculture on the coastal zone. Ocean and Coastal Management 49, 531e545. Ramsar Convention Bureau, 1971. Convention on Wetlands of International Importance Especially as Waterfowl Habitats. Available online: www.ramsar. org/cda/en/ramsar-documents-texts-convention-on/main/ramsar. Robertson, A.I., Phillips, M.J., 1995. Mangroves as filters of shrimp pond effluent: predictions and biogeochemical research needs. Hydrobiologia 295, 311e321. Saenger, P., 2002. Mangrove Ecology, Silviculture and Conservation. Kluwer Academic Publishers, Dodrecht, Netherland, pp. 1e10. Shimoda, T., Fujioka, Y., Srithong, C., Aryuthaka, C., 2005. Phosphorus budget in shrimp aquaculture pond with mangrove enclosure and aquaculture performance. Fisheries Science 71, 1249e1255. SOA (State Oceanic Administration, People’s Republic of China), 1998. Criteria of Marine Monitoring and Determination (GB 17378-1998). Standard Press, Beijing, pp. 176e178. SOA (State Oceanic Administration, People’s Republic of China), 2012. Marine Environmental Quality Bulletin. Available online: www.coi.gov.cn/hygb/hjzl. Stevenson, N.J., Lewis, R.R., Burbridge, P.R., 1999. Disused shrimp ponds and mangrove rehabilitation. In: Streever, W. (Ed.), An International Perspective on Wetland Rehabilitation. Kluwer Academic Publishers, Dodrecht, Netherland, pp. 277e297. UNEP, 2004. Wetlands Bordering the South China Sea. UNEP/GEF/SCS Technical Publication No. 4. Bangkok, Thailand, p. 8. Wu, K.L., Peng, Y.S., Zheng, K.Z., Li, X.L., Chen, G.Z., 2010. Responses of aerenchyma in five mangrove species on artificial-non-tidal habitats. Acta Ecologica Sinica 30 (24), 6927e6934. Xu, S.N., Chen, Z.Z., Huang, H.H., Huang, X.P., Li, S.Y., 2010. Food sources of Oreochromis niloticus in the mangrove and plantation-aquaculture ecological coupling systems. Acta Scientiarum Naturalium Universitatis Sunyatseni 49 (1), 101e106. Xu, S.N., Chen, Z.Z., Li, S.Y., He, P.M., 2011. Modeling trophic structure and energy flows in a coastal artificial ecosystem using mass-balance ecopath model. Estuaries and Coasts 34, 351e363. Ye, Y., Tam, N.F.Y., Wong, Y.S., 2003. Growth and physiological responses of two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to waterlogging. Environmental and Experimental Botany 49, 209e221. Zheng, D.Z., Li, M., Zheng, S.F., Liao, B.W., Chen, Y.J., 2003. Headway of study on mangrove recovery and development in China. Guangdong Forestry Science and Technology 19 (1), 10e14.