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Livestock Wastewater Treatment by a Mangrove Pot-cultivation System and the Effect of Salinity on the Nutrient Removal Efficiency
PII: S0025-326X(00)00196-X
Marine Pollution Bulletin Vol. 42, No. 6, pp. 513±521, 2001 Ó 2001 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0025-326X/01 $ - see front matter
Livestock Wastewater Treatment by a Mangrove Pot-cultivation System and the Eect of Salinity on the Nutrient Removal Eciency Y. YE *, NORA F. Y. TAMà and Y. S. WONGà Marine Biotechnology Key Lab, Ningbo University, Ningbo, Zhejiang, People's Republic of China àDepartment of Biology and Chemistry, City University of Hong Kong, Hong Kong The present investigation compared the capacity of greenhouse pot-cultivation systems under two salinity conditions (freshwater and saline water) with two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to remove nutrients from livestock wastewater. During the whole treatment period there were relatively stable leachate TOC concentrations for wastewater-treated pots. Leachate NH 4 -N concentration of B. gymnorrhiza pots was generally lower than that of K. candel pots. Leachate PO34 -P concentration of pots receiving wastewater under freshwater condition was higher than that under saline water condition. Soil inorganic N content was more than two times higher for the wastewater treatments than that for the controls under low salinity condition and slower rate of increase under saline water condition. Soil P nutrients of both total and extractable inorganic forms signi®cantly increased for both systems due to the discharges of livestock wastewater under both salinity conditions. The rate of increase in P contents for plants receiving livestock wastewater was 1±4 times that of the controls, much more than that in N contents (0.04± 1.30 times). N nutrient removal eciencies were 84.3% (65.6% by soil and 18.7% by plant) and 95.5% (32.2% by soil and 63.4% by plant), respectively by Kandelia candel and B. gymnorrhiza pot-cultivation systems under freshwater condition. Under saline water condition, N nutrient removal eciencies by K. candel and B. gymnorrhiza potcultivation systems were 92.7% (80.7% by soil and 12.0% by plant) and 98.0% (67.6% by soil and 30.3% by plant), respectively. P nutrient removal eciencies by K. candel and B. gymnorrhiza systems under freshwater condition were 79.2% (76.6% by soil and 2.6% by plant) and 91.8% (88.2% by soil and 3.6% by plant), respectively. The corresponding values were 88.0% (84.2% by soil and 3.8% by plant) and 97.8% (95.9% by soil and 1.9% by plant)
*Corresponding author. Tel.: +86-574-7600590. E-mail address: [email protected] (Y. Ye).
under saline water condition. Ó 2001 Elsevier Science Ltd. All rights reserved. Keywords: Bruguiera gymnorrhiza; Kandelia candel; mangrove; livestock wastewater treatment; nutrient removal eciency; salinity.
Introduction Natural and constructed wetlands including mangroves have been considered to be low-cost and eective for wastewater treatment for pollutants from many sources, and especially ecient in the removal and bene®cial reuse of nutrients (Clough et al., 1983, Corbitt and Bowen, 1994, Breaux et al., 1995). Nutrients, especially N and P, are de®cient in coastal intertidal areas such as mangrove wetlands (Boto and Wellington, 1983; Clough et al., 1983; Lin, 1999). Therefore, mangrove wetlands may be particularly suitable for the treatment of wastewater rich in nutrients. Few researches have been done on nutrient removal from wastewater by mangrove systems (e.g. Chen et al., 1996, Wong et al., 1997). Furthermore, these several documents mainly focused on mangrove systems with Kandelia candel and the eect of salinity, an important environmental factor for mangrove wetlands, on the treatment eciency has not been well recognized. Mangroves are naturally distributed in areas with wide range of water salinity from nearly freshwater to seawater (Lin, 1999). Naidoo (1990) suggested that growth enhancement in response to added N occurs only at low salinity for Bruguiera gymnorrhiza cultured in solution. From this, habitat salinity may in¯uence the N uptake by mangrove plants and then aect its removal eciency, although the eect of salinity on nutrient removal by mangrove soil has not been clear. In addition, plants range widely in their nutrient needs due to inherent dierences between species 513
Marine Pollution Bulletin
including growth rates, eciency of nutrient use in the growth process and translocation of nutrients prior to senescing old tissue (Cole, 1995). Some documents showed that natural mangrove distribution was related to soil texture and soil nutrient concentrations (e.g. Zheng and Liao, 1989; Lan et al., 1994). For example, B. gymnorrhiza mangroves are generally distributed in loamy-clayey soil with wide range of nutrient contents, while K. candel mangroves grow in sandy-loamy soil with low nutrient contents (Lan et al., 1994), suggesting that these two main mangrove species have dierent capacity to use nutrients. The present investigation aims to compare the capacity of greenhouse pot-cultivation systems with two main mangrove species, B. gymnorrhiza and K. candel, to remove nutrient N and P from livestock wastewater. Another purpose is to evaluate the eect of salinity on the removal eciency. This work may be of signi®cance in the site selection of mangrove wetlands to treat wastewater rich in nutrients.
Materials and Methods Experiment design In April 1997, mature propagules of B. gymnorrhiza were collected at Mai Po Mangrove Nature Reserve (114° 050 E, 22° 320 N) in Hong Kong and planted into plastic pots in greenhouse with four individuals per pot. In November 1998, K. candel seedlings of 1.5 years old were transplanted from Wong Chuk Wan mangrove of Hong Kong into greenhouse pots with three individuals per pot. Each pot (18 cm in diameter and 20 cm in height) contained 4 kg soils (loamy± sandy soil texture with contents of sand, silt and clay of 73.11%, 15.93% and 10.96%, respectively) collected from Sai Keng mangrove forest and was daily irrigated with about 300 ml of tap water. The pot had six draining holes (0.6 cm in diameter) at the bottom so water was able to drain freely by gravitational force. There was one plastic tray underneath the pot to collect leachates. On 3 March 1999, 12 B. gymnorrhiza pots and 12 K. candel pots were selected as experimental materials for treating livestock wastewater collected at the Ta Kwu Ling Pig Farm of Hong Kong after being primarily treated by sedimentation and secondarily treated by
aeration. The wastewater has high P content and low 3 NH 4 -N/PO4 -P ratio of 1:1.5 (Table 1), dierent from most of other wastewater rich in nutrients with the N/P ratio of more than 40:1. The stem basal diameter and stem height of B. gymnorrhiza before the experiment were 0:82 0:08 cm and 24:2 3:2 cm, respectively (n 48), while the basal stem diameter of K. candel was 0:64 0:05 cm and the stem height was 25:2 3:9 cm (n 36). During treatment, each pot was daily watered with 300 ml treatment liquid. For each species, four treatments were triplicately setup: 1. F, each pot was irrigated with tap water every day; 2. FW, each pot was irrigated with 100% wastewater once in every three days and tap water every other day; 3. S, each pot was irrigated with arti®cial saline water (30 ppt salinity, prepared by dissolving a commercial salt purchased from Instant Ocean, Aquarium Systems, Mentor, Ohio) every day; 4. SW, each pot was irrigated with 100% wastewater once in every three days and saline water every other day. The intention of discharging wastewater once in every three days, i.e. wastewater was added between twice additions of tap water or saline water, was to partly simulate the ®eld situation that wastewater should be received between the two high tidal times of one day. Every three days was considered one treatment period and all treatments lasted for 48 periods, i.e. 144 days. Water, soil and plant analyses Wastewater, tap water, saline water and leachate samples were analysed for pH, conductivity, NH 4 -N, NO3 NO2 -N, PO34 -P and TOC every six treatment periods. Soil samples were analysed at the end of the experiment for extractable inorganic N (extracted with 2 N KCl followed by steam distillation), extractable inorganic P (extracted with 0.5 N NaHCO3 ), total N and total P (after conc. H2 SO4 digestion). At the end of the experiment, plants were harvested and dried at 105°C. Biomass and contents of total N and total P were analysed for leaf, stem and root, respectively. All of the chemical analyses were followed by the standard methods as described by Allen et al. (1974).
TABLE 1 Characteristics of livestock wastewater, tap water and saline water used in this experiment.a Parameter pH Conductivity (ms cm 1 ) TOC (mg l 1 ) 1 NH 4 -N (mg l ) NOx -N (mg l 1 ) PO34 -P (mg l 1 ) a
Wastewater 7.24 1.39 65.9 36.1
(7.00±7.35) (1.14±1.77) (48.1±88.3) (21.2±58.7) < 0:05 53.7 (22.5±94.6)
Note: Mean and range values (in brackets) of nine samples were shown.
514
Tap water
Saline water
7.64 (7.10±8.03) 0.22 (0.18±0.23) 2.3 (0.5±5.4) 0.3 (0.0±1.0) < 0:05 0.2 (0.0±0.5)
8.01 (7.32±8.26) 36.60 (34.83±38.49) 5.2 (2.1±7.0) 1.9 (0.0±5.9) < 0:05 0.2 (0.0±0.7)
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Statistical analysis The eects of salinity and wastewater and their interaction on soil nutrient status and plant total N and total P contents were analysed by two-way ANOVA. Signi®cant dierences among multiple means were determined by All Pairwise Multiple Comparison Procedures (Student±Newman±Keuls method).
Results and Discussion Leachate properties During the whole treatment period there were relatively stable values of leachate TOC concentrations for FW and SW of both species (Fig. 1), showing that the mangrove systems can eectively remove organics from livestock wastewater. No signi®cant dierences were found between FW and SW for both K. candel and B. gymnorrhiza pots, indicating that both plant species and habitat salinity have no signi®cant eects on the removal of organic matters in mangrove ecosystems. When livestock wastewater was added under either freshwater or saline water conditions, leachate NH 4 -N concentration of B. gymnorrhiza pots was generally lower than that of K. candel pots (Fig. 2). This indicated that plant species is important for NH 4 -N removal by mangrove systems and B. gymnorrhiza mangrove system has stronger capacity to remove NH 4 -N than K. candel mangrove system. On the ®rst wastewater adding date, leachate PO34 -P contents were similarly low for FW and SW of both K. candel and B. gymnorrhiza pots (Fig. 3). However, after the sixth wastewater addition, leachate PO34 -P contents were dierent between freshwater and saline water
Fig. 2 Changes in leachate NH 4 -N concentrations of K. candel pots (Kc) and B. gymnorrhiza pots (Bg) with treatment time (one treatment period was three days).
Fig. 3 Changes in leachate PO34 -P concentrations of K. candel pots (Kc) and B. gymnorrhiza pots (Bg) with treatment time (one treatment period was three days).
Fig. 1 Changes in leachate TOC contents of K. candel pots (Kc) and B. gymnorrhiza pots (Bg) with treatment time (one treament period was three days).
conditions for the two systems: lower for SW than FW, indicating that salinity will enhance the PO34 -P removal by mangrove systems. When livestock wastewater was added, higher leachate PO34 -P contents were generally found for K. candel pots than B. gymnorrhiza pots, 515
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showing that plant species is also important for wastewater PO34 -P removal by mangrove systems, similar to the removal of NH 4 -N. Soil nutrient status Additions of N or P have been found to increase plant production directly by increasing the amount of nutrients available for plant uptake. The increases in the contents of soil extractable inorganic N due to the discharge of livestock wastewater were signi®cant but not for that in soil total N (Fig. 4 and Table 2). Chen
Fig. 4 Soil extractable inorganic N and P, total N and P contents of K. candel pots (Kc) and B. gymnorrhiza pots (Bg) after 144 days' treatment. Values are the mean SD of three replicates. See Table 2 and text for results of statistical analysis.
et al. (1996) reported soil total N content of a simulated K. candel wetland system (under 15 ppt salinity condition) was 0.08 mg g 1 higher after one year's discharge of arti®cial wastewater than the control. For K. candel and B. gymnorrhiza pots in our study, the increase in soil total N content was about 0.04 mg g 1 and the dierences between wastewater treatments and their controls were not statistically signi®cant. This is due to shorter treatment time and lower N contents in wastewater. In a mangrove forest in Shenzhen of China, Wong et al. (1997) observed that the sediment inorganic N in the most landward region of a site receiving arti®cial wastewater was at least two times higher than that at the same distance in a control site. However, they found much slower rates of increase in sediment inorganic N contents in seaward region with high salinity condition. Similarly, soil inorganic N contents in this study were also over two times (2.32 and 2.09 for the K. candel and B. gymnorrhiza pots, respectively) higher for the wastewater treatments than those for the controls under low salinity condition (freshwater). However, slower rates of increase resulted from the wastewater treatments under saline water condition (1.37 and 2.03 for the K. candel and B. gymnorrhiza pots, respectively). Small proportions of total N existed in inorganic forms, ranging from 0.8% to 1.2% for the freshwater and saline water controls and a little higher for the wastewater treatments (1.5± 2.6%). Tam and Wong (1998) also reported a very small proportion of inorganic N to total N (about 6.8%) in soils of a mangrove forest in Hong Kong. Wong et al. (1997) also found small portions (about 0.6±1.6%) of the total N was inorganic N in sediments of both the site received wastewater and the site control of a mangrove forest in Shenzhen. Unlike N, soil P nutrients signi®cantly increased in both total and extractable inorganic forms for both systems due to the discharges of livestock wastewater in both systems under both salinity conditions (Fig. 4 and Table 2). Generally, higher rates of increase were found in extractable inorganic P than those in extractable inorganic N. The contents of extractable inorganic P increased 5.74 and 6.87 times for K. candel and B. gymnorrhiza pots, respectively due to discharges of livestock wastewater treatments under freshwater
TABLE 2 Results of two-way ANOVA for the eects of livestock wastewater discharge and salinity on soil properties of K. candel (Kc) and B. gymnorrhiza (Bg) pot-cultivation systems.a Kc
Parameter
Extractable inorganic N Extractable inorganic P Total N Total P a
Bg
Salinity
Wastewater
SW
Salinity
Wastewater
SW
2.98 0.21 0.08 0.03
11.15 23:86 0.34 30:40
3.38 0.13 0.00 0.74
0.16 3.79 0.03 0.09
21:95 564:02 2.78 89:49
0.04 2.29 0.06 0.09
Note: F-values are given in the table and signi®cance indicated by p < 0:05;
516
0:05 < p < 0:01;
p < 0:005.
Volume 42/Number 6/June 2001
condition. This was similar to the increase times (5.50 and 6.75 for K. candel and B. gymnorrhiza pots) under saline water condition. The total P contents in soils of wastewater treatment pots under freshwater condition were 1.93 and 2.34 times those of the controls for K. candel and B. gymnorrhiza pots, respectively. The rates of increase in total P due to wastewater were 2.16 and 2.43 for K. candel and B. gymnorrhiza pots under saline water condition. This is dierent from Wong et al.'s (1997) results that sediment total P concentration did not signi®cantly increase due to one year's wastewater discharge, because the P content in their wastewater (about 1 mg l 1 ) was much lower than that in this study (about 57 mg l 1 , see Table 1).
Fig. 5 Total N contents in root, stem and leaf of K. candel (Kc) and B. gymnorrhiza (Bg) seedlings after 144 days' treatment. Values are the mean SD of three replicates. See Table 3 and text for results of statistical analysis.
Plant N and P content Discharges of wastewater signi®cantly increased total N contents in leaf and for both K. candel and B. gymnorrhiza (Fig. 5, Table 3). After receiving livestock wastewater, N concentration in all parts of both species under saline conditions (SW) were slightly lower than thatunder freshwater condition (Fig. 5). This is similar to the conclusion by Stewart et al. (1979) that most halophyte species show an apparent decrease in N contents with an increase in external salt concentration. Under freshwater condition, the foliar N concentrations of K. candel and B. gymnorrhiza plants received livestock wastewater were 2.064% and 1.651%, respectively, higher than their respective control values (1.516% and 1.008%). Under saline water condition, the foliar N concentrations of K. candel and B. gymnorrhiza plants that received livestock wastewater were 1.933% and 1.409%, respectively, higher than their respective control values (1.422% and 1.028%). These were similar to most previous results. Henley (1978) reported that the nutrient level in the foliage of mangrove plants receiving wastewater was signi®cantly higher than that in the control site. Boto and Wellington (1983) also observed a signi®cant increase in foliar N (from initial 1.20% to 1.43%) and P (from initial 0.088% to 0.095%) for new leaves of Rhizophora collected from the fertilized site in Australia. Similarly, Clough et al. (1983) reported a foliar N concentration of 2.04% for a mangrove forest receiving long-term treated sewage euent, compared with a value of 1.15% at nearby undisturbed control sites. However, in an Aegiceras corniculatum, K. candel mangrove, subtle increases in foliar nutrient status were found after one year's discharge of settled municipal sewage (Wong et al., 1995, 1997). This is because, the total input of N from wastewater was only 200 kg for the site of 180 m 10 m 0:926 mg cm 2 month 1 , a value which was much lower than the estimated retention capacity of N by mangrove forest (Boto, 1992). In this study, the loading N rate was only about 0:393 mg cm 2 month 1 , but the foliar N signi®cantly increased compared with the controls. In our mangrove systems only seedlings were used and less biomass existed, so the eect of wastewater on plant nutrient status
TABLE 3 Results of two-way ANOVA for the eects of livestock wastewater discharge and salinity on total N and total P contents in root, stem and leaf of K. candel (Kc) and B. gymnorrhiza (Bg) under a pot-cultivation condition.a Parameter
Kc
Component Salinity
Wastewater
Bg SW
Total N
Root Stem Leaf
0.12 1.75 1.31
0.52 34:22 28:91
0.00 12.17 0.04
Total P
Root Stem Leaf
17:65 1.47 1.73
154:47 14:54 16:52
17:26 1.53 0.22
a
Salinity
Wastewater
SW
0.44 2.09 3.02
9.16 45:21 64:66
4.97 4.98 4.21
0.42 29:46 33:83
24:09 96:70 100:23
0.07 21:14 36:08
Note: F-values are given in the table and signi®cance indicated by p < 0:05; 0:05 < p < 0:01; p < 0:005.
517
Marine Pollution Bulletin
was obvious. However, less signi®cant increases were found for N contents in roots of K. candel and B. gymnorrhiza between wastewater treatments (FW and SW) and their controls (F and S), showing that plant absorbed N from wastewater mainly cumulated in the above-ground parts. Salinity did not show signi®cant eects on the N contents in each organ of both species. The P contents reported for mangrove plants are markedly low, e.g. the average whole plant-P concentrations in the Malaysian, Panamanean and Brazil mangroves are 0.91, 0.80 and 0.15 mg g 1 , respectively (Salcedo and Medeiros, 1995). In this study, similarly low P contents (0.28±0.77 mg g 1 ) were detected for the controls. However, the wastewater treatments generally increased the values by about 0.4 mg g 1 . The rates of increase in P contents for plants receiving livestock wastewater were 1±4 times that of the controls (Fig. 6), much more than those of N contents (0.04±1.30 times). This diered from the results from Boto and Wellington (1983) that higher increasing times were found for N contents than P contents. The reason is that livestock wastewater in this study has higher contents of P than that of N (Table 1). Unlike N, P contents in not only leaf and stem but also root of both K. candel and B. gymnorrhiza extremely signi®cantly increased due to the discharges of livestock wastewater (Fig. 6 and Table 3), indicating that all parts were important for mangrove plants to absorb P from wastewater. The eects of salinity on P contents were dierent with species and plant parts (Table 3). For P contents in K. candel, extremely
Fig. 6 Total P contents in root, stem and leaf of K. candel (Kc) and B. gymnorrhiza (Bg) seedlings after 144 days' treatment. Values are the mean SD of three replicates. See Table 3 and text for results of statistical analysis.
518
signi®cant interactions between salinity and wastewater were found in root but not in leaf and stem. Under saline water condition, P contents in roots more greatly increased due to the discharges of livestock wastewater than that under freshwater condition. For B. gymnorrhiza, however, signi®cant interactions between salinity and wastewater were found in leaf and stem but not in root. Under freshwater condition, P contents in leaf and stem more greatly increased due to the discharges of livestock wastewater than that under saline water condition. The mechanisms for this dierence were not well known and should be further researched. Mass balance and removal eciencies of N and P from wastewater From the dierences between loaded and leached quantities of N and P (the quantities of the respective controls were subtracted), the N and P quantities retained in the mangrove systems (soil and plant subsystems) due to wastewater discharge were obtained. N and P quantities absorbed from wastewater by plants were calculated by the multiplication of biomass and the dierence in N and P concentrations between wastewater treatments (FW and SW) and their respective controls (F and S). In order to know the nutrient loss and the error in this experiment, we compared the calculated soil nutrient removal quantities (dierence of retained and the total plant absorbed values) with the soil accumulated quantities obtained by the dierence in stock nutrients between the wastewater treatment pots and their controls. All the mass balance data were shown in Table 4. Mangrove ecosystems are highly productive, exporting organic matter to the adjacent waters (Boto and Wellington, 1988) and are sinks for N and P (RiveraMonroy et al., 1995). However, Thong et al. (1993) suggested that the ¯oor of a mangrove forest is a major source of inorganic N in the western coast of Peninsular Malaysia. In this study, most of N nutrients from livestock wastewater were 84.3% and 95.5%, respectively, removed by K. candel and B. gymnorrhiza pot-cultivation systems under freshwater condition and 92.7% and 98.0% under saline water condition (Table 5). P nutrient removal eciencies by K. candel and B. gymnorrhiza systems under freshwater condition were 79.2% and 91.8%, respectively, and 88.0% and 97.8% under saline water condition (Table 5). Obarska-Pempkowiak (1997) reported that removal of nutrients due to assimilation by reeds can be deemed insigni®cant because the mass balance of nutrients indicated that just over 9% N was converted into reed biomass. This N removal eciency by reed was lower than that by mangrove plants in this study (18.7% and 63.4%, respectively, for K. candel and B. gymnorrhiza systems under freshwater condition; 12.0% and 30.3% under saline water condition). This indicated that mangrove plants may be more eective in treating wastewater N nutrients than reed, a common high plant
Volume 42/Number 6/June 2001 TABLE 4 Mass balance of nutrient from livestock wastewater discharge into K. candel (Kc) and B. gymnorrhiza (Bg) pot-cultivation systems in mg. Item
N
Component
P
Kc
Loading Leached Retained Plant absorption
Soil removal Soil accumulationb Accumulated/removed
Root Stem Leaf Litter fall Subtotal
Bg
Kc
Bg
0a
30a
0a
30a
0a
30a
515 81 434 4 34 39 20 96 338 96 28.4%
492 36 456 4 9 39 8 59 397 192 48.4%
515 23 492 28 67 203 29 326 166 89 53.6%
492 10 482 4 31 108 6 149 333 118 35.4%
770 160 610 12 4 3 1 20 590 543 92.0%
769 92 677 25 2 2 0 29 648 647 99.8%
0a 770 63 707 8 10 9 1 28 679 688 101.3%
30a 769 17 752 9 3 2 0 14 738 738 100.0%
c
a
0 and 30 indicate salinity condition. Soil accumulation, determined by the dierence in stock nutrients between the wastewater treatment pots and their controls, was the increase in soil nutrient due to wastewater discharges. c The percentage was a little over 100% probably because of analytical error. b
TABLE 5 Treatment eciency (%) for livestock wastewater by K. candel (Kc) and B. gymnorrhiza (Bg) pot-cultivation systems and the eect of salinity. Subsystem
N
Component
P
Kc
Plant
Soil Total a
Root Stem Leaf Litter fall Subtotal
Bg
Kc
Bg
0a
30a
0a
30a
0a
30a
0a
30a
0.7 6.6 7.5 3.8 18.7 65.6
0.7 1.8 7.8 1.6 12.0 80.7
5.4 13.0 39.4 5.6 63.4 32.2
0.8 6.3 22.0 1.2 30.3 67.6
1.6 0.5 0.3 0.2 2.6 76.6
3.2 0.3 0.3 0.1 3.8 84.2
1.0 1.3 1.1 0.2 3.6 88.2
1.1 0.4 0.3 0.0 1.9 95.9
84.3
92.7
95.5
98.0
79.2
88.0
91.8
97.8
0 and 30 indicate salinity condition.
used to treat wastewater. Chen et al. (1996) obtained a N removal eciency of 12.70% by K. candel plants in a simulated wetland system receiving arti®cial wastewater under 15 ppt salinity. This is similar to those of K. candel in this study under both freshwater and 30 ppt salinity conditions, indicating that salinity condition has no signi®cant eect on the N nutrient removal by K. candel plants. N nutrient removal capacity by B. gymnorrhiza plants were relatively higher than those by K. candel under both freshwater and saline water conditions and high salinity had negative eects on the N removal. Leaf is the most important organ to absorb wastewater N nutrient for both species under both salinity conditions. It should be pointed out that small removal proportions existed as litter leaves because only seedlings were used in this study and little litter leaves appeared. However, nutrient removal by plants should not be omitted because plants can continuously assimilate N from soil and water due to their in®nite growth. P is generally considered the second most important plant nutrient after N (Willett et al., 1998). Jenssen et al.
(1997) showed that the potential for P removal by plants is lower than that for N removal. The P removal eciencies by K. candel and B. gymnorrhiza plants in this study were 1.9±4% and lower than the N removal percentages. Unlike N removal by plants, root and stem seem to be more important in P nutrient absorption than leaf, indicating that excessive P absorbed by roots cannot be transferred upward to the above-ground parts. Mangrove plants in natural forests generally have a N/P ratio of about 10 (Lin, 1999). The plant absorption ratios of N and P from livestock wastewater richer in P nutrient than N nutrient changed with salinity condition and plant species. Under both salinity conditions, higher N/P absorption ratios were found in B. gymnorrhiza plants (11.64 and 10.64 under freshwater and saline water conditions, respectively). The ratios of K. candel plants were lower than those of B. gymnorrhiza plants and had a higher value (4.28) under freshwater condition than that (2.03) under saline water condition. This indicated that the discharges of this kind of 519
Marine Pollution Bulletin
wastewater and salinity condition will aect the balance of plant N and P for K. candel but not for B. gymnorrhiza. From the mass balance of each system, most of the nutrients retained in the systems due to the discharges of livestock wastewater were removed by soil. This is similar to the previous results from mangrove ®elds and greenhouse simulated mangrove systems (Chen et al., 1996; Wong et al., 1997). Nutrients become unavailable for plant uptake through immobilization by soil microorganisms and through chemical and mineralogical reactions including precipitation and adsorption reactions and ionic ®xation within lattice structures of clay minerals. Except for plant absorption, N can be removed by physical, chemical and microbiological reactions of soils. Ammonium is easily adsorbed by soil under anaerobic conditions in mangrove systems. The conditions for denitri®cation, an anaerobic (anoxic) environment, are easily met in a mangrove system (Brix and Schierup, 1990). A relatively low percentage of the wastewaterborne inorganic N (less than 30%) was accumulated in the mangrove sediments (Wong et al., 1995, 1997). In this study, the accumulated total N in the soils of K. candel and B. gymnorrhiza systems due to livestock wastewater discharges were only 28.4% and 53.6%, respectively under freshwater condition and 48.4% and 35.4%, respectively under saline water condition (Table 5). The extractable inorganic N accumulated in soil from wastewater for K. candel and B. gymnorrhiza systems were 22 and 11 mg (only 6.5% and 6.6% of the removal quantities by soil), respectively, under freshwater condition. The corresponding values were 7 and 10 mg (only 1.8% and 3.0% of the removal quantities by soil), respectively, under saline water condition. Most of the N nutrients lost away from the systems. Some N might also be lost to the air via denitri®cation process (in the form of nitrogen gas) or via volatilization (in the form of NH3 ). Although very little information on the rate of either of these processes in mangrove sediments is available, the anaerobic and reduced condition together with the supply of the organic matter from wastewater would be in favor of denitri®cation activities in mangrove soils. The P removal eciencies by soil were near to those by the whole systems (total values in Table 5), indicating that wastewater P nutrients were treated mainly by soil. Jenssen et al. (1997) showed that the potential for P removal by plants is lower than that for N removal. Tam and Wong (1993, 1995) revealed that mangrove sediments were eective in trapping phosphorus, which had lower mobility and solubility than N. The removal of P, therefore, has to rely on adsorption/precipitation reactions. When soluble reactive phosphate is added to soils, it is usually rapidly immobilized by adsorption reactions depending to a large extent on the soil clay mineralogy, iron content and redox status (Boto, 1992). Surface Al OH, Fe OH, Al OH2 and Fe OH2 group are important sites for sorption of phosphate anions (Mansell et al., 1985). The transformations of fertilizer P are 520
controlled by the physical and chemical conditions in a particular soil which include clay mineralogy, clay content, exchangeable Al and soil organic matter level (Ruaysoongnern and Keerati-kasikorn, 1998). Allen, S. E., Grimshaw, H. W., Parkinson, J. A. and Quarmby, C. (1974) Chemical Analysis of Ecological Materials, Blackwell Scienti®c publications, Oxford. Boto, K. G. and Wellington, J. T. (1988) Seasonal variations in concentrations and ¯uxes of dissolved organic materials in a tropical, tidally-dominated, mangrove waterway. Marine Ecology Progress Series 50, 151±160. Boto, K. G. and Wellington, J. T. (1983) Nitrogen and phosphorus nutritional status of a northern Australian mangrove forest. Marine Ecology Progress Series 11, 63±69. Boto, K. G. (1992) Nutrient and mangroves. In Pollution in Tropical Aquatic Systems, eds. D. W. Connell, Hawler, pp. 129±145. CRC Press, Ann Arbor. Breaux, A. S., Farber, S. and Day, J. (1995) Using natural coastal wetlands systems for wastewater treatment: an economic bene®t analysis. Journal of Environmental Management 44, 285±291. Brix, H. and Schierup, H. H. (1990) Soil oxygenation in constructed reed beds-German experiences and ATV-guidelines H 262. In Use of Constructed Wetlands in Water Pollution Control, eds. P. F. Cooper, B. C. Findlater, pp. 505±515. Pergamon Press, Oxford. Chen, G. Z., Miao, S. Y., Wong, Y. S. and Tam, N. F. Y. (1996) Allocation, cycle and purged eects of nutrient pollutant N in arti®cial wastewater in simulated K. candel wetland system. Acta Scientiae Circumstantiae 16, 44±50. Clough, B. F., Boto, K. G. and Attiwill, P. M. (1983) Mangrove and sewage: a reevaluation. In Biology and Ecology of Mangroves. Tasks for Vegetation Science Series, ed. H. J. Teas, vol. 8, pp. 151±162. Dr W. Junk Publishers, Lancaster. Cole, D. W. (1995) Soil nutrient supply in natural and managed forests. Plant and Soil 168±169, 43±53. Corbitt, R. A. and Bowen, P. T. (1994) Constructed wetlands for wastewater treatment. In Applied Wetlands Science and Technology, ed. D. Kent, pp. 221±242. Lewis Publishers. Henley, D. A. (1978) An investigation of proposed euent discharge into a tropical mangrove estuary. In Proceedings of International Conference on Water Pollution Control in Developing Countries, pp. 43±64. September 1978, Thailand. Jenssen, P. D., Krogstad, T. and Mhlum, T. (1997) Wastewater treatment by aerated ponds and constructed wetlands in the Norwegian climate: results and design considerations. In Ecological Engineering for Wastewater Treatment, eds. C. Etnier, B. Guterstam, pp. 237±250. CRC Press, Ann Arbor. Lan, F. S., Li, R. T., Chen, P., Mo, Q. H., Liang, F. Y. and Ye, D. (1994) The relationshipn between mangroves and soils on the beach of Guangxi. Guihaia 14, 54±59. Lin, P. (1999) Mangrove Ecosystem in China. Science Press. Mansell, R. S., McKenna, P. J, Flaig, E. and Hall, M. (1985) Phosphate movement in columns of sandy soil from a wastewater irrigated site. Soil Science 140, 59±68. Naidoo, G. 1990. Eects of nitrate, ammonium and salinity on growth of the mangrove Bruguiera gymnorrhiza (L.) Lam. Aquatic Botany 38, 209±219. Obarska-Pempkowiak, H. (1997) Seasonal variations in the eciency of nutrient removal from domestic euent in a quasi-natural ®eld of reeds (Phragmites australis). In Ecological Engineering for wastewater treatment, eds. C. Etnier, B. Guterstam, pp. 207±216. CRC Press, Ann Arbor. Rivera-Monroy, V. H., Day, J. W., Twilley, R. R., Vera-Herrera, F. and Coronado-Molina, C. (1995) Flux of nitrogen and sediment in a fringe mangrove forest in Terminos Lagoon, Mexico. Estuarine Coastal and Shelf Science 40(2), 139±160. Ruaysoongnern, S. and Keerati-kasikorn, P. (1998) Role of phosphorus fertilization in improving the soil fertility of acid tropical and subtropical soils in Asia. In Nutrient Management for Sustainable Crop Production in Asia, eds. A. E. Johnston, J. K. Syers, pp. 61±74. CAB INTERNATIONAL. Salcedo, I. H. and Medeiros, C. (1995) Phosphorus transfer from tropical terrestrial to aquatic systems-mangroves. In Phosphorus in the Global Environment, ed. H. Tiessen, pp. 347±362. Wiley, New York.
Volume 42/Number 6/June 2001 Stewart, G. R., Larher, F., Ahmad, I. and Lee, J. A. (1979) In Ecological Progresses in Coastal Environments, eds. R. L. Jeeries, A. J. Davy, pp. 211±227. Blackwell Scienti®c Publications, Oxford. Tam, N. F. Y. and Wong, Y. S. (1993) Retention of nutrients and heavy metals in mangrove sediment receiving wastewater of dierent strengths. Environmental Technology 14, 719±729. Tam, N. F. Y. and Wong, Y. S. (1995) Mangrove soils as sinks for wastewater-borne pollutants. Hydrobiologia 295, 231±242. Tam, N. F. Y. and Wong, Y. S. (1998) Variation of soil nutrient and organic matter content in a subtropical mangrove ecosystem. Water, Air and Soil Pollution 103, 245±261. Thong, K. L., Sasakumar, A. and Marshall, N. (1993) Nitrogen concentrations in a mangrove creek with a large tidal range, Peninsular Malaysia. Hydrobiologia 254, 125±132.
Willett, I. R., Moody, P. W. and Blamey, F. P. C. (1998) The essential role of phosphorus in crop production. In Nutrient Management for Sustainable Crop Production in Asia, eds. A. E. Johnston, J. K. Syers. pp. 51±60. CAB INTERN. Wong, Y. S., Lan, C. Y., Chen, G. Z., Li, S. H., Chen, X. R., Liu, Z. P. and Tam, N. F. Y. (1995) Eect of wastewater discharge on nutrient contamination of mangrove soils and plants. Hydrobiologia 295, 243±254. Wong, Y. S., Tam, N. F. Y. and Lan, C. Y. (1997) Mangrove wetlands as wastewater treatment facility: a ®eld trial. Hydrobiologia 352, 49±59. Zheng, D. Z. and Liao, B. W. (1989) The investigation of mangrove and its habitat in both Qinglan Harbour and Dongzhai Harbour in Hainan Island. Forest Research 2, 433±441.
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Marine Pollution Bulletin Vol. 42, No. 6, pp. 513±521, 2001 Ó 2001 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0025-326X/01 $ - see front matter
Livestock Wastewater Treatment by a Mangrove Pot-cultivation System and the Eect of Salinity on the Nutrient Removal Eciency Y. YE *, NORA F. Y. TAMà and Y. S. WONGà Marine Biotechnology Key Lab, Ningbo University, Ningbo, Zhejiang, People's Republic of China àDepartment of Biology and Chemistry, City University of Hong Kong, Hong Kong The present investigation compared the capacity of greenhouse pot-cultivation systems under two salinity conditions (freshwater and saline water) with two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to remove nutrients from livestock wastewater. During the whole treatment period there were relatively stable leachate TOC concentrations for wastewater-treated pots. Leachate NH 4 -N concentration of B. gymnorrhiza pots was generally lower than that of K. candel pots. Leachate PO34 -P concentration of pots receiving wastewater under freshwater condition was higher than that under saline water condition. Soil inorganic N content was more than two times higher for the wastewater treatments than that for the controls under low salinity condition and slower rate of increase under saline water condition. Soil P nutrients of both total and extractable inorganic forms signi®cantly increased for both systems due to the discharges of livestock wastewater under both salinity conditions. The rate of increase in P contents for plants receiving livestock wastewater was 1±4 times that of the controls, much more than that in N contents (0.04± 1.30 times). N nutrient removal eciencies were 84.3% (65.6% by soil and 18.7% by plant) and 95.5% (32.2% by soil and 63.4% by plant), respectively by Kandelia candel and B. gymnorrhiza pot-cultivation systems under freshwater condition. Under saline water condition, N nutrient removal eciencies by K. candel and B. gymnorrhiza potcultivation systems were 92.7% (80.7% by soil and 12.0% by plant) and 98.0% (67.6% by soil and 30.3% by plant), respectively. P nutrient removal eciencies by K. candel and B. gymnorrhiza systems under freshwater condition were 79.2% (76.6% by soil and 2.6% by plant) and 91.8% (88.2% by soil and 3.6% by plant), respectively. The corresponding values were 88.0% (84.2% by soil and 3.8% by plant) and 97.8% (95.9% by soil and 1.9% by plant)
*Corresponding author. Tel.: +86-574-7600590. E-mail address: [email protected] (Y. Ye).
under saline water condition. Ó 2001 Elsevier Science Ltd. All rights reserved. Keywords: Bruguiera gymnorrhiza; Kandelia candel; mangrove; livestock wastewater treatment; nutrient removal eciency; salinity.
Introduction Natural and constructed wetlands including mangroves have been considered to be low-cost and eective for wastewater treatment for pollutants from many sources, and especially ecient in the removal and bene®cial reuse of nutrients (Clough et al., 1983, Corbitt and Bowen, 1994, Breaux et al., 1995). Nutrients, especially N and P, are de®cient in coastal intertidal areas such as mangrove wetlands (Boto and Wellington, 1983; Clough et al., 1983; Lin, 1999). Therefore, mangrove wetlands may be particularly suitable for the treatment of wastewater rich in nutrients. Few researches have been done on nutrient removal from wastewater by mangrove systems (e.g. Chen et al., 1996, Wong et al., 1997). Furthermore, these several documents mainly focused on mangrove systems with Kandelia candel and the eect of salinity, an important environmental factor for mangrove wetlands, on the treatment eciency has not been well recognized. Mangroves are naturally distributed in areas with wide range of water salinity from nearly freshwater to seawater (Lin, 1999). Naidoo (1990) suggested that growth enhancement in response to added N occurs only at low salinity for Bruguiera gymnorrhiza cultured in solution. From this, habitat salinity may in¯uence the N uptake by mangrove plants and then aect its removal eciency, although the eect of salinity on nutrient removal by mangrove soil has not been clear. In addition, plants range widely in their nutrient needs due to inherent dierences between species 513
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including growth rates, eciency of nutrient use in the growth process and translocation of nutrients prior to senescing old tissue (Cole, 1995). Some documents showed that natural mangrove distribution was related to soil texture and soil nutrient concentrations (e.g. Zheng and Liao, 1989; Lan et al., 1994). For example, B. gymnorrhiza mangroves are generally distributed in loamy-clayey soil with wide range of nutrient contents, while K. candel mangroves grow in sandy-loamy soil with low nutrient contents (Lan et al., 1994), suggesting that these two main mangrove species have dierent capacity to use nutrients. The present investigation aims to compare the capacity of greenhouse pot-cultivation systems with two main mangrove species, B. gymnorrhiza and K. candel, to remove nutrient N and P from livestock wastewater. Another purpose is to evaluate the eect of salinity on the removal eciency. This work may be of signi®cance in the site selection of mangrove wetlands to treat wastewater rich in nutrients.
Materials and Methods Experiment design In April 1997, mature propagules of B. gymnorrhiza were collected at Mai Po Mangrove Nature Reserve (114° 050 E, 22° 320 N) in Hong Kong and planted into plastic pots in greenhouse with four individuals per pot. In November 1998, K. candel seedlings of 1.5 years old were transplanted from Wong Chuk Wan mangrove of Hong Kong into greenhouse pots with three individuals per pot. Each pot (18 cm in diameter and 20 cm in height) contained 4 kg soils (loamy± sandy soil texture with contents of sand, silt and clay of 73.11%, 15.93% and 10.96%, respectively) collected from Sai Keng mangrove forest and was daily irrigated with about 300 ml of tap water. The pot had six draining holes (0.6 cm in diameter) at the bottom so water was able to drain freely by gravitational force. There was one plastic tray underneath the pot to collect leachates. On 3 March 1999, 12 B. gymnorrhiza pots and 12 K. candel pots were selected as experimental materials for treating livestock wastewater collected at the Ta Kwu Ling Pig Farm of Hong Kong after being primarily treated by sedimentation and secondarily treated by
aeration. The wastewater has high P content and low 3 NH 4 -N/PO4 -P ratio of 1:1.5 (Table 1), dierent from most of other wastewater rich in nutrients with the N/P ratio of more than 40:1. The stem basal diameter and stem height of B. gymnorrhiza before the experiment were 0:82 0:08 cm and 24:2 3:2 cm, respectively (n 48), while the basal stem diameter of K. candel was 0:64 0:05 cm and the stem height was 25:2 3:9 cm (n 36). During treatment, each pot was daily watered with 300 ml treatment liquid. For each species, four treatments were triplicately setup: 1. F, each pot was irrigated with tap water every day; 2. FW, each pot was irrigated with 100% wastewater once in every three days and tap water every other day; 3. S, each pot was irrigated with arti®cial saline water (30 ppt salinity, prepared by dissolving a commercial salt purchased from Instant Ocean, Aquarium Systems, Mentor, Ohio) every day; 4. SW, each pot was irrigated with 100% wastewater once in every three days and saline water every other day. The intention of discharging wastewater once in every three days, i.e. wastewater was added between twice additions of tap water or saline water, was to partly simulate the ®eld situation that wastewater should be received between the two high tidal times of one day. Every three days was considered one treatment period and all treatments lasted for 48 periods, i.e. 144 days. Water, soil and plant analyses Wastewater, tap water, saline water and leachate samples were analysed for pH, conductivity, NH 4 -N, NO3 NO2 -N, PO34 -P and TOC every six treatment periods. Soil samples were analysed at the end of the experiment for extractable inorganic N (extracted with 2 N KCl followed by steam distillation), extractable inorganic P (extracted with 0.5 N NaHCO3 ), total N and total P (after conc. H2 SO4 digestion). At the end of the experiment, plants were harvested and dried at 105°C. Biomass and contents of total N and total P were analysed for leaf, stem and root, respectively. All of the chemical analyses were followed by the standard methods as described by Allen et al. (1974).
TABLE 1 Characteristics of livestock wastewater, tap water and saline water used in this experiment.a Parameter pH Conductivity (ms cm 1 ) TOC (mg l 1 ) 1 NH 4 -N (mg l ) NOx -N (mg l 1 ) PO34 -P (mg l 1 ) a
Wastewater 7.24 1.39 65.9 36.1
(7.00±7.35) (1.14±1.77) (48.1±88.3) (21.2±58.7) < 0:05 53.7 (22.5±94.6)
Note: Mean and range values (in brackets) of nine samples were shown.
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Tap water
Saline water
7.64 (7.10±8.03) 0.22 (0.18±0.23) 2.3 (0.5±5.4) 0.3 (0.0±1.0) < 0:05 0.2 (0.0±0.5)
8.01 (7.32±8.26) 36.60 (34.83±38.49) 5.2 (2.1±7.0) 1.9 (0.0±5.9) < 0:05 0.2 (0.0±0.7)
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Statistical analysis The eects of salinity and wastewater and their interaction on soil nutrient status and plant total N and total P contents were analysed by two-way ANOVA. Signi®cant dierences among multiple means were determined by All Pairwise Multiple Comparison Procedures (Student±Newman±Keuls method).
Results and Discussion Leachate properties During the whole treatment period there were relatively stable values of leachate TOC concentrations for FW and SW of both species (Fig. 1), showing that the mangrove systems can eectively remove organics from livestock wastewater. No signi®cant dierences were found between FW and SW for both K. candel and B. gymnorrhiza pots, indicating that both plant species and habitat salinity have no signi®cant eects on the removal of organic matters in mangrove ecosystems. When livestock wastewater was added under either freshwater or saline water conditions, leachate NH 4 -N concentration of B. gymnorrhiza pots was generally lower than that of K. candel pots (Fig. 2). This indicated that plant species is important for NH 4 -N removal by mangrove systems and B. gymnorrhiza mangrove system has stronger capacity to remove NH 4 -N than K. candel mangrove system. On the ®rst wastewater adding date, leachate PO34 -P contents were similarly low for FW and SW of both K. candel and B. gymnorrhiza pots (Fig. 3). However, after the sixth wastewater addition, leachate PO34 -P contents were dierent between freshwater and saline water
Fig. 2 Changes in leachate NH 4 -N concentrations of K. candel pots (Kc) and B. gymnorrhiza pots (Bg) with treatment time (one treatment period was three days).
Fig. 3 Changes in leachate PO34 -P concentrations of K. candel pots (Kc) and B. gymnorrhiza pots (Bg) with treatment time (one treatment period was three days).
Fig. 1 Changes in leachate TOC contents of K. candel pots (Kc) and B. gymnorrhiza pots (Bg) with treatment time (one treament period was three days).
conditions for the two systems: lower for SW than FW, indicating that salinity will enhance the PO34 -P removal by mangrove systems. When livestock wastewater was added, higher leachate PO34 -P contents were generally found for K. candel pots than B. gymnorrhiza pots, 515
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showing that plant species is also important for wastewater PO34 -P removal by mangrove systems, similar to the removal of NH 4 -N. Soil nutrient status Additions of N or P have been found to increase plant production directly by increasing the amount of nutrients available for plant uptake. The increases in the contents of soil extractable inorganic N due to the discharge of livestock wastewater were signi®cant but not for that in soil total N (Fig. 4 and Table 2). Chen
Fig. 4 Soil extractable inorganic N and P, total N and P contents of K. candel pots (Kc) and B. gymnorrhiza pots (Bg) after 144 days' treatment. Values are the mean SD of three replicates. See Table 2 and text for results of statistical analysis.
et al. (1996) reported soil total N content of a simulated K. candel wetland system (under 15 ppt salinity condition) was 0.08 mg g 1 higher after one year's discharge of arti®cial wastewater than the control. For K. candel and B. gymnorrhiza pots in our study, the increase in soil total N content was about 0.04 mg g 1 and the dierences between wastewater treatments and their controls were not statistically signi®cant. This is due to shorter treatment time and lower N contents in wastewater. In a mangrove forest in Shenzhen of China, Wong et al. (1997) observed that the sediment inorganic N in the most landward region of a site receiving arti®cial wastewater was at least two times higher than that at the same distance in a control site. However, they found much slower rates of increase in sediment inorganic N contents in seaward region with high salinity condition. Similarly, soil inorganic N contents in this study were also over two times (2.32 and 2.09 for the K. candel and B. gymnorrhiza pots, respectively) higher for the wastewater treatments than those for the controls under low salinity condition (freshwater). However, slower rates of increase resulted from the wastewater treatments under saline water condition (1.37 and 2.03 for the K. candel and B. gymnorrhiza pots, respectively). Small proportions of total N existed in inorganic forms, ranging from 0.8% to 1.2% for the freshwater and saline water controls and a little higher for the wastewater treatments (1.5± 2.6%). Tam and Wong (1998) also reported a very small proportion of inorganic N to total N (about 6.8%) in soils of a mangrove forest in Hong Kong. Wong et al. (1997) also found small portions (about 0.6±1.6%) of the total N was inorganic N in sediments of both the site received wastewater and the site control of a mangrove forest in Shenzhen. Unlike N, soil P nutrients signi®cantly increased in both total and extractable inorganic forms for both systems due to the discharges of livestock wastewater in both systems under both salinity conditions (Fig. 4 and Table 2). Generally, higher rates of increase were found in extractable inorganic P than those in extractable inorganic N. The contents of extractable inorganic P increased 5.74 and 6.87 times for K. candel and B. gymnorrhiza pots, respectively due to discharges of livestock wastewater treatments under freshwater
TABLE 2 Results of two-way ANOVA for the eects of livestock wastewater discharge and salinity on soil properties of K. candel (Kc) and B. gymnorrhiza (Bg) pot-cultivation systems.a Kc
Parameter
Extractable inorganic N Extractable inorganic P Total N Total P a
Bg
Salinity
Wastewater
SW
Salinity
Wastewater
SW
2.98 0.21 0.08 0.03
11.15 23:86 0.34 30:40
3.38 0.13 0.00 0.74
0.16 3.79 0.03 0.09
21:95 564:02 2.78 89:49
0.04 2.29 0.06 0.09
Note: F-values are given in the table and signi®cance indicated by p < 0:05;
516
0:05 < p < 0:01;
p < 0:005.
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condition. This was similar to the increase times (5.50 and 6.75 for K. candel and B. gymnorrhiza pots) under saline water condition. The total P contents in soils of wastewater treatment pots under freshwater condition were 1.93 and 2.34 times those of the controls for K. candel and B. gymnorrhiza pots, respectively. The rates of increase in total P due to wastewater were 2.16 and 2.43 for K. candel and B. gymnorrhiza pots under saline water condition. This is dierent from Wong et al.'s (1997) results that sediment total P concentration did not signi®cantly increase due to one year's wastewater discharge, because the P content in their wastewater (about 1 mg l 1 ) was much lower than that in this study (about 57 mg l 1 , see Table 1).
Fig. 5 Total N contents in root, stem and leaf of K. candel (Kc) and B. gymnorrhiza (Bg) seedlings after 144 days' treatment. Values are the mean SD of three replicates. See Table 3 and text for results of statistical analysis.
Plant N and P content Discharges of wastewater signi®cantly increased total N contents in leaf and for both K. candel and B. gymnorrhiza (Fig. 5, Table 3). After receiving livestock wastewater, N concentration in all parts of both species under saline conditions (SW) were slightly lower than thatunder freshwater condition (Fig. 5). This is similar to the conclusion by Stewart et al. (1979) that most halophyte species show an apparent decrease in N contents with an increase in external salt concentration. Under freshwater condition, the foliar N concentrations of K. candel and B. gymnorrhiza plants received livestock wastewater were 2.064% and 1.651%, respectively, higher than their respective control values (1.516% and 1.008%). Under saline water condition, the foliar N concentrations of K. candel and B. gymnorrhiza plants that received livestock wastewater were 1.933% and 1.409%, respectively, higher than their respective control values (1.422% and 1.028%). These were similar to most previous results. Henley (1978) reported that the nutrient level in the foliage of mangrove plants receiving wastewater was signi®cantly higher than that in the control site. Boto and Wellington (1983) also observed a signi®cant increase in foliar N (from initial 1.20% to 1.43%) and P (from initial 0.088% to 0.095%) for new leaves of Rhizophora collected from the fertilized site in Australia. Similarly, Clough et al. (1983) reported a foliar N concentration of 2.04% for a mangrove forest receiving long-term treated sewage euent, compared with a value of 1.15% at nearby undisturbed control sites. However, in an Aegiceras corniculatum, K. candel mangrove, subtle increases in foliar nutrient status were found after one year's discharge of settled municipal sewage (Wong et al., 1995, 1997). This is because, the total input of N from wastewater was only 200 kg for the site of 180 m 10 m 0:926 mg cm 2 month 1 , a value which was much lower than the estimated retention capacity of N by mangrove forest (Boto, 1992). In this study, the loading N rate was only about 0:393 mg cm 2 month 1 , but the foliar N signi®cantly increased compared with the controls. In our mangrove systems only seedlings were used and less biomass existed, so the eect of wastewater on plant nutrient status
TABLE 3 Results of two-way ANOVA for the eects of livestock wastewater discharge and salinity on total N and total P contents in root, stem and leaf of K. candel (Kc) and B. gymnorrhiza (Bg) under a pot-cultivation condition.a Parameter
Kc
Component Salinity
Wastewater
Bg SW
Total N
Root Stem Leaf
0.12 1.75 1.31
0.52 34:22 28:91
0.00 12.17 0.04
Total P
Root Stem Leaf
17:65 1.47 1.73
154:47 14:54 16:52
17:26 1.53 0.22
a
Salinity
Wastewater
SW
0.44 2.09 3.02
9.16 45:21 64:66
4.97 4.98 4.21
0.42 29:46 33:83
24:09 96:70 100:23
0.07 21:14 36:08
Note: F-values are given in the table and signi®cance indicated by p < 0:05; 0:05 < p < 0:01; p < 0:005.
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was obvious. However, less signi®cant increases were found for N contents in roots of K. candel and B. gymnorrhiza between wastewater treatments (FW and SW) and their controls (F and S), showing that plant absorbed N from wastewater mainly cumulated in the above-ground parts. Salinity did not show signi®cant eects on the N contents in each organ of both species. The P contents reported for mangrove plants are markedly low, e.g. the average whole plant-P concentrations in the Malaysian, Panamanean and Brazil mangroves are 0.91, 0.80 and 0.15 mg g 1 , respectively (Salcedo and Medeiros, 1995). In this study, similarly low P contents (0.28±0.77 mg g 1 ) were detected for the controls. However, the wastewater treatments generally increased the values by about 0.4 mg g 1 . The rates of increase in P contents for plants receiving livestock wastewater were 1±4 times that of the controls (Fig. 6), much more than those of N contents (0.04±1.30 times). This diered from the results from Boto and Wellington (1983) that higher increasing times were found for N contents than P contents. The reason is that livestock wastewater in this study has higher contents of P than that of N (Table 1). Unlike N, P contents in not only leaf and stem but also root of both K. candel and B. gymnorrhiza extremely signi®cantly increased due to the discharges of livestock wastewater (Fig. 6 and Table 3), indicating that all parts were important for mangrove plants to absorb P from wastewater. The eects of salinity on P contents were dierent with species and plant parts (Table 3). For P contents in K. candel, extremely
Fig. 6 Total P contents in root, stem and leaf of K. candel (Kc) and B. gymnorrhiza (Bg) seedlings after 144 days' treatment. Values are the mean SD of three replicates. See Table 3 and text for results of statistical analysis.
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signi®cant interactions between salinity and wastewater were found in root but not in leaf and stem. Under saline water condition, P contents in roots more greatly increased due to the discharges of livestock wastewater than that under freshwater condition. For B. gymnorrhiza, however, signi®cant interactions between salinity and wastewater were found in leaf and stem but not in root. Under freshwater condition, P contents in leaf and stem more greatly increased due to the discharges of livestock wastewater than that under saline water condition. The mechanisms for this dierence were not well known and should be further researched. Mass balance and removal eciencies of N and P from wastewater From the dierences between loaded and leached quantities of N and P (the quantities of the respective controls were subtracted), the N and P quantities retained in the mangrove systems (soil and plant subsystems) due to wastewater discharge were obtained. N and P quantities absorbed from wastewater by plants were calculated by the multiplication of biomass and the dierence in N and P concentrations between wastewater treatments (FW and SW) and their respective controls (F and S). In order to know the nutrient loss and the error in this experiment, we compared the calculated soil nutrient removal quantities (dierence of retained and the total plant absorbed values) with the soil accumulated quantities obtained by the dierence in stock nutrients between the wastewater treatment pots and their controls. All the mass balance data were shown in Table 4. Mangrove ecosystems are highly productive, exporting organic matter to the adjacent waters (Boto and Wellington, 1988) and are sinks for N and P (RiveraMonroy et al., 1995). However, Thong et al. (1993) suggested that the ¯oor of a mangrove forest is a major source of inorganic N in the western coast of Peninsular Malaysia. In this study, most of N nutrients from livestock wastewater were 84.3% and 95.5%, respectively, removed by K. candel and B. gymnorrhiza pot-cultivation systems under freshwater condition and 92.7% and 98.0% under saline water condition (Table 5). P nutrient removal eciencies by K. candel and B. gymnorrhiza systems under freshwater condition were 79.2% and 91.8%, respectively, and 88.0% and 97.8% under saline water condition (Table 5). Obarska-Pempkowiak (1997) reported that removal of nutrients due to assimilation by reeds can be deemed insigni®cant because the mass balance of nutrients indicated that just over 9% N was converted into reed biomass. This N removal eciency by reed was lower than that by mangrove plants in this study (18.7% and 63.4%, respectively, for K. candel and B. gymnorrhiza systems under freshwater condition; 12.0% and 30.3% under saline water condition). This indicated that mangrove plants may be more eective in treating wastewater N nutrients than reed, a common high plant
Volume 42/Number 6/June 2001 TABLE 4 Mass balance of nutrient from livestock wastewater discharge into K. candel (Kc) and B. gymnorrhiza (Bg) pot-cultivation systems in mg. Item
N
Component
P
Kc
Loading Leached Retained Plant absorption
Soil removal Soil accumulationb Accumulated/removed
Root Stem Leaf Litter fall Subtotal
Bg
Kc
Bg
0a
30a
0a
30a
0a
30a
515 81 434 4 34 39 20 96 338 96 28.4%
492 36 456 4 9 39 8 59 397 192 48.4%
515 23 492 28 67 203 29 326 166 89 53.6%
492 10 482 4 31 108 6 149 333 118 35.4%
770 160 610 12 4 3 1 20 590 543 92.0%
769 92 677 25 2 2 0 29 648 647 99.8%
0a 770 63 707 8 10 9 1 28 679 688 101.3%
30a 769 17 752 9 3 2 0 14 738 738 100.0%
c
a
0 and 30 indicate salinity condition. Soil accumulation, determined by the dierence in stock nutrients between the wastewater treatment pots and their controls, was the increase in soil nutrient due to wastewater discharges. c The percentage was a little over 100% probably because of analytical error. b
TABLE 5 Treatment eciency (%) for livestock wastewater by K. candel (Kc) and B. gymnorrhiza (Bg) pot-cultivation systems and the eect of salinity. Subsystem
N
Component
P
Kc
Plant
Soil Total a
Root Stem Leaf Litter fall Subtotal
Bg
Kc
Bg
0a
30a
0a
30a
0a
30a
0a
30a
0.7 6.6 7.5 3.8 18.7 65.6
0.7 1.8 7.8 1.6 12.0 80.7
5.4 13.0 39.4 5.6 63.4 32.2
0.8 6.3 22.0 1.2 30.3 67.6
1.6 0.5 0.3 0.2 2.6 76.6
3.2 0.3 0.3 0.1 3.8 84.2
1.0 1.3 1.1 0.2 3.6 88.2
1.1 0.4 0.3 0.0 1.9 95.9
84.3
92.7
95.5
98.0
79.2
88.0
91.8
97.8
0 and 30 indicate salinity condition.
used to treat wastewater. Chen et al. (1996) obtained a N removal eciency of 12.70% by K. candel plants in a simulated wetland system receiving arti®cial wastewater under 15 ppt salinity. This is similar to those of K. candel in this study under both freshwater and 30 ppt salinity conditions, indicating that salinity condition has no signi®cant eect on the N nutrient removal by K. candel plants. N nutrient removal capacity by B. gymnorrhiza plants were relatively higher than those by K. candel under both freshwater and saline water conditions and high salinity had negative eects on the N removal. Leaf is the most important organ to absorb wastewater N nutrient for both species under both salinity conditions. It should be pointed out that small removal proportions existed as litter leaves because only seedlings were used in this study and little litter leaves appeared. However, nutrient removal by plants should not be omitted because plants can continuously assimilate N from soil and water due to their in®nite growth. P is generally considered the second most important plant nutrient after N (Willett et al., 1998). Jenssen et al.
(1997) showed that the potential for P removal by plants is lower than that for N removal. The P removal eciencies by K. candel and B. gymnorrhiza plants in this study were 1.9±4% and lower than the N removal percentages. Unlike N removal by plants, root and stem seem to be more important in P nutrient absorption than leaf, indicating that excessive P absorbed by roots cannot be transferred upward to the above-ground parts. Mangrove plants in natural forests generally have a N/P ratio of about 10 (Lin, 1999). The plant absorption ratios of N and P from livestock wastewater richer in P nutrient than N nutrient changed with salinity condition and plant species. Under both salinity conditions, higher N/P absorption ratios were found in B. gymnorrhiza plants (11.64 and 10.64 under freshwater and saline water conditions, respectively). The ratios of K. candel plants were lower than those of B. gymnorrhiza plants and had a higher value (4.28) under freshwater condition than that (2.03) under saline water condition. This indicated that the discharges of this kind of 519
Marine Pollution Bulletin
wastewater and salinity condition will aect the balance of plant N and P for K. candel but not for B. gymnorrhiza. From the mass balance of each system, most of the nutrients retained in the systems due to the discharges of livestock wastewater were removed by soil. This is similar to the previous results from mangrove ®elds and greenhouse simulated mangrove systems (Chen et al., 1996; Wong et al., 1997). Nutrients become unavailable for plant uptake through immobilization by soil microorganisms and through chemical and mineralogical reactions including precipitation and adsorption reactions and ionic ®xation within lattice structures of clay minerals. Except for plant absorption, N can be removed by physical, chemical and microbiological reactions of soils. Ammonium is easily adsorbed by soil under anaerobic conditions in mangrove systems. The conditions for denitri®cation, an anaerobic (anoxic) environment, are easily met in a mangrove system (Brix and Schierup, 1990). A relatively low percentage of the wastewaterborne inorganic N (less than 30%) was accumulated in the mangrove sediments (Wong et al., 1995, 1997). In this study, the accumulated total N in the soils of K. candel and B. gymnorrhiza systems due to livestock wastewater discharges were only 28.4% and 53.6%, respectively under freshwater condition and 48.4% and 35.4%, respectively under saline water condition (Table 5). The extractable inorganic N accumulated in soil from wastewater for K. candel and B. gymnorrhiza systems were 22 and 11 mg (only 6.5% and 6.6% of the removal quantities by soil), respectively, under freshwater condition. The corresponding values were 7 and 10 mg (only 1.8% and 3.0% of the removal quantities by soil), respectively, under saline water condition. Most of the N nutrients lost away from the systems. Some N might also be lost to the air via denitri®cation process (in the form of nitrogen gas) or via volatilization (in the form of NH3 ). Although very little information on the rate of either of these processes in mangrove sediments is available, the anaerobic and reduced condition together with the supply of the organic matter from wastewater would be in favor of denitri®cation activities in mangrove soils. The P removal eciencies by soil were near to those by the whole systems (total values in Table 5), indicating that wastewater P nutrients were treated mainly by soil. Jenssen et al. (1997) showed that the potential for P removal by plants is lower than that for N removal. Tam and Wong (1993, 1995) revealed that mangrove sediments were eective in trapping phosphorus, which had lower mobility and solubility than N. The removal of P, therefore, has to rely on adsorption/precipitation reactions. When soluble reactive phosphate is added to soils, it is usually rapidly immobilized by adsorption reactions depending to a large extent on the soil clay mineralogy, iron content and redox status (Boto, 1992). Surface Al OH, Fe OH, Al OH2 and Fe OH2 group are important sites for sorption of phosphate anions (Mansell et al., 1985). The transformations of fertilizer P are 520
controlled by the physical and chemical conditions in a particular soil which include clay mineralogy, clay content, exchangeable Al and soil organic matter level (Ruaysoongnern and Keerati-kasikorn, 1998). Allen, S. E., Grimshaw, H. W., Parkinson, J. A. and Quarmby, C. (1974) Chemical Analysis of Ecological Materials, Blackwell Scienti®c publications, Oxford. Boto, K. G. and Wellington, J. T. (1988) Seasonal variations in concentrations and ¯uxes of dissolved organic materials in a tropical, tidally-dominated, mangrove waterway. Marine Ecology Progress Series 50, 151±160. Boto, K. G. and Wellington, J. T. (1983) Nitrogen and phosphorus nutritional status of a northern Australian mangrove forest. Marine Ecology Progress Series 11, 63±69. Boto, K. G. (1992) Nutrient and mangroves. In Pollution in Tropical Aquatic Systems, eds. D. W. Connell, Hawler, pp. 129±145. CRC Press, Ann Arbor. Breaux, A. S., Farber, S. and Day, J. (1995) Using natural coastal wetlands systems for wastewater treatment: an economic bene®t analysis. Journal of Environmental Management 44, 285±291. Brix, H. and Schierup, H. H. (1990) Soil oxygenation in constructed reed beds-German experiences and ATV-guidelines H 262. In Use of Constructed Wetlands in Water Pollution Control, eds. P. F. Cooper, B. C. Findlater, pp. 505±515. Pergamon Press, Oxford. Chen, G. Z., Miao, S. Y., Wong, Y. S. and Tam, N. F. Y. (1996) Allocation, cycle and purged eects of nutrient pollutant N in arti®cial wastewater in simulated K. candel wetland system. Acta Scientiae Circumstantiae 16, 44±50. Clough, B. F., Boto, K. G. and Attiwill, P. M. (1983) Mangrove and sewage: a reevaluation. In Biology and Ecology of Mangroves. Tasks for Vegetation Science Series, ed. H. J. Teas, vol. 8, pp. 151±162. Dr W. Junk Publishers, Lancaster. Cole, D. W. (1995) Soil nutrient supply in natural and managed forests. Plant and Soil 168±169, 43±53. Corbitt, R. A. and Bowen, P. T. (1994) Constructed wetlands for wastewater treatment. In Applied Wetlands Science and Technology, ed. D. Kent, pp. 221±242. Lewis Publishers. Henley, D. A. (1978) An investigation of proposed euent discharge into a tropical mangrove estuary. In Proceedings of International Conference on Water Pollution Control in Developing Countries, pp. 43±64. September 1978, Thailand. Jenssen, P. D., Krogstad, T. and Mhlum, T. (1997) Wastewater treatment by aerated ponds and constructed wetlands in the Norwegian climate: results and design considerations. In Ecological Engineering for Wastewater Treatment, eds. C. Etnier, B. Guterstam, pp. 237±250. CRC Press, Ann Arbor. Lan, F. S., Li, R. T., Chen, P., Mo, Q. H., Liang, F. Y. and Ye, D. (1994) The relationshipn between mangroves and soils on the beach of Guangxi. Guihaia 14, 54±59. Lin, P. (1999) Mangrove Ecosystem in China. Science Press. Mansell, R. S., McKenna, P. J, Flaig, E. and Hall, M. (1985) Phosphate movement in columns of sandy soil from a wastewater irrigated site. Soil Science 140, 59±68. Naidoo, G. 1990. Eects of nitrate, ammonium and salinity on growth of the mangrove Bruguiera gymnorrhiza (L.) Lam. Aquatic Botany 38, 209±219. Obarska-Pempkowiak, H. (1997) Seasonal variations in the eciency of nutrient removal from domestic euent in a quasi-natural ®eld of reeds (Phragmites australis). In Ecological Engineering for wastewater treatment, eds. C. Etnier, B. Guterstam, pp. 207±216. CRC Press, Ann Arbor. Rivera-Monroy, V. H., Day, J. W., Twilley, R. R., Vera-Herrera, F. and Coronado-Molina, C. (1995) Flux of nitrogen and sediment in a fringe mangrove forest in Terminos Lagoon, Mexico. Estuarine Coastal and Shelf Science 40(2), 139±160. Ruaysoongnern, S. and Keerati-kasikorn, P. (1998) Role of phosphorus fertilization in improving the soil fertility of acid tropical and subtropical soils in Asia. In Nutrient Management for Sustainable Crop Production in Asia, eds. A. E. Johnston, J. K. Syers, pp. 61±74. CAB INTERNATIONAL. Salcedo, I. H. and Medeiros, C. (1995) Phosphorus transfer from tropical terrestrial to aquatic systems-mangroves. In Phosphorus in the Global Environment, ed. H. Tiessen, pp. 347±362. Wiley, New York.
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