Agriculture, Ecosystems and Environment 122 (2007) 192–202

www.elsevier.com/locate/agee

Nutrient flows in small-scale peri-urban vegetable farming systems

in Southeast Asia—A case study in Hanoi
Nguyen Manh Khai a,*, Pham Quang Ha b, Ingrid Öborn a
a
Department of Soil Sciences, Swedish University of Agricultural Sciences (SLU), P.O. Box 7014, SE-750 07 Uppsala, Sweden
b
Vietnam National Institute for Soils and Fertilisers, Chem, Tu Liem, Hanoi, Vietnam
Received 7 June 2006; received in revised form 28 December 2006; accepted 11 January 2007
Available online 8 February 2007

Abstract

In many peri-urban areas of Southeast Asia, land use has been transformed from rice-based to more profitable vegetable-based systems in
order to meet the increasing market demand. The major management related flows of nitrogen (N), phosphorus (P), potassium (K), copper
(Cu) and zinc (Zn) were quantified over a 1-year period for intensive small-scale aquatic and terrestrial vegetable systems situated in two peri-
urban areas of Hanoi City, Vietnam. The two areas have different sources of irrigation water; wastewater from Hanoi City and water from the
Red River upstream of Hanoi. The first nutrient balances for this region and farming systems are presented. The main sources of individual
elements were quantified and the nutrient use efficiency estimated. The environmental risks for losses and/or soil accumulation were also
assessed and discussed in relation to long-term sustainability and health aspects.
The primary source of nutrient input involved a combination of chemical fertilisers, manure (chicken) and irrigation water. A variable
composition and availability of the latter two sources greatly influenced the relative magnitude of the final total loads for individual elements.
Despite relatively good nutrient use efficiencies being demonstrated for N (46–86%) and K (66–94%), and to some extent also for P (19–
46%), high inputs still resulted in substantial annual surpluses causing risks for losses to surface and ground waters. The surplus for N ranged
from 85 to 882 kg ha1 year1, compared to P and K which were 109–196 and 20–306 kg ha1 year1, respectively. Those for Cu and Zn
varied from 0.2 to 2.7 and from 0.6 to 7.7 kg ha1 year1, respectively, indicating high risk for soil accumulation and associated transfers
through the food chain.
Wastewater irrigation contributed to high inputs, and excess use of organic and chemical fertilisers represent a major threat to the soil and
water environment. Management options that improve nutrient use efficiency represent an important objective that will help reduce annual
surpluses. A sustainable reuse of wastewater for irrigation in peri-urban farming systems can contribute significantly to the nutrient supply
(assuming low concentrations of potential toxic or hazardous substances in the water). Nutrient inputs need to be better related to the crop
need, e.g. through better knowledge about the nutrient concentrations in the wastewater and improved management of the amount of irrigation
water being applied.
# 2007 Elsevier B.V. All rights reserved.

Keywords: Element balance; Nutrients; Copper; Zinc; Peri-urban; Southeast Asia

1. Introduction
Peri-urban areas are the transition or interaction zone,
where urban and rural activities meet. The landscape
features in peri-urban areas are subject to rapid anthro-
pogenic modification and development. In many peri-urban
* Corresponding author. Tel.: +46 18 671257; fax: +46 18 672795.
E-mail address: Nguyen.Manh.Khai@mv.slu.se (N.M. Khai).
areas of Southeast Asia, land use has been transformed from
rice-based to more profitable vegetable-based systems
(Richter and Roelcke, 2000). Vegetable production in
peri-urban areas is now a key sector of the regional
agricultural economy (Jansen et al., 1996; AVRDC, 2002;
Midmore and Jansen, 2003). Peri-urban agriculture is
important for food supply to the growing city population.
For example, van den Berg et al. (2003) estimated that in the
year 2000 about half the total area of Hanoi City was used

0167-8809/$ – see front matter # 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.agee.2007.01.003
 N.M. Khai et al. / Agriculture, Ecosystems and Environment 122 (2007) 192–202 193

for agriculture which supplied 62–83% of the vegetables,
50–73% of the pork and about 46% of the fish that was
consumed in Hanoi City.
The intensive nature of peri-urban cropping systems
suggests that they are likely to be the subject of large
element flows (Hedlund et al., 2003; Wolf et al., 2003;
Huang et al., 2006). These take the form of daily transport
of produce to adjacent cities with a variable but potentially
significant proportion being returned as waste products
(biosolids and wastewater). It is also possible for
potentially toxic contaminants to be recycled along with
the waste effluent (Duong et al., 2006; Singh and Kumar,
2006). Large quantities of nutrients in the form of chemical
fertilisers and livestock manures are also applied. The
relative contribution that individual sources make to the
total nutrient flow within these systems has received
limited study compared to typical European agricultural
systems (e.g. Goodlass et al., 2003). There is the strong
possibility that intensive vegetable production systems
currently operate at a considerable annual nutrient surplus
with potential deleterious environmental consequences.
The accumulation of potentially toxic elements derived
from industrial sources (Midmore and Jansen, 2003; Zhang
et al., 2007) and transferred in wastewater and biosolids
represents a further health issue (Oron et al., 2004; El-
Mowelhi et al., 2006; Huang et al., 2006; Singh and
Kumar, 2006).
The continual increase in demand for vegetables as an
effect of urbanization can, in the short-term, only be satisfied
through some combination of intensification of existing peri-
urban agriculture together with an increase in the land area
utilized for this type of production (Jansen et al., 1996; van
den Berg et al., 2003). Improved understanding of nutrient
flows within these peri-urban agricultural systems should
help in maintaining productivity and soil quality and assess
the potential environmental impact. An inventory and
quantification of element balances is the first step to provide
a basis for management decisions on improved practices
(e.g. Smaling et al., 1999; Öborn et al., 2003). This would
contribute to the development of policies as well as locally
adapted advice in order to achieve sustainable production
systems from economic, health and environmental perspec-
tives.
The aim was to investigate the management related
nutrient fluxes and balances (surpluses) in peri-urban
vegetable farming systems using two villages in the
outskirts of Hanoi City, Vietnam, as case studies. More
specifically, our objectives were (i) to identify and quantify
the field (plot) level fluxes of some macro and micro nutrient
elements, i.e. nitrogen (N), phosphorus (P), potassium (K),
copper (Cu) and zinc (Zn), (ii) to assess the imbalance
between measured inputs and outputs in terms of nutrient
use efficiency, and (iii) to assess the rate at which these
elements are accumulating in peri-urban soils.

Table 1
Characteristics of the two study sites (villages) in peri-urban Hanoi, Vietnam
Characteristics
Administration
Position
Annual rainfall
Rainfall during the study
period (12 months)
Mean monthly temperature
Humidity
Number of house holds
Land area of village
Agricultural area
Irrigation
Farming system
Main vegetables typesc
Bang B site
Bang B village, Hoang Liet commune, Thanh Tri district
N: 20857.4020 , E: 105849.6640
1628a mm, >50% of the rainfall June–August
1540 mm
17 (December/January)–29 (June/August) 8C
68–83%
361
49 ha
39 ha (80% of the total land)
Irrigation channels using water from Kim Nguu river
Vegetables, rice, fishery, animal husbandry
Aquatic vegetables (8 ha): morning glory (Impomoea aquatica
Foskal), water celery (Oenanthe javanica L.), water cress
(Rorippa Scop), water mimosa (Neptunia oleracea Loureiro L.)
Terrestrial vegetables (4 ha): cabbage (Brassica oleraceae L.),
cucumber (Cucumis sativus L.), kohlrabi (Brassica oleracea
L. var. gongylodes L.), lettuce (Lactuca satica L.), onion
(Allium fistulosum L.), spinach (Spinacea oleracea L.)
Phuc Ly site
Phuc Ly village, Minh Khai commune, Tu Liem district
N: 21804.0120 , E: 105844.7150
1564b mm, >50% of the rainfall June–August
1360 mm
17 (December/January)–29 (June/August) 8C
68–83%
700
125 ha
107 ha (86% of the total land)
Irrigation channels using water from Nhue river
(one branch of Red River)
Vegetables, flowers, rice, fruit trees, animal husbandry
Terrestrial vegetables (40 ha): anethum (Anethum
graveoleus L.), basil (Ocimum africamum), cabbage,
Chinese mustard (Brassica juncea L.), choisum (Brassica
chinensis L.), coriander (Coriandrum sativum L.),
cucumber, garland (Chrysanthemum coronarium L.),
lettuce, mustard (Brassica campestris L.), onion, perilla
(Perrila ocymoides L.)

Other crops Rice (Oryza sativa L.) Rice, fruits, flowers

Fertilisers NPK, urea, P-fert, K-fert, chicken manure, horn, ash NPK, urea, P-fert K-fert, chicken manure, bio fertiliser,
foliar spray, ash
Soild Eutric Fluvisol Eutric Fluvisol
a
Average rainfall from 1990 to 2004.
b
Average rainfall from 2000 to 2004.
c
Groups of common vegetables in the villages.
d
According to Tra and Egashira (1999) and Pham et al. (2005).
194 N.M. Khai et al. / Agriculture, Ecosystems and Environment 122 (2007) 192–202

2. Materials and methods 2.2. Quantifying element flows

2.1. Description of study area
The study was carried out in Hanoi, the capital of
Vietnam that has an official population of 3 million (Hanoi
Statistical Office, 2003) and where the urbanization process
is presently going on very rapidly. Hanoi City comprises
nine inner city districts and five outer city districts of a total
area of 92,100 ha. Vegetables are produced in the outer city
peri-urban districts including Thanh Tri and Tu Liem in
which two villages, Bang B and Phuc Ly, were selected for
this study (Table 1). Vegetable production is the main
farming activity in both villages and it generates about 61–
66% of the average household income (Pham et al., 2005;
Hoang Fagerström et al., 2006). At the Phuc Ly site farmers
are specialized in terrestrial (dry-land) vegetable production,
which is intensive in terms of number of crops per year and
inputs used (manure, chemical fertilisers and pesticide).
Bang B is located downstream of industrial and urban areas
and here farmers specialize in aquatic vegetables grown
under submerged conditions in addition to some production
of rice, fish and dry-land vegetables. Both sites have
sufficient water which is supplied through irrigation
systems. For Phuc Ly this is sourced from the Red River
upstream of Hanoi City, while Bang B receives wastewater
from the Kim Nguu River.
At each study site, two plots were selected having different
cropping histories with respect to the number of years under
vegetable cultivation and the type of crops grown. In Bang B
(BB1 and BB2) aquatic, and in Phuc Ly (PL1 and PL2)
terrestrial vegetable plots were studied (Table 2).
A range of materials acted as potential sources for the
input of elements, including seedlings, urban waste, manure,
chemical fertilisers, irrigation water, rainwater, and soil
amendments such as horn and ash. The composition of
individual sources varied widely (Table 2). Output of each
element through the harvested crop products was also
quantified.
All relevant farming related activities were monitored
and quantified during the experimental year (starting autumn
2003). Individual farmers were provided with a ‘note book’
in which to document all field activities. Study sites were
visited at least once a week by a member of the research
team during which each farmer was interviewed, and notes
checked and reviewed.
Manure and chemical fertilisers were weighed before
application. Harvested crop yield was estimated by either
weighing every 10th bunch or by sampling and weighing
material removed from three 0.25 m2 areas and multiplied
by the number of bunches or total crop area harvested. At
Bang B, water levels in each study plot were recorded before
and after irrigation to estimate the volume of water applied.
At Phuc Ly, plots were hand irrigated and total volume of
water applied was estimated by multiplying the number of
buckets emptied with the average water volume (5–10
buckets measured at random). Data from the local weather
stations (either Lang 10 km north of Bang B or a site
adjacent to Phuc Ly) were used to estimate the rainfall.
Nutrients (N, P, K, Cu and Zn) in crop, manure, ash,
irrigation water and rainwater (only N, P, K) were analyzed
while the composition of the chemical fertilisers were given

Table 2
Description of the study plots in Bang B (BB1 and BB2) and Phuc Ly (PL1 and PL2) villages, Hanoi, and quantification of the major input flows for a 12-month
period through fertiliser and irrigation water
BB1 BB2 PL1 PL2
Farmer Mr. Lan Mr. Lan Mrs. Sau Mr. Dan
Plot area (m2) 192 408 356 287
Position N: 20857.5530 N: 20857.4460 N: 21804.0530 N: 21804.1860
E: 105849.6560 E: 105849.5280 E: 105845.1020 E: 105845.2220
Number of sub-plotsa 10 7
Sub-plot area (m2) 32–40 36–45
Vegetableb Aquatic Aquatic Terrestrial Terrestrial
Seedling/seed typec Seedling Seedling Seed Seed
Chicken manure (t ha1)d 18.4 17.9
Chemical fertilisers NPK, urea, P-fert, K-fert NPK, urea, P-fert, K-fert NPK, urea, P-fert NPK, urea, P-fert
1
Other fertiliser (t ha )
Ash 1.5 2.1 1.1
Horn 0.8
Irrigation water (m3 ha1)e
Wastewater 13,400 52,700
Natural river water 7900 7800
a
Plot was divided into 7 or 10 sub-plots with different planting date and/or crop species.
b
Aquatic vegetables grow in permanent flooded plots. The water depth in the field varies from 5 to 60 cm.
c
Inputs through seedlings were quantified, whereas inputs through seeds was not included since it was considered to be of minor importance.
d
Fresh weight, the water content varied from 38 to 64% (PL1) and 25 to 70% (PL2). Chemical composition given in Fig. 2.
e
Chemical composition given in Fig. 1.
 N.M. Khai et al. / Agriculture, Ecosystems and Environment 122 (2007) 192–202
by the manufacturer, and N fixation was estimated based on
the findings by Roy et al. (2003).
Element fluxes were estimated by multiplying the mass of
material by their element concentrations (Eq. (1)).
X
n
F¼ Qi C i (1)
i¼1
where F is the total element flow (input or output) over the
period of measurement, n the number of events (application
of fertiliser, irrigation water, rain, or harvested crop pro-
ducts, etc.), Qi the quantity of raw material at event i and Ci
is the element concentration in raw material at event i.
2.3. Sampling and preservation of samples
Top soil samples were taken to a depth of 0–20 cm using a
stainless steel trowel. Five sub-samples collected from
within an area of 5 m  5 m were bulked and mixed in the
field. Soil samples were air-dried and crushed to pass
through a 2 mm nylon sieve and used for the determination
of pH. For analysis of N, P, K, Cu and Zn soil (<2 mm) was
ground with an agate mortar to pass through a 0.25 mm
nylon mesh.
Manure samples (a minimum of five sub-samples on each
occasion) were collected from the field just before each
application event.
Samples (consisting of at least five sub-samples) of
vegetable material were principally collected at the time of
harvesting or transplanting (for seedling samples). Some
frequently grown short-duration crops were not sampled for
analyses at each harvest whereas some long-duration crops,
from which leaves were repeatedly harvested (e.g. morning
glory), more than one sample was taken for chemical
determination. The plant samples were rinsed with tap water
and then washed thoroughly with distilled water. After air-
drying, samples were cut into small pieces, mixed evenly,
dried to constant weight in an oven at 60–70 8C, finely
ground to pass a 0.4 mm nylon sieve before digestion and
chemical analysis.
The dry matter content of fresh vegetable and manure
samples was determined by drying at 105 8C as soon as
possible after collection. Dry matter content of air-dried soil,
manure and crop samples was also determined at 105 8C.
Irrigation water was sampled two to three times a month
at the time of irrigation and subsequently stored in pre-
washed (acid and distilled water) polyethylene bottles.
Rainwater was sampled once a week during the rainy season
and on each significant precipitation event in the dry season.
After sampling a few drops of concentrated HCl were added
to all water samples prior to chemical analysis.
2.4. Chemical analysis
Soil pH was determined using a combination electrode on
a 1:5 soil to water (w:v) mixture (Le et al., 1996; Stevens
195
et al., 2003). Micronutrient concentrations of soil and
manure samples, were determined after digestion using a
reverse aqua-regia (HNO3:HCl = 3:1) procedure (Zarcinas
et al., 1996; Stevens et al., 2003), while plant samples were
digested using a nitric and perchloric acid mixture. Copper
and Zn were determined on filtered digest samples using
flame atomic absorption (Perkin Elmer 3300). Total N in
soil, manure (fresh sample) and plant samples was
determined using the Kjeldahl procedure (Mickelson and
Weaver, 1994) while concentrated HNO3 and H2SO4
digestion (Le et al., 1996) was used for total P and K.
Digests were neutralized by addition of NH4OH (10%), P
was determined colorimetrically (Eaton et al., 1995) and K
by flame emission spectrometry.
Irrigation water samples were analyzed for P, K, Cu and
Zn, and rainwater samples for P and K after digestion with
boiling concentrated HNO3 (Eaton et al., 1995). Total N was
quantified as the sum of four N forms: nitrate-N (NO3-N),
nitrite-N (NO2-N), ammonium-N (NH3-N) and organic-N
(Norg). NO2-N and NO3-N were determined color-
imetrically, NH3-N was determined by a titration method
after distillation, and Norg was determined by macro-
Kjeldahl methods (Eaton et al., 1995).
For quality control of soil, vegetable, manure and water
some samples in each batch were analyzed in duplicate and
blanks were included. Some samples including reference
material were also reanalyzed at the Swedish University of
Agricultural Sciences, Uppsala.
2.5. Balance calculation
Basically, an element balance equation for any system
can be stated as:
DPE ¼ I E  OE (2)
where DPE, IE and OE stand for the change in the pool, the
input and the output of element E.
Applying Eq. (2) for field balance of a nutrient element in
an agricultural system, the input flows were derived from
seedlings (SE), irrigation water (IWE), rainwater (RWE),
fertilisers (F E), atmospheric deposition (ADE), pesticide
(CE), nitrogen fixation (NE) and other input flows (#IE), the
output flows from harvested crops (HE), leaching (LE), run-
off (RE), air emission (AEE) and other output flows (#OE),
and DPE is the net change in soil storage of element E
(DSoilE). Thus, Eq. (2) can be modified to:
DSoilE ¼ SE þ IWE þ RWE þ F E þ ADE þ C E þ N E þ # IE
 ðH E þ LE þ RE þ AEE þ # OE Þ (3)
In intensive vegetable cultivation, where both inputs from
fertiliser and outputs from harvest are large, the omission of
variables such as CE, #IE, and #OE in Eq. (3) is unlikely to
introduce much error. According to Roy et al. (2003),
nitrogen fixation varies between 2 and 5 kg N ha1 year1
for non-symbiotic crops which is small in comparison to the
196 N.M. Khai et al. / Agriculture, Ecosystems and Environment 122 (2007) 192–202

input from fertiliser. Excluding these factors, Eq. (3) calculations included all crops in the rotation from planting
becomes: to harvesting during an approximately 1-year period, all data
were subsequently recalculated to provide 12-month
DSoilE ¼ SE þ IWE þ RWE þ F E þ ADE estimates. Crop residues were returned to the plots and
 ðH E þ LE þ RE þ AEE Þ (4) were not considered.

Since the loss terms were not quantified they are moved to
the left-hand side of the equation,
DSoilE þ LE þ RE þ AEE
¼ SE þ IWE þ RWE þ F E þ ADE  H E
The right-hand side of Eq. (5) represents the balance
(surplus or deficit). So:
BalanceE ¼ SE þ IWE þ RWE þ F E þ ADE  H E
The variable BalanceE can have any value and is likely to
differ between individual elements on the same plot. Where
the BalanceE is positive, the risk of losses (RE or LE)
increases. A negative BalanceE points to decreasing soil
storage of E and a deficiency may develop. The atmospheric
deposition (ADE) is an input that can be significant for Cu
and Zn, but unfortunately no data are available for the Hanoi
area.
Field element balances were calculated for the individual
sub-plots at the Phuc Ly site (Table 2). Element balance
2.6. Statistical analysis
Data on the quantity of irrigation water and on element
concentrations in crops, manure, irrigation water and
(5) rainwater were analyzed by one-way ANOVA using plot
as a factor (MINITAB1 Release 14, 2003). The significance
level was P < 0.05.
(6)
3. Results
3.1. Irrigation water and rainwater
The aquatic vegetables received much more irrigation
water than the terrestrial and the total volume used varied
between plots (Table 2). The two sources differed signifi-
cantly in water quality (Fig. 1). The irrigation water that
included wastewater used at Bang B contained significantly
higher concentrations of all nutrients than the ‘natural’ river
water applied in Phuc Ly. Potassium concentration was

Fig. 1. Box and whisker plots of the concentrations of N, P, K, Cu and Zn (mg L1) in irrigation water in Bang B (BB-Ir) and Phuc Ly (PL-Ir); and rainwater in
Bang B (BB-Ra) and Phuc Ly (PL-Ra). The number of samples (n) for each component was the same for all elements, n BB-Ir = 33, n PL-Ir = 25, n BB-Ra = 16
and n PL-Ra = 17. Horizontal line represents the median, the box the 25 and 75 percentiles, outlier values are plotted with (*). A different letter indicates a
significant difference between individual sources (P < 0.05).
 N.M. Khai et al. / Agriculture, Ecosystems and Environment 122 (2007) 192–202 197

Fig. 2. Box and whisker plots of the concentrations of N, P, K (g kg1 dw), and Cu and Zn (mg kg1 dw) in chicken manure for PL1 and PL2. The number of
samples (n) for each component was the same for all elements, n PL1 = 8 and n PL2 = 17. Horizontal line represents the median, the box the 25 and 75
percentiles, outlier values are plotted with (*).

significantly higher in natural river water than in rainwater. No
other statistically significant differences in element concen-
trations were detected between ‘natural’ river water and
rainwater.
3.2. Manure and chemical fertilisers
The amounts of manure and chemical fertilisers applied
are presented in Table 2. Chicken manure (often mixed with
ash and rice straw) was only applied at Phuc Ly and at PL1
contained (g kg1 dw) 5.7–11.6 N, 8.0–11.8 P, 16.2–43.7 K,
compared to 1.4–14.5 N, 1.2–12.0 P, and 8.7–36.3 K at PL2.
Chicken manure contained between (mg kg1 dw) 32 and 52
Cu and 164–197 Zn at PL1 while the corresponding ranges
at PL2 were 19 and 89 Cu, and 111–290 Zn (Fig. 2).
3.3. Harvested crops
Crop yields are shown in Table 3 and analyses of the
edible parts presented in Table 4. Concentrations of Cu and
Zn were below the Vietnamese and FAO/WHO (Cu) safety
standard at both sites. Higher concentration of Cu and Zn in
morning glory and water celery from BB1 compared with
those from BB2 probably reflect the combined effect of an
older crop (Table 3) and greater dry matter content (Table 4).
3.4. Element flows and field balances
The large application of irrigation water at BB2 resulted
in it being the main input source of N, K, Cu and Zn here
while for P chemical fertilisers represented the main source

Table 3
Duration (days) and crop yield of the vegetable species included in the multiple cropping systems in the study plots in Bang B and Phuc Ly villages (12 months)
Village Vegetable BB1 BB2
No Days Y No Days Y
a b
Bang B Morning glory 6 38  14 33  15 2 19  3 27  8
Water celery 2 75  28 a 45  14 3 58  12 a 36  7
Water cress 3 41  8 a 30  9
Water mimosa 9 12  3 b 76

Village Vegetable PL1 PL2

No Days Y No Days Y
Phuc Ly Anethum 8 43  14 27  20
Basil 24 33  6 11  2
Chinese mustard 9 21  3 31  16 3 38  6 30  17
Choisum 18 29  8 26  7
Coriander 1 36 19 6 32  7 41
Garland 4 35  1 20  1 4 37  1 13  1
Lettuce 16 45  12 39  19 6 39  3 22  3
Mustard 7 32  1 12  1
Onion 19 41  5 24  8
Perilla 2 39  1 27  0
No: number of crops of the same species grown during the study period. Days: (i) for vegetables in Phuc Ly, the duration of the crop from transplanting seedling
to harvest and (ii) for vegetable in Bang B. Y: yield per crop (t ha1 fw).
a
Duration from transplanting to harvest.
b
Duration from one harvest to the next harvest of above ground biomass from the same root. During 1 year, the farmer can take 6–9 crops and/or 6–15
harvests at the same plot.
198 N.M. Khai et al. / Agriculture, Ecosystems and Environment 122 (2007) 192–202

Table 4
Concentration (mean  standard deviation) of some selected parameters in the edible parts of fresh vegetables from the plots in Bang B and Phuc Ly villages
Vegetable n Dry mattera N P K Cu Zn
BB1
Morning glory 7 8.3  2.8 4.08  1.35 0.28  0.14 1.60  0.60 1.01  0.67 2.87  1.22
Water celery 3 7.2  2.8 2.56  1.44 0.33  0.18 1.89  0.72 1.10  0.26 3.09  1.71
BB2
Morning glory 3 5.3  2.6 2.72  1.24 0.17  0.05 1.87  0.70 0.18  0.02 2.29  1.53
Water celery 5 6.0  1.4 2.09  0.55 0.31  0.15 1.55  0.98 0.69  0.30 2.44  1.22
Water cress 5 5.6  0.8 2.34  0.82 0.15  0.05 1.78  0.55 0.31  0.11 3.56  0.86
Water mimosa 8 9.8  1.8 4.46  1.07 0.21  0.10 2.18  0.77 0.61  0.56 5.41  2.32
PL1
Chinese mustard 10 4.7  0.6 2.08  0.43 0.25  0.08 1.61  0.15 0.38  0.13 2.12  0.16
Choisum 6 5.9  2.0 2.46  1.09 0.30  0.10 1.86  0.37 0.42  0.15 2.87  0.44
Coriander 3 10.4  2.3 5.16  1.34 0.45  0.02 3.96  0.08 1.13  0.71 3.97  0.22
Garland 1 11.3 4.29 0.80 5.80 1.41 5.65
Lettuce 3 3.9  0.8 1.24  0.49 0.18  0.03 1.14  0.27 0.34  0.15 1.94  0.20
Onion 6 8.3  1.3 2.70  0.76 0.25  0.06 1.67  0.30 0.98  0.27 3.30  0.62
PL2
Anethum 4 10.3  2.9 3.73  0.83 0.29  0.07 3.52  1.09 0.82  0.31 2.78  0.75
Basil 8 12.9  4.1 3.29  1.41 0.40  0.25 3.16  1.51 1.33  0.50 7.30  3.22
Chinese mustard 6 4.2  0.5 1.35  0.62 0.31  0.06 1.79  0.53 0.35  0.14 2.12  0.58
Coriander 4 10.7  2.5 5.01  1.43 0.47  0.12 4.66  2.12 1.46  0.48 4.22  1.22
Garland 4 4.1  0.7 1.65  0.39 0.22  0.01 1.65  0.10 0.99  0.24 1.64  0.15
Lettuce 4 4.6  1.2 1.52  0.80 0.24  0.06 1.85  0.14 0.45  0.19 1.59  0.38
Mustard 3 8.9  1.2 3.04  0.44 0.26  0.19 3.59  1.21 0.65  0.33 3.60  1.23
Perrila 2 17.9  1.6 6.13  0.29 0.61  0.16 4.29  2.37 3.07  0.25 5.69  0.78

Vietnamese safety standardb 5 10

FAO/WHO safety standardsc 5 –
The values are given in g (N, P and K) kg1 fw or mg (Cu and Zn) kg1 fw. n: number of samples of a vegetable species being sampled for chemical analyses.
a
Dry matter content of fresh vegetable (%).
b
Ministry of Agriculture and Rural Development (2003).
c
FAO/WHO (1993).

(Table 5). For all remaining plots, chemical fertilisers
represented the largest input of N and P. At Phuc Ly, chicken
manure accounted for the main input of K, Cu and Zn.
The largest N surplus (kg N ha1 year1) was calculated
for BB2 at 882 compared to 427, 131 and 85 kg N ha1
year1 for BB1, PL1 and PL2, respectively (Table 5). The P
and K surplus were also positive, ranging from 109 to 196
and from 20 to 306 kg ha1 year1, respectively.
The Phuc Ly site showed an annual surplus (g ha1) for
Cu of between 258 and 314, and 1363–1683 for Zn (Table 5).
The surplus values for BB1 were 176 g Cu ha1 year1 and
646 g Zn ha1 year1 compared to 2683 and 7700 g ha1
year1 for Cu and Zn, respectively at BB2.
4. Discussion
was smaller but still accounted for up to 30% of the total.
The wastewater used at Bang B had lower P concentration
(0.1–4.6 mg l1) than those reported by van der Hoek et al.
(2002). Wastewater also represented the largest source of Zn
and Cu (Table 6). In Bang B wastewater accounted for 83–
94% of the measured input of Zn and 92–98% of Cu, and
contributed 1.3–6 (Zn) and 1.5–12 (Cu) times the amount
taken off in harvested products.
These results support previous studies showing that use of
municipal wastewater can help farmers in peri-urban areas
to reduce the requirement and therefore cost involved with
purchasing fertiliser (Pescod, 1992; Vu, 2001; van der Hoek
et al., 2002; Horswell et al., 2003). However, large excess of
Zn and Cu, and other potential toxic elements and
pathogenic organisms (Trang et al., 2006), can represent
environmental and health concerns.

4.1. Element inputs through irrigation water 4.2. Element inputs through fertiliser

Wastewater represented a significant source of nutrients,
accounting for 21–61 and 31–66% of the total measured
input for N and K, respectively. The variation was due to
difference in altitude between study plots where the plot at a
lower position (BB2) received more wastewater. The
proportion of measured P derived from irrigation water
The intensive peri-urban vegetable systems at Bang B used
fertiliser as a complementary nutrient source to those supplied
by wastewater, while at Phuc Ly it represented the main
nutrient input. The amounts of N, P and K applied were one to
four, three to eight and two to three times, respectively, larger
in these vegetable systems compared to rice based systems in
 N.M. Khai et al. / Agriculture, Ecosystems and Environment 122 (2007) 192–202 199

Table 5
Element balances in vegetable plots in Bang B and Phuc Ly villages during a 12-month period showing input and output flows, balance (input  output) and
nutrient use efficiency ((output/input)  100)
N (kg ha1) P (kg ha1) K (kg ha1) Cu (g ha1) Zn (g ha1)
BB1
Input (total) 1071 261 399 440 1723
Seedling 21 2 27 11 41
Irrigation water 226 13 124 406 1423
Rainwater 14 2 11 n.d. n.d.
Ash 2 16 90 23 259
Chemical fertilisers 808 228 147 n.d. n.d.
Output (harvest) 644 65 334 264 1077
Balance 427 196 65 176 646
Efficiency (%) 60 25 84 60 63

BB2
Input (total) 1643 200 903 2932 9107
Seedling 45 6 38 14 68
Irrigation water 995 59 594 2878 8574
Rainwater 14 2 11 n.d. n.d.
Ash 3 22 127 32 361
Horn 94 <1 <1 8 104
Chemical fertilisers 492 111 133 n.d. n.d.
Output (harvest) 761 91 597 249 1407
Balance 882 109 306 2683 7700
Efficiency (%) 46 46 66 8 15

PL1
Input (total) 617  109 251  16 512  33 454  51 2331  222
Irrigation water 15  2 61 65  8 96  11 689  79
Rainwater 17  0 10 10  0 n.d. n.d.
Manure 76  7 101  14 359  29 358  51 1642  223
Chemical fertilisers 509  109 143  16 78  7 n.d. n.d.
Output (harvest) 486  214 58  26 385  167 140  49 648  199
Balance 131  314 193  26 127  163 314  82 1683  312
Efficiency (%) 86  49 23  10 75  32 31  12 28  9

PL2
Input (total) 361  148 197  34 325  124 366  216 1783  870
Irrigation water 72 40 48  5 75  6 581  69
Rainwater 17  0 10 10  0 n.d. n.d.
Manure 91  73 76  63 150  131 276  208 1111  818
Ash 11 11 30  28 15  14 91  87
Chemical fertilisers 245  97 115  62 87  59 n.d. n.d.
Output (harvest) 276  64 37  7 305  65 108  27 420  89
Balance 85  90 160  29 20  67 258  226 1363  950
Efficiency (%) 83  20 19  3 94  22 43  27 32  20
For the Phuc Ly plots mean and standard deviation () for sub-plots is given (PL1 = 10; PL2 = 7). n.d.: not determined.

northern Vietnam (Nguyen, 2003). Chemical fertilisers
accounted for between 30 and 82, 56 and 87, and 15 and
37% of the total input of N, P and K, respectively. Manure
represented the largest contributor of K, Cu and Zn at Phuc Ly
and has been noted as a source of Cu and Zn for other farming
systems (e.g. Alloway, 1997; Bengtsson et al., 2003).
The variable composition of chicken manure at Phuc Ly
(Fig. 2) was partly due to it being mixed with other biosolids
such as rice bran and straw before application. Mixing
manure with ash produced a drier material which helped
facilitate application although this was associated with
increased risk of ammonia volatilization probably giving
rise to lower N concentration in some samples.
4.3. Nutrient use efficiency
The value of recording operational information was
demonstrated by the variation that existed in application
timings between sub-plots, crops and seasons (Table 5). It is
possible that a lack of optimizing the timing of fertiliser
application with crop demand might be responsible for some
of the poor nutrient use efficiencies found.
200 N.M. Khai et al. / Agriculture, Ecosystems and Environment 122 (2007) 192–202

Table 6
Soil pH, total P, K (g kg1) and reverse aqua regia extractable Cu and Zn (mg kg1) concentrations, soil pools (0–20 cm) (P, K, kg ha1; Cu, Zn, g ha1), balance
(input  output, P, K, kg ha1 year1; Cu, Zn, g ha1 year1), estimated annual change in the soil pool (%), annual change in soil concentration (P, K, g kg1;
Cu, Zn, mg kg1), and years to reach the maximum allowable concentrations (MAC)
Systems n pHH2 O Element
P K Cu Zn
Soil concentration Bang B 8 6.7 1.07 7.97 25.20 74.00
Phuc Ly 18 7.6 1.01 8.41 30.70 76.80
Soil poola Bang B 2456 18,362 58,086 170,570
Phuc Ly 2552 21,288 77,671 194,304
Balance (surplus)
BB1 Bang B 196 65 176 646
BB2 Bang B 109 306 2,683 7,700
PL1 Phuc Ly 193 127 314 1,683
PL2 Phuc Ly 160 20 258 1,363
% Change in soil poolb
BB1 Bang B 8.0 0.4 0.3 0.4
BB2 Bang B 4.4 1.7 4.6 4.5
PL1 Phuc Ly 7.6 0.6 0.4 0.9
PL2 Phuc Ly 6.3 0.1 0.3 0.7
Annual change in concentration
BB1 Bang B 0.09 0.03 0.08 0.28
BB2 Bang B 0.05 0.13 1.16 3.34
PL1 Phuc Ly 0.08 0.05 0.12 0.67
PL2 Phuc Ly 0.06 0.01 0.10 0.54
Years to reach MAC c
BB1 Bang B 325 450
BB2 Bang B 21 38
PL1 Phuc Ly 156 185
PL2 Phuc Ly 189 229
Permitted metal load (g ha1 year1)d
Germany 1,300 2,500
Sweden (by sewage sludge) 300 600
EU, directive 86/278EEC 12,000 30,000
EU proposed long-term limits 1,800 4,500
a
Soil bulk density was 1.15 and 1.27 g dm3 for Bang B and Phuc Ly, respectively.
b
Annual change in the soil pool calculated as surplus/soil pool (0–20 cm)  100.
c
The maximum allowable concentrations (MAC) for Vietnamese agricultural soils are 50 mg Cu kg1 soil and 200 mg Zn kg1 soil (MOST, 2002).
d
According to Landner and Reuther (2004).

Nutrient use efficiency was generally lower for P
compared to N and K (Table 5). The differences between
sites were apparent with the efficiency of N and K use being
lower at Bang B. Huang et al. (2006) estimated that for
intensive vegetable peri-urban systems of the Yangtze River
delta in China the N and P use efficiency was generally low
(21–55 and 15–20% for N and P, respectively). Although in
our study the efficiency of nutrient use was higher for N (46–
86%) and K (66–94%), it remained poor for P (19–46%).
4.4. Implication for the environment and health
Nutrient balances demonstrate the extent to which any
surplus might exist while also indicating a wider potential
for nutrient loss and environmental impact (Öborn et al.,
2003). Field scale balances provide information on nutrient
use efficiency and long-term sustainability for individual
cropping systems. The large N and P surplus in peri-urban
vegetable systems indicate a certain risk for nutrient loss
with the potential for contributing to eutrophication (Huang
et al., 2006).
The continued accumulation of micronutrients by soil–
plant systems can result in situations which represent direct
health and environment risks (Giller et al., 1999). The
limited mobility of many micronutrients increases the rate of
accumulation within biologically active topsoil layers
(Chang et al., 1984; McGrath, 1987; Dowdy et al., 1991).
The maximum allowable concentration (MAC) for Vietna-
mese agricultural soil is 50 mg Cu and 200 mg Zn kg1 soil
(MOST, 2002). None of the sites currently exceed these
concentrations. An estimate of time required for surface soil
(0–20 cm) to reach the MAC, assuming a similar surplus as
at present (without taking leaching losses in to accout),
ranged from 21 to 325 years for Cu and 38 to 450 years for
Zn (Table 6). If atmospheric deposition was included and
was similar to data reported by Wong et al. (2003) for
 N.M. Khai et al. / Agriculture, Ecosystems and Environment 122 (2007) 192–202
Guangzhou, China (60–225 g Cu ha1 year1 and 387–
847 g Zn ha1 year1), these calculated times to reach
MAC would decrease.
5. Conclusions
Peri-urban vegetable production systems are intensive,
continuously cropped using high application rates of
nutrients and water. The investigated cropping systems
showed large macro (N, P and K) and micro (Zn and Cu)
nutrient surpluses. Nutrient inputs were derived from a range
of sources, each having a variable composition and relative
contribution. In aquatic vegetable systems wastewater
represented an important input source of N, K, Cu and
Zn. Where used, manure (mainly chicken) was an important
source of K, P, Cu, Zn and to some extent also N.
Despite the relatively high nutrient use efficiency (e.g., for
N 46–86%, P 19–46% and K 66–94% of that applied)
associated with these intensive cropping systems, the large
quantities of nutrients actually applied meant that any surplus
still represented a major input to the soil–plant system. The
accumulation of Cu and Zn was considerable in all vegetable
systems with 8–60% of measured input for Cu and 15–63%
for Zn being removed in harvested products. This was
primarily attributed to use of wastewater or biosolid (chicken
manure), in aquatic and terrestrial systems respectively. The
origin of Cu and Zn in wastewater is likely to be industrial
activities in or downstream of Hanoi City while for manure
they may come from a combination of animal feed additives
and ash (from rice straw) added to the manure before
spreading. There is some concern regarding the fast soil
accumulation rate of Cu and Zn. The accumulated impact of
surplus could be considerable in the context of long-term
productivity, environment and human health.
Options to improve nutrient management could include
the development of strategies that better adjust nutrient use
efficiency and reduce the reliance on purchased fertilisers.
Phosphorus in particular had a large surplus which could
usefully be reduced. A sustainable reuse of wastewater for
irrigation in peri-urban farming systems can contribute
significantly to the nutrient supply (assuming low concen-
trations of potential toxic or hazardous substances in the
water). Nutrient inputs need to be better related to the crop
need, e.g. through better knowledge about the nutrient
concentrations in the wastewater and improved management
of the amount of irrigation water being applied.
Acknowledgements
This study is a part of the EU funded ‘‘RURBIFARM
project – sustainable farming at the rural–urban interface –
an integrated knowledge based approach for nutrient and
water recycling in small-scale farming systems in peri-urban
areas of China and Vietnam’’ (contract number: ICA4-CT-
201
CT-2002-10021). We kindly thank the Ministry of Education
and Training (MOET) in Vietnam for supporting the PhD
study of Mr Nguyen Manh Khai. We also wish to thank staff
at NISF and VESDI for all help and collaboration with the
field and laboratory work. Many thanks to farmer families in
Phuc Ly, Mrs. Sau and Mr. Dan, and in Bang B, Mr. Lan for
their good collaborations. We also wish to thank Anthony
Edwards and Jon Petter Gustafsson for valuable comments
on this manuscript.
References
Alloway, B.J., 1997. Soil process and the behaviour of metals. In: Alloway,
B.J. (Ed.), Heavy Metals in Soils. Chapman & Hall, London, pp. 11–57.
AVRDC, 2002. AVRDC Report 2001. Asian Vegetable Research and
Development Center. Shanhua, Tainan, Taiwan, pp. 1–159.
Bengtsson, H., Öborn, I., Jonsson, S., Nilsson, I., Andersson, A., 2003. Field
balances of some mineral nutrients and trace elements in organic and
conventional dairy farming—a case study at Öjebyn, Sweden. Eur. J.
Agron. 20, 101–116.
Chang, A., Warneke, J., Page, A., Lund, L., 1984. Accumulation of heavy
metals in sewage-sludge treated soils. J. Environ. Qual. 13, 87–91.
Dowdy, R.H., Latterell, J.J., Hinesly, T.D., Grossman, R.B., Sullivan, D.L.,
1991. Trace-metal movement in an Aeric ochraqualf following 14 years
of annual sludge applications. J. Environ. Qual. 20, 119–123.
Duong, T.T., Coste, M., Feurtet-Mazel, A., Dang, D.K., Gold, C., Park, Y.S.,
Boudou, A., 2006. Impact of urban pollution from the Hanoi area on
benthic diatom communities collected from the Red, Nhue and Tolich
rivers (Vietnam). Hydrobiologia 563, 201–216.
Eaton, A.D., Clesceri, L.S., Greenberg, A.E. (Eds.), 1995. Standard
Methods for Examination of Water and Wastewater. 19th ed. American
Public Health Association, Washington.
El-Mowelhi, N.M., Soliman, S.M.S.A., Barbary, S.M., El-Shahawy, M.I.,
2006. Agronomic aspects and environmental impact of reusing marginal
water in irrigation: a case study from Egypt. Water. Sci. Technol. 53,
229–237.
FAO/WHO, 1993. FAO/WHO Standards of FAO/WHO Codex Alimentarius
2003.
Giller, K.E., Witter, E., McGrath, S.P., 1999. Assessing risks of heavy metal
toxicity in agricultural soils: do microbes matter? Hum. Ecol. Risk
Assess. 5, 683–689.
Goodlass, G., Halberg, N., Verschuur, G., 2003. Input output accounting
systems in the European community—an appraisal of their usefulness
in raising awareness of environmental problems. Eur. J. Agron. 20,
17–24.
Hanoi Statistical Office, 2003. Hanoi Statistical Yearbook. City Statistical
Office, Hanoi.
Hedlund, A., Witter, E., An, B.X., 2003. Assessment of N, P and K
management by nutrient balances and flows on peri-urban smallholder
farms in southern Vietnam. Eur. J. Agron. 20, 71–87.
Hoang Fagerström, M.H., Yem, T., Ha, P.Q., Tuan, V.D., Valhed, C.,
Kvamme, K., Nyberg, Y., 2006. Characterization and diagnosis of
rural-urban interface farming in the Tu Liem and Thanh Tri districts
of Hanoi city, Vietnam. Int. J. Agr. Sustain. 3, 177–188.
Horswell, J., Speir, T.W., van Schaik, A.P., 2003. Bio-indicators to assess
impacts of heavy metals in land-applied sewage sludge. Soil Biol.
Biochem. 35, 1501–1505.
Huang, B., Shi, X., Yu, D., Öborn, I., Blombäck, K., Pagella, T.F., Wang, H.,
Sun, W., Sinclair, F.L., 2006. Environmental assessment of small-scale
vegetable farming systems in peri-urban areas of the Yangtze River
Delta Region, China. Agric. Ecosyst. Environ. 112, 391–402.
Jansen, H.G.P., Midmore, D.J., Binh, P.T., Valasayya, S., Tru, L.C., 1996.
Profitability and sustainability of peri-urban vegetable production sys-
tems in Vietnam. Netherlands J. Agric. Sci. 44, 125–143.
202 N.M. Khai et al. / Agriculture, Ecosystems and Environment 122 (2007) 192–202
Landner, L., Reuther, R., 2004. Heavy Metals in Society and in the
Environment: A Critical Review of Current Knowledge on Fluxes,
Speciation, Bioavailability and Risk for Adverse: Effects of Copper,
Chromium, Nickel and Zinc. Kluwer Academic Press, Dordrecht.
Le, V.K., Nguyen, X.C., Le, D., Tran, K.H., Cai, V.T., 1996. Methods for
Soil, Water, Fertiliser and Plant Analysis. Education Publish House,
Hanoi (in Vietnamese).
McGrath, S.P., 1987. Long-term studies of metal transfers following applica-
tions of sewage sludge. In: Coughtrey, P.J., Martin, M.H., Unsworth,
M.H. (Eds.), Pollutant Transport and Fate in Ecosystems. Blackwell
Scientific, Oxford, pp. 301–317.
Mickelson, S.H., Weaver, R.W., Methods of Soil Analysis. Part 2.
Microbiological and Biochemical Properties. Madison, Wisconsin,
1994.
Midmore, M.J., Jansen, H.G.P., 2003. Supplying vegetables to Asian cities:
is there a case for peri-urban production? Food Pol. 28, 13–27.
Ministry of Agriculture and Rural Development (MARD), 2003. 10TCN—
Maximum Permission Content of Some Heavy Metal and Toxic Che-
micals (Appendix 3). MARD, Hanoi.
MOST, 2002. TCVN 7209: 2002, Soil quality—Maximum Allowable
Limits of Heavy Metals in the Soil. Ministry of Science and Technology,
Hanoi.
Nguyen, V.L., 2003. Rice Plant of Vietnam in 21st Century. Vietnam
Agricultural Publishing House, Hanoi (in Vietnamese).
Öborn, I., Edwards, A.C., Witter, E., Oenema, O., Ivarsson, K., Withers,
P.J.A., Nilsson, S., Stinzing, A., 2003. Element balances as a tool for
sustainable nutrient management: a critical appraisal of their merits and
limitations within an agronomic and environmental context. Eur. J.
Agron. 20, 211–225.
Oron, G., Bick, A., Gillerman, L., Manor, Y., 2004. Hybrid membrane
systems for secondary effluent polishing for unrestricted reuse for
agricultural irrigation. Water. Sci. Technol. 50, 305–312.
Pescod, M.B., 1992. Wastewater Treatment and Use in Agriculture. Food
and Agriculture Organization, Rome.
Pham, Q.H., Nguyen, M.K., Vu, D.T., Fagerstrom, M.H., Öborn, I., 2005.
Nutrient and heavy metal study for sustainable farming in peri-urban
intensive vegetable cropping, Hanoi, Vietnam. Bulletin of the Institute
of Tropical Agriculture Kyushu University, Japan 28 (Special issue), pp.
111–119.
Richter, J., Roelcke, M., 2000. The N-cycle as determined by intensive
agriculture—examples from central Europe and China. Nutr. Cycl.
Agroecosys. 57, 33–46.
Roy, R.N., Misra, R.V., Lesschen, J.P., Smaling, E.M.A., 2003. Assessment
of soil nutrient balance approaches and methodologies. Rome, Food and
Agriculture Organization of the United Nations. FAO Fertilizer and
Plant Nutrition Bulletin, 14.
Singh, S., Kumar, M., 2006. Heavy metal load of soil, water and vegetables
in peri-urban Delhi. Environ. Monit. Assess. 120, 79–91.
Smaling, E.M.A., Oenema, O., Fresco, L.O. (Eds.), 1999. Nutrient Dis-
equilibria in Global Agro-Ecosystems. Concepts and Case Studies. CAB
International, Cambridge.
Stevens, D., Smart, M., Cozens, G., Zarcinas, B., Barry, G., Cockley, T.,
McLaughlin, M., 2003. CSIRO Land and Water’s Methods Manual.
ACIAR and CSIRO Land and Water.
Tra, H.T.L., Egashira, K., 1999. Heavy metal status of agricultural soils in
Tuliem and Thanhtri districts of Hanoi city, Vietnam. J. Fac. Agric.
Kyushu Univ. 43, 489–497.
Trang, D.T., Cam, P.D., van der Hoek, W., Vinh, K.T., Hoa, N.V., Dalsgaard,
A., 2006. Low risk for helminth infection in wastewater-fed rice
cultivation in Vietnam. J. Water Health 4, 321–331.
van den Berg, L.M., van Wijk, M.S., van Hoi, P., 2003. The transformation
of agriculture and rural life downstream of Hanoi. Environ. Urban. 15,
35–52.
van der Hoek, W., Hassan, M.U., Ensink, J.H.J., Feenstra, S., Raschid-Sally,
L., Munir, S., Aslam, R., Ali, N., Hussain, R., Matsuno, Y., 2002. Urban
wastewater: a valuable resource for agriculture. A case study from
Haroonabad, Pakistan. IWMI Research Report no. 63. International
Water Management Institute, Colombo.
Vu, T.T.H., 2001. Treatment of domestic wastewater and its reuse in farm
irrigation in the Red River delta. Wastewater reuse in agriculture in
Vietnam: Water management, environment and human health aspects.
In: Proceedings of a Workshop Held in Hanoi, Vietnam, International
Water Management Institute, Colombo, March 14, 2001.
Wolf, J., van Wijk, M.S., Cheng, X., Hu, Y., van Diepen, C.A., Jongbloed,
A.W., van Keulen, H., Lu, C.H., Roetter, R., 2003. Urban and peri-urban
agricultural production in Beijing municipality and its impact on water
quality. Environ. Urban. 15, 141–156.
Wong, C.S.C., Li, X.D., Zhang, G., Qi, S.H., Peng, X.Z., 2003. Atmospheric
deposition of heavy metals in the Pearl River delta, China. Atmos.
Environ. 37, 767–776.
Zarcinas, B.A., McLaughlin, M.J., Smart, M.K., 1996. The effect of acid
digestion technique on the performance of nebulization systems used in
inductively coupled plasma spectrometry. Commun. Soil. Sci. Plant
Anal. 27, 1331–1354.
Zhang, Q., Shi, X., Huang, B., Yu, D., Öborn, I., Blomback, K., Wang, H.,
Pagella, T.F., Sinclair, F.L., 2007. Surface water quality of factory-based
and vegetable-based peri-urban areas in the Yangtze River Delta region,
China. Catena 69, 57–64.