3.1 Borderline concentrations of trace elements
The maximum limits tolerated for ET in different matrices are shown in TABLE 2. These limits were used as a guide to establish the presence of ET in concentrations above those allowed in the samples collected in urban gardens.
Table 2. Maximum tolerated limit for analyzed trace elements for soil, water and leafy vegetables in different countries.
Organization or country
|
Variable
|
Maximum tolerated limit for the analyzed trace elements (mg.Kg-1 or mg.L-1)
|
Source
|
As
|
Cd
|
Cr (V)
|
Cu
|
Fe
|
Mn
|
Ni
|
Pb
|
Zn
|
Brazil
|
Potable water
|
0.01
|
0.005
|
0.05*
|
2
|
2.4
|
0.1
|
0.07
|
0.01
|
ni
|
(Brasil 2009)
(Brasil 2011)
(Brasil 2013)
(Brasil 2021)
|
Soil
|
15
|
1.3
|
75*
|
60
|
ni
|
ni
|
30
|
72
|
300
|
Leafy vegetable
|
0.3
|
0.2
|
ni
|
ni
|
ni
|
ni
|
ni
|
0.3
|
ni
|
USA
|
Potable water
|
0.01***
|
0.005
|
0.1*
|
1.3**
|
ni
|
0.05
|
0.02
|
0.015***
|
5****
|
(USEPA 2021)
(USEPA 2005a)
(Kinuthia et al. 2020)
|
Soil residential
|
ni
|
0.48
|
11
|
ni
|
ni
|
ni
|
72
|
200
|
ni
|
Vegetable
|
ni
|
0.2
|
2.3*
|
ni
|
ni
|
ni
|
ni
|
0.3
|
ni
|
FAO / WHO
|
Natural water
|
0.1
|
0.003
|
ni
|
ni
|
ni
|
ni
|
ni
|
0.01
|
ni
|
(FAO/WHO 2019)
(FAO/WHO 2021)
|
Leafy vegetable
|
ni
|
0.2
|
ni
|
ni
|
ni
|
ni
|
ni
|
0.3
|
ni
|
China
|
Soil
|
ni
|
0.3-0.6
|
150-300
|
ni
|
ni
|
ni
|
40-60
|
80
|
ni
|
(Kinuthia et al. 2020)
(Antoniadis et al. 2019)
|
Leafy vegetable
|
0.5
|
0.2
|
0.5
|
ni
|
ni
|
ni
|
ni
|
0.3
|
ni
|
* Total Cr. ** Cu dissolved. *** The maximum target for contaminant level considering public health for As and Pb is zero, because neither level is considered safe, however USEPA has set this reference value for monitoring drinking water. **** USEPA recommends secondary standards for potable water systems. Not informed (n.i).
3.1 Trace elements in irrigation water
No detectable levels of As, Cd, Cr, Pb, or Ni were encountered in the irrigation water samples taken from the five community gardens analyzed (Table 3). It is important to note that the concentrations of the other trace elements detected in the irrigation water samples were within environmentally permitted limits (Table 2).
Table 3. Mean concentrations of trace elements detected in irrigation water samples collected in urban gardens in Curitiba City, PR, Brazil, and in the Centro Paranaense de Referência em Agroecologia garden in Pinhas City, PR, Brazil.
Trace elements (mg.mL-1)
|
Gardens
|
Cu
|
Fe
|
Mn
|
Zn
|
Esquina Verde
|
0.013ns
|
0.393ns
|
nd
|
0.494ns
|
Marumbi 1
|
0.013ns
|
0.143ns
|
nd
|
0.955ns
|
Marumbi 2
|
0.019ns
|
0.215ns
|
nd
|
0.763ns
|
Pantanal
|
0.020ns
|
0.224ns
|
0.010
|
1.454ns
|
CPRA
|
0.020ns
|
0.147ns
|
nd
|
0.646ns
|
The means were compared using the Tukey Test (p < 0.05). ns = not significant;
nd = not detected.
The irrigation water used in the HEV, HM1, HM2, and HP gardens is fit for human consumption and is supplied by the Paraná Water Company (SANEPAR); the water used for irrigating the HCPRA garden is taken from the Canguiri River in Pinhas, PR, Brazil. Even though they are derived from distinct sources, our results indicate that the irrigation water used in the community gardens studied here do not constitute sources of contamination of the trace elements As, Cd, Cr, Cu, Fe, Mn, Ni, Pb, or Zn.
3.2 Trace elements in the soil (cultivation substrate)
The analyses of the soil samples did not detect any Cd in any of the urban gardens. In general, independent of the specific garden analyzed, the following order of trace element concentrations were identified in the soils: Ni < As < Pb < Cu < Cr < Zn < Mn < Fe (Table 4). The concentrations of all of the trace elements analyzed (As, Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn) were within the maximum legal environmentally tolerable limits (Table 2).
Table 4. Mean concentrations of the trace elements detected in soil samples collected from urban gardens in Curitiba City, PR, Brazil.
Trace elements (mg.Kg-1)
|
Gardens
|
As**
|
Cr*
|
Cu*
|
Fe
|
Mn
|
Ni*
|
Pb**
|
Zn*
|
Esq. Verde
|
8.35±0.11c
|
28.52±0.88a
|
18.03±0.39c
|
14020.65±163.69cd
|
100.69±1.14bc
|
6.83±0.07a
|
12.34±0.15c
|
61.92±0.59b
|
Marumbi 1
|
9.41±0.31b
|
25.61±1.85ab
|
20.73±0.72b
|
17840.94±899.30ab
|
140.22±33.54ab
|
5.00±0.20c
|
15.49±2.14bc
|
48.52±3.54bc
|
Marumbi 2
|
3.97±0.30e
|
17.14±0.43b
|
16.78±0.59c
|
15854.62±988.82bc
|
95.62±23.81c
|
3.87±0.18d
|
14.42±0.62bc
|
39.93±6.61c
|
Pantanal
|
10.65±0.31a
|
29.44±1.54a
|
24.26±1.31a
|
18845.94±444.60a
|
344.44±116.91a
|
8.66±0.62a
|
15.29±0.68ab
|
97.28±7.86a
|
CPRA
|
5.78±0.00d
|
29.09±0.00a
|
23.62±0.00a
|
8373.71±0.00d
|
79.97±0.00c
|
6.36±0.00b
|
23.80±0.00a
|
80.90±0.00a
|
Mean concentrations of trace elements ± standard deviation (SD). * Detection limits using ICP-OES (0.01). ** Detection limits using ICP-OES (0.02). Means followed by the same lowercase letter in any column not significantly differ by the Tukey test (p < 0.05).
The variations of the permitted concentrations of the trace elements will depend on the characteristics of the different soil types. The permitted limits for As are: 75 mg.kg-1 according to USEPA (2005), 30 mg.kg-1 according to SEPA China (1995), and 20 mg.kg-1 according to FAO/WHO (2021), while the permitted limits for Cr, Cu, Fe, Mn, and Zn are similar among almost all of the regulatory bodies of different countries and organizations.
The results of the analyses of the water used for irrigating the urban gardens studied here, as well as their soils, demonstrated that neither constitute sources of trace element contamination in the cultivated plants. The concentrations of trace elements in the HP soil, however, were more elevated (Table 4). That result apparently reflects the location of that garden in a low elevation urban area very near a railyard used for the maintenance, movement, and fueling of locomotives. Galera and Staszewski (Galera and Staszewski 2012) cited train traffic as a source of environmental pollution, especially of heavy metals.
Staszewski et al. (Staszewski et al. 2015) reported trace metal contamination in soils and plants cultivated near train yards in northern Varsóvia, Poland, and toxic levels of As, Mn, and Ni were found in plants growing there (Daucus carota, Pastinaca sativa, Taraxacum officinale, and Sonchus oleraceus). Those authors noted that rail transport is an important source of metal contamination in soils, making it advisable to evaluate the environments surrounding urban gardens to identify potential contamination and pollution problems and to suggest subsidies for their management and control.
3.3 Trace elements in plant biomasses
The trace elements Cd, Ni, and Pb were not detected in any of the L. sativa plants collected in the urban community gardens studied; the concentrations of the trace elements Cr, Cu, Fe, Mn, and Zn are presented in Figures 1A, 1B, 1C, 1D, 1E and 1F respectively. The concentrations of trace elements detected in the studied plants are in accordance with the maximum tolerated limits (Table 2).
Arsenic was only identified in plants grown in the HCPRA garden (Figure 1A), but its concentration was within the limits established by both Brazilian (0.30 mg.kg-1) and Chinese (0.50 mg.kg-1) norms (Table 2). The mean concentration of As in L. sativa plants from the HCPRA garden (0.13 mg.kg-1) was well below the concentration observed in leafy vegetables harvested from conventional agricultural plots (which can reach up to 4.50 mg.kg-1) (Bati et al. 2017). That observation is related to the pillars of ecological agriculture – no use of industrialized fertilizers and pesticides (which constitute typical sources of As contamination) (Bati et al. 2017).
It is important to note that when As is encountered in leafy vegetables (such as L. sativa), close monitoring of the garden should be undertaken, as species of the Asteraceae family are known accumulators of that metalloid (Ramirez-Andreotta et al. 2013). The tolerable daily consumption of As by humans is only 0.003 mg.kg-1 (WHO 2019). Therefore a 70 kg person should only digest (at most) 0.21 mg of As, which corresponds to ingesting approximately 1.61 kg of lettuce produced in the HCPRA per day, which is much higher than the average consumption of L. sativa in Brazil (0.69 Kg.year-1) (HFBrasil 2021). Additionally, L. sativa is not the only possible source of As that can enter the human diet, which reinforces the necessity of monitoring production from urban gardens.
The soils of urban gardens must also be considered. Although the As concentration in the HCPRA soil was less than was observed in the other gardens evaluated, it is an organosol rich in organic material that, according to (Kabata-Pendias 2011; Meunier et al. 2011), increases the bio-availability of metalloids. Smith et al. (2002) noted that the bio-availability of As in a given soil is controlled by both adsorption and desorption reactions. Those reactions, and the available concentration of As, are controlled by the physical, chemical, and biological attributes of the soil.
The trace elements As, Cd, Ni, and Pb were not detected in any of the analyses performed on B. oleracea plants grown in the urban gardens studied here; the concentrations of the trace elements Cr, Cu, Fe, Mn, and Zn are presented in Figures 2A, 2B, 2C, 2D and 2F respectively.
Chrome concentrations in samples of L. sativa plants varied from 0.53 to 2.06 mg.kg-1, and from 0.16 to 1.98 mg.kg-1 in samples of B. oleracea. The greatest concentrations of Cr in L. sativa plants were observed in the HP and HM1 gardens (Fig. 1A), and were significantly higher than levels seen in the other urban gardens. The greatest concentrations of Cr in B. oleracea plants were observed in the HP, HM1, and HM2 gardens, and were significantly higher than in the other two gardens examined. The levels of Cr in both vegetables were found to be below the safe upper limits set by USEPA and FAO/WHO (2021) of 2.30 mg.kg-1. The Cr concentrations in L. sativa as encountered here were similar to those reported by De León et al. (2010) in peri-urban areas located in the southern region of Mexico City in a non-protected area and in an area protected (covered by a filtering mech to diminish atmospheric pollution) from atmospheric pollution (2.60 and 1.60 mg.kg -1 respectively). The values reported here were, however, greater than those reported by Chang et al. (2014) in L. sativa plants sold in a supermarket (0.13 mg.kg-1).
In relation to Cr levels in B. oleracea, greater concentrations were observed in Brassica oleracea var. capitataem (0.36 mg.kg-1) by Bati et al. (2017) and in Brassica rapa subsp. pekinensis (0.36 mg.kg-1) produced through conventional cultivation (Chang et al. 2014); Bati et al. (2017) did not observe any Cr in samples of B. oleracea plants grown in peri-urban gardens.
In relation to Cu, the concentrations observed in L. sativa varied from 6.69 to 8.92 mg.kg-1, while the concentrations observed in B. oleracea varied from 2.25 to 5.24 mg.kg-1. Cu levels of both of the vegetables studied here were found to be below the safe limits set by FAO/WHO (1989) (73.30 mg.kg-1). França et al. (2017) evaluated the concentrations of Cu in L. sativa plants produced in conventional gardens in peri-urban gardens in Pernambuco State, Brazil, and reported only low Cu concentrations (varying from 3.7 to 5.3 mg.kg-1). De León et al. (2010) likewise encountered low Cu concentrations in L. sativa plants cultivated in both protected and unprotected gardens in the southern region of Mexico City (3.60 and 5.90 mg.kg -1 respectively). In relation to Cu concentrations found in B. oleracea plants from the gardens studied here, there values were inferior to those obtained by Bati et al. (2017) from B. oleracea plants grown in conventional gardens (8.06 mg.kg-1), and by Radulescu et al. (2013) from B. oleracea plants cultivated in urban and peri-urban gardens (14.23 mg.kg-1).
The concentrations of Fe, Mn, and Zn identified in L. sativa plants grown in the urban garden studied here varied from 101.60 to 218.21 mg.kg-1, from 11.01 to 26.95 mg.kg-1, and from 50.32 to 99.28 mg.kg-1 respectively. Those concentrations were below the concentrations observed in L. sativa samples from a supermarket as evaluated by Nali et al. (2009), which were 560 mg.kg-1 for Fe, 45 mg.kg-1 for Mn, and 75 mg.kg-1 for Zn. In terms of the B. oleracea plants examined in this study, the concentrations of Fe, Mn, and Zn varied from 61.96 to 105.17 mg.kg-1, from 4.70 to 22.80 mg.kg-1, and from 24.20 to 59.51 mg.kg-1 respectively. The levels of Fe and Zn in both vegetables studied were found to be below the safe limits set by WHO (2001, 1995), see Table 5.
The concentrations of Fe reported here for B. oleracea (Figure 2C) were inferior to those observed by Radulescu et al. (2013) for plants raised in urban and peri-urban gardens (206.34 mg.kg-1). The concentrations of Mn and Zn (Figures 2D and 2E) reported here, however, were greater than those encountered by Harmanescu et al. (2011) in Brassica oleracea var. capitata plants cultivated in an agroecology garden (3.85 mg.kg-1 of Mn and 59,51 mg.kg-1 of Zn), in an industrial and mining area (10.47 mg.kg-1 of Mn and 8.51 mg.kg-1 of Zn), and in an urban and peri-urban region (9.15 mg.kg-1 of Mn and 3.28 mg.kg-1 of Zn).
Our results are within the values and/or limits of the average concentrations of the potentially toxic elements Cr, Cu, Fe, Mn, and Zn reported in the literature (Table 5).
Table 5. Reported values of potentially toxic elements in the edible portions of Lactuca sativa and Brassica oleracea plants (mg.kg-1, dry weight).
Trace elements in Lactuca sativa
|
City
|
Local
|
Cr
|
Cu
|
Fe
|
Mn
|
Zn
|
Source
|
Iwate Prefecture, Japan
|
Vegetables on the market
|
4.38
|
5.38
|
157
|
78.2
|
52.7
|
(ITOH et al. 2006)
|
Mexico City, Mexico
|
Peri-urban area – protect site
|
2.6
|
3.6
|
-
|
21.7
|
-
|
(De León et al. 2010)
|
Peri-urban area – unprotect site
|
1.6
|
5.9
|
-
|
67.3
|
-
|
Copenhagen, Denmark
|
Urban gardening
|
0.24-0.38
|
5.99-8.66
|
-
|
-
|
43.30-77.90
|
(Warming et al. 2015)
|
Recife, Brazil
|
Urban garden
|
0.69-2.27
|
10.45 -11.62
|
160.00-170.0 0
|
20.00
|
59.00-65.00
|
(Mancarella et al. 2016)
|
Marrakech, Morocco
|
Urban area
|
1.3
|
12.9
|
-
|
35.2
|
46.7
|
(Laaouidi et al. 2020)
|
São Paulo Region Metropolitan, Brazil
|
Urban garden
|
7.0
|
4.0-6.0
|
169.0
|
18.0
|
38.0
|
(Sussa et al. 2022)
|
Curitiba, Brazil
|
Urban garden
|
0.53-2.06
|
6.69-8.92
|
101.60-218.21
|
11.01-26.95
|
50.32-99,28
|
This research
|
Trace elements in Brassica oleracea
|
Zanzibar, Tanzania
|
Markets
|
1.80
|
3.54
|
176.00
|
35.80
|
16.2
|
(Mohammed and Khamis 2012)
|
Farms (production sites)
|
2.06
|
10.3
|
574.2
|
52.2
|
26.3
|
Copenhagen, Denmark
|
Urban gardening
|
0.20-0.24
|
3.08-5.50
|
-
|
-
|
23.30-66.40
|
(Warming et al. 2015)
|
Jhenaidah district, Bangladesh
|
Sub-urban industrial area
|
-
|
-
|
-
|
6.1
|
38.0
|
(Islam et al. 2018)
|
Curitiba, Brazil
|
Urban garden
|
0.16-1.98
|
2.25-5.24
|
61.96-105.17
|
4.70-22.80
|
24.20-59.51
|
This research
|
Limits values
|
Edible parts of vegetables
|
2.3*
|
40**
|
-
|
500*
|
100**
|
*(WHO 2001)
**(WHO 1995)
|
It is important to note that the consumption of L. sativa and B. oleracea plants cultivated in the urban gardens in Curitiba City can contribute to the daily ingestion of the trace elements Cr, Cu, Fe, Mn, and Zn (Table 6).
Table 6. The concentrations of trace elements supplied by the daily consumption of L. sativa and B. oleracea plants grown in urban gardens, based on the mean annual consumption of 0.69 kg.
Species (source)
|
Trace elements
|
Cr
|
Cu
|
Fe
|
Mn
|
Zn
|
Lactuca sativa
|
Daily consumption (mg.kg-1.d-1)
|
0.002
|
0.014
|
0.291
|
0.028
|
0.118
|
Dietary contribution (%)
|
0.71
|
10.37
|
10.77
|
0.11
|
0.10
|
Brassica oleracea
|
Ingestão diária (mg.kg-1.d-1)
|
0.002
|
0.043
|
0.005
|
0.030
|
0.081
|
Dietary contribution (%)
|
0.64
|
32.35
|
0.18
|
0.12
|
0.07
|
*The daily ingestion calculation is based on the mean concentrations of trace elements among all of the gardens evaluated.
**Values obtained according to Brasil (2018).
Chrome is an essential element for humans – being required for the metabolism of carbohydrates and lipids (Nali et al. 2009). The consumption of Cr in human diets, however, is often sub-optimal as most diets contain less than 60% of the suggested minimum daily intake of that trace element for adults (0.005 mg.kg-1) (Nali et al. 2009). Considering that the mean annual consumption of L. sativa and B. oleracea by a 70 kg person is 0.69 kg (HFBrasil 2021) and the mean concentration of Cr in plants produced in the urban gardens analyzed here, the consumption of L. sativa and B. oleracea contribute to the daily ingestion of only 0.002 mg.kg-1, equivalent to only 0.71% and 0.64%, respectively, of the daily recommended intake of that trace element (Table 6) – although it represents a contribution to the suggested daily consumption well above that provided by L. sativa plants sold in supermarkets (Chang et al. 2014).
The recommended minimum daily consumption of Cu by adults is 0.135 mg (Brasil 2018). The L. sativa and B. oleracea plants cultivated in the urban garden studied here therefore contribute to daily ingestions of 0.014 mg.kg-1 and 0.043 mg.kg-1 of Cu (approximately 10% and 32% of the recommended minimum daily requirement respectively) (Table 6).
Finally, considering the recommended minimum daily requirement of Fe (2.7 mg), Mn (24.5 mg), and Zn (115.5 mg) by a 70 kg person (BRASIL, 2018), the L. sativa plants grown in the urban gardens studied here can contribute approximately 10%, 0.11%, and 0.10% of those requirements respectively (Table 6). The B. oleracea plants from those gardens can contribute approximately 0.18%, 0.12%, and 0.07% of the recommended daily requirement of Fe, Mn, and Zn respectively (Table 6).