Ecotoxicology and Environmental Safety 101 (2014) 233–239 Contents lists available at ScienceDirect Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv Orchards for edible cities: Cadmium and lead content in nuts, berries, pome and stone fruits harvested within the inner city neighbourhoods in Berlin, Germany Laura Pauline von Hoffen, Ina Säumel n Department of Ecology, Technische Universität Berlin, Ernst Reuter Platz 1 (BH 9-1), D-10587 Berlin, Germany art ic l e i nf o a b s t r a c t Article history: Received 28 August 2013 Received in revised form 21 November 2013 Accepted 22 November 2013 Available online 25 January 2014 Today's urban gardening focuses mainly on vegetable production and rarely includes fruit trees. Health effects of consuming urban crops are questioned due to high local pollution loads. Here, we determined cadmium and lead content in the edible parts of nuts, berries, pome, and stone fruits harvested from fruit trees and shrubs within inner city neighbourhoods of Berlin, Germany. We analysed how local settings at sampling sites shaped the trace metal content. We revealed significant differences in trace metal content depending on species, fruit type, local traffic, and parameters related to barriers between the sampling site and neighbouring roads. Higher overall traffic burden and proximity to roads increased whereas buildings or vegetation as barriers reduced trace metal content in the edible biomass. We demonstrate, that the consumption of non-vegetable fruits growing in inner city sites in Berlin does not pose a risk on human health as long as the fruits are thoroughly washed and it is provided that site pollutions and impacts are considered in garden concepts and guidelines. & 2013 Elsevier Inc. All rights reserved. Keywords: Urban horticulture Agroforestry Fruit trees Trace metals Traffic burden 1. Introduction Urban gardening is booming worldwide and enhances food security, particularly in developing countries (FAO (Food and Agriculture Organisation of the United Nations), 2007). The interest of city dwellers for producing their own fresh food is also rising in developed countries (Leake et al., 2009) and food production for low-income citizens is supported by self-organisation and local authorities (Hancock, 2001). Beyond local food production, urban gardening provides a broad range of ecosystem services and is recognised as a key instrument in environmental education (Krasny and Bonney, 2005), for community building (Bendt et al., 2013; Glover et al., 2005), and for enhancing urban biodiversity (Galluzzi et al., 2010). Fruit tree species have been used for ornamental purposes as a reminiscence of rural landscapes (Lenné, 1825) and fruit trees along urban roads or in parks have been leased to get financial support for street or park maintenance in the 19th century (Schmidlin, 1852). Currently, fruit trees remain unused although abundant in public urban green spaces (see Fig. 1A for Berlin) and the urban gardeners focus mainly on vegetable production (Bendt et al., 2013; Hough et al., 2004). n Corresponding author. Fax: þ 49 30 314 29022. E-mail address: [email protected] (I. Säumel). 0147-6513/$ - see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ecoenv.2013.11.023 The effect on human health caused by the consumption of urban gardening products is discussed controversially, mainly due to the high pollution loads in urban areas (Alloway, 2004; Finster et al., 2004; Hough et al., 2004; Leake et al., 2009). Studies of vegetables demonstrated, that the uptake and accumulation of trace metals differed among crop type, species, and among plant parts (Alexander et al., 2006; Finster et al., 2004; Säumel et al., 2012). Few studies investigated the relation between trace metal content in the edible parts of vegetables and local traffic burden (Kloke et al., 1984; Säumel et al., 2012). Planting and building structures (i.e. hedges, shrubs, lead free painted houses or walls) can function as barrier between planting site and road, decreasing trace metal content in the crops (Säumel et al., 2012). Yet, there are only few studies analysing trace metal content in fruit tree products growing in urban environments (Li et al., 2006; Rossini Oliva and Valdés, 2003; Rossini Oliva et al., 2008; SamsøePetersen et al., 2002). Consequently, the aim of this study was to analyse the cadmium (Cd) and lead (Pb) content in the edible parts of different non-vegetable fruit types and fruit tree species. We determined the influence of traffic burden (i.e. traffic burden of the nearest and the nearest main arterial road, distances from the planting site to nearest and nearest main arterial road, overall traffic burden at sampling site) on trace metal content in the fruits. We evaluated whether characteristics of the planting site (i.e. sampling height, presence or absence of barriers between planting site and roads, barrier width or height, degree of enclosure of the sampling site by barriers) influence the trace 234 L. Pauline Hensel, I. Säumel / Ecotoxicology and Environmental Safety 101 (2014) 233–239 Fig. 1. (A) Number of fruit trees and shrubs in public green spaces in Berlin, Germany including pome and stone fruit trees (i.e. apple, apricot, cheery, mirabelle, pear, plum, quince, sloe), berries (i.e. blackberry, blueberry, currant, elder, juniper berry, mulberry, raspberry, sea buckthorn), and nuts (i.e. chestnut, hazel, walnut) according to Mundraub (2013) added by own survey data. Internet domains such as www.mundraub.org document fruit trees for a public use. (B) Sample sites per species in the inner city of Berlin, Germany (pome and stone fruits indicated by squares; berries indicated by circles and nuts indicated by diamonds). (C) Examples of different local conditions of the sample sites (black points: sampling sites with different distances to the nearest street or to the nearest arterial street and different traffic burden (red, orange or green line indicate high, medium or low traffic burden); open circles are sampling sites with a barrier between street and sampling site). Photos for typical sites are given (i.e., 1: sampling site along small street with low traffic burden; 2: sampling site along street with medium traffic burden; 3: sampling site along street with high traffic burden and 4 sampling site within a courtyard with a barrier between streets and sampling site; Photos taken by von Hoffen). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) metal content. Furthermore, we compared the trace metal content of the urban non-vegetable fruits with supermarket products to assess health risks by consuming these urban fruits. 2. Materials and methods We collected nuts, berries, pome and stone fruits of nine different species at 172 randomly chosen sites of the inner city of Berlin, Germany (Fig. 1B). The sampling sites represented different urban conditions (Fig. 1C) and were characterised by the following parameters: distance to nearest road (d1) and to nearest main arterial road (d2) in meters, traffic burden on the nearest road (tb1) and on the nearest main arterial road (tb2) according to the number of vehicles per day (1 r 5000; 2 ¼5001–10000; 3¼ 10001–15.000; 4 ¼15001–20000; 5¼20001– 30000; 6¼ 30001–40000; 7¼ Z 40001; Berlin Department for Urban Development, 2009), presence and absence of barriers between planting sites and nearest roads (b); height of barrier (bh) and width of barrier (bw) in meters; the degree of enclosure of the sampling site by barriers (eb), and sampling height in meters (sh). Furthermore, we classified the overall traffic burden (otb) within a radius of 250 m around the planting sites (low: low traffic burden, existing barriers or high distance between planting site and nearest street; medium: low to medium traffic burden and lacking barriers between planting sites and streets, lower distance to the nearest street; high: high traffic burden and lacking barriers, small distance between planting site and nearest street). All fruits were collected in 2012 at the usual harvest time of each fruit species. We classified fruit types as follows: ‘nuts' (dry fruits with a hard woody shell including almond nuts); ‘berries’ (fleshy fruits including aggregate fruits such as blackberries or strawberries); ‘stone fruits’ (drupes with an outer edible fleshy part surrounding a seed containing shell); and ‘pome fruits’ (fruits with an outer edible fleshy part surrounding cores). In total, we sampled nuts: walnut (Jugland regia, N¼ 18), hazel (Corylus avellana, N ¼ 13), ginkgo (Ginkgo biloba, N ¼ 3); berries: blackberry (Rubus fruticosus agg, N ¼ 16), seabuckthorn (Hippophae rhamnoides, N¼ 12), elder (Sambucus nigra, N ¼ 27); and pome and stone fruits: apple (Malus domestica, N ¼29), mirabelle (Prunus domestica subsp. syriaca N ¼28), plum (Prunus domestica subsp. domestica, N ¼ 26). For each fruit species, we collected mixed samples of common supermarket fruits (N¼ 3) except for ginkgo, elder, and seabuckthorn. Elder and seabuckthorn were not available in supermarkets; therefore we harvested samples from rural sites far away from potential pollution sources. In gingko, no trace metals were detected. We used these samples to compare the potential dietary exposure to trace metals of someone consuming urban horticulture products versus supermarket products. Directly after the harvest, the edible parts of the berries, pome and stone fruits were thoroughly washed and afterwards frozen similar to the supermarket samples. The nuts were stored dry in their nutshells. Edible parts of all fruits were dried at a temperature of 60 1C for 72 h to 14 d depending on sample size and fruit species. After drying, the samples were ground ( o 100 mm) and stored in a dehydrator. Then the samples were dried at a temperature of 105 1C for 48 h. Approximately 500 mg dry fruit powder and creamy nut powder was digested in 10 ml HNO3 (69 percent) in a drying chamber at a temperature of 185 1C. After the digestion, the samples were filled up to a volume of 40 ml with ultrapure water. The determination of the trace metal content in the biomass was made with an atomic absorption spectroscopy using the Atomic Absorption Spectrometer AA880Z (Varian, Australia). The used wave lengths/ detection limits of the elements were 228.8/2.0 mg/l for Cd and 217.0/3.0 mg/l for Pb. We used a melon powder (IPE 950) as standard to assess the quality of our measurement (reference/measured values in mg/kg DW for N ¼20: Cd: 1.03/1.34; N ¼ 28: Pb: 3.50/3.55). We used analysis of variance (ANOVA) for data analysis. Cd or Pb content in the dried biomass is the response variables and species, fruit type, and the parameters characterising local settings at sampling site (overall traffic burden, distance to the nearest road and number of vehicles of the nearest road, distance to the nearest arterial road and the number of vehicles per day of the nearest arterial road, presence and absence of a barrier and type, height, width and degree of enclosure L. Pauline Hensel, I. Säumel / Ecotoxicology and Environmental Safety 101 (2014) 233–239 of the sampling site by barriers, sampling height) were taken as explanatory variables. Homogeneity of data (Brown–Forsythe's test) and normal distribution of data (Shapiro–Wilk test) were tested before applying the ANOVA. Log transformations were applied if necessary to comply with the assumptions of the residual normality and variance homogeneity needed for the analysis. We used the Tukey test for the comparison of means. Effects were considered significant at p o 0.05 level. The statistical analysis was done by using R version 2.15.2 (R Foundation for Statistical Computing, Vienna, Austria). 3. Results The trace metal contents differed significantly among species and fruit types (Table 1) and depended on traffic related and on barrier related parameters (Table 2). 235 Cd content of blackberry and seabuckthorn berries were up to 26 times higher compared to nuts, pome and stone fruits, and elder berries (Fig. 2A). Compared to the inner city fruit samples, the Cd content in control samples was higher in hazel (39 times), blackberry (2 times) and mirabelle (3 times), similar in walnut, elder, plum and apple—and lower in seabuckthorn (2 times; Table 1). Pb content of pome and stone fruits was 8 times higher and up to 17 times higher in berries than in nuts (Table 1, Fig. 2B). Compared to the inner city fruit samples, Pb content in control samples was higher in apple (2 times), mirabelle (4 times) and plum (16 times) and was in the same range in seabuckthorn and elder (Table 1). The sampling height of the fruits affected the trace metal contents significantly (Table 2). A decreasing sampling height Table 1 Content of Cd and Pb in nuts, berries and pome and stone fruits grown in the city of Berlin in mg/kg biomass dry weight (DW): median (Med), minimum (Min), maximum (Max); values for N samples and the control value (C) refers to the median concentrations from supermarket products (N¼ 3) are given. nd ¼ not determined. In 28 percent of the samples the content of Cd was below the detection limit of 10 ppm. In 17 percent of the samples the Pb content were below the detection limit of 10 ppm. European standards for Pb: 0.20 mg/kg FW for berries and small fruits and 0.10 mg/kg FW for other fruits and for Cd: 0.05 mg/kg FW for fruits). Content of trace metals [mg/kg DW] Element Nuts Berries Pome and stone fruits Cd Pb Species N Min Med Max C Min Med Max C Jugland regia Corylus avellana Ginkgo biloba Rubus fruticosus agg Sambucus nigra Hippophae rhamnoides Malus domestica Prunus domestica subsp. Syriaca Prunus domestica subsp. Domestica 18 13 3 16 27 12 29 28 26 0.0 0.0 0.0 4.5 0.0 1.2 0.0 0.0 0.0 0.0 0.5 0.0 8.1 0.0 12.9 1.1 0.9 1.2 0.7 5.7 0.0 180.4 9.2 37.6 3.7 9.3 13.3 0.0 19.7 nd 16.7 0.0 8.3 1.1 2.7 1.4 0.0 0.0 0.0 4.5 19.1 21.6 0.0 5.7 8.1 0.0 6.5 0.0 59.5 51.9 57.4 29.3 23.1 23.2 5.7 15.2 0.0 1438.1 149.4 100.4 170.3 567.8 143.4 0.0 6.7 nd 12.8 55.2 50.2 60.1 87.2 290.1 Table 2 ANOVA results of the species, fruit type (i.e. nuts, berries and pome and stone fruits) and site effects as well as the interactions between species and site effects on content of Cd and lead [in mg/kg biomass dry weight (DW)]. Minimum adequate linear models were chosen using a step-by-step reduction of the maximum model to find the minimum value of Akaike's information criterion (AIC). The maximum model considered Cd or Pb content of biomass [mg/kg DW] in relation to species (sp), fruit type (ft), overall traffic burden (otb), number of vehicles per day on the nearest road (tb1), distance (m) to the nearest road (d1), number of vehicles per day on the nearest main arterial road (tb2), distance (m) to the nearest main arterial road (d2), Presence or absence of barrier (b; i.e. no barriers, buildings, plantings or buildings and plantings) and the degree of enclosures by barriers (de) between fruit tree or shrub and streets and relevant interactions between parameters. The models with the lowest AIC value were Cd content spnshnd1ntb2notbnbnbhnbwnde and Pb content spnshnd1ntb1notbnbnbhnde. F and p values of the ANOVA are given (ns, not significant). F value is the ratio between the variance of the group means and the mean of the within group variances. Element Content of trace metals in mg/kg DW Cd Pb Parameter F p F p Species (sp) Fruit type (ft) Sampling height (sh) Overall traffic burden (otb) Distance (m) to nearest road (d1) Number of vehicles per day on the nearest road (tb1) Distance (m) to the nearest main arterial road (d2) Number of vehicles per day on the nearest main arterial road (tb2) Presence/absence of barrier (b) Height (m) of barrier (bh) Width (m) of barrier (bw) Degree of enclosure by barriers (de) Relevant interactions between parameters: sp sh sp tb1 sp otb sp b sp d1 d1 b d1 bh Residuals df MS 105.1 7.1 15.2 5.9 213 ns ns 90.7 16.5 55.9 56.8 53.3 o 0.001 0.001 0.001 0.030 o 0.001 22.1 4.6 19.7 20.6 8.3 ns ns ns 11.1 9.6 ns 29.0 o 0.001 0.011 o 0.001 o 0.001 0.009 18.2 ns ns 8.1 234.7 11.5 185.7 o 0.001 28.8 14.5 11.8 29.8 7.2 10.3 52.1 o 0.001 o 0.001 o 0.001 o 0.001 o 0.001 o 0.001 o 0.001 39 57356 o 0.001 o 0.001 o 0.001 o 0.001 o 0.001 o 0.001 o 0.001 0.001 o 0.001 22 40009 o 0.001 0.005 o 0.001 236 L. Pauline Hensel, I. Säumel / Ecotoxicology and Environmental Safety 101 (2014) 233–239 Pb content, than fruits at sampling sites without a barrier between planting sites and roads (Fig. 3M, Q, and V). Cd content µg/kg DW 50 b 40 4. Discussion 30 b 20 a a a 10 a a a Jr Ca Gb a 0 Rf Sn Hr Md Pd Ps Pb content in µg/kg DW 300 b 250 ab 200 ab b 150 b ab 100 50 a a a Jr Ca Gb 0 Nuts Rf Sn Hr Md Pd Ps Species Berries Pome & Stone fruits Fig. 2. Content of Cd and Pb in the nuts, berries and, pome and stone fruit biomass in mg/kg biomass dry weight (DW). The boxplots indicate the 25th and 75th percentiles and means of the distribution. Different lower case letters associated with the boxplots indicate significant interspecific differences and identical lower case letter indicate groups not significantly different from each other. The sampled vegetable types are walnut (Jr), hazel (Ca), gingko (Gb), blackberry (Rf), elder (Sn), seabuckthorn (Hr), apple (Md), plum (Pd), mirabelle (Ps). The significance level is p o0.05. For ANOVA results see Table 2. Red lines indicate the control value (i.e. median concentrations from supermarket products or samples from rural sites far away from potential pollution sources). Only one sample of 172 different fruit samples exceeds European limits for lead in fruits. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) increased Pb and Cd content of blackberries (pcd ¼0.01; ppb ¼ 0.001). Some traffic related parameters of sampling sites (i.e. overall traffic burden, distance to the nearest road, the number of vehicles per day on the nearest main arterial road) affected the trace metal contents of the fruits (Table 2). Cd content in apple, plum, blackberry and seabuckthorn increased significantly with increasing overall traffic burden at the sampling site (Fig. 3A, B, E–F). Pb content of fruits increased with increasing overall traffic burden at sampling sites for plum, mirabelle, and blackberry (Fig. 3H–L). Trace metal contents of other fruits varied largely among different overall traffic burdens and were not related to different traffic burdens (Fig. 3C, D and G). The presence or absence of a barrier, the height of a barrier, and the degree of site enclosure by barriers influenced the Cd and Pb contents of fruits (Table 2). Apples growing behind a barrier had significantly lower Cd content and blackberries had lower Cd and Our study highlighted that (1) urban non-vegetable fruits in Berlin accumulated considerably less Cd or Pb in the edible tissues compared to urban vegetables and partially to supermarket products (i.e. hazel, mirabelle, apple, plum) and did not exceed European standards for trace metals; (2) accumulation of health relevant trace metals differed among fruit types (i.e. nuts opome and stone fruits oberries); and (3) beyond general urban pollution load, site-specific parameters (i.e. traffic burden, characteristics of barriers between sampling site and road, sampling height) affected the trace metal contents of fruits. Previous studies on trace metal contents in edible fruits focused mainly on rural sites with diverse pollution sources such as spill contamination (Madejón et al., 2006), sewage irrigation (Batarseh et al., 2010; Menti et al., 2006a, 2006b), usage of compost and fertilisers (Merino et al., 2006; Pinamonti et al., 1997) or vicinity of contaminating industries (Arik and Yaldiz, 2010). In general, Cd and Pb content of non-vegetable fruits from Berlin's inner city were similar or lower compared to fruits from uncontaminated rural sites (Ademoroti, 1986; Bi et al., 2010; Yaman et al., 2000) and significantly lower compared to fruits irrigated with sewage water or sludge (Batarseh et al., 2010; Menti et al., 2006a, 2006b). Cd and Pb content of stone fruits from Berlin were lower compared to unwashed mango fruits growing on rural sites that were classified as uncontaminated (Bi et al., 2010). Cd and Pb content of orange fruits growing in the inner city of Seville and Palermo were higher or similar to our berry samples (Rossini Oliva and Valdés, 2003). Fruits from Copenhagen, Denmark, had higher trace metal contents compared to our samples (SamsøePetersen et al., 2002). A previous study on trace metal contents of vegetables grown in Berlin's inner city demonstrated that urban crops are not automatically ‘healthy' or ‘safe' compared to supermarket products (Säumel et al., 2012). In the present study, trace metal contents of urban non-vegetable fruits were in the range of supermarket and control samples (Table 1). Moreover, supermarket samples of some non-vegetable fruits exhibited higher levels of Pb or Cd than inner city samples (Table 1). Almost all urban fruits analysed in this study had significantly lower Cd and Pb content compared to vegetables harvested in the same study area (Säumel et al., 2012). Similar differences between non-vegetable fruits and vegetables have been reported for medium contaminated urban sites (Samsøe-Petersen et al., 2002). None of our samples exceeded the EU standards for Cd in fruits (0.05 mg/kg FW) and only one sample of the 172 samples exceeded the EU standards for Pb (0.20 mg/kg FW for berries and small fruits and 0.10 mg/kg FW for other fruits; European Commission, 2006). The WHO dietary intake limits for adults are 0.060 mg for Cd and 0.214 mg for Pb per day (FAO/WHO Joint Expert Committee on Food Additives, 1999). The recommended daily vegetable and fruit consumption is 400 g for adults. Thus, an adult consuming an average of 200 g of non-vegetable urban fruits would be ingesting less than 0.3 percent and 2 percent of the accepted daily intake of Cd and Pb, respectively. Thus, we did not prove a human health risk by consuming fruits from inner city areas. In contrast to our results, Cd content of the edible fruits from orchards in a large Chinese metropolis markedly exceeded Chinese and EU standards (Li et al., 2006). A further important finding of our study is, that accumulation of health relevant trace metals differed between non-vegetable fruit types. Similar to our samples, carambola berries had generally L. Pauline Hensel, I. Säumel / Ecotoxicology and Environmental Safety 101 (2014) 233–239 237 Fig. 3. Content of Cd (above) and Pb (below) in the edible fruit parts in mg/kg dry weight (DW) in relation to the overall traffic burden at sampling site (green: low; orange: medium and red: high traffic burden; (A–L) and in relation to the absence and presence of a barrier between sampling site and nearest road (M–V). Lower case letters associated with the boxplots indicate significant interspecific differences. The significance level is p o 0.05. Significant differences are indicated (**p o0.01; *p o 0.05; ns, not significant). The boxplots indicate the 25th and 75th percentiles of the distribution. For ANOVA results see Table 2. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) higher Cd content compared to pome and stone fruits (i.e. wampee and longan fruits; Li et al., 2006). Menti et al. (2006a, 2006b) reported higher Cd contents in lemons than in almonds. Adapting the concept of low and high accumulators from vegetable crops to address species-specific differences in the capacity for uptake, accumulation, and tolerance of trace metals (e.g. Alexander et al., 2006; Finster et al., 2004), our results provide evidence that nonvegetable fruits can be addressed as low accumulators for both trace metals. Nuts with a compact protecting shell accumulate almost no Pb or Cd. Pome and stone fruits accumulate more Pb compared to nuts. Blackberry and seabuckthorn accumulate more Cd compared to the other fruit types whereas elder berries did not (Fig. 2). Our data provide evidence, that the higher sampling height of the elder berries compared to the other berries reduced trace metal contents (Table 2). Shielding properties of nut and fruit shells isolate the edible parts during growth from the environment and reduce airborne pollution (Wyttenbach and Tobler, 1998; Rodushkina et al., 2008). In contrast to our results, nuts from Copenhagen, Denmark, had higher Pb contents compared to berries and stone fruits (Samsøe-Petersen et al., 2002). However, more research is needed to highlight the mechanisms beyond these patterns. The high variability of our data seen in Table 1 might be due to the heterogeneity of urban soil. Contaminated sites in urban environments can increase trace metal contents in fruits growing in a low overall traffic burden (Alloway, 2004). However, trace metal contents of urban fruits and vegetables were not always correlated with different degrees of soil contaminations (SamsøePetersen et al., 2002). Pb uptake from soils is generally passive and Pb is not directly translocated to the edible parts of a fruit tree (Ward and Savage, 1994). The atmospheric deposition of trace metals on the fruit surfaces apparently has a stronger effect than uptake from the soils (Madejón et al., 2006; Samsøe-Petersen et al., 2002) and more traffic related Pb was deposited on rough surfaces such as tree bark compared to rather smoth fruit skins (Ademoroti, 1986). Consequently, unwashed olive fruits growing in spill-affected soils compared to non-affected soils showed no significant differences with regard to Cd and Pb contents (Madejón et al., 2006). 238 L. Pauline Hensel, I. Säumel / Ecotoxicology and Environmental Safety 101 (2014) 233–239 Traffic related pollutants are strongly enhanced along roads compared to background values. Pollutants deposited in the soil remain there for a long time and acting as a source of further pollution in urban environments (Hjortenkrans et al., 2008; Querol et al., 2007). We revealed that a high traffic burden and proximity to the nearest road significantly increased the Cd and Pb contents in non-vegetable fruits (Table 2, Fig.3). The accumulation of Pb and Cd in the soils decreased with increasing distance from the road (Hjortenkrans et al., 2008). Cd and Pb contents in apple and grape fruits did not decrease with increasing distances to roads but with decreasing traffic densities (Bakirdere and Yaman, 2008). Pb deposits on unwashed fruit skin varied according to traffic volume in Benin City, Nigeria (Ademoroti, 1986). Furthermore, our study revealed that barriers between planting site and road reduced Pb and Cd in the edible parts of fruit trees (Fig. 3M, Q, and V). As particles washed off of painted houses and walls doubled Pb contents in the topsoil (Alloway, 2004), closeness of buildings and walls can also increase trace metal contents in the topsoil. Our data showed that the increasing height and width of a barrier decrease the trace metal contents in the edible part of fruits. Traffic related particles could be immobilised on plant surfaces of vegetation barriers such as hedges and thus reduce the deposition of traffic related pollution on the fruits (Hodel and Chang, 2004). Studies from the 1970s already demonstrated, that hedges or trees near roads efficiently reduced traffic related Pb emissions (Keller, 1974). However, the function of barriers was discussed controversially and it was assumed that the windbreak effect and the related higher deposition rates inside the hedges might be more important than the filtration effects of hedges (Keller, 1974; Bouvet et al., 2007). The integration of productive fruit trees in urban gardening can support long-term establishment of local production and thus urban sustainability efforts (Deelstra and Girardet, 2000) and strengthen the environmental benefit of gardens for city-dwellers, urban flora, and fauna. Horticultural studies on rural landscapes have demonstrated benefits derived from an integration of productive fruit trees in gardens: shading and cooling effects of fruit trees between vegetables patches increased the crop yields (Huang et al., 1990), reduced soil erosion and functioning of leaf litter as organic fertiliser (Marten, 1986), enhanced agrobiodiversity (Altieri, 1999) as fruit trees attract a wide range of insect and bird species (e.g. Davies et al., 2009). In addition to these benefits, urban trees improve air quality (Akbari et al., 2001). Finally, our study provides evidence for the development of planting concepts for urban gardens. Hedges or walls minimise contamination effects, especially within high traffic areas. Nut trees can form the outer and pome and stone fruits the medium boundary of urban garden areas, whereas berries and vegetables should preferably be cultivated in the central area of urban gardens. 5. Conclusion Our study demonstrated that the Cd and Pb contents in fruits harvested from trees growing within inner city neighbourhoods were below the EU standards for fruits (European Commission, 2006), partially below values found in fruit samples from supermarkets and were considerably lower in urban non-vegetable fruits than in urban vegetables (Samsøe-Petersen et al., 2002; Säumel et al., 2012). However, more research is needed to identify harmless and risky fruit species for urban gardening. Based on our data, the consumption of urban fruits is not harmful to human health and fruit trees and shrubs can be considered more suitable for urban gardening in highly polluted areas compared to vegetables. Overall, our study gives evidence that the consumption of nonvegetable fruits growing on inner city sites in Berlin does not pose a risk on human health, as long as the fruits are thoroughly washed and it is provided that site pollutions are considered in garden concepts and guidelines (e.g. minimum distance to roads, usage of barriers, planting concepts). Capsule Urban non-vegetable fruits accumulated less cadmium or lead in the edible tissues compared to urban vegetables and to some supermarket products and did not exceed European limits for trace metals in fruits. Acknowledgments This study was funded by Peter Dornier Stiftung Lindenau and by the Freunde der TU Berlin e.V. Special thanks go to Christa Müller and the Stiftungsgemeinschaft Anstiftung & Ertomis for supporting our research. We want to thank Claudia Kuntz, Iris Pieper, and Kotan Yildiz for technical assistance. References Ademoroti, C.M.A., 1986. Levels of heavy metals on bark and fruit of trees. J. Environ. Pollut. (Series B) 11, 241–253. Akbari, H., Pomerantz, M., Taha, H., 2001. Cool surfaces and shade trees to reduce energy use and improve air quality in urban areas. Sol. Energy 70, 295–310. Alexander, P.D., Alloway, B.J., Dourado, A.M., 2006. Genotypic variations in the accumulation of Cd, Cu, Pb and Zn exhibited by six commonly grown vegetables. Environ. Pollut. 144, 736–745. Alloway, B.J., 2004. Contamination of soils in domestic gardens and allotments: a brief overview. Land Contam. Reclam. 12, 179–187. Altieri, M.A., 1999. The ecological role of biodiversity in agroecosystems. Agric. Ecosyst. Environ 74, 19–31. Arik, F., Yaldiz, T., 2010. Heavy Metal Determination and Pollution of the Soil and Plants of Southeast Tavşanli (Kütahya, Turkey). CLEAN—Soil, Air, Water 38, 1017–1030. Bakirdere, S., Yaman, M., 2008. Determination of lead, cadmium and copper in roadside soil and plants in Elazig, Turkey. Environ. Monit. Assess. 136, 401–410. Batarseh, M.I., Rawajfeh, A., Ioannis, K.K., Prodromos, K.H., 2010. Treated municipal wastewater irrigation impact on olive trees (Olea Europaea L.) at Al-Tafilah, Jordan. Water, Air, Soil Pollut. 217, 185–196. Bendt, P., Barthel, S., Colding, J., 2013. Civic greening and environmental learning in public-access community gardens in Berlin. Landscape Urban Plann. 109, 18–30. Bi, X., Ren, L., Gong, M., He, Y., Wang, L., Ma, Z., 2010. Transfer of cadmium and lead from soil to mangoes in an uncontaminated area, Hainan Island, China. GEODERMA 155, 115–120. Bouvet, T., Loubet, B., Wilson, J.D., Tuzet, A., 2007. Filtering of windborne particles by a natural windbreak. Boundary-layer Meteorol. 123, 481–509. Davies, Z.G., Fuller, R.A., Loram, A., Irvine, K.N., Sims, V., Gaston, K.J., 2009. A national scale inventory of resource provision for biodiversity within domestic gardens. Biol. Conserv. 142, 761–771. Deelstra, T., Girardet, H., 2000. Urban Agriculture and Sustainable Cities. In: Bakker, N., Dubbeling, M., Gündel, S. (Ed.). Growing Cities, Growing Food. Urban Agriculture on the Policy Agenda. Feldafing: German Foundation for International Development, DSE.; 2000. pp. 43–65. European Commission. Commission Regulation (EC) No. 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off. J. Eur. Union, L 364 (5). FAO (Food and Agriculture Organisation of the United Nations), 2007. Urban Farming Against Hunger. Safe, Fresh Food for City Dwellers. Last access in May, 2013. URL: 〈http://www.fao.org/newsroom/en/news/2007/1000484/ index.html〉. FAO/WHO Joint Expert Committee on Food Additives, 1999. Summary and Conclusions. In: 53rd Meeting, Rome, June 1–10. Finster, M.E., Gray, K.A., Binns, H.J., 2004. Lead levels of edibles grown in contaminated residential soils: a field survey. Sci. Total Environ. 320, 245–257. Galluzzi, G., Eyzaguirre, P., Negri, V., 2010. Home gardens: neglected hotspots of agro-biodiversity and cultural diversity. Biodivers. Convers. 19, 3635–3654. Glover, T.D., Shinew, K.J., Parry, D.C., 2005. Association, sociability, and civic culture: the democratic effect of community gardening. Leisure Sci. 27, 75–92. Hancock, T., 2001. People, partnerships and human progress: building community capital. Health Promotion Int. 16, 275–280. L. Pauline Hensel, I. Säumel / Ecotoxicology and Environmental Safety 101 (2014) 233–239 Hjortenkrans, D.S., Bergbäck, B.G., Häggerud, A.V., 2008. Transversal immission patterns and leachability of heavy metals in road side soils. J. Environ. Monit. 10, 739–746. Hodel, D.R., Chang, A.C., 2004. Trace Elements and Urban Gardens. University of California Cooperative Extension, UCCE Newsletter 3, 14–19. Hough, R.L., Breward, N., Young, S.D., Crout, N.M.J., Tye, A.M., Moir, A.M., Thornton, I., 2004. Assessing potential risk of heavy metal exposure from consumption of home-produced vegetables by urban populations. Environ. Health Perspect. 112, 215–221. Huang, Y.J., Akbari, H., Taha, H., 1990. The Wind-shielding and Shading Effects of Trees on Residential Heating and Cooling Requirements. Lawrence Berkeley Lab., CA (USA). Keller, T., 1974. Filtering effect of hedges on traffic induced airborne dust pollutionlead compounds. Schweiz, z. Forstwes 125, 719–735. Kloke, A., Sauerbeck, D.R., Vetter, H., 1984. The Contamination of Plants and Soils with Heavy Metals and the Transport of Metals in Terrestrial Food Chains. Changing Metal Cycles and Human Health. Springer, Berlin Heidelberg, pp. 113–141. Krasny, M.E., Bonney, R., 2005. Environmental education through citizen science and participatory action research. In: Johnson, E.A., Mappin, M.J. (Eds.), Environmental Education and Advocacy: Changing Perspectives of Ecology and Education. Cambridge University Press, pp. 292–319. (Chapter 13). Leake, J., Adam-Bradford, A., Rigby, J.E., 2009. Health benefits of ‘grow your own’ food in urban areas: implications for contaminated land risk assessment and risk management? Environ. Health 8, S6. Lenné, P.J., 1825. Über die Anlage eines Volksgartens bei der Stadt Magdeburg. Verhandlungen des Vereins zur Beförderung des Gartenbaus in den königlich preußischen Staaten, 147–159. Li, J.T., Qiu, J.W., Wang, X.W., Zhong, Y., Lan, C.Y., Shu, W.S., 2006. Cadmium contamination in orchard soils and fruit trees and its potential health risk in Guangzhou, China. Environ. Pollut. 143, 159–165. Madejón, P., Marañón, T., Murillo, J.M., 2006. Biomonitoring of trace elements in the leaves and fruits of wild olive and holm oak trees. Sci. Total Environ 355, 187–203. Marten, G.G., 1986. Traditional Agriculture in Southeast Asia: A Human Ecology Perspective. Westview Press p. 358. Menti, J., Roulia, M., Tsadilas, E., Christodoulakis, N.S., 2006a. Long-term application of sludge and water from a sewage treatment plant and the aftermath on the almond trees (Prunus dulcis). Bull. Environ. Contamin. Toxicol 76, 1021–1030. 239 Menti, J., Roulia, M., Tsadilas, E., Christodoulakis, N.S., 2006b. Aftermath of the longterm application of sludge and water from a sewage treatment plant to a lemon tree (Citrus limon) plantation. Bull. Environ. Contamin. Toxicol 76, 33–43. Merino, A., Otero, V., Omil, B., Lastra, B., Piñeiro, V., Gallego, P.P., 2006. Application of wood ash compared with fertigation for improving the nutritional status and fruit production of kiwi vines. J. Plant Nutr. Soil Sci 169, 127–133. Mundraub, 2013. Last access in April, 2013. URL: 〈www.mundraub.org〉. Pinamonti, F., Stringari, G., Gasperi, F., Zorzi, G., 1997. The use of compost: its effects on heavy metal levels in soil and plants. Resour. Conserv. Recycl. 21, 129–143. Querol, X., Viana, M., Alastuey, A., Amato, F., Moreno, T., Castillo, S., Pey, J., De la Rosa, J., Sanchez de la Campa, A., Artinano, B., Zabalza, J., 2007. Source origin of trace elements in PM from regional background, urban and industrial sites of Spain. Atmos. Environ 41, 7219–7231. Rodushkina, I., Engström, E., Sörlinb, D., Baxter, D., 2008. Levels of inorganic constituents in raw nuts and seeds on the Swedish market. Sci. Total Environ. 392, 290–304. Rossini Oliva, S.R., Valdés, B., 2003. Metal concentrations in Seville orange (Citrus aurantium) fruits from Seville (Spain) and Palermo (Italy). Annales Botanici Fennici 40, 339–344. Rossini Oliva, S.R., Valdés, B., Mingorance, M.D., 2008. Evaluation of some pollutant levels in bitter orange trees: implications for human health. Food Chem. Toxicol 46, 65–72. Säumel, I., Kotsyuk, I., Hölscher, M., Lenkereit, C., Weber, F., Kowarik, I., 2012. How healthy is urban horticulture in high traffic areas? Trace metal concentrations in vegetable crops from plantings within inner city neighbourhoods in Berlin, Germany. Environ. Pollut 165, 124–132. Samsøe-Petersen, L., Larsen, E.H., Larsen, P.B., Bruun, P., 2002. Up- take of trace elements and PAHs by fruit and vegetable from contaminated soils. Environ. Sci. Technol. 36, 3057–3063. Schmidlin, E., 1852. Die Bürgerliche Gartenkunst. Stuttgart, 131–142. Ward, N.I., Savage, J.M., 1994. Metal dispersion and transportation activities using food crops as biomonitors. Sci. Total Environ. 146/147, 309–319. Wyttenbach, A., Tobler, L., 1998. Effect of surface contamination on results of plant analysis. Commun. Soil Sci. Plant Anal. 29, 809–823. Yaman, M., Dilgin, Y., Gucer, S., 2000. Speciation of lead in soils and relation with its concentration in fruits. Anal. Chim. Acta 410, 119–125.