ecotoxicology and environmental safety · berry (2 times) and mirabelle (3 times), similar in...

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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 article info Article history: Received 28 August 2013 Received in revised form 21 November 2013 Accepted 22 November 2013 Available online 25 January 2014 Keywords: Urban horticulture Agroforestry Fruit trees Trace metals Trafc burden abstract 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 signicant differences in trace metal content depending on species, fruit type, local trafc, and parameters related to barriers between the sampling site and neighbouring roads. Higher overall trafc 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. 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 inter- est 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 nancial 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). 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 trafc 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; Samsøe- Petersen 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 inuence of trafc burden (i.e. trafc burden of the nearest and the nearest main arterial road, distances from the planting site to nearest and nearest main arterial road, overall trafc 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) inuence the trace Contents lists available at ScienceDirect journal homepage: www.elsevier.com/locate/ecoenv Ecotoxicology and Environmental Safety 0147-6513/$ - see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ecoenv.2013.11.023 n Corresponding author. Fax: þ49 30 314 29022. E-mail address: [email protected] (I. Säumel). Ecotoxicology and Environmental Safety 101 (2014) 233239

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Page 1: Ecotoxicology and Environmental Safety · berry (2 times) and mirabelle (3 times), similar in walnut, elder, plum and apple—and lower in seabuckthorn (2 times; Table 1 ). Pb content

Orchards for edible cities: Cadmium and lead content in nuts, berries,pome and stone fruits harvested within the inner city neighbourhoodsin 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

a r t i c l e i n f o

Article history:Received 28 August 2013Received in revised form21 November 2013Accepted 22 November 2013Available online 25 January 2014

Keywords:Urban horticultureAgroforestryFruit treesTrace metalsTraffic burden

a b s t r a c t

Today's urban gardening focuses mainly on vegetable production and rarely includes fruit trees. Healtheffects of consuming urban crops are questioned due to high local pollution loads. Here, we determinedcadmium and lead content in the edible parts of nuts, berries, pome, and stone fruits harvested from fruittrees and shrubs within inner city neighbourhoods of Berlin, Germany. We analysed how local settings atsampling sites shaped the trace metal content. We revealed significant differences in trace metal contentdepending on species, fruit type, local traffic, and parameters related to barriers between the samplingsite and neighbouring roads. Higher overall traffic burden and proximity to roads increased whereasbuildings 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 onhuman health as long as the fruits are thoroughly washed and it is provided that site pollutions andimpacts are considered in garden concepts and guidelines.

& 2013 Elsevier Inc. All rights reserved.

1. Introduction

Urban gardening is booming worldwide and enhances foodsecurity, particularly in developing countries (FAO (Food andAgriculture Organisation of the United Nations), 2007). The inter-est of city dwellers for producing their own fresh food is also risingin developed countries (Leake et al., 2009) and food production forlow-income citizens is supported by self-organisation and localauthorities (Hancock, 2001).

Beyond local food production, urban gardening provides abroad range of ecosystem services and is recognised as a keyinstrument 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 areminiscence of rural landscapes (Lenné, 1825) and fruit treesalong urban roads or in parks have been leased to get financialsupport for street or park maintenance in the 19th century(Schmidlin, 1852). Currently, fruit trees remain unused althoughabundant in public urban green spaces (see Fig. 1A for Berlin) andthe urban gardeners focus mainly on vegetable production (Bendtet al., 2013; Hough et al., 2004).

The effect on human health caused by the consumption ofurban gardening products is discussed controversially, mainly dueto the high pollution loads in urban areas (Alloway, 2004; Finsteret al., 2004; Hough et al., 2004; Leake et al., 2009). Studies ofvegetables demonstrated, that the uptake and accumulation oftrace metals differed among crop type, species, and among plantparts (Alexander et al., 2006; Finster et al., 2004; Säumel et al.,2012). Few studies investigated the relation between trace metalcontent in the edible parts of vegetables and local traffic burden(Kloke et al., 1984; Säumel et al., 2012). Planting and buildingstructures (i.e. hedges, shrubs, lead free painted houses or walls)can function as barrier between planting site and road, decreasingtrace metal content in the crops (Säumel et al., 2012).

Yet, there are only few studies analysing trace metal content infruit tree products growing in urban environments (Li et al., 2006;Rossini Oliva and Valdés, 2003; Rossini Oliva et al., 2008; Samsøe-Petersen et al., 2002). Consequently, the aim of this study was toanalyse the cadmium (Cd) and lead (Pb) content in the edible partsof different non-vegetable fruit types and fruit tree species. Wedetermined the influence of traffic burden (i.e. traffic burden of thenearest and the nearest main arterial road, distances from theplanting site to nearest and nearest main arterial road, overalltraffic burden at sampling site) on trace metal content in thefruits. We evaluated whether characteristics of the planting site(i.e. sampling height, presence or absence of barriers betweenplanting site and roads, barrier width or height, degree ofenclosure of the sampling site by barriers) influence the trace

Contents lists available at ScienceDirect

journal homepage: www.elsevier.com/locate/ecoenv

Ecotoxicology and Environmental Safety

0147-6513/$ - see front matter & 2013 Elsevier Inc. All rights reserved.http://dx.doi.org/10.1016/j.ecoenv.2013.11.023

n Corresponding author. Fax: þ49 30 314 29022.E-mail address: [email protected] (I. Säumel).

Ecotoxicology and Environmental Safety 101 (2014) 233–239

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metal content. Furthermore, we compared the trace metal contentof the urban non-vegetable fruits with supermarket products toassess health risks by consuming these urban fruits.

2. Materials and methods

We collected nuts, berries, pome and stone fruits of nine different species at172 randomly chosen sites of the inner city of Berlin, Germany (Fig. 1B). Thesampling sites represented different urban conditions (Fig. 1C) and were charac-terised by the following parameters: distance to nearest road (d1) and to nearestmain arterial road (d2) in meters, traffic burden on the nearest road (tb1) and onthe nearest main arterial road (tb2) according to the number of vehicles per day(1r5000; 2¼5001–10000; 3¼10001–15.000; 4¼15001–20000; 5¼20001–30000; 6¼30001–40000; 7¼Z40001; Berlin Department for Urban Develop-ment, 2009), presence and absence of barriers between planting sites and nearestroads (b); height of barrier (bh) and width of barrier (bw) in meters; the degree ofenclosure 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 maround the planting sites (low: low traffic burden, existing barriers or high distancebetween planting site and nearest street; medium: low to medium traffic burdenand lacking barriers between planting sites and streets, lower distance to thenearest street; high: high traffic burden and lacking barriers, small distancebetween 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 shellincluding almond nuts); ‘berries’ (fleshy fruits including aggregate fruits such asblackberries or strawberries); ‘stone fruits’ (drupes with an outer edible fleshy partsurrounding a seed containing shell); and ‘pome fruits’ (fruits with an outer ediblefleshy part surrounding cores). In total, we sampled nuts: walnut (Jugland regia,

N¼18), hazel (Corylus avellana, N¼13), ginkgo (Ginkgo biloba, N¼3); berries:blackberry (Rubus fruticosus agg, N¼16), seabuckthorn (Hippophae rhamnoides,N¼12), elder (Sambucus nigra, N¼27); and pome and stone fruits: apple (Malusdomestica, N¼29), mirabelle (Prunus domestica subsp. syriaca N¼28), plum (Prunusdomestica subsp. domestica, N¼26). For each fruit species, we collected mixedsamples of common supermarket fruits (N¼3) except for ginkgo, elder, andseabuckthorn. Elder and seabuckthorn were not available in supermarkets; there-fore we harvested samples from rural sites far away from potential pollutionsources. In gingko, no trace metals were detected. We used these samples tocompare the potential dietary exposure to trace metals of someone consumingurban horticulture products versus supermarket products.

Directly after the harvest, the edible parts of the berries, pome and stone fruitswere thoroughly washed and afterwards frozen similar to the supermarketsamples. The nuts were stored dry in their nutshells. Edible parts of all fruits weredried at a temperature of 60 1C for 72 h to 14 d depending on sample size and fruitspecies. After drying, the samples were ground (o100 mm) and stored in adehydrator. 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 in10 ml HNO3 (69 percent) in a drying chamber at a temperature of 185 1C. After thedigestion, 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 anatomic absorption spectroscopy using the Atomic Absorption Spectrometer AA880Z(Varian, Australia). The used wave lengths/ detection limits of the elements were228.8/2.0 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 valuesin mg/kg DW for N¼20: Cd: 1.03/1.34; N¼28: Pb: 3.50/3.55).

We used analysis of variance (ANOVA) for data analysis. Cd or Pb content in thedried biomass is the response variables and species, fruit type, and the parameterscharacterising local settings at sampling site (overall traffic burden, distance to thenearest road and number of vehicles of the nearest road, distance to the nearestarterial 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

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 toMundraub (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 innercity 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 ofthe 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 greenline 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 and4 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 figurelegend, the reader is referred to the web version of this article.)

L. Pauline Hensel, I. Säumel / Ecotoxicology and Environmental Safety 101 (2014) 233–239234

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of the sampling site by barriers, sampling height) were taken as explanatoryvariables. Homogeneity of data (Brown–Forsythe's test) and normal distribution ofdata (Shapiro–Wilk test) were tested before applying the ANOVA. Log transforma-tions were applied if necessary to comply with the assumptions of the residualnormality and variance homogeneity needed for the analysis. We used the Tukeytest for the comparison of means. Effects were considered significant at po0.05level. The statistical analysis was done by using R version 2.15.2 (R Foundation forStatistical Computing, Vienna, Austria).

3. Results

The trace metal contents differed significantly among speciesand fruit types (Table 1) and depended on traffic related and onbarrier related parameters (Table 2).

Cd content of blackberry and seabuckthorn berries were up to 26times higher compared to nuts, pome and stone fruits, and elderberries (Fig. 2A). Compared to the inner city fruit samples, the Cdcontent in control samples was higher in hazel (39 times), black-berry (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 upto 17 times higher in berries than in nuts (Table 1, Fig. 2B).Compared to the inner city fruit samples, Pb content in controlsamples was higher in apple (2 times), mirabelle (4 times) andplum (16 times) and was in the same range in seabuckthorn andelder (Table 1).

The sampling height of the fruits affected the trace metalcontents significantly (Table 2). A decreasing sampling height

Table 1Content 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 (N¼3) are given. nd¼not determined. In 28 percent ofthe 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. Europeanstandards 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 Cd Pb

Species N Min Med Max C Min Med Max C

Nuts Jugland regia 18 0.0 0.0 0.7 0.0 0.0 0.0 5.7 0.0Corylus avellana 13 0.0 0.5 5.7 19.7 0.0 6.5 15.2 6.7Ginkgo biloba 3 0.0 0.0 0.0 nd 0.0 0.0 0.0 nd

Berries Rubus fruticosus agg 16 4.5 8.1 180.4 16.7 4.5 59.5 1438.1 12.8Sambucus nigra 27 0.0 0.0 9.2 0.0 19.1 51.9 149.4 55.2Hippophae rhamnoides 12 1.2 12.9 37.6 8.3 21.6 57.4 100.4 50.2

Pome and stone fruits Malus domestica 29 0.0 1.1 3.7 1.1 0.0 29.3 170.3 60.1Prunus domestica subsp. Syriaca 28 0.0 0.9 9.3 2.7 5.7 23.1 567.8 87.2Prunus domestica subsp. Domestica 26 0.0 1.2 13.3 1.4 8.1 23.2 143.4 290.1

Table 2ANOVA 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 ofCd and lead [in mg/kg biomass dry weight (DW)]. Minimum adequate linear models were chosen using a step-by-step reduction of the maximummodel to find the minimumvalue 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 trafficburden (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 ofenclosures by barriers (de) between fruit tree or shrub and streets and relevant interactions between parameters. The models with the lowest AIC value were Cdcontent�spnshnd1ntb2notbnbnbhnbwnde and Pb content�spnshnd1ntb1notbnbnbhnde. F and p values of the ANOVA are given (ns, not significant). F value is the ratio betweenthe variance of the group means and the mean of the within group variances.

Content of trace metals in mg/kg DWElement Cd Pb

Parameter F p F p

Species (sp) 105.1 o0.001 22.1 o0.001Fruit type (ft) 7.1 0.001 4.6 0.011Sampling height (sh) 15.2 0.001 19.7 o0.001Overall traffic burden (otb) 5.9 0.030 20.6 o0.001Distance (m) to nearest road (d1) 213 o0.001 8.3 0.009Number of vehicles per day on the nearest road (tb1) ns nsDistance (m) to the nearest main arterial road (d2) ns nsNumber of vehicles per day on the nearest main arterial road (tb2) 90.7 o0.001 nsPresence/absence of barrier (b) 16.5 o0.001 11.1 o0.001Height (m) of barrier (bh) 55.9 o0.001 9.6 0.005Width (m) of barrier (bw) 56.8 o0.001 nsDegree of enclosure by barriers (de) 53.3 o0.001 29.0 o0.001Relevant interactions between parameters:sp� sh 18.2 o0.001 28.8 o0.001sp� tb1 ns 14.5 o0.001sp�otb ns 11.8 o0.001sp�b 8.1 o0.001 29.8 o0.001sp�d1 234.7 o0.001 7.2 o0.001d1�b 11.5 0.001 10.3 o0.001d1�bh 185.7 o0.001 52.1 o0.001Residuals

df 39 22MS 57356 40009

L. Pauline Hensel, I. Säumel / Ecotoxicology and Environmental Safety 101 (2014) 233–239 235

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increased Pb and Cd content of blackberries (pcd¼0.01; ppb¼0.001).

Some traffic related parameters of sampling sites (i.e. overalltraffic burden, distance to the nearest road, the number of vehiclesper day on the nearest main arterial road) affected the trace metalcontents of the fruits (Table 2). Cd content in apple, plum, black-berry and seabuckthorn increased significantly with increasingoverall traffic burden at the sampling site (Fig. 3A, B, E–F). Pbcontent of fruits increased with increasing overall traffic burden atsampling sites for plum, mirabelle, and blackberry (Fig. 3H–L).Trace metal contents of other fruits varied largely among differentoverall traffic burdens and were not related to different trafficburdens (Fig. 3C, D and G).

The presence or absence of a barrier, the height of a barrier, andthe degree of site enclosure by barriers influenced the Cd and Pbcontents of fruits (Table 2). Apples growing behind a barrier hadsignificantly lower Cd content and blackberries had lower Cd and

Pb content, than fruits at sampling sites without a barrier betweenplanting sites and roads (Fig. 3M, Q, and V).

4. Discussion

Our study highlighted that (1) urban non-vegetable fruits inBerlin accumulated considerably less Cd or Pb in the edible tissuescompared to urban vegetables and partially to supermarketproducts (i.e. hazel, mirabelle, apple, plum) and did not exceedEuropean standards for trace metals; (2) accumulation of healthrelevant trace metals differed among fruit types (i.e. nutsopomeand stone fruitsoberries); and (3) beyond general urban pollutionload, site-specific parameters (i.e. traffic burden, characteristics ofbarriers between sampling site and road, sampling height)affected the trace metal contents of fruits.

Previous studies on trace metal contents in edible fruits focusedmainly on rural sites with diverse pollution sources such as spillcontamination (Madejón et al., 2006), sewage irrigation (Batarsehet al., 2010; Menti et al., 2006a, 2006b), usage of compost andfertilisers (Merino et al., 2006; Pinamonti et al., 1997) or vicinity ofcontaminating industries (Arik and Yaldiz, 2010).

In general, Cd and Pb content of non-vegetable fruits fromBerlin's inner city were similar or lower compared to fruits fromuncontaminated rural sites (Ademoroti, 1986; Bi et al., 2010;Yaman et al., 2000) and significantly lower compared to fruitsirrigated with sewage water or sludge (Batarseh et al., 2010; Mentiet al., 2006a, 2006b). Cd and Pb content of stone fruits from Berlinwere lower compared to unwashed mango fruits growing on ruralsites that were classified as uncontaminated (Bi et al., 2010). Cdand Pb content of orange fruits growing in the inner city of Sevilleand Palermo were higher or similar to our berry samples (RossiniOliva and Valdés, 2003). Fruits from Copenhagen, Denmark, hadhigher trace metal contents compared to our samples (Samsøe-Petersen et al., 2002).

A previous study on trace metal contents of vegetables grownin Berlin's inner city demonstrated that urban crops are notautomatically ‘healthy' or ‘safe' compared to supermarket products(Säumel et al., 2012). In the present study, trace metal contents ofurban non-vegetable fruits were in the range of supermarket andcontrol samples (Table 1). Moreover, supermarket samples of somenon-vegetable fruits exhibited higher levels of Pb or Cd than innercity samples (Table 1).

Almost all urban fruits analysed in this study had significantlylower Cd and Pb content compared to vegetables harvested in thesame study area (Säumel et al., 2012). Similar differences betweennon-vegetable fruits and vegetables have been reported for med-ium 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 samplesexceeded the EU standards for Pb (0.20 mg/kg FW for berriesand small fruits and 0.10 mg/kg FW for other fruits; EuropeanCommission, 2006). The WHO dietary intake limits for adults are0.060 mg for Cd and 0.214 mg for Pb per day (FAO/WHO JointExpert Committee on Food Additives, 1999). The recommendeddaily vegetable and fruit consumption is 400 g for adults. Thus, anadult consuming an average of 200 g of non-vegetable urban fruitswould be ingesting less than 0.3 percent and 2 percent of theaccepted daily intake of Cd and Pb, respectively. Thus, we did notprove a human health risk by consuming fruits from inner cityareas. In contrast to our results, Cd content of the edible fruitsfrom orchards in a large Chinese metropolis markedly exceededChinese and EU standards (Li et al., 2006).

A further important finding of our study is, that accumulationof health relevant trace metals differed between non-vegetablefruit types. Similar to our samples, carambola berries had generally

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Fig. 2. Content of Cd and Pb in the nuts, berries and, pome and stone fruit biomassin mg/kg biomass dry weight (DW). The boxplots indicate the 25th and 75thpercentiles and means of the distribution. Different lower case letters associatedwith the boxplots indicate significant interspecific differences and identical lowercase letter indicate groups not significantly different from each other. The sampledvegetable types are walnut (Jr), hazel (Ca), gingko (Gb), blackberry (Rf), elder (Sn),seabuckthorn (Hr), apple (Md), plum (Pd), mirabelle (Ps). The significance level ispo0.05. For ANOVA results see Table 2. Red lines indicate the control value(i.e. median concentrations from supermarket products or samples from rural sitesfar away from potential pollution sources). Only one sample of 172 different fruitsamples exceeds European limits for lead in fruits. (For interpretation of thereferences to color in this figure legend, the reader is referred to the web version ofthis article.)

L. Pauline Hensel, I. Säumel / Ecotoxicology and Environmental Safety 101 (2014) 233–239236

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higher Cd content compared to pome and stone fruits (i.e. wampeeand longan fruits; Li et al., 2006). Menti et al. (2006a, 2006b)reported higher Cd contents in lemons than in almonds. Adaptingthe concept of low and high accumulators from vegetable crops toaddress 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 non-vegetable fruits can be addressed as low accumulators for bothtrace metals. Nuts with a compact protecting shell accumulatealmost no Pb or Cd. Pome and stone fruits accumulate more Pbcompared to nuts. Blackberry and seabuckthorn accumulate moreCd compared to the other fruit types whereas elder berries did not(Fig. 2). Our data provide evidence, that the higher samplingheight of the elder berries compared to the other berries reducedtrace metal contents (Table 2). Shielding properties of nut and fruitshells isolate the edible parts during growth from the environmentand reduce airborne pollution (Wyttenbach and Tobler, 1998;Rodushkina et al., 2008). In contrast to our results, nuts fromCopenhagen, 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 beyondthese patterns.

The high variability of our data seen in Table 1 might be due tothe heterogeneity of urban soil. Contaminated sites in urbanenvironments can increase trace metal contents in fruits growingin a low overall traffic burden (Alloway, 2004). However, tracemetal contents of urban fruits and vegetables were not alwayscorrelated with different degrees of soil contaminations (Samsøe-Petersen et al., 2002). Pb uptake from soils is generally passive and Pbis not directly translocated to the edible parts of a fruit tree (Ward andSavage, 1994). The atmospheric deposition of trace metals on the fruitsurfaces apparently has a stronger effect than uptake from the soils(Madejón et al., 2006; Samsøe-Petersen et al., 2002) and more trafficrelated Pb was deposited on rough surfaces such as tree barkcompared to rather smoth fruit skins (Ademoroti, 1986). Conse-quently, unwashed olive fruits growing in spill-affected soils com-pared to non-affected soils showed no significant differences withregard to Cd and Pb contents (Madejón et al., 2006).

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 lettersassociated with the boxplots indicate significant interspecific differences. The significance level is po0.05. Significant differences are indicated (**po0.01; *po0.05; ns, notsignificant). 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 figurelegend, the reader is referred to the web version of this article.)

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Traffic related pollutants are strongly enhanced along roadscompared to background values. Pollutants deposited in the soilremain there for a long time and acting as a source of furtherpollution in urban environments (Hjortenkrans et al., 2008; Querolet al., 2007). We revealed that a high traffic burden and proximityto the nearest road significantly increased the Cd and Pb contentsin non-vegetable fruits (Table 2, Fig.3). The accumulation of Pb andCd in the soils decreased with increasing distance from the road(Hjortenkrans et al., 2008). Cd and Pb contents in apple and grapefruits did not decrease with increasing distances to roads but withdecreasing traffic densities (Bakirdere and Yaman, 2008). Pbdeposits on unwashed fruit skin varied according to traffic volumein Benin City, Nigeria (Ademoroti, 1986).

Furthermore, our study revealed that barriers between plantingsite 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 andwalls doubled Pb contents in the topsoil (Alloway, 2004), closenessof buildings and walls can also increase trace metal contents in thetopsoil. Our data showed that the increasing height and width of abarrier decrease the trace metal contents in the edible part offruits. Traffic related particles could be immobilised on plantsurfaces of vegetation barriers such as hedges and thus reducethe deposition of traffic related pollution on the fruits (Hodel andChang, 2004). Studies from the 1970s already demonstrated, thathedges or trees near roads efficiently reduced traffic related Pbemissions (Keller, 1974). However, the function of barriers wasdiscussed controversially and it was assumed that the windbreakeffect and the related higher deposition rates inside the hedgesmight be more important than the filtration effects of hedges(Keller, 1974; Bouvet et al., 2007).

The integration of productive fruit trees in urban gardening cansupport long-term establishment of local production and thusurban sustainability efforts (Deelstra and Girardet, 2000) andstrengthen the environmental benefit of gardens for city-dwellers,urban flora, and fauna. Horticultural studies on rural landscapeshave demonstrated benefits derived from an integration of pro-ductive fruit trees in gardens: shading and cooling effects of fruittrees between vegetables patches increased the crop yields (Huanget al., 1990), reduced soil erosion and functioning of leaf litter asorganic fertiliser (Marten, 1986), enhanced agrobiodiversity(Altieri, 1999) as fruit trees attract a wide range of insect and birdspecies (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 ofplanting concepts for urban gardens. Hedges or walls minimisecontamination effects, especially within high traffic areas. Nuttrees can form the outer and pome and stone fruits the mediumboundary of urban garden areas, whereas berries and vegetablesshould preferably be cultivated in the central area of urbangardens.

5. Conclusion

Our study demonstrated that the Cd and Pb contents in fruitsharvested from trees growing within inner city neighbourhoodswere below the EU standards for fruits (European Commission,2006), partially below values found in fruit samples from super-markets and were considerably lower in urban non-vegetablefruits than in urban vegetables (Samsøe-Petersen et al., 2002;Säumel et al., 2012). However, more research is needed to identifyharmless and risky fruit species for urban gardening. Based on ourdata, the consumption of urban fruits is not harmful to humanhealth and fruit trees and shrubs can be considered more suitablefor urban gardening in highly polluted areas compared tovegetables.

Overall, our study gives evidence that the consumption of non-vegetable fruits growing on inner city sites in Berlin does not posea risk on human health, as long as the fruits are thoroughlywashed and it is provided that site pollutions are considered ingarden concepts and guidelines (e.g. minimum distance to roads,usage of barriers, planting concepts).

Capsule

Urban non-vegetable fruits accumulated less cadmium or leadin the edible tissues compared to urban vegetables and to somesupermarket products and did not exceed European limits fortrace metals in fruits.

Acknowledgments

This study was funded by Peter Dornier Stiftung Lindenau andby the Freunde der TU Berlin e.V. Special thanks go to ChristaMüller and the Stiftungsgemeinschaft Anstiftung & Ertomis forsupporting our research. We want to thank Claudia Kuntz, IrisPieper, and Kotan Yildiz for technical assistance.

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