Environ Monit Assess (2011) 173:315323 DOI 10.

1007/s10661-010-1389-4

Determination of pesticide residues in Turkeys table grapes: the effect of integrated pest management, organic farming, and conventional farming
Cafer Turgut Hakan Ornek Teresa J. Cutright

Received: 22 July 2009 / Accepted: 11 February 2010 / Published online: 7 March 2010 Springer Science+Business Media B.V. 2010

Abstract Turkey is one of the worlds largest producers and exporters of table grapes. Growing social concerns over excessive pesticide use have led to farming to move from conventional to organic practices. Table grapes were collected from 99 different farms in three Aegean regions. Pesticide residues were only detected in farms using conventional agriculture practices while no pesticides were detected in grapes from farms using organic or integrated pest management. A risk assessment model indicated that lambda-cyhalothrin posed the most significant risk at conventional farms. Keywords Pesticide residues Table grapes Organic farming IPM Conventional farming

Introduction Turkey is the fourth biggest grape producer in the world with a table grape production of 5.8 million tons (Cesnik et al. 2008). Table grapes are mainly exported (Oztekin et al. 1999); therefore, their quality of production has influences both in the exported countries as well as European countries. The export of table grapes increased by only 50% in the last 5 years and reached 39,772,604 tons (Anonymous 2008). The increase in grape production to meet food demand of growing population has led to massive and indiscriminate use of pesticides. Most production of grapes in Turkey comes from conventional agricultural practice in the Aegean region (Doymaz and Pala 2002). Conventional farming poses a negative impact on the environment, agriculture, and human health. The agriculture industry has been estimated to use over 1.5 million tons of pesticides and over 160 million tons of fertilizer. Pesticides may kill pests, diseases, and weed, but they also end up as residues on our food (Rehber and Turhan 2002). The largest negative impact of conventional farming is its contamination of our freshwater supply (Turgut and Fomin 2002; Turgut 2007b). Farmers use chemicals on the crops, which then soak into the soil and migrate into water supplies or enter to the air and can also transported to other areas where no pesticides are used (Turgut 2003; Barlas

C. Turgut (B) Faculty of Agriculture, Adnan Menderes University, Aydin, Turkey e-mail: cturgut@adu.edu.tr H. Ornek Bornova Plant Protection Research Institute, Izmir, Turkey T. J. Cutright Department Civil Engineering, The University of Akron, Akron, OH, USA

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et al. 2006; Kolankaya 2006). Pesticide use has a negative impact on natural predators as well in that they not only kill the targeted pests but also other beneficial organisms (Morales 2002). Regular application of pesticides ends up breeding a stronger, more resistant community to pesticides. As a result, farmers either use larger quantities of pesticides or more toxic forms to eradicate the pest (Ahmad et al. 2008). The intensive usage of pesticides has raised concerns regarding negative impact on the environment, toxicity to aquatic and soil organisms, and impacts on human health (Anonymous 2005; Turgut 2006, 2007a). Many agencies worldwide are trying to monitor pesticide residues in fruits and vegetables to ensure the consumers health (European Commission Health 2005; USFDA 2005). As a result, many European Union candidate countries including Turkey have been trying to establish national monitoring laboratories for pesticide residues in vegetables and fruits (Steiner et al. 2007). There is a growing social desire to reduce pesticide usage in vineyards to decrease the risk of pesticide residues. As a result, many countries are moving away from an unsustainable agriculture system. integrated pest management (IPM) was developed as an effective and environmentally sensitive alternative approach to pest management (Dasgupta et al. 2007). IPM programs use current, comprehensive information on the life cycles of pests and their interaction with the environment. This information, in combination with available pest control methods, is used to manage pest damage by the most economical means, while simultaneously posing the least possible hazard to people, property, and the environment. Pest prevention is the preferred approach before application of pesticides. Effective, less risky pest controls are chosen first including highly targeted chemicals, such as pheromones to disrupt pest mating, or mechanical control, such as trapping or weeding. For example, the use of sticky traps in greenhouse vegetables was found to be healthier and more cost effective for vegetable production in western Turkey (Civelek et al. 2004). If further monitoring and action thresholds indicate that less risky controls are not working, then additional pest control methods would be employed, such as

targeted spraying of pesticides. Broad spraying of nonspecific pesticides is a last resort (Morales 2002). Organic farming is defined as an approach to agriculture that creates integrated, humane, environmentally, and economically sustainable agricultural production systems. The main aim is to protect the long-term fertility of soils by maintaining organic matter levels, encouraging soil biological activity, and careful mechanical intervention (Carvalho 2006; Wood et al. 2006). Many analytical methods have been developed and published for determining pesticide residues in table grapes (Oliva et al. 1999, 2000; Gonzalez et al. 2003; Angioni et al. 2005; Cunha et al. 2007; Navarro et al. 2000). Many of the traditional techniques are very time-consuming and expensive. Anastassiades et al. (2003) recently developed the quick, easy, cheap and effective (QuEChERS) method for determining pesticide concentration. Regardless of the analytical

Table 1 GCMS SIM conditions for the monitored pesticides Pesticides Bromopropylate Captan Chlorothalonil Chlorpyrifos-ethyl Chlorpyrifos-methyl Cypermethrin Deltamethrin Diazinon Dichlofluanid Endosulfan ( ) Endosulfan ( ) Esfenvalerate Folpet Hexaconazole Imazalil Iprodione Lambda-cyhalothrin Metalaxyl Methidathion Myclobutanil Parathion-methyl Permethrin Pirimiphos-methyl Procymidone Thiabendazole Vinclozolin Ion(s) 341 + 339 + 343 79 + 149 266 + 268 314 + 316 286 + 125 191 + 163 + 165 + 181 181 + 251 + 253 304 123 + 224 + 167 241 + 239 241 + 239 + 195 + 243 + 197 225 + 167 260 + 262 214 + 216 + 231 172 + 173 + 217 124 + 187 + 244 197 + 248 + 181 206 85 + 145 179 + 245 + 150 263 + 125 + 129 183 + 163 + 165 290 + 276 + 305 96 + 67 + 283 202 + 242 + 205 212 + 198 + 214 + 200

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method, the concentration of pesticide residues in harvested table grapes will be dependent on the pests and disease in grape vine associated for each vine-growing region and type of grape production (conventional, IPM, or organic). These results are obviously needed to support consumer confidence in the growing market of table grapes and exporters to European Community. The agriculture structure of Turkey is different from European Countries because of very small farms and large populations live in rural areas. The production of table grapes, as well as other vegetables and fruits, come from a variety of small farms; therefore, a large number of samples are required to monitor pesticide residues. The best way to reduce the pesticide residues is to produce new strategies for this purpose. One method to achieve this goal is to conduct an experiment in controlled conditions and taken samples directly from known vineyards. The goal of this study was to investigate the concentrations of pestiTable 2 Recovery of pesticide with 0.01 vs. 0.05 mg/kg fortification level and RSD (percent; n = 5) Pesticides

cide residues in table grapes from vineyard included in organic, IPM, and conventional agricultural practice. Grapes were collected from 99 different farms: 20 from IPM farms, ten organic farms, and 69 farms using conventional agriculture techniques.

Materials and methods Sampling Grapes were sampled from a total of 99 different farms across three different Aegean regions. Ten organic and 20 IPM farms were analyzed. Of the 69 conventional farms, ten were located in Izmir, 45 in Manisa, and 14 in Denizli. Twelve different vines were randomly collected from each farm following the sampling procedure outlined in European Union Directive 91/4/4/EC.

Fortification level 0.01 mg/kg % Recovery % RSD 4.76 5.90 1.55 3 4.40 1.77 3.76 2.44 0.05 mg/kg % Recovery 79 96 99 100 99 84 93 100 97 93 99 87 88 94 98 97 81 88 93 87 90 95 91 92 92 90 % RSD 2.91 4.32 3.64 1.53 2.10 7.96 4.33 1.52 5.21 2.72 4.68 9.12 6.49 2.67 3.57 3.72 1.43 5.21 3.44 4.66 7.59 4.27 1.68 3.26 2.73 3.92

ND not detected

Bromopropylate Captan Chlorothalonil Chlorpyrifos-ethyl Chlorpyrifos-methyl Cypermethrin Deltamethrin Diazinon Dichlofluanid Endosulfan ( ) Endosulfan ( ) Esfenvalerate Folpet Hexaconazole Imazalil Iprodione Lambda-cyhalothrin Metalaxyl Methidathion Myclobutanil Parathion-methyl Permethrin Pirimiphos-methyl Procymidone Thiabendazole Vinclozolin

95 ND 93 99 102 95 ND 98 93 95 ND ND ND 97 92 90 83 ND 95 96 ND 98 97 95 97 99

2.73 3.31 1.28 5.45 1.60 3.61 2.04 6.65 2.18 1.57 4.79

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Sample preparation Acetonitrile (high-performance liquid chromatography grade), ammonia solution, formic acid 98%, sodium chloride, and MgSO4 were obtained from Merck (Darmstadt, Germany). Bondesil sorbents (primary and secondary amine, PSA) were purchased from Varian (Palo Alto, CA, USA). Pesticide standards (99%) were obtained from Dr. Ehrensdorfer GmbH, Germany. The homogenous, frozen samples were taken out from deep freeze and an extraction procedure similar to QuEChERS (Cunha et al. 2007) was used as follows: 10 g table grapes were put in a 50 ml fluoroethylenepropylene centrifugation tube, and 10 ml MeCN was added for homogenization by ultra turrax. After that, 4 mg MgSO4 and 1 g NaCl were added to the mixture and shaken for 1 min by hand and centrifuged for 5 min. Then, supernatant was transferred to other tubes containing 150 mg MgSO4 and 50 mg PSA, 50 mg C18 and 50 mg graphitized carbon black and vortexed for 1 min. The recovery and repeatability of the experiments were evaluated with pesticide standards. Pure pesticides were mixed into a stock solution. Two concentrations (0.01 and 0.05 mg kg1 ) were used with five replicates per concentration.

Results and discussion The performance of QuEChERS method was checked by evaluating quality recovery and precision values of pesticides in table grapes. Recovery rate and relative standard deviation (RSD) were measured by analysis of five replicates. The recovery values ranged from 83% to 102% for the 0.01 mg kg1 and 79100% in 0.05 mg/kg1 (Table 2). The most frequently found pesticides were lambda-cyhalothrin (22 samples), deltamethrin (15 samples), chlorpyrifos-methyl (15), and chlorpyrifos-ethyl (12). The residues were found only at the vineyards using conventional farming practices. No residues were detected in IPM and organic farming agriculture. The lack of pesticide residue at organic farms was not surprising.

Table 3 Pesticides and associated MRLs analyzed for in table grapes residues Pesticide Acephate Bromopropylate Captan Chlorothalonil Chlorpyrifos-ethyl Chlorpyrifos-methyl Cypermethrin Deltamethrin Diazinon Dichlofluanid Endosulfan ( ) Endosulfan ( ) Esfenvalerate Folpet Hexaconazole Imazalil Iprodione Lambda-cyhalothrin Metalaxyl Methidathion Myclobutanil Parathion-methyl Permethrin Pirimiphos-methyl Procymidone Thiabendazole Vinclozolin
a EU

MRL 0.01 2 2 1 1 0.2 0.5 0.2 0.2 3 0.5 0.5 1 5 0.02 0.2 10 0.2 2 0.2 1 0.1 1 0.05a 5 0.05a 5a

Analysis A Varian gas chromatography (GC)mass spectrometry (MS)MS (GC 3800, MS 2200) equipped with an Agilent MS5 column (30 m, 0.25 mm id 0.25 m film thickness) was used for analysis. Helium was used as carrier gas with a constant flow at 1.2 ml min1 . The oven temperature was programmed as follows: 70 C held for 2 min, ramped to 220 C at 30 C/min, and finally ramped to 260 C at 45 C/min and held for 10 min. The MS transfer line was at 280 C. Electron ionization was used at 70 eV in selective ion monitoring (SIM) and full-scan (50600 m/z) modes in different experiments. The mass spectrometry was used to identify the pesticides in the grape residues. The specific analytes tracked are listed in Table 1.

value

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Organic farming was initiated in Turkey in 1986 (Rehber and Turhan 2002). As long as the farms have maintained the quality control needed to stay certified, pesticides should not pose a serious problems. The lack of residues at the IPM farms was a little surprising. Some of the farms have only been using IPM practices for a year. Other studies have found pesticide residues to persist at new IPM farms. For instance, cyprodinil and fludioxonil exceeded acceptable concentrations in Slovenia 2 years after the farm switched from conventional to IPM practices (Cesnik et al. 2008). The largest grape production comes from Manisa Province in Turkey. Forty-five samples from different vineyards were obtained for pesticide residue analysis. Seven of 45 pesticides were found above detection limit (Table 3) of known pesticides in Manisa. Insecticides chlorpyrifosethyl, chlorpyrifos-methyl, deltamethrin, and

lambda-cyhalothrin were the most common pesticides in table grape samples (Table 4). As shown in Table 4, 15 samples (33%) contained lambdacyhalothrin with the concentration of 0.0022 0.52 mg kg1 . Chlorpyrifos-methyl and deltamethrin were detected only in nine samples with the concentration range 0.0440.57 and 0.032 0.33 mg kg1 , respectively. In the study from Slovenia (Cesnik et al. 2008), 19.1% of samples were contaminated with 0.020.13 mg kg1 chlorpyrifos, which was lower than levels found in grapes from Manisa. Chlorpyrifos-methyl was detected in 30 samples from Italian grapes in a monitoring study (Poulsen et al. 2007). Only five samples exceeded the level of maximum residue level (MRL). The fungicide residues were met lower than insecticides in table grape samples from Manisa. Twelve fungicides were searched by GC/MS/MS and only three active ingredients of fungicides were detected in table

Table 4 Pesticides residues in table grapes in conventional farming from Manisa (total 45 farms)

Pesticides

Number of samples with pesticides 9 9 9 15 6 3 7

Concentration (mg/kg) ND ND 0.0090.95 0.0440.57 ND 0.0320.33 ND ND ND 0.0220.52 ND ND ND ND ND ND ND 0.1011.33 ND ND ND 0.3550.85 ND ND 0.030.962 ND ND

Proportion (%) 20 20 20 33.3 13.3 6.7 15.5

Samples above MRL 2 2 1 4 0 0 0

Acephate Bromopropylate Chlorpyrifos-ethyl Chlorpyrifos-methyl Cypermethrin Deltamethrin Diazinon Endosulfan Esfenvalerate Lambda-cyhalothrin Methamidophos Methidathion Parathion-methyl Permethrin Pirimiphos-methyl Captan Chlorothalonil Dichlofluanid Folpet Hexaconazole Imazalil Iprodione Metalaxyl Myclobutanil Procymidone Thiabendazole Vinclozolin

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grapes. The highest residue among fungicides was dichlofluanid with a concentration of 1.33 mg kg1 . Approximately 13 of the samples contained dichlofluanid at 0.11 to 1.33 mg kg1 . The concentration of iprodione was lower (6.7%) than dichlofluanid and higher than procymidone (15.5%). The Izmir province is the third largest table grape producer in Turkey. Four samples from 12 vineyards in district Menemen contained pesticide residues (chlorpyrifos-methyl and lambdacyhalothrin) which were all above the allowed MRL (Table 3). Two samples contained chlorpyrifos-methyl with concentrations of 0.59 0.64 mg kg1 . Deltamethrin and lambdacyhalothrin were most prevalent insecticides, and their proportion was calculated 30% of samples (Table 5). The concentration of deltamethrin was between 0.044 and 0.08 ppm and lambda-cyhalothrin ranged from 0.062 to

1.42 mg kg1 . Only two fungicides dichlofluanid and iprodione were found in 30% samples tested. The concentration of dichlofluanid was between 0.36 and 1.33 mg kg1 whereas iprodione was higher and ranged from 0.57 to 1.85 mg kg1 . Cesnik et al. (2008) found lower residue in Slovenia grapes, and their concentration reached up to 0.3 ppm in two samples. This was not surprising since the Slovenia grapes were grown on a farm using IPM for 2 years while the data in Table 3 was from farms using conventional agricultural practices. The significantly lower residues even after only 2 years shows that IPM can be effective at reducing pesticide levels in table grapes. Denizli has very large vineyards in comparison to Izmir and has the second highest production of table grapes. Fourteen different vineyards were chosen for collecting samples for further analysis of table grapes grown using conven-

Table 5 Pesticide residues in table grapes in conventional farming from Izmir (total 10 farms)

Pesticides

Number of samples with pesticides 2 3 3 3 3

Concentration

Proportion (%) 20 30 30 30 30

Samples above MRL 2 0 2 0 0

Acephate Bromopropylate Chlorpyrifos-ethyl Chlorpyrifos-methyl Cypermethrin Deltamethrin Diazinon Endosulfan Esfenvalerate Lambda-cyhalothrin Methamidophos Methidathion Parathion-methyl Permethrin Pirimiphos-methyl Captan Chlorothalonil Dichlofluanid Folpet Hexaconazole Imazalil Iprodione Metalaxyl Myclobutanil Procymidone Thiabendazole Vinclozolin

ND ND ND 0.590.64 ND 0.0440.08 ND ND ND 0.0621.42 ND ND ND ND ND ND ND 0.361.33 ND ND ND 0.571.85 ND ND ND ND ND

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tional farming techniques. There were four insecticides and three fungicides identified in table grape samples (Table 6). Only one sample contained chlorpyrifos-ethyl with the concentration 0.55 mg kg1 . Chlorpyrifos-methyl and lambdacyhalothrin were found in four samples from four vineyards. The concentration of chlorpyrifosmethyl ranged from 0.032 to 0.96 mg kg1 , meaning 28.6% of samples contained chlorpyrifosmethyl. Lambda-cyhalothrin residue was higher than other insecticide residues, with concentrations between 0.025 and 1.79 mg kg1 . Deltamethrin was detected at 0.0450.18 mg kg1 . As shown in Table 4, seven samples exceeded MRL values. Residues of three fungicides, dichlofluanid, iprodione, and procymidone, were detected in the grapes. However, none exceeded the MRL value. Approximately 7% of the samples contained dichlofluanid (below detection to 0.43 mg kg1 ).
Table 6 Pesticide residues in table grapes in conventional farming from Denzili (total 14 farms)

Iprodiones concentration was between 0.76 and 0.89 ppm with 21.4% proportion of samples with residues. It is important to note that the farms that had pesticide residues were all conventional farms. No pesticides were detected at IPM or organic farms. Pesticide Safety Directorate (PSD, York, UK) has established a model for acute exposure of pesticides. A risk assessment performed with this model for acute exposure to deltamethrin. The concentration level for deltamethrin was 0.33 mg kg1 , and acceptable daily intake (ADI) of 0.01 mg kg1 . The acute reference dose 0.01 mg kg1 showed that the national estimate of short-term intake (NESTI) found in ADI percentage ranged from 2% for 1518 year-old to 45% for 24-year-old children. ADI values for chlorpyrifos-ethyl and chlorpyrifos-methyl ranged from 6% for 1518-year-old to 45% for 24year-old children. Lambda-cyhalothrin showed a

Pesticides

Number of samples with pesticides 1 4 3 4 1 2 3

Concentration

Proportion (%) 7.1 28.6 21.4 28.6 7.1 14.3 21.4

Samples above MRL 1 3 1 2 0 0 0

Acephate Bromopropylate Chlorpyrifos-ethyl Chlorpyrifos-methyl Cypermethrin Deltamethrin Diazinon Endosulfan Esfenvalerate Lambda-cyhalothrin Methamidophos Methidathion Parathion-methyl Permethrin Pirimiphos-methyl Captan Chlorothalonil Dichlofluanid Folpet Hexaconazole Imazalil Iprodione Metalaxyl Myclobutanil Procymidone Thiabendazole Vinclozolin

ND ND ND0.55 0.0320.96 ND 0.0450.18 ND ND ND 0.0251.79 ND ND ND ND ND ND ND ND0.43 ND ND ND 0.720.89 ND ND 0.760.89 ND ND

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Environ Monit Assess (2011) 173:315323 ion trap mass spectrometry determination of zoxamide residues in grape, grape processing, and in the fermentation process. Journal of Chromatography A, 1097, 165170. Barlas, N., Cok, I., & Akbulut, N. (2006). The contamination levels of organochlorine pesticides in water and sediment samples in Uluabat Lake, Turkey. Environmental Monitoring and Assessment, 118, 383 391. Carvalho, F. P. (2006). Agriculture, pesticides, food security and food safety. Environmental Science & Policy, 9, 685692. Cesnik, H. B., Gregorcic, A., & Cus, F. (2008). Pesticide residues in grapes from vineyards included in integrated pest management in Slovenia. Food Additives and Contaminants, 25, 438443. Civelek, H. S., Yoldas, Z., & Ulusoy, M. R. (2004). Seasonal population trends of Liriomyza huidobrensis (Blanchared, 1926) (Diptera: Agromyzidae) on cucumber (Cucumis sativus L.) in Western Turkey. Journal of Pest Sciences, 77, 8589. Cunha, S. C., Lehotay, S. J., Mastovska, K., Fernandes, J. O., Beatriz, M., & Oliveira, P. P. (2007). Evaluation of the QuEChERS sample preparation approach for the analysis of pesticide residues in olives. Journal of Separation Science, 30, 620632. Dasgupta, S., Meisner, C., & Wheeler, D. (2007). Is environmentally friendly agriculture less profitable for farmers? Evidence on integrated pest management in Bangladesh. Review of Agricultural Economics, 29, 103118. Doymaz, I., & Pala, M. (2002). The effects of dipping pretreatments on air-drying rates of the seedless grapes. Journal of Food Engineering, 52, 413417. European Commission Health (2005). Pesticides EU-MRL Regulation (EC) No 396/2005. Gonzalez, C. F., Otero, R. R., Grande, B. C., & Gandara, J. S. (2003). Determination of fungicide residues in white grapes for winemaking by gas chromatography with mass spectrometric detection and assessment of matrix effects. Journal of AOAC International, 86, 10081014. Kolankaya, D. (2006). Organochlorine pesticide residues and their toxic effects on the environment and organisms in Turkey. International Journal of Environmental Analytical Chemistry, 86, 147160. Morales, H. (2002). Pest management in traditional tropical agroecosystems: lessons fro pest prevention research and extension. Integrated Pest Manage Review, 7, 145163. Navarro, S., Oliva, J., Barba, A., Navarro, G., Garcia, M. A., & Zamorano, M. (2000). Evolution of chlorpyrifos, fenarimol, metalaxyl, penconazole, and vinclozolin in red wines elaborated by carbonic maceration of Monastrell grapes. Journal of Agricultural and Food Chemistry, 48, 35373541. Oliva, J., Navarro, S., Barba, A., & Navarro, G. (1999). Determination of chlorpyrifos, penconazole, fenarimol, vinclozolin and metalaxyl in grapes, must and wine by on-line microextraction and gas chromatography. Journal of Chromatography A, 833, 4351.

higher ADI value that was between 23% for 15 18-year-old and 168% for 24-year-old children. In general, risk assessment of pesticides that exceeded MRL values did not present any risk. The exception was lambda-cyhalothrin. NESTI was used as a percent of ADI and was below 100%; therefore, MRL of lambda-cyhalothrin should be reconsidered or preharvest intervals of table grapes should be changed.

Conclusions Table grapes were collected from 99 different farms in three Aegean regions. Pesticide residues were only detected in farms using conventional agriculture practices. No pesticides were detected in grapes from farms using organic or IPM. The significantly lower residues even after only 2 years show that IPM can be effective at reducing pesticide levels in food crops. The number of pesticides detected at conventional farms that were above acceptable MRL varied for the three regions studied. A cursory risk assessment indicated that most of the pesticides did pose a significant risk, with the exception of lambda-cyhalothrin. Therefore, the MRL of lambda-cyhalothrin should be reconsidered or preharvest intervals of table grapes should be changed.
Acknowledgement We would like to thank Adnan Menderes University Research Fund for funding this project.

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