Pesticide residue legislations challenge international trade of food and feed - Eurofins
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Peer Review Pesticide testing / MRL / rice trade Pesticide residue legislations challenge international trade of food and feed Werner Nader, Michelle Maier, Marco Miebach and Gabriel Linder Abstract The diversity of maximum residue levels (MRLs) for plant protection products among the countries worldwide challenges the international food trade. This article describes this diversity and its impacts on the rice supply chain based on the practical experience of an international inspection and analytical company and pesticide testing of 2,592 samples in 2019. Economic impacts of MRLs are illustrated with the example of Basmati rice imports into the EU, where Indian rice exporters lost estimated revenues of over 200 million USD from January 1st 2018 to August 31st 2019 due to a drop in the MRL for tricyclazole from 1 to 0.01 mg/kg. The article furthermore describes that certain substances in food are frequently interpreted as residues from agricultural practices and fall under the EU MRL regulation for pesticides, although they might be - and frequently are - of natural origin or are contaminants not related to agrochemical applications. Examples are high concentrations of the natural plant hormone indole-3- acetic acid in cereal seeds, accumulation of bromide by Brazil nuts, phthalimide and mepiquat generated during food processing involving heat, chlorate from chlorinated water, and nicotine, diethyl-meta- toluamide (DEET) and icaridin from the hands of workers during harvesting and further handling of the crop. Phosphonate can be introduced into the food by agricultural applications of the fungicide fosetyl or plant strengthening phosphonate salts. But it can be also of natural origin, as microorganisms produce the chemical in biogeochemical phosphorous cycles in various environments. Problems arise not only, when these chemicals exceed the legal MRLs. For organic food they are often interpreted as indicators of forbidden pesticide applications and in infant food they frequently exceed the stringent default MRL of 0.01 mg/kg of the EU. Regarding the occurrence of phthalimide and phosphonate results from the analysis of 3,210 tea and spice samples and 1,417 further food samples are presented, which were obtained in the period of 2017 to 2019. 1. Introduction García Martinez and Poole (2004) focused on the market barriers created by diverse fresh produce Internationally, food safety legislations are diverse safety standards of the European retail chains on and the economic impacts of this diversity have developing Mediterranean exporting countries. been studied in detail by Bremmers et al. (2011) on the example of meat exports to the USA and the In 2005, the EU implemented harmonized MRLs European Union. Melo et al. (2014) describe the for plant protection products (Regulation (EC) No burden of regulations and standards on exporting 396/2005) followed by stringent enforcement and countries with Chilean fruit exports as an example. reporting in the RASFF (Rapid Alert System for Food 84 I cereal technology 02/2020
Pesticide testing / MRL / rice trade Peer Review and Feed), when limits are exceeded. The USA fol- not exceed the legal MRLs and are of no health con- lowed with the tolerance levels of the Environmen- cern, trade with organic and infant food will be af- tal Protection Agency (EPA) in the Code of Federal fected, because these substances are interpreted as Regulations, Title 40, Chapter I, Subchapter E, Part residues from forbidden agricultural applications. 180 (Electronic Code of Federal Regulations, 2020, A position paper of a German quality circle of lab- 40 CFR 180) and their enforcement in food imports oratories in the field of pesticide and contaminant by detentions without physical examination (DWPE) analysis (relana®, 2019) summarizes some of these of the Food and Drug Authority (FDA). Australia contaminants in food and feed samples. This knowl- and New Zealand set up MRLs in schedule 20 of the edge is primarily based on the practical experience Food Standards Code and Japan with various regu- of the trade and analytical laboratories and rarely lations of the Ministry of Health, Labour and Wel- substantiated by scientific studies, which are pub- fare. Many countries like Saudi Arabia adapted the lished in the public domain, which is the case e.g. Codex Alimentarius MRLs and appended MRLs for for mepiquat (Yuan et al., 2017) and nicotine (Ro- additional pesticides (Saudi Food and Drug Admin- manotto et al., 2018). In the following, the article istration, 2019, SFDA.FD 382:2019). Pesticides, for will describe several of these cases with a special which no MRLs have been defined, should not be focus on phosphonate, where recent literature pro- present and a default MRL of 0.01 mg/kg applies vides scientific evidence that this compound is gen- within the EU and zero tolerance in the USA. In ad- erated by microorganisms and occurs ubiquitous- dition, these MRLs are undergoing permanent re- ly in significant concentrations in the environment visions depending on safety evaluations and deci- (Pasek et al., 2014). sions made by the national food control authorities (European Food Safety Authority (EFSA), 2008). 2. Source of results Rice is the most important staple food of mankind This article is based in part on the practical expe- and traded in large quantities over national bor- rience and analytical results obtained during pre- ders. The international diversity of these MRLs, the shipment inspections of various food products pri- dynamics of MRL definitions and the consequential or to export to the EU, USA and Australia, primar- economic impacts on the trade, will be described ily outside of the EU. Results from the analyses of in the following, taking Basmati rice as an example. 2,592 rice samples in 2019 and 3,210 tea and spice samples from 2017 to 2019 were evaluated in an an- Even more diverse is the interpretation of pesti- onymized form. Furthermore 1,417 samples of var- cides in food from ecological agriculture, where res- ious food products were analysed from 2017 and idues are tolerated differently by the control bodies 2019 for the fungicide fosetyl and its metabolite of the EU member states (Forschungsinstitut für bi- phosphonate. Results are primarily based on analy- ologischen Landbau (FiBL), 2013). These differences ses by the QuEChERS method (Anastassiades et al., will be described below including the tolerance lev- 2003) adapted to these matrices. Due to their high- els defined by the National Organic Program (NOP) ly highly polar characteristics fosetyl-aluminum and of the USA. phosphonate were analysed by a special method re- cently published by Anastassiades et al. (2019). In addition to this international diversity in food legislations several substances commonly found in 3. Global diversity of MRL regulations – food are interpreted as residues of pesticides or example rice their corresponding metabolites in the EU and are regulated by MRLs, although they might be of nat- Rice is the most important food commodity feed- ural origin or contaminate the food independent- ing nearly half of the world population and being ly of agricultural applications. But even if they do traded on a global scale in large quantities over the cereal technology 02/2020 I 85
Peer Review Pesticide testing / MRL / rice trade boarders. The EU has defined maximum limits for and carbendazim, which are mainly applied against residues of 495 plant protection products in rice the fungal rice blast, and the insecticides imidaclo- (EU pesticide data base, 2020), Japan 313 (The Ja- prid, buprofezin, chlorpyrifos and thiamethoxam pan Food Chemical Research Foundation, 2020), were found in over 10% of the samples each (fig- Australia/New Zealand 173 (Australia New Zealand ure 1). Carbendazim is normally not applied in the Food Standards Code, 2020), the US 140 (Bryant paddy fields and is most probably the metabolite Christie Inc., 2020) and Saudi Arabia 59 (Saudi Food of thiophanate-methyl. The MRLs defined for these and Drug Administration, 2019). With the exception chemicals differ significantly between the coun- of Saudi Arabia residues of chemicals without a MRL tries. Rice with high residue levels of isoprothiolane are not permitted. For these zero tolerance applies and tebuconazole is perfectly fine for the EU mar- in the USA and a default MRL of 0.01 mg/kg is set in ket while triggering import alerts in the USA. On the the EU. In Saudi Arabia pesticides, which are not in- other hand high levels of tricyclazole and buprofe- cluded in the national MRL list, are judged based on zin might cause a rapid alert in the EU RASFF, but either EU or US MRL definitions. the rice can be imported without problems into the US. Japan and Australia New Zealand tolerate car- Table 1 comprises the top 40 pesticides detected bendazim residues of 1 and 2 mg/kg respectively, by analyses of 2,592 rice samples in 2019 with the whereas the default limit applies in the EU and zero number of findings above the limit of quantifica- tolerance in the USA. tion and the average and maximum concentrations. Furthermore listed are the corresponding MRLs in MRLs are not only diverse, but also subject to con- the EU (previous, current and anticipated), USA, Aus- tinuous changes depending on human and environ- tralia New Zealand and Japan. The fungicides tebu- mental safety evaluations. Changes of MRLs for 9 of conazole, tricyclazole, isoprothiolane, propiconazole the top 40 pesticides, which have been implemented Graphic: Werner Nader 2020 Fig. 1: Top 9 fungicides and insecticides occuring as residues in rice. Top, fungicides: (a) tebuconazole, (b) tricyclazole, (c) isoprothiolane, (d) propiconazole and (e) thiophanat-methyl (mostly detected by its metabolite carbendazim). Bottom, insecticides: (f) imidacloprid, (g) bu- profezin, (h) chlorpyrifos-ethyl and (i) thiomethoxam. 86 I cereal technology 02/2020
Pesticide testing / MRL / rice trade Peer Review Table 1: Top 40 Pesticide findings in 2,592 rice samples analysed in 2019 and MRLs in the EU (past, current and anticipated), the USA, Australia New Zealand and Japan. Chemical Findings Maximum Average MRL (mg/kg) EU current/ EU past Japan Number mg/kg mg/kg anticipated USA Australia NZ (brown rice) (brown rice) (brown rice) Tebuconazol 583 0.670 0.031 1.5 1.5 zero tol. 0.2 0.1 Imidacloprid 461 0.190 0.020 1.5 (0.01) * zero tol. 0.1 Tricyclazole 366 0.250 0.042 1 0.01 3 3 Isoprothiolane 364 0.980 0.091 5 6 zero tol. 10 Propiconazole 342 0.230 0.016 1.5 (0.01) * 7 0.1 0.1 Buprofezin 300 0.120 0.020 0.5 0.01 1.5 0.1 0.5 Chlorpyrifos (-ethyl) 294 0.650 0.027 0.5 (0.01) * zero tol. 0.1 0.1 Carbendazim 279 0.076 0.013 0.01 0.01 zero tol. 2** 1 Thiamethoxam 267 0.110 0.023 0.01 0.01 6 0.01 0.3 Difenoconazole 185 0.260 0.015 3 3 7 0.01 0.1 Azoxystrobin 170 0.480 0.021 5 5 5 0.1 0.2 Triazophos 115 0.085 0.013 0.02 0.02 zero tol. Acetamiprid 108 0.083 0.015 0.01 0.01 zero tol. 0.1 Malathion 107 59.800 1.610 8 (0.01) * 8 8 0.1 Profenofos 79 0.057 0.010 0.01 0.01 zero 0.02 Trifloxystrobin 75 0.260 0.017 5 5 3.5 0.1 3 Carbofuran 66 0.006 0.001 0.01 0.01 0.2 0.2 0.1 Clothianidin 65 0.028 0.006 0.5 (0.01) * 0.01 1 Piperonyl butoxide 64 0.940 0.065 synergist, no MRL set 20 20 24 Acephate 59 0.200 0.018 0.01 0.01 zero tol. Quinclorac 56 0.075 0.011 5 5 5 5 5 4-Bromo-2-Chlorophenol 52 0.150 0.012 profenofos metabolite, no MRL set Hexaconazole 37 0.028 0.008 0.01 0.01 zero tol. Fenobucarb 36 0.065 0.009 0.01 0.01 zero tol. 1 Pirimiphos-methyl 36 0.270 0.013 0.5 0.5 zero tol. 10 / 2 / 1 *** 0.2 Fipronil 33 0.054 0.007 0.01 0.01 0.04 0.01 0.01 Diphenylamine 32 0.058 0.021 0.1 0.1 zero tol. Flubendiamide 23 0.140 0.031 0.2 0.2 0.5 0.1 Methamidophos 23 0.034 0.011 0.01 0.01 zero tol. Dichlorvos 22 0.120 0.032 0.01 0.01 zero tol. 5.00 0.2 Cyhalothrin. lambda 20 0.042 0.015 0.01 0.2 1 0.01 0.5 Dithiocarbamates 18 0.050 0.011 0.1 0.1 indiv. 0.5 0.3 Flutriafol 18 0.037 0.012 1.5 1.5 zero tol. 0.02 2,4-D 16 0.018 0.007 0.1 0.1 0.5 0.2 0.1 Cyproconazole 16 0.063 0.034 0.1 0.1 zero tol. 0.01 0.1 Source: Werner Nader / Graphic: ct 2020 Cypermethrin 14 0.110 0.029 2 2 1.5 1 0.9 Diethyltoluamide 14 0.035 0.011 biocide, no MRL set zero tol. Dinotefuran 12 0.150 0.035 8 8 9 0.02 2 Phorate-sulfoxide 10 0.023 0.008 0.02 0.02 zero tol. 0.1 Thiophanate-methyl 10 0.018 0.005 0.01 0.01 zero tol. * MRL change anticipated for 2020 | ** MRL defined for the husked rice | *** MRL of 10 for rice, 2 for husked and 1 for the polished rice cereal technology 02/2020 I 87
Peer Review Pesticide testing / MRL / rice trade over the last 4 years or are anticipated in the EU, MS (gas chromatography with a mass spectrometer are shown in table 1. Only in two cases the MRL detector). As a consequence, Indian Basmati imports increased (isoprothiolane, from 5 to 6 mg/kg and dropped by 22% or 47,613 metric tons (mt) in the fis- lambda cyhalothrin, from 0.01 to 0.2 mg/kg), for all cal year of 2010/2011 with imports from Pakistan sub- others the MRL was lowered or will be lowered to stituting this volume (figure 2). Assuming an average the default level of 0.01 mg/kg on short term. price of 800 US Dollar (USD) per mt of cargo Basmati rice the financial loss for the Indian rice exporters can 4. Economic impacts of MRLs on the rice be estimated to 38 million USD. After an EFSA evalu- trade – example Basmati rice ation of the chemical, revealing no food safety con- cerns, the MRL was set to 5 mg/kg in July 2012 and In- Frequent MRL changes cause disturbances for interna- dian Basmati imports increased by 105,442 mt or 60% tional trade and the development of Basmati rice im- in the fiscal year 2011/2012, whereas Pakistani im- ports into the EU in figure 2 during the last 10 years ports dropped by 88,285 mt during the same period. is a good example. In 2010 isoprothiolane was de- tected in Indian Basmati rice, but was not included Till 2017 the MRL for tricyclazole in rice was 1 mg/ in the EU MRL list and therefore the default limit of kg, but was lowered to 0.01 mg/kg for all Basmati im- 0.01 mg/kg applied (The Economic Times, 2010, Na- ports after January 1st, 2018, because the fungicide der et al., 2014). It was also not included in the ana- failed the EU wide approval. As a consequence Indi- lytical scope of the laboratories, until the QuEChERS an Basmati rice imports declined and volumes were method (Anastassiades et al., 2003) was adapted to to a large extent substituted by Pakistani Basmati rice in 2010 and the pesticide showed up in the GC- (figure 2). Source: Werner Nader / Graphic: ct 2020 Fig. 2: Imports of Basmati cargo rice from India and Pakistan into the EU (Source: issued import certificates - communication of EU Mem- ber States, Rice News Today, 2020) 88 I cereal technology 02/2020
Source: Werner Nader / Graphic: ct 2020 Pesticide testing / MRL / rice trade Peer Review Source: Werner Nader / Graphic: ct 2020 Fig. 3: Basmati rice imports into the EU from 13.01.2017 till 26.08.2019. Accumulated revenue (a) and market shares of Indian and Pakista- ni Basmati (b) (Source: issued import certificates - communication of EU Member States, Rice News Today, 2020). The accumulating Basmati rice import volumes into Tricyclazole also affected Indian Basmati exports to the EU and the market shares of India and Pakistan the USA, which dropped in the fiscal year 2012/2013 in the period from January 13th, 2017 and August due to residues of this fungicide, but recovered af- 26th, 2019 are shown in figure 3 a and b, respective- ter the import tolerance was increased from 0.01 to ly. In the three months before the deadline of the 3 mg/kg in 2014 (Nader et al., 2014). MRL change, January 1st, 2018, imports of Basma- ti from India increased significantly, flattened im- 5. Diversity of tolerance levels for pesticide mediately thereafter and were then to a great por- residues in organic products tion substituted by imports from Pakistan (figure 3 a). The average market share of Indian Basmati de- Under the current EU regulation (EC) No 834/2007 creased from 73% during 2017 to 28% for the peri- and the repealing regulation (EU) No 2018/848, od from 01.01.2018 to 26.08.2019. The total Basma- which will apply from January 1st, 2021, only plant ti import volume into the EU was 635,243 mt during protection agents are permitted for organic pro- this latter period. Assuming the same market share duction, which have been authorised in accordance for Indian rice exporters as in 2017 their loss in rev- with Regulation (EC) No 1107/2009 and have been enue due to the drop of the MRL for tricyclazole is assessed and found to be compatible with the ob- estimated to 232 million USD at a price of 800 USD jectives and principles of organic production. Cur- per mt. rently these products are listed in annex II of the implementation regulation (EC) No 889/2008 and But also for Pakistani rice exporters there is trouble do not include synthetic chemicals, with some ex- ahead, as the MRL for chlorpyrifos-ethyl (figure 1 h), ceptions for traps and dispensers. Due to their vast commonly detected in their rice, will drop in Octo- applications synthetic plant protection agents be- ber 2020 from 0.5 to 0.01 mg/kg, after it had been came ubiquitous and might occur in traces in or- increased from 0.05 to 0.5 mg/kg just in 2018. Also ganic products by cross contaminations, e.g. due the MRLs of four other pesticides common for rice to drifts from neighbouring conventional farms. will drop to default soon. Propiconazole is now ille- The current and the new EU regulation do not de- gal in the EU and the use of imidacloprid, clothian- fine tolerance levels and leave the interpretation din and malathion (table 1) is restricted to green- of residues to the private sector and national con- houses only due to risks for bees (imidacloprid and trol authorities. Limits are set by Italian law and in clothiandin) and birds (malathion). Belgium by the regional government of Wallonia cereal technology 02/2020 I 89
Peer Review Pesticide testing / MRL / rice trade not even tolerate traces of residues, also not in pro- cessed food. In the USA pesticide residues in organ- ic products are tolerated up to a level of 5% of the corresponding MRL (40 CFR Part 180, see above) under title 7 of the Code of Federal Regulations, section 205.671 (7 CFR § 205.671). This means that pesticides with high MRLs are tolerated in high con- centrations also in organic products, e.g. 1 mg/kg glyphosate in organic soya beans due to the MRL of Graphic: Werner Nader 2020 20 mg/kg. 6. Potential misinterpretation of substances in food as pesticide residues Fig. 4: Natural plant hormone (auxin) indole-3-acetic acid 6.1. Indole-3-acetic acid –natural plant hor- mone or synthetic growth regulator from agri- cultural applications? (Forschungsinstitut für biologischen Landbau (Fi- BL), 2013). In Germany, the Association of Organ- Indole-3-acetic acid (Figure 4) is the most promi- ic Processors, Wholesalers and Retailers defines an nent plant hormone belonging to the group of aux- orientation value of 0.01 mg per kg of the prima- ins. It promotes length growth and root initiation. ry product (Bundesverband Naturkost Naturwaren Synthetic indole-3-acetic acid is used as a plant e.V. (BNN), 2012). Processing affecting the pesticide growth regulator to cause rooting of cuttings of concentration has to be considered and residue lev- plants, e.g. as a power dip on ornamental cuttings. els have to be calculated back to the original prod- Based on unclear toxicological data and indications uct. Up to two synthetic plant protection products of teratogenic effects in animal studies its use in are tolerated as residues in concentrations at the the EU is not approved. Natural concentrations be- orientation value. A measurement uncertainty of tween 0.01 and 0.1 in vegetative plant tissues (Ep- 50 % (relative, EU Commission, SANTE, 2019) can be stein and Ludwig-Müller, 1993) were considered by considered, if the laboratory value exceeds 0.01 mg/ the EFSA during the definition of a MRL of 0.1 mg/ kg. In other member states like the Netherlands the kg. But results from an earlier study by Bandurski national control bodies for organic agriculture do and Schulze (1977) were not taken into account, Graphic: Werner Nader 2020 Fig. 5: The fungicide fosetyl-aluminum (a) and its metabolite phosphonate (oxidation state +4, b). Furthermore 2 other oxidation states in the biogeochemical cycle of phosphorous, phosphinate (oxidation state +1, c) and phosphate (oxidation state +5, d) (Pasek et al., 2014). 90 I cereal technology 02/2020
Pesticide testing / MRL / rice trade Peer Review Table 2: Results of phosphonate analysis at Eurofins Global Control, 1,360 samples, 2017 to 2020. Further 57 samp- les of other products like millet, cacao, lineseed etc. are not listed, as neither fosetyl or phosmet nor phosphonate were detected in them. Total samples fosetyl phosphonate EU MRL > MRL Product tested positive positive average maximum sample number % mg/kg % Rice 522 0 10.2% 1.10 11.00 2 1% Lentil 318 0 14.5% 1.96 18.70 2 2.2% Apple 130 0 32.3% 0.86 5.00 150 0% Chickpea 103 0 39.8% 0.62 4.00 2 3.9% Bean 77 0 28.6% 5.55 34.50 2 10.4% Banana 48 0 33.3% 0.41 0.68 2 0% Quinoa 36 0 11.1% 0.57 3.30 2 5.6% Wheat 34 0 11.8% 0.71 1.30 2 0% Pea 33 0 12.1% 0.60 0.64 2 0% Maize 16 0 25% 0.24 0.33 2 0% Grapefruit 12 0 25% 1.07 1.60 75 0% Grape 6 3 50% 1.73 2.70 100 0% Broccoli 6 2 50% 16.97 28.70 10 33.3% Almond 4 0 75% 3.54 6.20 500 0% Source: Werner Nader / Graphic: ct 2020 Pistachio 4 0 75% 4.05 6.90 500 0% Ginger 3 0 66.7% 0.37 0.37 400 0% Avocado 2 2 100% 21.75 41.90 50 0% Cranberry 2 0 50% 0.58 0.91 2 0% Mango 2 0 50% 0.89 0.89 2 0% Fennel 1 0 100% 0.69 0.69 400 0% Pear 1 0 100% 2.60 2.60 150 0% which revealed much higher concentrations in cere- based on the sum of captan and tetrahydrophthal- al seeds. In rice kernels the plant hormone was de- imid, expressed as captan. But many chemicals can tected in concentrations of 1.7 for free and 2.7 mg/ be also compounds naturally occurring in environ- kg for total indole-3-acetic acid. Maize kernels even ment, by-products of food processing or environ- contained up to 78.5 mg/kg of the total plant hor- mental contaminants rather than residues from mone. It might be speculated that the seeds store pesticide applications. these high amounts of auxin to stimulate rapid length growth of the stem during germination. Ce- Fosetyl-aluminum (figure 5 a) is a fungicide and reals therefore fail the EU MRL regulation by nature. phosphonate (or phosphite) its metabolite (figure 5 b). MRLs in the EU are therefore defined for the 6.2. Phosphonate sum of fosetyl, phosphonic acid and their salts, ex- pressed as fosetyl. This definition also includes po- Numerous chemicals are included in the EU MRL tassium and disodium phosphonate, which are ap- list, which are considered to be metabolites gener- proved for a variety of applications. Due to the low ated by degradation of plant protection products, toxicity of these compounds MRLs between 2 (e.g. e.g. tetrahydrophthalimid, which can be clearly at- for cereals) and 500 mg/kg (e.g. for tree nuts) have tributed to the fungicide captan. The MRL is then been defined in the EU for plant products. EU reg- cereal technology 02/2020 I 91
Peer Review Pesticide testing / MRL / rice trade ulation (EU) 2016/127 defines a limit of 0.01 mg/kg Six hundred seventy two samples were from organ- for residues of most pesticides in infant food and ic agriculture. Of these 71 or 10.6 % exceeded the phosphonate falls under this limit. BNN orientation value. In contrast to the BNN the European Organic Certifiers Council sets the lim- For organic products, the BNN released a fact sheet it for further investigations at 0.2 mg/kg (EOCC, on phosphonic acid, potassium phosphonate and 2018). Even considering this higher limit still 50 or fosetyl-Al (Bundesverband Naturkost Naturwaren, 7.8% of the samples would fail. 2017). When fosetyl is not detected in the sample, BNN considers applications of potassium phospho- But recent scientific data reveal that phosphonate is nate as the most probable source of phosphonate also produced by microorganisms, might occur ubiqui- residues. Potassium phosphonate is applied as a tously in the environment in significant concentra- plant strengthener against fungal infections, partic- tions and can therefore be of natural origin also in ularly in grapes, which is not permitted in the EU for the food. Pasek et al. (2014) analysed water from var- organic production since 2013. An orientation value ious lakes and rivers in Florida and found phospho- of 0.05 mg/kg at the limit of quantification of most nate and phosphinate (figure 5 c) in 28 of 32 samples laboratories was defined by the BNN, above which in significant concentrations of up to 0.46 mg / l or the unauthorized use of plant strengtheners or fer- 33% of the total dissolved phosphorus compounds. tilizers should be investigated at farm level. The Further studies reveal that micro-organisms produce BNN fact sheet argues against a natural occurrence organic and inorganic phosphonates continuously by of phosphonate in the environment in significant reduction of phosphate within biogeochemical phos- concentrations based on expert opinions, which re- phorous cycles (Han et al., 2013, van Mooy et al, fer to the rapid oxidation of phosphonate to phos- 2015). The phosphate (figure 5 d) is regenerated by phate under aerobic conditions (Hofmann, 2012). oxidation of phosphonate either by assimilatory or dissimilatory processes. Figueroa and Coates (2017) Table 2 summarizes the results from testing of 1,417 provided evidence that the bacteria catalysing these samples of different foodstuff from 2017 to 2019. cyclic processes occur ubiquitously. Fosetyl was detected in 7 samples (broccoli, avoca- do and grape juice), but phosphonate in 259 or 18% A study by Varadarajan et al. (2002) furthermore in- of all samples. For pulses (lentils, chickpeas, peas dicates that plants might accumulate phosphonate, and beans) 23% of the samples contained phos- which could explain the high concentrations ob- phonate with an average concen- tration of 2.2 mg/kg and a maxi- mum of 34.5 mg/kg (beans). For cereals (rice, wheat, quinoa and maize) 21.6% of all samples were tested positive for phosphonate with an average concentration of 0.66 mg/kg and a maximum of 11 mg/kg (rice). The EU MRL for the sum of fosetyl and its metabo- Graphic: Werner Nader 2020 lite phosphonate was exceeded in 4.1% of the samples of pulses, 1% of rice and 5.6% of quinoa. All 259 samples would have failed the 0.01 mg/kg limit set for in- fant food. Fig. 6: The fumigation gases methylbromide (a) and phosphane (b) 92 I cereal technology 02/2020
Pesticide testing / MRL / rice trade Peer Review served for certain products in table Graphic: Werner Nader 2020 2. Plants take up phosphate via so- called Pi transporters, which do not differentiate between phosphate and phosphonate. In contrast to phosphate phosphonate cannot be metabolized and will therefore ac- cumulate. Significant concentrations of phos- phonate were found in rice, which is grown submerged under anaero- bic conditions in the root area with a low redox potential. Even higher phosphonate concentrations than in rice are observed in pulses. The Fig. 7: Mepiquat-chloride (a) and phthalimide (b), potentially generated during food cause of these high concentrations processing. Phthalimide is produced under heat from phthalic anhydride (c) and pri- has to be further investigated and mary amines, but can be also a metabolite of the fungicide folpet (d) or the insectici- de phosmet (e). both agricultural applications of phosphonate salts or accumulation of phosphonate produced by mi- cro-organisms naturally seem feasible at present. chemicals have in common that they either rapid- Pasek et al. (2014) reported particularly high con- ly dilute into the atmosphere or decay to chemicals, centrations of phosphonate in anaerobic waters, which also occur naturally in the environment, in which could be also the case in the water flooded particular bromide and phosphorous compounds. paddy fields. Van Mooy et al. (2015) reported that nitrogen-fixing cyanobacteria in the oligotrophic The MRL for inorganic bromide in the EU is 50 surface ocean play a critical role in the reduction mg/kg. According to BNN bromide concentrations of phosphate to organic and inorganic phospho- above 5 mg/kg indicate fumigation with the chem- nate. Legumes live in symbiosis with nitrogen-fixing ical and the source of this high value should be in- bacteria. The BNN fact sheet considers convention- vestigated. But both the EU regulation and the BNN al phosphorous fertilizer as a potential source of guideline do not consider that certain plants might phosphonate, but excludes the ground rock phos- naturally accumulate bromide from the soil in high phate authorized for organic farming as a source. concentrations. Furr et al. (1979) reported bromide We detected phosphonate in concentrations of 0.2 concentrations of 87 mg/kg in Brazil nuts. These mg/kg in a biodynamic fertilizer prepared from cow high concentrations were confirmed in a study per- and sheep manure, which can be also of microbi- formed by the food laboratory Wiertz-Eggert-Jöris- al origin, e.g. from the anaerobic microflora in the sen GmbH (today part of the Eurofins group) on be- foregut of the ruminants. half of the trade association Warenverein e.V. in Hamburg. Samples of Brazil nuts were directly ob- 6.3. Bromide and phosphane, tained from the Peruvian rain forest and concen- residues from fumigation trations of 40 to 190 mg/kg bromide were detected (Warenverein Hamburg, letter, 2015). As a conse- Fumigation with methyl bromide or phosphane (fig- quence a MRL of 200 mg/kg for Brazil nuts was de- ure 6 a and b) is a common procedure to protect fined in the German national regulation for residues food and feed against insect infestations. These in food (Rückstandshöchstmengenverordnung, RH- cereal technology 02/2020 I 93
Peer Review Pesticide testing / MRL / rice trade MVO) which is still valid and contradicts the MRL pan frying of potatoes and vegetables and might of 50 mg/kg defined under EU regulation (EC) No exceed the MRLs of 0.02 mg/kg defined for these 395/2005. foods (Yuan et al., 2017). Recently trace amounts of phosphane below 0.005 The fungicide folpet (figure 7 d) is used broadly mg/kg in rice were interpreted as an indication for the cultivation of grapes, tomatoes and hops. of fumigation, which is not permitted for organ- During analysis the chemical frequently decays to ic products (Stiftung Warentest, 2018). But also a phthalimide (figure 7 b) in the injection system of natural origin of phosphane should be taken into the gas chromatograph. In order to prevent an un- consideration, as recent literature indicates its for- derestimation of its content the EU defined the MRL mation by methanogenic bacteria under anaerobic on the basis of the sum of folpet and phthalimide. conditions (Cao et al., 2017). In 492 out of 3,210 samples of tea and spices ana- 6.4. Mepiquat and phthalimide – chemicals lysed by Eurofins Global Control phthalimide was potentially produced during food processing detected in concentrations above the LOQ (0.01 mg/kg) with a maximum of 0.63 mg/kg. None of the During processing of food products certain chem- samples contained folpet. The insecticide phosmet icals can be formed, which are possibly misinter- (figure 7 e), another potential source of phthalim- preted as pesticide residues. Mepiquat (figure 7 a) ide, was detected in only 2 samples. Phthalimide is a plant growth regulator, which is applied in agri- can be prepared by heating of phthalic anhydride culture to control stem growth, in particular in ce- (figure 7 c) with ammonia or primary amines. This reals and some oils seeds. It is approved in the EU process might also occur during food processing with MRLs of 3 and 4 mg/kg for certain cereals and under heat (drying of tea and herbs, milling of spice up to 40 mg/kg for certain oil seeds, but not al- etc.). Phthalic anhydride and its precursor phthal- lowed in organic agriculture. During roasting of cof- ic acid are used in many technical products and oc- fee the chemical is generated by chemical reac- cur ubiquitously in dusts. In food it finds its reaction tions involving the Maillard reaction and a further partner in the primary amines of the amino acids. N-methylation in concentrations above the MRL for The food laboratory Labor Friedle GmbH detected coffee, 0.2 mg/kg. It is also produced during baking and phthalic anhydride in many different food samples Graphic: Werner Nader 2020 Fig. 8: Chemicals in food frequently caused by cross contaminations: chlorate (a), N,N-Diethyl-meta-toluamide (b), icaridin (c) and nicotine (d) 94 I cereal technology 02/2020
Pesticide testing / MRL / rice trade Peer Review and could even demonstrate a positive correlation are harvested or processed by hand, e.g. pine nut between the phthalimide and phthalic anhydride kernels, berries, wild mushrooms, herbs and spic- concentrations (relana, 2016). es. DEET was detected above 0.01 mg/kg in 33 out of the 3,210 samples of tea and spices, which are Similarly to phosphonate phthalimide rarely ex- mentioned above. The EU plans to set reference val- ceeds the MRLs of the EU. But problems might arise, ues between 0.05 to 1 mg/kg for internal trade with when it is detected in organic food. Therefore the certain products. BNN recommends applying the orientation value only, when folpet or phosmet are also detected in Nicotine (figure 8 d) has been used as a natural in- the sample (Bundesverband Naturkost Naturwaren, secticide and is banned in the EU with a MRL of 0.01 2016). mg/kg for most products. But it might occur in food by cross contaminations, e.g. from hands of smok- 6.5. Chlorate, diethyl-meta-toluamide, ing workers or from air and dust from neighbouring icaridin and nicotine tobacco fields, as was recently shown by Romanot- to et al. (2019) for Indian tea gardens. According- Salts of chlorate (figure 8 a) have been used as non- ly the EU defined higher transition MRLs up to 0.6 selective herbicides and are banned in the EU. A de- mg/kg for tea, wild mushrooms, certain herbs and fault MRL of 0.01 mg/kg applies. But the chemical spices, until the causes of these contents have been can also be generated as a side product in chlorinat- clarified. ed water by disproportionation of chlorine to chlo- ride and chlorate. Since chlorinated drinking wa- 7. Resume ter is a standard in many countries, chlorate can be detected in many food products above the default Imports of Basmati rice from India and Pakistan in- MRL. This even includes rice, which has been pol- to the EU and the USA are good examples for the ished under a mist of water to achieve a silky shine impacts of pesticide MRLs on the trade and rev- of the kernels. Due to the frequent occurrence of enue losses for exporters can be significant, as is chlorate the EU plans to define MRLs above the cur- shown above. In particular, for farmers in these re- rent default limit ranging from 0.05 mg/kg for cere- mote source countries it is difficult to adapt to per- als to 0.7 mg/kg for leaf vegetables, herbs etc. (EU manent changes in MRLs as was shown for the EU Commission, SANTE 10684-2015 rev. 8). Residues of with isoprothiolane, tricyclazole, buprofezin, chlor- disinfectants like chlorate and quarternary ammo- pyrifos-ethyl, propiconazole, imidacloprid, clothian- nium compounds (e.g. didecyldimethylammonium din and malathion. In the USA, zero tolerance was chloride and benzalkonium chloride) in food will be- repealed for tricyclazole, buprofezin and difecona- come even more frequent due to the vast applica- zole, but persists for tebuconazole and isoprothi- tions of these chemicals during the COVID-19 pan- olane. In addition farmers and exporters have to demic. watch developments in other major markets for Basmati rice, the Gulf States, the Iran, Canada and Diethyl-meta-toluamide (DEET) and icaridin (figure 8 b Australia. and c) are common insect repellents, classified as bi- ocides by EU legislation and not covered by regulation Not only for the layman it is difficult to understand, (EC) No 396/2005 with defined MRLs. Until recently they why a product like rice with residues of tricyclazole fell under § 1 (4) Nr. 2 b of the German regulation for and buprofezin slightly above 0.01 mg/kg cannot be maximum limits of residues (RHMVO, Bundesministeri- commercialized in the EU, but is perfect for the US mar- um für Justiz und Verbraucherschutz, 2020) with a de- ket in even 100 fold higher concentrations. Tebucon- fault MRL of 0.01 mg/kg. This limit has been deleted. azole and isoprothiolane cause problems in the USA, The chemicals occur primarily in plant products, which but are totally fine for the EU in high concentrations. cereal technology 02/2020 I 95
Peer Review Pesticide testing / MRL / rice trade Global trade with food and feed products would ben- The diversity and frequent changes of MRLs as well efit from the harmonization of MRLs on a global scale as the misinterpretation of substances suppos- and regulation (EC) No 396/2005 is a good example, as edly resulting from the application of agrochemi- it brought the different residue limits of the member cals have serious implications on the internation- states into line for the common market. But even de- al trade. It is therefore important to permanently spite this harmonization discrepancies persist within question these MRL definitions and to revise them the EU, e.g. for bromide in Brazil nuts with an EU MRL in a flexible and swift manner, not only to avoid fi- of 50 mg/kg and a German MRL of 200 mg/kg. Insect re- nancial losses, but also frustrations about rules, pellents are not considered pesticides under EU law while which might lose sight of the major goals – food until recently they fell under the German national MRL safety and authenticity. regulation with a default limit of 0.01 mg/kg. Authors: Discrepancies are even higher for pesticide tolerance lev- Dr. Werner Nader 1 , Michelle Maier 1 , Dr. Marco els in organic products and also occur among the mem- Miebach2 and Gabriel Linder1 ber states of the common EU market. The new organ- 1 Eurofins Global Control GmbH, Am Neuländer ic regulation (EU) No 2018/848 and its predecessor (EC) Gewerbepark 8, 21079 Hamburg, Germany No 834/2007 do not define tolerance levels and leave 2 Eurofins Dr. Specht Express GmbH, Am Neuländer this to the national control authorities and private sector. Gewerbepark 2, 21079 Hamburg, Germany The current discrepancy of zero tolerance in the Nether- lands and other EU countries in contrast to the German orientation value will persist and traders are treated dif- DOI: 10.23789/1869-2303-2020-2-84 ferently by the control bodies depending into what coun- try they import. References Bromide in Brazil nuts, indole-3-acetic acid in cereals and phthalimide and mepiquat in heat treated food are good Anastassiades M., Lehotay S.J., Stajnbaher D. and examples that the MRL definitions by EU law still require Schenck F.J. (2003): Fast and easy multiresidue further revisions based on scientific evidence, which is al- method employing acetonitrile extraction/parti- ready in the public domain. Similarly the control bodies tioning and dispersive solid-phase extraction for for organic agriculture have to accept that in most cases the determination of pesticide residues in produce. the presence of these substances is natural, adventitious Journal of AOAC International 86(2), 412-431 or technically unavoidable. Anastassiades M., Kolberg, D. I., Eichhorn E., Ben- kenstein A., Wachtler A.-K., Zechmann S., Mack D., The presence of phosphonate in a variety of food re- Wildgrube C., Barth A., Sigalov I., Görlich S., Dörk D. quires further investigations, as recent scientific da- and Cerchia G. (2019): Quick method for the analy- ta reveal that the compound is found in significant sis of numerous highly polar pesticides in foods of concentrations in various environments, might occur plant origin via LC MS/MS involving simultaneous ubiquitously in the environment and is an interme- extraction with methanol (QuPPe Method). EU Ref- diate in a biogeochemical phosphorous cycle driv- erence Laboratory for Pesticides requiring Single en by microorganisms. High concentrations in cer- Residue Methods, https://www.eurl-pesticides.eu/ tain crops like rice and pulses (table 2) might be ex- userfiles/file/EurlSRM/meth_QuPPe-PO_EurlSRM. plained with the efficient uptake of the substance pdf. Last checked March 28, 2020 by plant Pi transporters (Varadarajan et al., 2002). Australia New Zealand Food Standards Code, Sched- Notwithstanding agricultural applications are most ule 20 (2020): Maximum residue limits. https:// probable in many instances and have to be always www.legislation.gov.au/Details/F2020C00200. Last considered. checked March 28, 2020 96 I cereal technology 02/2020
Pesticide testing / MRL / rice trade Peer Review Bandurski R.S. and Schulze A. (1977): Concentration labelling and control. Official Journal of the Europe- of indole-3-acetic acid and its derivatives in plants. an Union L250, 1–83 Plant Physiology 60, 211-213 Commission delegated Regulation (EU) 2016/127 as Bremmers H., van der Meulen B, Wijnands J. and regards the specific compositional and information Poppe K. (2011): A legal-economic analysis of in- requirements for infant formula and follow-on for- ternational diversity in food safety legislation: con- mula and as regards requirements on information tent and impact. European Food and Feed Law Re- relating to infant and young child feeding. Official view 1, 41-50 Journal of the European Union L25, 1–29 Bryant Christie Inc.: Pesticide MRLS. https://www. Council Regulation (EC) No 834/2007 of 28 June bryantchristie.com/BCGlobal-Subscriptions/Pesti- 2007 on organic production and labelling of or- cide-MRLs. Last checked March 28, 2020 ganic products and repealing Regulation (EEC) No Bundesministerium für Justiz und Verbrauch- 2092/91834/2007. Official Journal of the European erschutz (2020): Verordnung über Höchstmen- Union L189, 1–23 gen an Rückständen von Pflanzenschutz- und Electronic Code of Federal Regulations (2020): Tol- Schädlingsbekämpfungsmitteln, Düngemitteln und erances and exemptions for pesticide chemical resi- sonstigen Mitteln in oder auf Lebensmitteln, RHMV. dues in food. Title 40, Chapter I, Subchapter E, Part http://www.gesetze-im-internet.de/rhmv_1994/. 180. https://www.ecfr.gov/cgi-bin/text-idx?tpl=/ Last checked March 28, 2020 ecfrbrowse/Title40/40cfr180_main_02.tpl. Last Bundesverband Naturkost Naturwaren e.V., BNN checked March 28, 2020 (2012): BNN Orientation Value for pesticides- a EOCC Factsheet on Phosphonic Acid. https://eocc. guideline to evaluate pesticide residues in organic nu/wp-content/uploads/2019/04/EOCC-Factsheet- products. https://n-bnn.de/sites/default/dateien/ Fosetyl-Phosphonic-Acid.pdf. Last checked March BNN-Orientierungswert_EN_09042019.pdf. Last 28, 2020 checked March 28, 2020 Epstein E., and Ludwig-Müller J. (1993): Indole- Bundesverband Naturkost Naturwaren e.V., BNN 3-butyric acid in plants: occurrence, synthesis, me- (2016): Interpretation guide for phthalimid detec- tabolism and transport. Physiologia Plantarum 88, tion in organic products. https://n-bnn.de/sites/ 382-389 default/dateien/bilder/Downloads/interpretation_ EU pesticide data base (2020). https://ec.europa. guide_Phthalimid_English.pdf. Last checked March eu/food/plant/pesticides/eu-pesticides-database/ 28, 2020 public/?event=homepage&language=EN. L ast Bundesverband Naturkost Naturwaren e.V., BNN checked May 13, 2020 (2017): Fact sheet phosphonic acid, potassium phos- European Commission document SANTE/12682/2019: phonate (potassium salt of phosphonic acid) and fo- Method Validation & Quality Control Procedures for setyl-aluminum. https://n-bnn.de/sites/default/ Pesticide Residues Analysis in Food & Feed. https:// dateien/bilder/Downloads/FactSheet_phosphon- ec.europa.eu/food/sites/food/files/plant/docs/ ic_acid_en_Mai_2017.pdf. Last checked March 28, pesticides_mrl_ guidelines_wrkdoc_2019-12682. 2020 pdf. Last checked March 28, 2020 Cao J., Zhang C., Rong H., Zhao M., Wei W. and Zhao European Commission document SANTE 10684- L. (2017): Study on effects of electron donors on 2015 rev. 8 (2018): Draft Commission Regulation phosphine production from anaerobic activated (EU) …/… of XXX amending Annex III to Regulation sludge. Water 9 (563); doi:10.3390/w9080563 (EC) No 396/2005 of the European Parliament and Commission Regulation (EC) No. 889/2008 of 5 of the Council as regards maximum residue levels September 2008 laying down detailed rules for for chlorate in or on certain products. https://www. the implementation of Council Regulation (EC) No meyerscience.com/images/publikationen/SANTE- 834/2007 on organic production and labelling of or- 10684-2015-Rueckstandsh%C3%B6chstgehalt_ ganic products with regard to organic production, Chlorat.pdf. Last checked March 28, 2020 cereal technology 02/2020 I 97
Peer Review Pesticide testing / MRL / rice trade European Food Safety Authority (2008): Opinion sues on the rice trade. Pages 159 – 176 in: Rice Pro- of the Scientific Panel on Plant Protection prod- cessing – The Comprehensive Guide to Global Tech- ucts and their Residues to evaluate the suitability nology and Innovative Products (J. Sontag, editor). of existing methodologies and, if appropriate, the Erling Verlag, Germany identification of new approaches to assess cumula- Pasek M. A., Sampson J. M. and Atlas Z. (2014). Re- tive and synergistic risks from pesticides to human dox chemistry in the phosphorus biogeochemi- health with a view to set MRLs for those pesticides cal cycle. Proceedings of the National Academy of in the frame of Regulation (EC) 396/2005. The EFSA Sciences of the United States of America, 111(43), Journal 704, 1-84. 15468-15473. Figueroa I.A. and Coates J.D. (2017): Microbial phos- Regulation (EC) No 396/2005 of the European Par- phite oxidation and its potential role in the global liament and of the Council of 23 February 2005 on phosphorus and carbon cycles. Advances in Applied maximum residue levels of pesticides in or on food Microbiology, 98, 93-115 and feed of plant and animal origin and amending Forschungsinstitut für biologischen Landbau (FiBL) Council Directive 91/414/EEC, Official Journal of the (2013): Guideline for handling pesticide residues European Union L70, 1–16 in Czech organic production, final report. https:// Regulation (EC) No 1107/2009 of the European Par- orgprints.org/34119/1/speiser-etal-2013-Residue_ liament and of the Council of 21 October 2009 con- guideline_June_2013.pdf. Last checked March 28, cerning the placing of plant protection products on 2020 the market and repealing Council Directives 79/117/ Furr A.K., MacDaniels L.H., St.John L.E., Gutenmann EEC and 91/414/EEC. Official Journal of the Europe- W.H., Pakkala I.S. and Lisk D.J. (1979) Elemental an Union L309, 1–49 composition of tree nuts. Bulletin of Environmental Regulation (EU) 2018/848 of the European Parlia- Contamination and Toxicology 21, 392–396 ment and of the Council of 30 May 2018 on organ- García Martinez M. and Poole N. (2004): The devel- ic production and labelling of organic products and opment of private fresh produce safety standards: repealing Council Regulation (EC) No 834/2007. Of- implications for developing Mediterranean export- ficial Journal of the European Union L150, 1–95 ing countries. Food Policy 29, 229–255 relana (2016): Phthalimid: metabolite of folpet or Han C., Geng J. Ren H. Gao S., Xie X. and Wang X. unavoidable artifact. Position paper No. 16-03, ver- (2013): Phosphite in sedimentary interstitial wa- sion 2016/07/22 https://www.relana-online.de/ ter of lake Taihu, a large eutrophic shallow lake in wp-content/uploads/2016/07/PP_16-03_Folpet-PI_ China. Environmental Science & Technology 47(11), vers20160722.pdf. Last checked March 28, 2020 5679-5685, https://doi.org/10.1021/es305297y relana (2019): Sources of contamination of sam- Hofmann U. (2012): Kann Kalium-Phosphonat als ples for analysis. Position paper No. 19-01, ver- mineralisch, natürlich vorkommend angesehen sion 2019/04/12 https://www.relana-online.de/ werden? Expert opinion for the Bund Ökologis- wp-content/uploads/2019/04/relana-pos.-paper- che Lebensmittelwirtschaft e.V. (BÖLW). https:// 19-01-Sources-of-Contaminations-20190412-final. www.yumpu.com/de/document/view/6035875/gu- pdf. Last checked May 13, 2020 tachten-bund-okologische-lebensmittelwirtschaft. Rice News Today (2020): Latest stats on export of Last checked March 28, 2020 brown (cargo) Basmati rice. http://ricenewstoday. Melo O., Engler A., Nahuehual L., Cofre G. and Bar- com/?page_id=248. Last checked May 13, 2020 rena J. (2014): Do sanitary, phytosanitary, and qual- Romanotto A., Hofmann A., Gassert K., Heidorn T. ity-related standards affect international trade? Ev- and Speer K. (2018): Tabakanbau als Quelle einer idence from Chilean fruit exports. World Develop- Nikotinbelastung indischer Tees. Lebensmittelche- ment 54, 350-359 mie 72, 143-144 Nader W.F., Grote A.-K. and Cuevas Montilla E. Saudi Food and Drug Administration (2019): Maxi- (2014): Impacts of food safety and authenticity is- mum limits of pesticide residues in agricultural and 98 I cereal technology 02/2020
Pesticide testing / MRL / rice trade Peer Review food products. Document SFDA.FD 382:2019 Stif- tung Warentest e.V. Berlin (2018): Auf der Suche nach Spitzenqualität. Zeitschrift Test 9, 10-18 The Economic Times, Mumbai (2010): Basmati ex- porters to haul European testing lab to court for ‘biased’ report. https://economictimes.indiatimes. com/news/economy/foreign-trade/basmati-ex- porters-to-haul-european-testing-lab-to-court- for-biased-report/articleshow/6108527.cms. Last checked May 13, 2020 The Japan Food Chemical Research Foundation (2020): Maximum Residue Limits (MRLs) List of Ag- ricultural Chemicals in Foods, http://db.ffcr.or.jp/ front/. Last checked March 28, 2020 Van Mooy B.A.S., Krupke A., Dyhrman S.T., Fredricks H.F., Frischkorn K.R., Ossolinski J.E., Repeta D. J., Rouco M., Seewald J. D. and Sylva S. P. (2015): Ma- jor role of planktonic phosphate reduction in the marine phosphorus redox cycle. Science 348 (6236), 783-735 Varadarajan D.K., Karthikeyan A.S., Matilda P.D. and Raghothama K.G. (2002): Phosphite, an analog of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiol- ogy 129, 1232-1240 Warenverein der Hamburger Börse e.V., letter dat- ed January 15th, 2015: Bromid in Paranüssen Yuan Y., Tarres A., Bessaire, T., Rademacher, W., Stadler, R.H. and Delatour, T. (2017): Heat-induced formation of mepiquat by decarboxylation of pipec- olic acid and its betaine derivative. Part 2: Natural formation in cooked vegetables and selected food products. Food Chemistry 228, 99-105 cereal technology 02/2020 I 99
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