A influência de 2,4-D e dicamba na fisiologia de mudas de oliveira

pab Pesquisa Agropecuária Brasileira Pesq. agropec. bras. 0100-204X 1678-3921 Embrapa Secretaria de Pesquisa e Desenvolvimento; Pesquisa Agropecuária Brasileira Resumo O objetivo deste trabalho foi avaliar a influência dos herbicidas 2,4-D e dicamba sobre a resposta fisiológica da clorofila a em mudas de oliveira (Olea europaea). As seguintes oito doses dos herbicidas 2,4-D (670 g a.e. ha-1) e dicamba (720 g a.e. ha-1) foram aplicadas: 0, 1,56, 3,13, 6,25, 12, 25, 50 e 100% das recomendadas para dessecação. Os herbicidas foram aplicados a 80 cm acima das mudas, por meio de um pulverizador costal pressurizado a CO2, com 150 L ha-1 de volume de calda. A troca gasosa das plantas foi medida por meio de um medidor portátil analisador de gases por infravermelho. A fluorescência da clorofila a foi avaliada por meio de um fluorômetro portátil de luz modulada. A aplicação de ambos os herbicidas causou diminuição no processo de assimilação de CO2 pelas plantas, o que reduziu a fotossíntese líquida e a condutância estomática. O herbicida 2,4 D causou os efeitos mais severos nas variáveis relacionadas à fluorescência da clorofila a. Baixos valores de rendimento quântico máximo foram observados após a aplicação dos herbicidas, dos quais o dicamba foi o mais prejudicial. Ambos os herbicidas danificam o aparelho fotossintético das mudas de oliveira. Introduction Fruit of olive trees [Olea europaea L., Oleaceae family] can be consumed pickled or as olive oil (Cavalheiro et al., 2014). In the 2020/2021 crop season, Brazil imported about 130,000 tonnes of table olives, and approximately 100,000 tonnes of olive oil (IOC, 2023). This demand is related to nutritional characteristics of the olive oil, which is rich in unsaturated fatty acids, vitamins, and phenolic compounds (El Riachy et al., 2011). The 2,4-D and dicamba have the same mechanism of action as herbicides (Group 4 of the Herbicide Resistance Action Committee ‒ HRAC), but they differ for chemical groups (Alves et al., 2021). These herbicides show differences for their physiological and biochemical effects on different plant species (Patton et al., 2018). The use of these auxin-mimicking herbicides in grain crops has been a problem for orchards, which is caused by drifting, since part of the applied product deviates from its main target and reaches adjacent areas (Godinho Júnior et al., 2017). This usually occurs in hot days, or low relative humidity of the air, or wind speed above 6 km h-1. The drifting problem in trees is frequent, especially after applying auxin-mimicking herbicides, such as 2,4-D and dicamba (Avila Neto et al., 2022). These herbicides are used in grain crops for burndown and weeding, especially the glyphosate and 2,4-D (Robinson et al., 2012). Auxin causes growth anomalies in plants with sensitive broadleaves (Grossmann, 2010). The most common symptoms are branch epinasty and leaf cupping, which can lead to plant death. Injuries due to low rates of 2.4-D and dicamba have been reported in sensitive species such as pecan trees (Wells et al., 2019), 'Ponkan' mandarin seedlings (Brochado et al., 2022), and tomato (Warmund et al., 2022). Few studies evaluated the impacts of these herbicides on the yield and photosynthetic physiology of plants (Brochado et al., 2022). There is a report of drifting of rates as low as 10 g of active ingredient equivalent per hectare (g a.e. ha-1) of dicamba and 2,4-D causing reduction of yield and seed quality in soybean, during the R2 and V5 phenological stages (Silva et al., 2018). Dicamba drifting was observed as reaching areas 250 m away, although it does not usually exceed 20 m (Soltani et al., 2020). In the state of Nebraska, in the USA, a survey found out that dicamba applications carried out in the hottest months had more than 50% chance to cause injury in nontarget areas (Werle et al., 2018). The problem of herbicide drifting in southern Brazil is very recurrent (Hupffer et al., 2020). In the 2019/2020 crop season, plant material was collected from orchards in Rio Grande do Sul state, in order to analyze the presence of pesticides. The results showed the presence of 2,4-D (Pinto, 2020a). In the 2020/2021 crop season, the Secretaria de Agricultura, Pecuária, e Desenvolvimento Rural (SEAPDR) fined approximately 600 producers, professionals, and companies for misusing auxin-mimicking herbicides (Pinto, 2020b). Although there are regulatory instructions on the use of auxin-mimicking herbicides (IN 05/2019) (Rio Grande do Sul, 2019), drifting has been causing problems in orchards in the state of Rio Grande do Sul, Brazil. The objective of this work was to evaluate the influence of herbicides 2,4-D and dicamba on the physiological response of chlorophyll a in olive seedlings. Materials and methods The experiment was carried out in a greenhouse, at the Universidade Federal de Santa Maria (UFSM), from July 2019 to February 2020. 'Koroneiki' olive seedlings of 50 cm height were used. They were transplanted into plastic pots of 7 L containing properly sieved and fertilized Argissoil soil. The fertilization followed recommendations for the olive culture and it was performed as follows: rates equivalent to 100, 60, and 90 kg ha-1 of N, P, and K, respectively (3.5 g N, 2.1 g P, and 3.2 g K, per pot). Pots were kept in the greenhouse for 60 days, where plants reached average 80 cm height of and 4 mm stem diameter. A dry soil was weighed, and saturated with water up to 100%. After three days, the saturated soil was weighed again and properly adjusted, to reach 75% of water retention capacity - WRC (Kämpf et al., 2006), using the following equation: W 75 % = ( W W r C - W dried ) × 0.40 + W dried where: W75% is the pot weight at 75% of WRC; WWRC is the pot weight at WRC (three days after satured soil); Wdried is the pot weight with dry soil. Irrigation was carried out daily to keep the pots at 75% WRC. In order to do that, each pot was weighed daily and water was added until it reached the W75%, if necessary. Every month, urea was added to each pot at an equivalent rate of 100 kg ha-1 N. The experiment was conducted in a completely randomized design with five replicates. Treatments were applied in a 2x8 factorial arrangement, with “herbicide” and “rates” as factors, respectively. The factor “herbicide” was composed of 2,4-D and dicamba. The factor “rates” tested eight levels of each herbicide at 0, 1.56, 3.13, 6.25, 12.5, 25, 50, and 100% of the recommended rates for burndown, that is, 670 g a.e. ha-1 of 2,4-D and 720 g a.e. ha-1 of dicamba. The lower rates simulate the occurrence of herbicide drifting. The experimental unit was the 7 L pots with one olive seedling each. The herbicide was applied using a CO2 pressurized backpack sprayer connected to a 2 m bar containing four XR Teejet 110.015 tips, at 1.76 kgf cm-2 pressure, which resulted in 150 L ha-1 application. The application was made outside the greenhouse. The environment conditions at the moment of the application were: 22.2°C temperature, 67% relative humidity, and 2.5 m s-1 wind speed. After the herbicide application, the pots were placed outside the greenhouse for 24 hours at 10 m distance from each other, to avoid phytotoxicity due to herbicide volatility. After the period of 24 hours, they were brought back into the greenhouse. The following variables were analyzed: gas exchange and chlorophyll a fluorescence. Fluorescence was measured at 24, 48, and 72 hours after application (HAA). Gas exchange was evaluated 30 days after application (DAA). Gas exchange was measured for the following parameters: net photosynthesis (Np); CO2 net assimilation rate (µmol CO2 m-2 s-1); stomatal conductance of water vapors (Gs) (mol H2O m-2 s-1); CO2 intercellular concentration (Ci) (µmol CO2 air mol-1); transpiration rate (Tr) (mol H2O m-2 s-1); and water use efficiency (WUE) [mol CO2 (mol H2O)-1]. WUE was determined according to the ratio between Np and Tr. A LI-COR portable infrared gas analyzer (IRGA), model LI-6400 XT, was used. The measurements were carried out using the last completely expanded leaf of the main stem. The photosynthetic radiation of 2,000 µmol m-2 s-1 and CO2 concentration of 400 µmol mol-1, inside the evaluation chamber of the IRGA’s equipment, were previously determined by increasing curves in which a higher photosynthetic rate was observed (data not shown). Fluorescence emission of chlorophyll a was analyzed using a portable light-modulated fluorometer (Junior Pam Chlorophyll Fluorometer, Heinz Walz, Germany). Leaves were previously adapted to the dark for 30 min, in order to measure the initial fluorescence (F0). After adaptation, a pulse of saturating light (10,000 µmol m-2 s-1) was applied for 0.6 s to determine the maximum fluorescence (Fm), the maximum quantic yield (MQY) of the photosystem II (PSII), and the variable fluorescence (Fv). Data were analyzed for normality and homoscedasticity, using the Shapiro-Wilk’s test and the O’neill-Matthews’ test, respectively. A factorial analysis of variance (α=0.05) was carried out using the statistical software R (R Core Team, 2022), and the ExpDes package (Ferreira et al., 2011). Once statistical significance was found, the means were compared, using the Scott-Knott’s test (α=0.05). Results and discussions All variables met the statistical assumptions tests. Significant relationships were observed as the following descriptions: between rates and net photosynthesis (Np), and between herbicides and Np, in the analyses performed at 24, 48, 72 HAA (Figure 1 A, B, and C); between dose and stomatal conductance of water vapors (Gs), and between herbicides and Gs, for the analysis performed at 48 HAA (Figure 1 D); between rates and internal CO2 concentration (Ci), in the analysis performed at 24 HAA (Figure 2 F); and between herbicides and internal CO2 concentration (Ci), in the analyses performed at 24 HAA (Figure 3A) and 48 HAA (Figure 3 B). Figure 1 Net photosynthesis of olive (Olea europaea) seedlings measured at the following times after treatment: (A) 24, (B) 48, (C) 72 hours. Stomatal conductance measured at 48 hours after treatment (D) of 2,4-D and dicamba. Uppercase letters indicate compared rates of each herbicide, and lowercase letters indicate compared herbicides, by Scott-Knott’s test, at 5% probability. Figure 2 Simple effect of 2,4-D and dicamba doses on olive (Olea europaea) seedlings, after application time: on the stomatal conductance, at 72 hours (A); on transpiration rate, at 24, 48 and 72 (B, C, and D); on the water use eficciency, at 24 h (E); and on the internal CO2 concentration at 24 h (F). Lowercase letters compared rates of herbicides, by Scott-Knott’s test, at 5% probability. Figure 3 Simple effect of 2,4-D and dicamba application, on the following variables of olive (Olea europaea) seedlings: internal CO2 concentration, measured at 24 (A) and 48 hours (B); initial fluorescence, at 24 (C) and 48 hours (D); fluorescence, measured at 24 hours (E); maximum fluorescence, measured at 48 hours (F); and maximum quantum yield of the PSII, measured at 24 (G) and 48 hours (H). Lowercase letters compared the herbicides, by Scott-Knott’s test, at 5% probability. There were also significant relationships between rates and initial fluorescence (F0), in the analysis at 24 HAA (Figure 4 A), and between herbicides and F0 in the analyses at 24 HAA (Figure 3 C) and 48 HAA (Figure 3 D). Significant relationships were also observed between rates and variable fluorescence (Fv), in the analysis at 24 HAA (Figure 4 B), and between herbicides and Fv, in the analysis at 24 HAA (Figure 3 E). Figure 4 Simple effect of 2,4-D and dicamba application on the following variables of olive (Olea europaea) seedlings: initial fluorescence measured at 48 hours after treatment (A); fluorescence measured at 24 hours after treatment (B); and maximum quantum yield of the photosystem II, measured at 24, 48 and 72 hours after treatment (C, D, and E). Lowercase letters compared rates of the herbicides, by Scott-Knott’s test, at 5% probability. Significant relationships were also found between herbicides and maximum fluorescence (Fm), in the analysis at 48 HAA (Figure 3 F); and between herbicides and maximum quantum yield (MQY) of photosystem II, in the analyses at 24 HAA (Figure 3 G) and 48 HAA (Figure 3 H). For Np, the evaluation carried out at 24 HAA showed a general increase of the values for both herbicides, according to the increase of their dose compared to the zero dose (Figure 1 A). The application of both herbicides resulted in decreases of the Np values, in comparison with the control, in the evaluation carried out at 48 HAA, and such decreases were more pronounced for the herbicide 2,4-D (Figure 1 B). In the other evaluations, the same decrease pattern was maintained for the herbicide 2,4-D. The evaluation carried out at 48 HAA showed that plants that received rates above 12.5% of the herbicide 2,4-D had Gs values decreased by about 60%, in comparison to the controls, with no such effect when dicamba was applied (Figure 1 D). There was a simple dose effect on the evaluation carried out at 72 HAA. Regardless of the herbicide applied, rates from 6.25% caused stress to the plants, decreasing the stomatal conductance values (Figure 4A ). The WUE showed a simple dose effect in the evaluation carried out at 24 HAA (Figure 2 E), with a decrease in its values from the dose of 1.56%, which was proportional to the increase in the dose of herbicides. The analysis performed at 24 HAA showed a simple dose and herbicide effects for the Ci variable, for which the values decreased by 30% in relation to the others from the dose of 3.13% (Figures 2 F and 3 A). Herbicide 2,4-D showed lower values in comparison with dicamba, and the same fact occurred in the evaluation carried out at 48 HAA (Figure 3 B). For variables related to chlorophyll a fluorescence, dicamba had a slight increase of the values for F0, showing that the plants suffered more significant stresses than those subjected to 2,4-D (Figure 3 C and D). The same behavior was verified for Fv, which showed a simple dose and herbicide effects only in the evaluation carried out at 24 HAA, when it was possible to observe that all rates applied displayed no variation in the values of Fv (Figures 3 E and 4 B). Likewise, for Fm, for which only the evaluation carried out at 48 HAA showed a simple herbicide effect, it was evident that dicamba was responsible for causing a more significant stress effect on the plants in the variables analyzed (Figure 3 F), regardless of the dose, as already seen for F0. In the analysis at 24 HAA, 2,4-D was responsible for the lowest values. At 48 HAA, dicamba obtained the lowest value of the relationship. At 72 HAA, both herbicides had the same value of MQY, leading to the conclusion that plants were under stress regardless of the herbicide applied. Photosynthesis and vegetative growth are linked, and when photosynthesis is inhibited under adverse conditions, such as damage caused by herbicide, the vegetative growth slows significantly. Stomata are the main channels of gas exchange between leaves and the environment, and the reduction in Gs due to the application of herbicides contributes to the loss of photosynthesis in olive plants. The analysis of dicamba at 72 HAA showed a decreased Np for plants that received rates above 25.00% (Figure 1 C). Decrease of Np about 51% was also observed when this herbicide was applied to wheat plants, in comparison with the control (Agostinetto et al., 2016). It seems that olive trees are susceptible to damage caused by the 2,4-D herbicide. In addition, the application of herbicides results in low Gs (Agostinetto et al., 2016), since they promote stomatal closure, resulting in lower O2 and CO2 flow to the cells, consequently decreasing photosynthesis. However, at 30 DAA, the plants that received 2,4-D herbicide showed a decrease of Gs, when using the 25.00% dose. At the other doses, there was an increase in the Gs value, indicating that the plants recovered after this evaluation period. In a similar study, dicamba caused a greater damage than 2,4-D on the photosynthetic apparatus of Brazilian peppertree (Schinus terebinthifolius Raddi), mainly on the net assimilation rate of CO2, stomatal conductance, intercellular CO2 concentration, transpiration rate, carboxylation efficiency of Rubisco, and on the fluorescence emission of chlorophyll a (Avila Neto et al., 2022). Dicamba also had the most phytotoxicity effect on non-herbicide tolerant soybean, on a simulated drifting trial (Brochado et al., 2023). As for broccoli (Brassica oleracea L.), low rates of 2,4-D (16.8 g ha-1) reduced 50% of total yield and showed more prominent phytotoxicity than dicamba (Mohseni-Moghadam & Doohan, 2015). These results suggest the potential of damage of low rates of auxin-mimicking herbicides in olive trees. A decrease in the values from the dose of 12.50% of the herbicides is evidenced for Tr, in the evaluations carried out at 48 and 72 HAA (Figure 2), showing that the plants decreased their transpiration after stomatal closure, since both variables are closely linked (Alves et al., 2019). Thus, the higher is the dose of the herbicide applied, the lower will be the Tr obtained. Auxin-mimicking herbicides take three weeks on average, to cause the death of weeds. However, even if some plants did not die, sensitive plants exposed to them, in the present work, underwent negative effects after 30 days of herbicide application. This can be explained by the fact that these herbicides act on the plant physiology, leading to stomatal closure and consequent decrease of the plant metabolism, even after a long time of application (Grossmann, 2010). That water use efficiency is directly related to stomatal closure and higher values for this parameter are found while the stomata are open (Araldi et al., 2012). In case the stomata are closed, the plants decrease the WUE, decreasing the amount of transpired water and, consequently, the production of dry matter (Machado et al., 2010). The internal concentration of CO2 is closely linked to the stomata, since, when closed (Ferraz et al., 2012), they decrease the intake of CO2, decreasing its values, subsequently interfering with the photosynthetic rate of the plants. The initial fluorescence indicates the energy absorbed by the antenna-complex not transmitted to photosynthetic pigments (Rascher et al., 2000). The values of F0 are not always constant, since they can increase if some damage occurs to the PSII reaction centers (Ferreira et al., 2015). Therefore, in the present work, the F0 low values indicate that the herbicide applications caused no damage to the PSII reaction centers, at 48 HAA. It was possible to observe a decrease for the values of MQY from the dose of 1.56% compared with the control (Figure 4 C, D, and E). When this happens, will be a reduction in the amount of energy used by the plant to perform photosynthesis (Catunda et al., 2005). Emissions of chlorophyll a are related to the state of PSII, which plays a vital role in plant photosynthesis (Buonasera et al., 2011). Low values of the potential quantum efficiency of PSII indicate damage to the photosynthetic apparatus of plants (Marques et al., 2020), which occurred in the present work, from the application of herbicides 2,4-D and dicamba on olive seedlings. Thus, the decrease of stomatal conductance directly affected Ci, WUE, and Tr (Figure 1), consequently decreasing Np (Cui et al., 2020), as seen in this work, when simulating herbicide drifting. Rates from 12.50% for both herbicides significantly affected the stomata conductance, net CO2 assimilation rate, transpiration rate, and initial fluorescence, and all in the initial analysis at 24 HAA. Dicamba influenced all other variables, except for WUE at 48 and 72 HAA, and intercellular CO2 concentration at 30 DAA. These results confirm the above mentioned, since, while the herbicide 2,4-D affected the variables related to gas exchange, the herbicide dicamba affected the variables related to PSII. In addition, it was evident that the plants were under stress, concerning the variables referring to chlorophyll a fluorescence, since the MQY showed lower values after applying the herbicides. Conclusions The drifting of auxin-mimicking herbicides causes damage to the photosynthetic apparatus of plants, as indicated by the low values of net photosynthesis, stomatal conductance of water vapors, and CO2 intercellular concentration. Herbicide 2,4-D decreases the gas exchange (stomatal conductance of water vapors, water use efficiency, transpiration rate, CO2 intercellular concentration, and net photosynthesis), and dicamba decreases the chlorophyll a fluorescence (initial fluorescence, variable fluorescence, maximum fluorescence, and maximum quantic yield). Acknowledgments To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), for financing, in part, this study (Finance Code 001). References AGOSTINETTO, D.; PERBONI, L.T.; LANGARO, A.C.; GOMES, J.; FRAGA, D.S.; FRANCO, J.J. Changes in photosynthesis and oxidative stress in wheat plants submmited to herbicides application. Planta Daninha, v.34, p.1-9, 2016. DOI: https://doi.org/10.1590/S0100-83582016340100001. AGOSTINETTO D. PERBONI L.T. LANGARO A.C. GOMES J. FRAGA D.S. FRANCO J.J. Changes in photosynthesis and oxidative stress in wheat plants submmited to herbicides application Planta Daninha 34 1 9 2016 https://doi.org/10.1590/S0100-83582016340100001 ALVES, C.; GALON, L.; HOLZ, C.M.; KAIZER, R.R.; WINTER, F.L.; CONCENÇO, G.; NONEMACHER, F.; PERIN, G.F. Características fisiológicas de plantas hibernais com potencial fitorremediador sob influência dos herbicidas fomesafen e sulfentrazone. Revista de Ciências Agroveterinárias, v.18, p.1-12, 2019. DOI: https://doi.org/10.5965/223811711812019001. ALVES C. GALON L. HOLZ C.M. KAIZER R.R. WINTER F.L. CONCENÇO G. NONEMACHER F. PERIN G.F. Características fisiológicas de plantas hibernais com potencial fitorremediador sob influência dos herbicidas fomesafen e sulfentrazone Revista de Ciências Agroveterinárias 18 1 12 2019 https://doi.org/10.5965/223811711812019001 ALVES, T.A.; ROBERTO, C.E.O.; PINHEIRO, P.F.; ALVES, T.A.; HENRIQUE, M.K.C.; FERREIRA, A.; CLARINDO, W.R.; PRACA-FONTES, M.M. Searching na auxin herbicide to use as positive control in toxicity assays. Anais da Academia Brasileira de Ciências, v.93, e20181262, 2021. DOI: https://doi.org/10.1590/0001-3765202120181262. ALVES T.A. ROBERTO C.E.O. PINHEIRO P.F. ALVES T.A. HENRIQUE M.K.C. FERREIRA A. CLARINDO W.R. PRACA-FONTES M.M. Searching na auxin herbicide to use as positive control in toxicity assays Anais da Academia Brasileira de Ciências 93 e20181262 2021 https://doi.org/10.1590/0001-3765202120181262 ARALDI, R.; GIROTTO, M.; VELINI, E.D.; GOMES, G.L.G.C.; JASPER, S.P.; CARBONARI, C.A.; TRINDADE, M.L.B. Eficiência fotossintética e consumo de água de Ipomoea triloba após aplicação de herbicidas. Planta Daninha, v.30, p.517-524, 2012. DOI: https://doi.org/10.1590/S0100-83582012000300007. ARALDI R. GIROTTO M. VELINI E.D. GOMES G.L.G.C. JASPER S.P. CARBONARI C.A. TRINDADE M.L.B. Eficiência fotossintética e consumo de água de Ipomoea triloba após aplicação de herbicidas Planta Daninha 30 517 524 2012 https://doi.org/10.1590/S0100-83582012000300007 AVILA NETO, R.C.; BERGHETTI, A.L.P.; TAROUCO, C.P.; HOLKEM, A.S.; NICOLOSO, F.T.; ARAUJO, M.M.; ULGUIM, A. da R. Phytotoxicity and physiological changes in Schinus terebinthifolius Raddi under simulated 2,4-D drift and dicamba. Revista Ceres, v.69, p.314-322, 2022. DOI: https://doi.org/10.1590/0034-737X202269030009. AVILA R.C. NETO BERGHETTI A.L.P. TAROUCO C.P. HOLKEM A.S. NICOLOSO F.T. ARAUJO M.M. ULGUIM A. da R. Phytotoxicity and physiological changes in Schinus terebinthifolius Raddi under simulated 2,4-D drift and dicamba Revista Ceres 69 314 322 2022 https://doi.org/10.1590/0034-737X202269030009 BROCHADO, M.G. da S.; GUIDI, Y.M.; LIMA, A. da C.; MEDEIROS, B.A. de P.; D’ANGIERI, R.; MENDES, K.F. Can herbicides of different mode of action cause injury symptoms in non-herbicide-tolerant young soybean due to simulated drift? Journal of Environmental Science and Health, Part B, v.58, p.726-746, 2023. DOI: https://doi.org/10.1080/03601234.2023.2275512. BROCHADO M.G. da S. GUIDI Y.M. LIMA A. da C. MEDEIROS B.A. de P. D’ANGIERI R. MENDES K.F. Can herbicides of different mode of action cause injury symptoms in non-herbicide-tolerant young soybean due to simulated drift? Journal of Environmental Science and Health, Part B 58 726 746 2023 https://doi.org/10.1080/03601234.2023.2275512 BROCHADO, M.G. da S.; MIELKE, K.C.; PAULA, D.F. de; LAUBE, A.F.S.; ALCÁNTARA-DE LA CRUZ, R.; GONZATTO, M.P.; MENDES, K.F. Impacts of dicamba and 2,4-D drift on 'Ponkan' mandarin seedlings, soil microbiota and Amaranthus retroflexus. Journal of Hazardous Materials Advances, v.6, art.100084, 2022. DOI: https://doi.org/10.1016/j.hazadv.2022.100084. BROCHADO M.G. da S. MIELKE K.C. PAULA D.F. de LAUBE A.F.S. ALCÁNTARA-DE LA CRUZ R. GONZATTO M.P. MENDES K.F. Impacts of dicamba and 2,4-D drift on 'Ponkan' mandarin seedlings, soil microbiota and Amaranthus retroflexus Journal of Hazardous Materials Advances 6 art.100084 2022 https://doi.org/10.1016/j.hazadv.2022.100084 BUONASERA, K.; LAMBREVA, M.; REA, G.; TOULOUPAKIS, E.; GIARDI, M.T. Technological applications of chlorophyll a fluorescence for the assessment of environmental pollutants. Analytical and Bioanalytical Chemistry, v.401, p.1139-1151, 2011. DOI: https://doi.org/10.1007/s00216-011-5166-1. BUONASERA K. LAMBREVA M. REA G. TOULOUPAKIS E. GIARDI M.T. Technological applications of chlorophyll a fluorescence for the assessment of environmental pollutants Analytical and Bioanalytical Chemistry 401 1139 1151 2011 https://doi.org/10.1007/s00216-011-5166-1 CATUNDA, M.G.; FREITAS, S.P.; OLIVEIRA, J.G.; SILVA, C.M.M. Efeitos de herbicidas na atividade fotossintética e no crescimento de abacaxi (Ananas comossus). Planta Daninha, v.23, p.115-121, 2005. DOI: https://doi.org/10.1590/S0100-83582005000100014. CATUNDA M.G. FREITAS S.P. OLIVEIRA J.G. SILVA C.M.M. Efeitos de herbicidas na atividade fotossintética e no crescimento de abacaxi (Ananas comossus Planta Daninha 23 115 121 2005 https://doi.org/10.1590/S0100-83582005000100014 CAVALHEIRO, C.V.; ROSSO, V.D.; PAULUS, E.; CICHOSKI, A.J.; WAGNER, R.; MENEZES, C.R. de; BARIN, J.S. Composição química de folhas de oliveira (Olea europaea L.) da região de Caçapava do Sul, RS. Ciência Rural, v.44, p.1874-1879, 2014. DOI: https://doi.org/10.1590/0103-8478cr20131139. CAVALHEIRO C.V. ROSSO V.D. PAULUS E. CICHOSKI A.J. WAGNER R. MENEZES C.R. de BARIN J.S. Composição química de folhas de oliveira (Olea europaea L.) da região de Caçapava do Sul, RS Ciência Rural 44 1874 1879 2014 https://doi.org/10.1590/0103-8478cr20131139 CUI, C.; XIE, X.; WANG, L.-Y.; WANG, R.-L.; LEI, W.; LV, J.; CHEN, L.; GAO, H.-H.; UE, S.; HUANG, L.; ZHOU, Q.Y. Photosynthetic index and nitrogen assimilation in rapeseed seedlings transplanted in soil with ammonium glufosinate. Ciência Rural, v.50, e20180911, 2020. DOI: https://doi.org/10.1590/0103-8478cr20180911. CUI C. XIE X. WANG L.-Y. WANG R.-L. LEI W. LV J. CHEN L. GAO H.-H. UE S. HUANG L. ZHOU Q.Y. Photosynthetic index and nitrogen assimilation in rapeseed seedlings transplanted in soil with ammonium glufosinate Ciência Rural 50 e20180911 2020 https://doi.org/10.1590/0103-8478cr20180911 EL RIACHY, M.; PRIEGO-CAPOTE, F.; LEÓN, L.; RALLO, L.; LUQUE DE CASTRO, M.D. Hydrophilic antioxidants of virgin olive oil. Part 1: Hydrophilic phenols: a key factor for virgin olive oil quality. European Journal of Lipid Science and Technology, v.113, p.678-691, 2011. DOI: https://doi.org/10.1002/ejlt.201000400. EL RIACHY M. PRIEGO-CAPOTE F. LEÓN L. RALLO L. LUQUE DE CASTRO M.D. Hydrophilic antioxidants of virgin olive oil. Part 1: Hydrophilic phenols: a key factor for virgin olive oil quality European Journal of Lipid Science and Technology 113 678 691 2011 https://doi.org/10.1002/ejlt.201000400 FERRAZ, R.L. de S.; MELO, A.S. de; SUASSUNA, J.F.; BRITO, M.E.B. de; FERNANDES, P.D.; NUNES JÚNIOR, E. da S. Trocas gasosas e eficiência fotossintética em ecótipos de feijoeiro cultivados no Semiárido. Pesquisa Agropecuária Tropical, v.42, p.181-188, 2012. DOI: https://doi.org/10.1590/S1983-40632012000200010. FERRAZ R.L. de S. MELO A.S. de SUASSUNA J.F. BRITO M.E.B. de FERNANDES P.D. NUNES E. da S. JÚNIOR Trocas gasosas e eficiência fotossintética em ecótipos de feijoeiro cultivados no Semiárido Pesquisa Agropecuária Tropical 42 181 188 2012 https://doi.org/10.1590/S1983-40632012000200010 FERREIRA, E.A.; MATOS, C. da C. de; BARBOSA, E.A.; SILVA, D.V.; SANTOS, J.B. dos; PEREIRA, G.A.M.; FARIA, A.T.; SILVA, C.T. da. Respostas fisiológicas da mandioca à aplicação de herbicidas. Semina: Ciências Agrárias, v.36, p.645-656, 2015. DOI: https://doi.org/10.5433/1679-0359.2015v36n2p645. FERREIRA E.A. MATOS C. da C. de BARBOSA E.A. SILVA D.V. SANTOS J.B. dos PEREIRA G.A.M. FARIA A.T. SILVA C.T. da. Respostas fisiológicas da mandioca à aplicação de herbicidas Semina: Ciências Agrárias 36 645 656 2015 https://doi.org/10.5433/1679-0359.2015v36n2p645 FERREIRA, E.B.; CAVALCANTI, P.P.; NOGUEIRA, D.A. Experimental designs: um pacote R para análise de experimentos. Revista da Estatística da Universidade Federal de Ouro Preto, v.1, p.1-9, 2011. FERREIRA E.B. CAVALCANTI P.P. NOGUEIRA D.A. Experimental designs: um pacote R para análise de experimentos Revista da Estatística da Universidade Federal de Ouro Preto 1 1 9 2011 GODINHO JÚNIOR, J. de D.; VIEIRA, L.C.; PEREIRA, L.O.A.; RUAS, R.A.A.; FARIA, V.R.; CARVALHO FILHO, A. Deriva do herbicida 2,4-D aplicado com pontas hidráulicas de jato plano tipo leque. Revista Brasileira de Ciências Agrárias, v.12, p.550-554, 2017. DOI: https://doi.org/10.5039/agraria.v12i4a5470. GODINHO J. de D. JÚNIOR VIEIRA L.C. PEREIRA L.O.A. RUAS R.A.A. FARIA V.R. CARVALHO A. FILHO Deriva do herbicida 2,4-D aplicado com pontas hidráulicas de jato plano tipo leque Revista Brasileira de Ciências Agrárias 12 550 554 2017 https://doi.org/10.5039/agraria.v12i4a5470 GROSSMANN, K. Auxin herbicides: current status of mechanism and mode of action. Pest Management Science, v.66, p.113-120, 2010. DOI: https://doi.org/10.1002/ps.1860. GROSSMANN K. Auxin herbicides: current status of mechanism and mode of action Pest Management Science 66 113 120 2010 https://doi.org/10.1002/ps.1860 HUPFFER, H.M.; FIGUEIREDO, J.A.S.; WEYERMULLER, A.R. Conflito e construção de riscos na sociedade complexa e globalizada: o caso da deriva do herbicida 2,4-D. Revista de Direito Brasileira, v.25, p.120-142, 2020. DOI: https://doi.org/10.26668/IndexLawJournals/2358-1352/2020.v25i10.5697. HUPFFER H.M. FIGUEIREDO J.A.S. WEYERMULLER A.R. Conflito e construção de riscos na sociedade complexa e globalizada: o caso da deriva do herbicida 2,4-D Revista de Direito Brasileira 25 120 142 2020 https://doi.org/10.26668/IndexLawJournals/2358-1352/2020.v25i10.5697 IOC. International Olive Council. Economic affairs & promotion unit. Madrid, 2023. Available at: <https://www.internationaloliveoil.org/what-we-do/economic-affairs-promotion-unit/#figures>. Accessed on: Nov. 1 2023. International Olive Council Economic affairs & promotion unit Madrid 2023 Available at: <https://www.internationaloliveoil.org/what-we-do/economic-affairs-promotion-unit/#figures>. Accessed on: Nov. 1 2023 KÄMPF, A.N.; TAKANE, R.J.; SIQUEIRA, P.T.V. de. Floricultura: técnicas de preparo de substratos. Brasília: LK, 2006. 132p. KÄMPF A.N. TAKANE R.J. SIQUEIRA P.T.V. de. Floricultura: técnicas de preparo de substratos Brasília LK 2006 132 MACHADO, A.F.L.; FERREIRA, L.R.; SANTOS, L.D.T.; FERREIRA, F.A.; VIANA, R.G.; MACHADO, M.S.; FREITAS, F.C.L. Eficiência fotossintética e uso da água em plantas de eucalipto pulverizadas com glyphosate. Planta Daninha, v.28, p.319-327, 2010. DOI: https://doi.org/10.1590/S0100-83582010000200011. MACHADO A.F.L. FERREIRA L.R. SANTOS L.D.T. FERREIRA F.A. VIANA R.G. MACHADO M.S. FREITAS F.C.L. Eficiência fotossintética e uso da água em plantas de eucalipto pulverizadas com glyphosate Planta Daninha 28 319 327 2010 https://doi.org/10.1590/S0100-83582010000200011 MARQUES, R.F.; PINHEIRO, G.H.R.; ARAÚJO, P.P. dos S.; SOUZA, R.M. de; MARCHI, S.R. de. Efeito de subdoses de 2,4-D sal colina na eficiência quântica do fotossistema II do algodoeiro. Colloquium Agrariae, v.16, p.60-71, 2020. DOI: https://doi.org/10.5747/ca.2020.v16.n2.a359. MARQUES R.F. PINHEIRO G.H.R. ARAÚJO P.P. dos S. SOUZA R.M. de MARCHI S.R. de. Efeito de subdoses de 2,4-D sal colina na eficiência quântica do fotossistema II do algodoeiro Colloquium Agrariae 16 60 71 2020 https://doi.org/10.5747/ca.2020.v16.n2.a359 MOHSENI-MOGHADAM, M.; DOOHAN, D. Response of bell pepper and broccoli to simulated drift rates of 2,4-D and dicamba. Weed Technology, v.29, p.226-232, 2015. DOI: https://doi.org/10.1614/WT-D-14-00105.1. MOHSENI-MOGHADAM M. DOOHAN D. Response of bell pepper and broccoli to simulated drift rates of 2,4-D and dicamba Weed Technology 29 226 232 2015 https://doi.org/10.1614/WT-D-14-00105.1 PATTON, A.J.; WEISENBERGER, D.V.; SCHORTGEN, G.P. 2,4-D- Resistant buckhorn plantain (Plantago lanceolate) in managed turf. Weed Technology, v.32, p.182-189, 2018. DOI: https://doi.org/10.1017/wet.2017.98. PATTON A.J. WEISENBERGER D.V. SCHORTGEN G.P. 2,4-D- Resistant buckhorn plantain (Plantago lanceolate) in managed turf Weed Technology 32 182 189 2018 https://doi.org/10.1017/wet.2017.98 PINTO, E. Levantamento constata deriva de 2,4-D em 87,13% das amostras na safra atual. 2020a. Available at: <https://www.agricultura.rs.gov.br/levantamento-constata-deriva-de-2-4-d-em-87-13-das-amostras-na-safra-atual>. Accessed on: July 19 2020. PINTO E. Levantamento constata deriva de 2,4-D em 87,13% das amostras na safra atual 2020a Available at: <https://www.agricultura.rs.gov.br/levantamento-constata-deriva-de-2-4-d-em-87-13-das-amostras-na-safra-atual>. Accessed on: July 19 2020 PINTO, E. RS contabiliza mais de 600 autos de infração por descumprimento de normativas sobre herbicidas hormonais. 2020b. Available at: <https://www.agricultura.rs.gov.br/rs-contabiliza-mais-de-600-autos-de-infracao-por-descumprimento-de-normativas-sobre-herbicidas-hormonais>. Accessed on: Nov. 3 2023. PINTO E. RS contabiliza mais de 600 autos de infração por descumprimento de normativas sobre herbicidas hormonais 2020b Available at: <https://www.agricultura.rs.gov.br/rs-contabiliza-mais-de-600-autos-de-infracao-por-descumprimento-de-normativas-sobre-herbicidas-hormonais>. Accessed on: Nov. 3 2023 R CORE TEAM. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2022. R CORE TEAM R: a language and environment for statistical computing Vienna R Foundation for Statistical Computing 2022 RASCHER, U.; LIEBIG, M.; LÜTTGE, U. Evaluation of instant light-response curves of chlorophyll fluorescence parameters obtained with a portable chlorophyll fluorometer on site in the field. Plant, Cell & Environment, v.23, p.1397-1405, 2000. DOI: https://doi.org/10.1046/j.1365-3040.2000.00650.x. RASCHER U. LIEBIG M. LÜTTGE U. Evaluation of instant light-response curves of chlorophyll fluorescence parameters obtained with a portable chlorophyll fluorometer on site in the field Plant, Cell & Environment 23 1397 1405 2000 https://doi.org/10.1046/j.1365-3040.2000.00650.x RIO GRANDE DO SUL. Secretaria da Agricultura, Pecuária e Desenvolvimento Rural. Instrução Normativa SEAPDR nº 5/2019. Estabelece o “Termo de Conhecimento de Risco e de Responsabilidade”. 2019. Available at: <https://www.agricultura.rs.gov.br/upload/arquivos/201907/09135609-instruc-a-o-normativa-5-e-6-seapdr-2-4-d.pdf>. Acessed on: July 1 2024. RIO GRANDE DO SUL. Secretaria da Agricultura, Pecuária e Desenvolvimento Rural Instrução Normativa SEAPDR nº 5/2019. Estabelece o “Termo de Conhecimento de Risco e de Responsabilidade” 2019 Available at: <https://www.agricultura.rs.gov.br/upload/arquivos/201907/09135609-instruc-a-o-normativa-5-e-6-seapdr-2-4-d.pdf>. Acessed on: July 1 2024 ROBINSON, A.P.; SIMPSON, D.M.; JOHNSON, W.G. Summer annual weed control with 2, 4-D and glyphosate. Weed Technology, v.26, p.657-660, 2012. DOI: https://doi.org/10.1614/WT-D-12-00081.1. ROBINSON A.P. SIMPSON D.M. JOHNSON W.G. Summer annual weed control with 2, 4-D and glyphosate Weed Technology 26 657 660 2012 https://doi.org/10.1614/WT-D-12-00081.1 SILVA, D.R.O. da; SILVA, E.D.N. da; AGUIAR, A.C.M. de; NOVELLO, B.D.; SILVA, A.A.A. da; BASSO, C.J. Drift of 2,4-D and dicamba applied to soybean at vegetative and reproductive growth stage. Ciência Rural, v.48, e20180179, 2018. DOI: https://doi.org/10.1590/0103-8478cr20180179. SILVA D.R.O. da SILVA E.D.N. da AGUIAR A.C.M. de NOVELLO B.D. SILVA A.A.A. da BASSO C.J. Drift of 2,4-D and dicamba applied to soybean at vegetative and reproductive growth stage Ciência Rural 48 e20180179 2018 https://doi.org/10.1590/0103-8478cr20180179 SOLTANI, N.; OLIVEIRA, M.C.; ALVES, G.S.; WERLE, R.; NORSWORTHY, J.K.; SPRAGUE, C.L.; YOUNG, B.G.; REYNOLDS, D.B.; BROWN, A.; SIKKEMA, P.H. Off-target movement assessment of dicamba in North America. Weed Technology, v.34, p.318-330, 2020. DOI: https://doi.org/10.1017/wet.2020.17. SOLTANI N. OLIVEIRA M.C. ALVES G.S. WERLE R. NORSWORTHY J.K. SPRAGUE C.L. YOUNG B.G. REYNOLDS D.B. BROWN A. SIKKEMA P.H. Off-target movement assessment of dicamba in North America Weed Technology 34 318 330 2020 https://doi.org/10.1017/wet.2020.17 WARMUND, M.R.; ELLERSIECK, M.R.; SMEDA, R.J. Sensitivity and recovery of tomato cultivars following simulated drift of dicamba or 2,4-D. Agriculture, v.12, art.1489, 2022. DOI: https://doi.org/10.3390/agriculture12091489. WARMUND M.R. ELLERSIECK M.R. SMEDA R.J. Sensitivity and recovery of tomato cultivars following simulated drift of dicamba or 2,4-D Agriculture 12 art.1489 2022 https://doi.org/10.3390/agriculture12091489 WELLS, M.L.; PROSTKO, E.P.; CARTER, O.W. Simulated single drift events of 2,4-D and dicamba on pecan trees. HortTechnology, v.29, p.360-366, 2019. DOI: https://doi.org/10.21273/HORTTECH04265-19. WELLS M.L. PROSTKO E.P. CARTER O.W. Simulated single drift events of 2,4-D and dicamba on pecan trees HortTechnology 29 360 366 2019 https://doi.org/10.21273/HORTTECH04265-19 WERLE, R.; OLIVEIRA, M.C.; JHALA, A.J.; PROCTOR, C.A.; REES, J.; KLEIN, R. Survey of Nebraska farmers’ adoption of dicamba-resistant soybean technology and dicamba off-target movement. Weed Technology, v.32, p.754-761, 2018. DOI: https://doi.org/10.1017/wet.2018.62. WERLE R. OLIVEIRA M.C. JHALA A.J. PROCTOR C.A. REES J. KLEIN R. Survey of Nebraska farmers’ adoption of dicamba-resistant soybean technology and dicamba off-target movement Weed Technology 32 754 761 2018 https://doi.org/10.1017/wet.2018.62