Emerging Contaminants Uptake by an Ultisol and a Vertisol from Puerto Rico

Received: 13 September 2019 Accepted: 22 January 2020 DOI: 10.1002/agg2.20022

ORIGINAL RESEARCH ARTICLE Agrosystems Emerging contaminants uptake by an Ultisol and a Vertisol from Puerto Rico

Mario L. Flores-Mangual1 Arturo J. Hernández-Maldonado2 Krisiam Ortíz-Martínez2 Natasha P. Quiñones1

1 Department of Agro-Environmental Abstract Sciences, Univ. of Puerto Rico, Mayagüez Campus, Call Box 9000, Mayagüez, Puerto Contaminants of emerging concern (CECs), including pharmaceutical compounds, Rico 00681–9000 have been found in irrigation waters and have found their way into crops through the 2Department of Chemical Engineering, Univ. uptake of contaminated water. Many farms in Puerto Rico are irrigated with water that of Puerto Rico, Mayagüez Campus, Call Box 9000, Mayagüez, Puerto Rico 00681–9000 might have considerable levels of CECs. The objective of this study was to determine the quantity of commonly detected CEC adsorbed onto soil particles of two contrast- Correspondence ing tropical soils of Puerto Rico (Fraternidad, basic Vertisol [fine, smectitic, isohy- Mario L. Flores-Mangual, Dep. of Agro- Environmental Sciences, Univ. of Puerto Rico, perthermic Typic Haplusterts], and Mariana series, acid Ultisol [fine, mixed, active, Mayagüez Campus, Call Box 9000, Mayagüez, isohyperthermic Typic Haplohumults]). A CECs single point and multicomponent Puerto Rico 00681–9000. adsorption experiments were carried out using the batch equilibrium technique. The Email: oxisol@gmail.com CECs were naproxen (NPX), O-desmethylnaproxen (O-DesNPX), caffeine (CFN), Funding information paraxanthine (PX), carbamazepine (CBZ), carbamazepine-10, 11-epoxide (Ep-CBZ), National Science Foundation, Grant/Award clofibric acid (ClofA), and salicylic acid (SA). The CEC concentrations in water Number: OIA-1632824 before and after adsorption were determined using a triple quadrupole mass spec- troscopy liquid chromatography. The results showed that SA was highly adsorbed by both soils, although in greater concentrations in Fraternidad than Mariana, probably because of greater cation-bridging. Paraxanthine was adsorbed only in the multicomponent test, probably as a co-adsorbate. Caffeine, CBZ, and their metabolites were adsorbed in both soils in lesser concentrations than SA and PX. However, NPX and ClofA were not adsorbed by either soil type. Thus, these CECs could potentially move more freely through the soil matrix and reach soil roots in greater quantities than other contaminants.

1 INTRODUCTION

Contaminants of emerging concern (CECs) are a group of Abbreviations: CBZ, carbamazepine; CECs, contaminants of emerging compounds related to human daily life, produced by the concern; CFN, caffeine; ClofA, clofibric acid; Ep-CBZ, consumption of antibiotics, and/or personal care products carbamazepine-10, 11-epoxide; DOM, dissolved organic matter; NPX, from human metabolites and other sources (Focazio et al., naproxen; O-DesNPX, O-desmethylnaproxen; OM, organic matter; PCs, 2008). Many CECs are not considered a threat when dis- pharmaceutical compounds; PX, paraxanthine; SA, salicylic acid. posed but can become problematic upon reaching different

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Agrosystems, Geosciences & Environment published by Wiley Periodicals, Inc. on behalf of Crop Science Society of America and American Society of Agronomy

Agrosyst Geosci Environ. 2020;3:e20022. wileyonlinelibrary.com/journal/agg2 1of9 https://doi.org/10.1002/agg2.20022 2of9 FLORES-MANGUAL ET AL. elements of the environment (Stuart, Lapworth, Crane, & Hart, 2012; Vidal-Dorsch et al., 2012). Certain pharmaceu- Core Ideas tical active compounds (e.g., caffeine, nicotine, and aspirin) have been known for over 20 yr to enter the environment, • Salicylic acid was adsorbed onto soils in greater especially in populated geographic areas (Daughton, 2001). amounts than other compounds. Moreover, CECs can enter the environment directly (dis- • The Vertisol adsorbed more salicylic acid than posal and wastage from external application) and indirectly the Ultisol. (excretion, washing, and swimming) primarily via treated and • Paraxanthine and salicylic acid were adsorbed as untreated sewage effluent and by terrestrial runoff and wind- co-adsorbates. borne drift of antimicrobials applied to crops (Daughton, • Caffeine, carbamazepine, and their metabolites 2001). Some of the common CECs in the United States and were adsorbed in lesser amounts. Puerto Rico in groundwater are carbamazepine (anticonvul- • Naproxen and clofibric acid were not adsorbed by sant drug), and 1,7-dimethylxanthine (caffeine metabolite) either soil type. (Focazio et al., 2008). The CECs in water can eventually find their way into crops via contaminated irrigation water (Jones-Lepp, Sanchez, on the occurrence and environmental fate of pharmaceutical Moy, & Kazemi, 2010; Reddy Pullagurala et al., 2018). residues, specially in the soil matrix, in Puerto Rico and other Malchi, Maor, Tadmor, Shenker, and Chefetz (2014) observed Caribbean islands. Therefore, the objective of this study was that carrot (Daucus carota L.) and sweet potato (Ipomea to determine how common CECs are potentially adsorbed to batatas L.) grown in loessial arid brown Calcisol soils (cal- soil particles of two contrasting tropical soils of Puerto Rico cic Aridisols, USDA Soil Taxonomy) irrigated with treated (Fraternidad [fine, smectitic, isohyperthermic Typic Haplus- wastewater had greater concentrations of nonionic pharma- terts] and Mariana [fine, mixed, active, isohyperthermic Typic ceutical compounds (PCs) (e.g., carbamazepine [CBZ] and Haplohumults]). Adsorption assays were performed to iden- caffeine [CFN]) than ionic PCs (e.g., naproxen, NPX). Also, tify the CECs that could potentially move freely throughout it was found that 10–11 epoxycarbamazepine (Ep-CBZ), a the soil matrix and eventually reach the root zone of edible metabolite of CBZ, was in greater amounts in crops than crops in Puerto Rico. This study is part of the groundwork on carbamazepine. Carbamazepine in particular has a low degra- the interactions of CECs with the soil matrix for the develop- dation in the soil matrix, and can move through plant mem- ment of filters to selectively reduce the CECs that are more branes, and into the plant phloem and xylem (Reddy Pullagu- likely to be adsorbed by crops from irrigation water. rala et al., 2018). The movement of the CECs in soil matrix and eventual uptake by crops is related to the sorption affinity of these con- 2 MATERIALS AND METHODS taminants to soil particles and soil amendments (Bair et al., 2016; Scheytt, Mersmann, & Heberer, 2006). In general, non- Soil samples were collected from Lajas Agricultural Experi- ionic CECs (e.g., CBZ) are more easily assimilated by plants ment Substation, University of Puerto Rico–Mayagüez Cam- than ionic CECs (e.g., NPX, clofibric acid [ClofA], ibupro- pus (Figure 1). The Fraternidad soil series is a basic Vertisol, fen) (Bhalsod et al., 2018; Goldstein, Shenker, & Chefetz, described as moderately well drained, very deep soil, and pos- 2014). However, ionic CECs such as clofibric acid and ibupro- sessing very low soil permeability (Soil Survey Staff, 2006). fen have been detected in tomato (Goldstein et al., 2014). This soil is formed from sediments high on clay materials These CECs are more easily assimilated in plants grown in that developed from the weathering of limestone and volcanic low organic matter content and low clay content (Goldstein rock. This series is located in basins and flood plains of the et al., 2014). Southern Coastal Plains of Puerto Rico. Mariana soil series is There is evidence of water contamination in Puerto Rico an acidic Ultisol, consisting of very deep, well drained, mod- related to urban development, industries (including pharma- erately permeable soil (Soil Survey Staff, 2007). Both sam- ceutical industries), agriculture, and sewage discharges (Envi- pled areas have not been used for farming for at least 10 yr. ronmental Quality Board, 2013; Hunter & Arbona, 1995; These areas have grasses, mostly guinea grass [Megathyr- Skanavis, 1999). Many vegetable farms in Puerto Rico may be sus maximus (Jacq.) B.K. Simon & S.W.L. Jacobs], and are using irrigation water contaminated with CECs with unknown mowed regularly. In the past the Fraternidad area was part of interactions with the different soil types of the island. In fact, a vegetable organic farm, whereas the Mariana area was used CBZ has been detected in superficial water in 16 of 17 sam- for pineapple [Ananas comosus (L.) Merr.] growth. This soil pled rivers around Puerto Rico and has been highly correlated is formed from colluvium and residuum of weathered mate- to population density (Wade, Otero, Poon-Kwong, Rozier, rial from tuff and basalt. They are located in summits and side & Bachoon, 2015). There is an evident lack of information slopes of hills of southern Puerto Rico. FLORES-MANGUAL ET AL. 3of9

FIGURE 1 Location of Vertisol (Fraternidad series) and Ultisol (Mariana series) in Lajas, Puerto Rico

The adsorption tests were done with composite samples lite). These were selected because of high concurrency reports randomly collected, one for each soil type. Soil samples for in water bodies and reclaimed water. All CECs metabolites each soil series were collected from the topsoil horizon (A were purchased from Sigma Aldric and used as received and horizon, at the 0- to 15-cm depth), then oven-dried at 105 ◦C the water was distilled/deionized with a pH of 6.5. Figure 2 for 48 h to reduce the amount of soil moisture. After drying, collects relevant properties for the aforementioned CECs. both soils were sieved using a no. 10 mesh (2-mm sieve open- Single point adsorption experiments were carried out in ing) prior to analysis. The chemical characteristics of both soil batch mode and in triplicates. For each experiment, 0.05 g series are included in Table 1. of the soil were mixed with 15 ml of a solution containing a = μ −1 The CECs and some of their metabolites used during single CEC (Ci 100 gL ) inside borosilicate centrifuge the single and multicomponent equilibrium adsorption tests tubes at 25 ◦C. The final aqueous mixture observed pH was were: CFN, paraxanthine (PX, CFN metabolite), CBZ, Ep- between 5 and 6 (Figure 2). No adjustments were made to pH. CBZ (CBZ metabolite), ClofA, salicylic acid (SA), NPX, The tubes and contents were shaken at room temperature for and O-desmethylnaproxen (O-DesNPX, naproxen metabo- at least 24 h. Upon completion of this stage, the solids and 4of9 FLORES-MANGUAL ET AL.

TABLE 1 Selected soil properties of Fraternidad and Mariana soil series Soil property Units Fraternidad Mariana pH (1:1) 6.8 5.3 Sand % 25 35 Silt % 24 23 Clay % 51 42 EC (1:1) mmhos cm−1 0.67 0.2 −1 N–NO3 (KCl) mg kg 22.48 22.38 −1 N–NH4 (KCl) mg kg 30.04 3.85 −1 P–PO4 (Bray 1) mg kg 5 4 −1 P–PO4 (Olsen) mg kg 3.0 6.7 −1 K(NH4OAc) mg kg 225 100 −1 Ca (NH4OAc) mg kg 4,492 1,155 −1 Mg (NH4OAc) mg kg 1,808 391 −1 Na (NH4OAc) mg kg 202 69 −1 S–SO4 (Ca-P) mg kg 18 15 Al (KCl) mg kg−1 <0.1 6.3 Organic matter (LOI)a % 4.9 4.1 b −1 ECEC cmolc kg 39.0 15.8 Note. Soil pH and EC were determined using a 1:1 soil/water extraction (McLean, 1982); soil particles were determined using the hydrometer method (Gee & Or, 2002);

N–NO3 and N–NH4 were extracted using KCl and analyzed with a spectrophotometer (Mulvaney, 1996); P–PO4 was determined using both the Bray I and Olsen methods (Bray & Kurtz, 1945; Olsen, Cole, & Watanabe, 1954); K, Ca, Mg, and Na were extracted with NH4OAc (Haby, Russelle, & Skogley, 1990; Warncke & Brown, 1998); S–SO4 was extracted with calcium phosphate (Combs, Denning, & Frank, 1998); Al was extracted with KCl (Bertsch & Bloom, 1996). aLOI, loss on ignition (360◦C for 2.25 h). bECEC, effective cation exchange capacity, determined by sum of exchangeable cations. aqueous phases were separated via centrifugation at 1643 rpm 3 RESULTS for 15 min. Samples were taken from the supernatant phase and the final concentration of each CEC or metabolite was The results from single-component tests are shown in Tables 2 estimated using an Agilent 1290 high performance liquid and 3. Overall, the order for the adsorption of the selected chromatography system coupled to an Agilent 6460 Triple CECs by Fraternidad follows: SA > CFN > CBZ > PX > Ep- Quadrupole mass spectrometer (HPLC-MS/MS). For addi- CBZ > O-DesNPX (Table 2). The ClofA and NPX were not tional information, please refer to Supplemental Tables S1 and adsorbed by this soil series. Likewise, for the adsorption of S2. The percentage of the CEC or metabolite removed from the selected CECs by the Mariana soil series follows: SA > water by the soil was calculated based on concentration dif- CFN > Ep-CBZ. O-desmethylnaproxen, ClofA, and NPX ferences using the following equation: were not adsorbed by this soil. Both soils removed significant amounts of SA compared with the other CECs (Tables 2 ( ) and 3); however, Fraternidad has a much better affinity toward 𝐶i − 𝐶 % Removed from water = × 100 this CEC compared with Mariana’s, where all the SA dosage 𝐶 (1) i ended up being adsorbed by Fraternidad. Removal in the multi-component tests in Fraternidad μ −1 > > > where Ci is the initial CEC concentration in water ( gL ) follows: PX SA CFN CBZ (Table 2). No adsorption and C is the CEC concentration in water after adsorption of Ep-CBZ, ClofA, NPX, or O-DesNPX was observed by the soil (μgL−1). Similar procedures and calculations (Table 2). In contrast, the lack of O-DesNPX adsorption were employed for the determination of multi-component suggests considerable adsorbate–adsorbate competition CEC adsorption. (Table 2). For Mariana soils, the removal order is: PX > Statistical analyses for all data were performed using anal- SA > CFN > CBZ (Table 3). No adsorption of Ep-CBZ, ysis of variance (ANOVA) using JMP Software (JMP 8, SAS ClofA, NPX, or O-DesNPX was observed (Table 3). Among Institute). ANOVAs were done for each soil type individually, the CECs tested, PX had the highest percentage removal by an ANOVA for single component, and another ANOVA for the Mariana (77.56% ± 1.1) and Fraternidad (76.62% ± 1.1) multi-component. Comparison of treatment means was per- soils, possibly due to co-adsorption of SA and PX (Tables 2 formed using Tukey means comparison and an alpha of .05. and 3). FLORES-MANGUAL ET AL. 5of9

FIGURE 2 Physicochemical properties for CECs tested. Values for the pKa and log Kow were gathered from the literature (Bui, Pham, Le, & Choi, 2013; Cabrera-Lafaurie, Román, & Hernández-Maldonado, 2012; Jurado et al., 2014; Konstantianos, Ioannou, & Stratikos, 1994; Nam, Jo, Yoon, & Zoh, 2014; Reyes-Contreras, Dominguez, & Bayona, 2012; Salgado et al., 2013; Sotelo et al., 2014). NE, nonexistent at pH range 1–14

TABLE 2 Means comparison for percentage of removal of contaminants of emerging concern (CECs) from water by soil particles of the Fraternidad soil series in single point, single component adsorption tests and multi-component adsorption tests Single componenta Multi-component CECs Means and SD of % of removal Caffeine 13.4 ± 0.20 B 13.1 ± 0.72 C Paraxanthine 7.5 ± 0.50 D 76.6 ± 0.33 A Carbamazepine 11.1 ± 0.08 C 3.3 ± 0.25 D Carbamazepine-10, 11-epoxide 3.1 ± 0.27 E 0.0 D Salicylic acid 99.9 ± 0.04 A 66.6 ± 2.03 B Clofibric acid 0.0 F 0.0 D Naproxen 0.0 F 0.0 D O-desmethylnaproxen 3.0 ± 0.32 E 0.0 D = < = = < Note. Whole model for single component test: CECs F7, 16 5,458.3, P value .0001. Whole model for multi-component test: CECs F7, 16 472.7, P value .0001. aPair-wise comparisons were done using Tukey LS means. Means with different capital letters within columns are significantly different (α=.05). 6of9 FLORES-MANGUAL ET AL.

TABLE 3 Means comparison for percentage of removal of contaminants of emerging concern (CECs) from water by soil particles of the Mariana soil series in single point, single component adsorption tests and multi-component adsorption tests Single componenta Multi-component CECs Means and SD of % of removal Caffeine 13.9 ± 0.40 B 16.8 ± 0.64 C Paraxanthine 9.5 ± 0.45 BC 77.6 ± 0.32 A Carbamazepine 11.1 ± 0.29 BC 0.21 ± 0.12 D Carbamazepine-10, 11-epoxide 4.2 ± 0.46 CD 0.0 D Salicylic acid 49.9 ± 0.04 A 32.9 ± 1.45 B Clofibric acid 0.0 D 0.0 D Naproxen 0.0 D 0.0 D O-desmethylnaproxen 0.0 D 0.0 D = < = < Note. Whole model for single component: CECs F7, 16 200.9, P value .0001. Whole model for multi-component: CECs F7, 16 636.5, P value .0001. aPair-wise comparisons were done using Tukey LS means. Means with different capital letters within columns are significantly different (α=.05).

4 DISCUSSION confound the adsorption percentages of SA; thus, the low recovery of SA could be a combination of adsorption and Single component CECs adsorption tests revealed that SA degradation of the molecule. Interestingly, ClofA, the other adsorbed in significantly greater quantities compared with acid among the selected CECs, was not adsorbed by any of other CECs (Tables 2 and 3), suggesting that this CEC is the soils probably due to its affinity toward the aqueous phase more likely found adhered to the soil solids than moving (i.e., lower octanol–water partition coefficient, log Kow;see freely throughout the soil matrix. Tables 2 and 3 show that Figure 2). more SA was removed by the Fraternidad soil compared with Caffeine, CBZ, and their metabolites were also adsorbed by the Mariana soil. This could be due to the Fraternidad soil both soils, but in significant lesser amounts compared with surface being more basic (pH ∼ 6.8) than that of the Mariana SA (Tables 2 and 3). These CECs exhibit larger pKa val- soil surface (pH ∼ 5.3), which enhances the potential for ues, so their adsorption could be the result of interactions ionization of compounds with low pKa values such as SA between neutrally charged adsorbates and a charged soil sur- (Figure 2). However, a higher cation exchange capacity, such face. Differences in percentage removal among the soils and as in Fraternidad, could repulse the negatively charged SA for these CECs were similar (Tables 2 and 3), which also (Table 1). Xu, Xiao, Zhang, Jiang, and Ji (2007) found, in two suggests that only weak electrostatic forces are taking place variable charge soils, that the SA and phthalic acid adsorption during the adsorption process. In the case of CFN it can be decreased with the increase of pH, because of greater cation degraded by microorganisms, especially under aerated soil exchange capacity. Lertpaitoonpan, Ong, and Moorman conditions (Topp, Hendel, Lu, & Chapman, 2006). In con- (2009) found that distribution coefficient (Kd) values of trast, CBZ is highly persistent in soils; thus, the adsorption sulfamethazine (pKa 7.4) decreased with increases in soil pH, percentages should not be affected by degradation of the thus favoring the anionic stage and the repulsion of the soil molecule (Li, Dodgen, Ye, & Gan, 2013; Monteiro & Boxall, particles. A mechanism that could partially explain the high 2009). A higher soil organic matter (OM) content and clay adsorption of SA could be the bridging of polyvalent cations content can enhance the uptake of non-ionic organic adsor- with the clay fraction (Dubus, Barriuso, & Calvet, 2001). bates (Goldstein et al., 2014; Karnjanapiboonwong, Morse, The greater number of polyvalent cations (e.g., Ca and Mg) Maul, & Anderson, 2010; Yue et al., 2017). This could plau- in Fraternidad could have caused a greater sorption than in sibly explain the greater adsorption of CBZ onto Fraternidad Mariana due to cation bridging (Table 1). Also, the presence rather than Mariana soil (Table 1). Navon, Hernadez-Ruiz, of oxides, especially in Mariana, could provide other sorption Chorover, and Chefetz (2011) found that CBZ adsorption sites for SA (Dubus et al., 2001). Another aspect that could can be enhanced by dissolved organic matter (DOM) that is explain Fraternidad’s superior uptake of SA is the soil’s bound to the soil particles. Moreover, it has been observed that higher content of exchangeable alkali and alkaline soil metals biosolids applications significantly increase the adsorption of (Table 1). This could result in enhanced electrostatic level CBZ, increasing Kd possibly due to an increase in SOM and interactions due to generation of electric fields by the metals, salinity (Williams, Williams, & Adamsen, 2006). Hydropho- adding another contribution to the overall interaction energy bic CECs can also be adsorbed to particulate OM (Guo, L, & between SA and Fraternidad effective surface. However, Ma, 2010). Guo et al. (2010) found that particulate organic C there are bacteria (e.g., Pseudomonas putida) capable of adsorption capacity is greater when the sorbate has a large log degrading SA in cultures (Patel et al., 2019). This could Kow value and lower solubility. FLORES-MANGUAL ET AL. 7of9

Tests for multicomponent CEC adsorption were performed higher concentrations of a CEC in the straw of wheat (Triticum to elucidate co-adsorption and/or competitive adsorption aestivum L.) samples compared to the grain. by the soils. Tables 2 and 3 show that, indeed, both co- adsorption and competitive adsorption are taking place as evidenced by a considerable decrease in removal capacity 5 CONCLUSION for SA, a significant increase in removal capacity for PX, and a significant reduced uptake of CBZ. Although, PX can Among the tested CECs, SA was significantly more adsorbed be biodegraded (Mazzafera, Olsson, & Sandberg, 1996), it in the single component tests, especially in the Vertisol, prob- does not appear to be the main cause for the lower recovery ably due to higher concentration of divalent cations and their and greater adsorption in the multi-component tests, due bridging capacity. However, this could be also related, to some to the high PX recovery values in the single component degree, to degradation of the molecule, especially by bacte- tests. It appears that the uptake of PX by Fraternidad and ria. Future adsorption research on these soils should test for Mariana is driven by co-adsorption with SA, probably due the degradation of the molecule. Although, the studied soils to interactions between both CECs. In the case of CFN, the are of different soil orders, for the other CECs, they behaved amounts removed by either soil remained similar to those very similar in the single component and multi-component observed during the single component CEC adsorption tests tests. In the multi-component test, paraxanthine was signif- (Tables 2 and 3). However, this also suggests that a plausible icantly more adsorbed than the other CECs plausible as co- site for interactions between SA and PX as co-adsorbates adsorbate of salicylic acid. This could result in less movement could take place around the amine bridge (–NH–) group of of paraxanthine in soils contaminated with both paraxanthine the piperidine section of PX (see molecule in Figure 2). and salicylic acid, than with paraxanthine alone. Of the stud- Tables 2 and 3 show that NPX and ClofA were not adsorbed ied CECs, naproxen and clofibric acid are the ones that are in either soil type, whether as single- or multi-component nor expected to move more freely in both soils, as they were not a multi-component adsorbates. This could imply that their adsorbed by either. These findings offer great motivation to transport is not going to be limited by the adsorptive forces pursue strategies to lessen or eliminate the transport of CECs in soils, including its organic matter; thus, these CECs could that could reach crops or even ground water. One such strategy very well end up in underground waters and crops. Siemens is the use of filters in irrigation water to reduce the amounts et al. (2010) tested the mobility of NPX, among other contam- of CECs, specially NPX and ClofA, which are not directly inants, in irrigation wastewater using soil columns collected adsorbed by soils like Fraternidad (Vertisol) and Mariana from a Vertisol. It was found that NPX had a high mobility in (Ultisol). the soil matrix and thus high potential for groundwater contamination partially because of NPX compact structure and ACKNOWLEDGMENTS high negative charge density. The pH of both soils indicates We thank Dr. Rebecca Tirado Corbalá for proofreading the that the NPX is ionized due to its low pKa value (Table 1 article and Dr. Raúl Machiavelli for the statistical advice. We and Figure 2). This could promote cation bridging but also acknowledge that support was provided by the U. S. National repulsion between the negatively charged NPX and the nega- Science Foundation (NSF) under Award OIA-1632824. tive charges of the soil particles (e.g., clay and OM) (Duran- Alvarez, Prado-Pano, & Jimenez-Cisneros, 2012). However, CONFLICT OF INTEREST SA had high adsorption percentage and low pKa; thus, other There are no conflicts of interest. mechanisms might be involved for the low NPX adsorption. Differences in the affinity of the deprotonated form of ORCID NPX compared with SA could be related to their adsorp- Mario L. Flores-Mangual tion differences. Also, the smaller molecular footprint of SA https://orcid.org/0000-0002-1842-6099 permits the molecule to reach smaller voids for adsorptions (Rivera-Jimenez, Lehner, Cabrera-Lafaurie, & Hernández- REFERENCES Maldonado, 2010). In addition, it has been found high desorp- Bair, D. A., Mukome, F. N. D., Popova, I. E., Ogunyoku, T. A., Jefferson, tion coefficients of NPX in soils (Duran-Alvarez et al., 2012). A., Wang, D., … Parikh, S. J. (2016). Sorption of pharmaceuticals, Therefore, NPX and ClofA could potentially reach plant roots heavy metals, and herbicides to biochar in the presence of biosolids. in greater quantities than SA, PX, and even CFN. Tanoue et al. Journal of Environmental Quality, 45(6), 1998–2006. https://doi.org/ (2012) studied the uptake of PCs by plants and found that 10.2134/jeq2016.03.0106 Bertsch, P. M., & Bloom, P. R. (1996). Aluminum. In D. L. Sparks, A. L. hydrophilic PCs tend to accumulate in roots. They also found Page,P.A.Helmke,&R.H.Loeppert(Eds.),Methods of soil anal- that there is a potential for these PCs to be taken up by shoot ysis. Part 3. Chemical methods (pp. 517–550). Madison, WI: SSSA of edible plants. In another study, Hmielowski (2016) found and ASA. https://doi.org/10.2136/sssabookser5.3.c18 8of9 FLORES-MANGUAL ET AL.

Bhalsod, G. D., Chuang, Y. H., Jeon, S., Gui, W., Li, H., Ryser, E. Haby, V. A., Russelle, M. P., & Skogley. E.O. (1990). Testing soils T., … Zhang, W. (2018). Uptake and accumulation of pharmaceu- for potassium, calcium, and magnesium. In R. L. Westerman (Ed.), ticals in overhead- and surface-irrigated greenhouse lettuce. Journal Soil testing and plant analysis (pp. 181–227). Madison, WI: SSSA. of Agricultural and Food Chemistry, 66(4), 822–830. https://doi.org/ https://doi.org/10.2136/sssabookser3.3ed.c8 10.1021/acs.jafc.7b04355 Hmielowski, T. (2016). Emerging contaminants in agricultural systems. Bray, R. H., & Kurtz, L. T. (1945). Determination of total, organic, and CSA News, 61(8), 4–9. https://doi.10.2134/csa2016-61-8-1 available forms of phosphorus in soils. Soil Science, 59, 39–46. https: Hunter, J. M., & Arbona, S. I. (1995). Paradise lost: An introduction to //doi.org/10.1097/00010694-194501000-00006 the geography of water pollution in Puerto Rico. Social Science & Bui, T. X., Pham, V. H., Le, S. T., & Choi, H. (2013). Adsorption of phar- Medicine, 40(10), 1331–1335. maceuticals onto trimethylsilylated mesoporous SBA-15. Journal of Jones-Lepp, T. L., Sanchez, C. A., Moy, T., & Kazemi, R. (2010). Hazardous Materials, 254–255, 345–353. https://doi.org/10.1016/j. Method development and application to determine potential plant jhazmat.2013.04.003 uptake of antibiotics and other drugs in irrigated crop production sys- Cabrera-Lafaurie, W. A., Román, F. R., & Hernández-Maldonado, A. J. tems. Journal of Agricultural and Food Chemistry, 58(22), 11568– (2012). Transition metal modified and partially calcined inorganic– 11573. https://doi.org/10.1021/jf1028152 organic pillared clays for the adsorption of salicylic acid, clofibric Jurado, A., Lopez-Serna, R., Vazquez-Sune, E., Carrera, J., Pujades, E., acid, carbamazepine, and caffeine from water. Journal of Colloid and Petrovic, M., & Barcelo, D. (2014). Occurrence of carbamazepine Interface Science, 386, 381–391. https://doi.org/10.1016/j.jcis.2012. and five metabolites in an urban aquifer. Chemosphere, 115, 47–53. 07.037 https://doi.org/10.1016/j.chemosphere.2014.01.014 Combs, S. M., Denning, J. L., & Frank, K. D. (1998). Sulfate–sulfur. Karnjanapiboonwong, A., Morse, A. N., Maul, J. D., & Anderson, T. A. In J. R. Brown (Ed.), Recommended chemical soil test procedures (2010). Sorption of estrogens, triclosan, and caffeine in a sandy loam for the North Central Region (pp. 35–40). North Central Publ. 221 and a silt loam soil. Journal of Soils and Sediments, 10, 1300–1307. (Revised). Columbia, MO: University of Missouri Agric. Exp. Stn. https://doi.org/10.1007/s11368-010-0223-5 Daughton, C.G. (2001). Pharmaceuticals and personal care products Konstantianos, D. G., Ioannou, P. C., & Stratikos, E. (1994). Simultane- in the environment: Overarching issues and overview. In C. G. ous determination of naproxen and its desmethyl metabolite in human Daughton & T. L. Jones-Lepp (Eds.), Pharmaceuticals and Care serum by second-derivative synchronous fluorescence spectrometry. Products in the Environment, ACS Symposium Series (pp. 2–38). Analytica Chimica Acta, 290, 34–39. https://doi.org/10.1016/0003- Washington, DC: American Chemical Society. 2670(94)80037-5 Dubus, I. G., Barriuso, E., & Calvet, R. (2001). Sorption of weak organic Lertpaitoonpan, W., Ong, S. K., & Moorman, T. B. (2009). Effect of acids in soils: Clofencet, 2,4-D and salicylic acid. Chemosphere, 45, organic carbon and pH on soil sorption of sulfamethazine. Chemo- 767–774. https://doi.org/10.1016/S0045-6535(01)00108-4 sphere, 76, 558–564. https://doi.org/10.1016/j.chemosphere.2009. Duran-Alvarez, J. C., Prado-Pano, B., & Jimenez-Cisneros, B. (2012). 02.066 Sorption and desorption of carbamazepine, naproxen and triclosan Li, J., Dodgen, L., Ye, Q., & Gan, J. (2013). Degradation kinetics and in a soil irrigated with raw wastewater: Estimation of the sorption metabolites of carbamazepine in soil. Environmental Science & Tech- parameters by considering the initial mass of the compounds in the nology, 47, 3678–3684. soil. Chemosphere, 88, 84–90. Malchi, T., Maor, Y., Tadmor, G., Shenker, M., & Chefetz, B. (2014). Environmental Quality Board. (2013). Puerto Rico 305(b)/303(d) Irrigation of root vegetables with treated wastewater: Evaluating Integrated Report. San Juan, PR: Plans and Special Projects uptake of pharmaceuticals and the associated human health risks. Division, Evaluation and Strategic Planning Area, Environmen- Environmental Science & Technology, 48(16), 9325–9333. tal Quality Board. Retrieved from http://visitponce.com/wp- Mazzafera, P., Olsson, O., & Sandberg, G. (1996). Degradation of caf- content/uploads/2019/09/2016-PREQB-305b303d-Integrated- feine and related methylxanthines by Serratia marcescens isolated Report.pdf from soil under coffee cultivation. Microbial Ecology, 31, 199–207. Focazio, M. J., Kolpin, D. W., Barnes, K. K., Furlong, E. T., Meyer, McLean, E. O. (1982). Soil pH and lime requirement. In A. L. Page, M. T., Zaugg, S. D., … Thurman, M. E. (2008). A national recon- R.H.Miller,D.R.Keeney(Eds.),Methods of soil analysis. Part 2. naissance for pharmaceuticals and other organic wastewater contam- Chemical and microbiological properties. (2nd ed., pp. 199–224). inants in the United States—II) untreated drinking water sources. Madison WI: SSSA and ASA. https://doi.10.2134/agronmonogr9.2. The Science of the Total Environment, 402(2–3), 201–216. https:// 2ed.c12 doi.org/10.1016/j.scitotenv.2008.02.021 Monteiro, C. S., & Boxall, A. B. A. (2009). Factors affecting the degra- Gee, G. W., & Or, D. (2002). Particle-size analysis. In J. H. Dane dation of pharmaceuticals in agricultural soils. Environmental Tox- & G. C. Topp (Eds.), Methods of soil analysis, Part 4. Physical icology and Chemistry, 28, 2546–2554. https://doi.org/10.1897/08- methods. (pp. 255–294). Madison, WI: SSSA. https://doi.10.2136/ 657.1 sssabookser5.4.c12 Mulvaney, R. L. (1996). Nitrogen—inorganic forms. In D. L. Sparks, Goldstein, M., Shenker, M., & Chefetz, B. (2014). Insights into the A. L. Page, P. A. Helmke, & R. H. Loeppert (Eds.), Methods of soil uptake processes of wastewater-borne pharmaceuticals by vegeta- analysis. Part 3. Chemical methods (pp. 1123–1184). Madison, WI: bles. Environmental Science & Technology, 48, 5593–5600. Soil SSSA and ASA. https://doi.10.2136/sssabookser5.3.c38 Guo, X., L, Luo, & Ma, Y. (2010). Sorption of polycyclic aromatic hydro- Nam, S. W., Jo, B. I., Yoon, Y., & Zoh, K. D. (2014). Occurrence carbons on particulate organic matters. Journal of Hazardous Mate- and removal of selected micropollutants in a water treatment plant. rials, 173(1–3), 130–136. https://doi.org/10.1016/j.jhazmat.2009.08. Chemosphere, 95, 156–165. https://doi.org/10.1016/j.chemosphere. 065 2013.08.055 FLORES-MANGUAL ET AL. 9of9

Navon, R., Hernadez-Ruiz, S., Chorover, J., & Chefetz, B. (2011). Inter- Science of the Total Environment, 416, 1–21. https://doi.org/10.1016/ actions of carbamazepine in soil: Effects of dissolved organic matter. j.scitotenv.2011.11.072 Journal of Environmental Quality, 40, 942–948. https://doi.org/10. Tanoue, R., Sato, Y., Motoyama, M., Nakagawa, S., Shinohara, R., & 2134/jeq2010.0446 Nomiyama, K. (2012). Plant uptake of pharmaceutical chemicals Olsen, S. R., Cole, C. V., & Watanabe, F. S. (1954). Estimation of avail- detected in recycled organic manure and reclaimed wastewater. Jour- able phosphorus in soils by extraction with sodium bicarbonate.U. nal of Agricultural and Food Chemistry, 60, 10203–10211. https:// S. Department of Agriculture Circ. 939. Washington, DC: USDA. doi.org/10.1021/jf303142t Patel, M., Kumar, R., Kishor, K., Mlsna, T., Pitman, C. U., Jr., & Mohan, Topp, E., Hendel, J. G., Lu, Z., & Chapman, R. (2006). Biodegradation D. (2019). Pharmaceuticals of emerging concern in aquatic sys- of caffeine in agricultural soils. Canadian Journal of Soil Science, tems: Chemistry, occurrence, effects, and removal methods. Chem- 86, 533–544. ical Reviews, 119, 3510–3673. https://doi.org/10.1021/acs.chemrev. Vidal-Dorsch, D. E., Bay, S. M., Maruya, K., Snyder, S. A., Trenholm, R. 8b00299 A., & Vanderford, B. J. (2012). Contaminants of emerging concern Reddy Pullagurala, V. L.. , Rawat, S., Adisa, I. O., Hernandez-Viezcas, in municipal wastewater effluents and marine receiving water. Envi- J. A., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2018). Plant ronmental Toxicology and Chemistry, 31(12), 2674–2682. https:// uptake and translocation of contaminants of emerging concern in soil. doi.org/10.1002/etc.2004 The Science of the Total Environment, 636, 1585–1596. Wade, C., Otero, E., Poon-Kwong, B., Rozier, R., & Bachoon, D. Reyes-Contreras, C., Dominguez, C., & Bayona, J. M. (2012). Determi- (2015). Detection of human-derived fecal contamination in Puerto nation of nitrosamines and caffeine metabolites in wastewaters using Rico using carbamazepine, HF183 bacteroides, and fecal indicator gas chromatography mass spectrometry and ionic liquid station- bacteria. Marine Pollution Bulletin, 101, 872–877. https://doi.org/10. ary phases. Journal of Chromatography A, 1261, 164–170. https:// 1016/j.marpolbul.2015.11.016 doi.org/10.1016/j.chroma.2012.05.082 Warncke, D., & Brown, J. R. (1998). Potassium and other basic Rivera-Jimenez, S. M., Lehner, M. M., Cabrera-Lafaurie, W. A., & cations. In J. R. Brown (Ed.), Recommended chemical soil test Hernández-Maldonado, A. J. (2010). Removal of naproxen, salicylic procedures for the North Central Region, NCR Publication 221 acid, clofibric acid, and carbamazepine by water phase adsorption (pp. 31–33). Columbia, MO: Missouri Agricultural Experiment onto inorganic–organic intercalated bentonites modified with transi- Station. tion metal cations. Environmental Engineering Science, 28(3), 171– Williams, C. F., Williams, C. F., & Adamsen, F. J. (2006). Sorption– 182. desorption of carbamazepine from irrigated soils. Journal of Envi- Salgado, R., Pereira, V. J., Carvalho, G., Soeiro, R., Gaffney, V., ronmental Quality, 35, 1779–1783. https://doi.org/10.2134/jeq2005. Almeida, C., … Noronha, J. P. (2013). Photodegradation kinetics 0345 and transformation products of ketoprofen, diclofenac and atenolol in Xu, R. K., Xiao, S. C., Zhang, H., Jiang, J., & Ji, G. L. (2007). Adsorp- pure water and treated wastewater. Journal of Hazardous Materials, tion of phthalic acid and salicylic acid by two variable charge soils 244–245, 516–527. https://doi.org/10.1016/j.jhazmat.2012.10.039 as influenced by sulphate and phosphate. European Journal of Soil Scheytt, T. J., Mersmann, P., & Heberer, T. (2006). Mobility of Science, 58, 335–342. https://doi.org/10.1111/j.1365-2389.2006. pharmaceuticals carbamazepine, diclofenac, ibuprofen, and propy- 00842.x phenazone in miscible-displacement experiments. Journal of Con- Yue, L., Ge, C., Feng, D., Yu, H., Deng, H., & Fu, B. (2017). Adsorption– taminant Hydrology, 83, 53–69. https://doi.org/10.1016/j.jconhyd. desorption behavior of atrazine on agricultural soils in China. Jour- 2005.11.002 nal of Environmental Sciences, 57, 180–189. https://doi.org/10.1016/ Siemens, J., Huschek, G., Walshe, G., Siebe, C., Kasteel, R., Wulf, S., … j.jes.2016.11.002 Kaupenjohann, M. (2010). Transport of pharmaceuticals in columns of a wastewater-irrigated Mexican clay soil. Journal of Environmen- tal Quality, 39, 1201–1210. https://doi.org/10.2134/jeq2009.0105 SUPPORTING INFORMATION Skanavis, C. (1999). Groundwater disaster in Puerto Rico: The need for environmental education. Environmental Health, 62, 29–35. Additional supporting information may be found online in the Soil Survey Staff. (2006). Fraternidad series. Washington, DC: Supporting Information section at the end of the article. USDA-NRCS. Retrieved from https://soilseries.sc.egov.usda.gov/ OSD_Docs/F/FRATERNIDAD.html Soil Survey Staff. (2007). Mariana series. Washington, DC: USDA- NRCS. Retrieved from https://soilseries.sc.egov.usda.gov/OSD_ How to cite this article: Flores-Mangual ML, Docs/M/MARIANA.html Hernández-Maldonado AJ, Ortíz-Martínez K, Sotelo, J. L., Ovejero, G., Rodríguez, A., Álvarez, S., Galán, J., & García, Quiñones NP. Emerging contaminants uptake by an J. (2014). Competitive adsorption studies of caffeine and diclofenac Ultisol and a Vertisol from Puerto Rico. Agrosyst aqueous solutions by activated carbon. Chemical Engineering Jour- Geosci Environ. 2020;3:e20022. nal, 240, 443–453. https://doi.org/10.1016/j.cej.2013.11.094 https://doi.org/10.1002/agg2.20022 Stuart, M., Lapworth, D., Crane, E., & Hart, A. (2012). Review of risk from potential emerging contaminants in UK groundwater. The