Abstract
Purpose
Although mitigation approaches have been developed to reduce Cd in cacao beans, the efficacy of the approaches have been inadequate to make them economically viable. The objective was to determine the application method that would be most efficacious with respect to rapidity of effect, magnitude of reduction and persistency of effect on Cd in cacao.
Method
A field study was conducted using two soil amendments, hydrated lime and biochar, at recommended rates using three methods of application, soil surface application with incorporation (SA), soil injection (SI) or deep placement using an auger (AA) along with a control. The experiment was arranged in randomized complete block design with three replications with 15 trees per replication. Phytoavailable soil Cd, soil pH, CEC and total leaf Cd concentration were monitored monthly on three guarded trees per plot over a one-year period.
Results
The efficacy of application of hydrated lime by SI was significantly better than SA in terms of rapidity of the effect on leaf Cd in comparison to the control (40% reduction compared to 30%) as well as its persistency. With biochar, again the SI was significantly better than SA with regards to reducing leaf Cd levels in comparison to the control (35% reduction compared to 20%) but the time taken to action and the persistency were lower compared to hydrated lime application. AA did not significantly reduce Cd level in the leaf with either hydrated lime or biochar application.
Conclusion
Overall the application of the amendments using SI was much more effective in reducing Cd accumulation in cacao leaves for both amendments.
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References
Adriano DC (2001) Trace elements in terrestrial environments biogeochemistry bioavailability and risks of metals, 2nd edn. Springer-Verlag, New York. https://doi.org/10.1007/978-0-387-21510-5
Ahmad M, Rajapaksha AU, Lim J, Zhang M, Bolan N, Mohan D, Vithanage M, Lee S, Ok Y (2014) Biochar as a sorbent for contaminant management in soil and water: A review. Chemosphere 99:19–33
Anawar HM, Akter F, Solaiman ZM, Strezov V (2015) Biochar: and emerging panacea for remediation of soil contaminants from mining, industry and sewage wastes. Pedosphere 25:654–665
Arévalo-Gardini E, Arévalo-Hernández CO, Baligar VC, He ZL (2017) Heavy metal accumulation in leaves and beans of cacao (Theobroma cacao L.) in major cacao growing regions in Peru. Sci Total Environ 605:792–800. https://doi.org/10.1016/j.scitotenv.2017.06.122
Argüello D, Chavez E, Lauryssen F, Vanderschueren R, Smolders E, Montalvo D (2019) Soil properties and agronomic factors affecting cadmium concentrations in cacao beans: a nationwide survey in Ecuador. Sci Total Environ 649:120–127. https://doi.org/10.1016/j.scitotenv.2018.08.292
Argüello D, Montalvo D, Blommaert H, Chavez E, Smolders E (2020) Surface soil liming reduces cadmium uptake in cacao seedlings but subsurface uptake is enhanced. J Environ Qual 49:1359–1369. https://doi.org/10.1002/jeq2.20123
Ashizawa A, Faroon O, Wright S, Tucker P, Jenkins K, Ingerman L, Rudisill C (2012) Toxicological profile for cadmium. Agency for Toxic Substances and Disease Registry, Atlanta
Aswathanarayana U (2001) Water resources management and the environment, 1st edn. CRC Press, pp 214. https://doi.org/10.1201/9780367807009
Barraza F, Schreck E, Lévêque T, Uzu G, López F, Ruales J, Prunier J, Marquet A, Maurice L (2017) Cadmium bioaccumulation and gastric bioaccessibility in cacao: a field study in areas impacted by oil activities in Ecuador. Environ Pollut 29:950–963. https://doi.org/10.1016/j.envpol.2017.07.080
Beesley L, Marmiroli M (2011) The immobilization and retention of soluble arsenic cadmium and zinc by biochar. Environ Pollut 159:474–480. https://doi.org/10.1016/j.envpol.2010.10.016
Borden KA, Anglaaere LCN, Adu-Bredu S, Isaac ME (2019) Root biomass variation of cocoa and implications for carbon stocks in agroforestry systems. Agroforest Syst 93:369–381
Brady NC, Weil RR (2004) Elements of the nature and properties of soils, 2nd edn. Pearson Prentice Hall, New Jersey, p 498
Gil JP, López-Zuleta S, Quiroga-Mateus RY, Benavides-Erazo J, Chaali N, Bravo D (2021) Cadmium distribution in soils, soil litter and cacao beans: a case study from Colombia. Int J Environ Sci Technol. https://doi.org/10.1007/s13762-021-03299-x
Chavez E, He ZL, Stoffella PJ, Mylavarapu RS, Li YC, Moyano B, Baligar VC (2015) Concentration of cadmium in cacao beans and its relationship with soil cadmium in southern Ecuador. Sci Total Environ 533:205–214. https://doi.org/10.1016/j.scitotenv.2015.06.106
Chavez E, He ZL, Stoffella PJ, Mylavarapu RS, Li YC, Baligar VC (2016) Chemical speciation of cadmium: an approach to evaluate plant-available cadmium in Ecuadorian soils under cacao production. Chemosphere 150:57–62. https://doi.org/10.1016/j.chemosphere.2016.02.013
Chen H, Zhang W, Yang X, Wang P, McGrath SP, Zhao FJ (2018) Effective methods to reduce cadmium accumulation in rice grain. Chemosphere 699–707. https://doi.org/10.1016/j.chemosphere.2018.05.143
Eckert D, Sims JT (1995) Recommended soil pH and lime requirement test. In: Smims JT, Wolf A (eds) Recommended Soil Testing Procedures for the Northeastern United States (Northeastern Regional Publication No. 493), pp 16–21
European Food Safety (2012) Cadmium dietary exposure in the European population. EFSA J 10(1):2551. https://doi.org/10.2903/j.efsa.2012.2551
Gee GW, Or D (2002) Particle-size analysis. In: Methods of soil analysis: Part 4 Physical methods. Dane Jacob H, Topp Clarke G (eds) Soil Science Society of America Madison WI, pp 255–293
Goulding KWT, Blake L (1998) Land use, liming and the mobilization of potentially toxic metals. Agric Ecosyst Environ 67:135–144
Gramlich A, Tandy S, Andres C, Chincheros Paniagua J, Armengot L, Schneider M, Schulin R (2017) Cadmium uptake by cacao trees in agroforestry and monoculture systems under conventional and organic management. Sci Total Environ 580:677–686. https://doi.org/10.1016/j.scitotenv.2016.12.014
Gramlich A, Tandy S, Gauggel C, López M, Perla D, Gonzalez V, Schulin R (2018) Soil cadmium uptake by cacao in Honduras. Sci Total Environ 612:370–378. https://doi.org/10.1016/j.scitotenv.2017.08.145
Grant CA, Sheppard SC (2008) Fertilizer impacts on cadmium availability in agricultural soils and crops. Human Ecol Risk Assess 14:210–228. https://doi.org/10.1080/10807030801934895
Greathouse DC, Laetsch WM, Phinney BO (1971) The shoot-growth rhythm of a tropical Theobroma cacao L. Am J Bot 58:281–286. https://doi.org/10.2307/2441407
Guo M, Song W, Tian J (2020) Biochar-facilitated soil remediation: Mechanisms and efficacy variations. Front Environ Sci 8:183. https://doi.org/10.3389/fenvs.2020.521512
He D, Cui J, Gao M, Wang W, Zhou J, Yang J, Wang J, Li Y, Jiang C, Peng Y (2019) Effects of soil amendments applied on cadmium availability soil enzyme activity and plant uptake in contaminated purple soil. Sci Total Environ 654:1364–1371. https://doi.org/10.1016/j.scitotenv.2018.11.059
Hussain M, Farooq M, Nawaz A, Al-Sadi AM, Solaiman ZM, Alghamdi SS, Ammara U, Ok YS, Siddique KHM (2017) Biochar for crop production: potential benefits and risks. J Soils Sediments 17:685–716. https://doi.org/10.1007/s11368-016-1360-2
Jain LK, Jain RK, Parewa HP, Ratnoo SD (2018) Manual on fundamentals of agronomy. Scientific publishers Jodhpur India, pp 45
Jiang J, Xu RK, Li Z (2012) Immobilization of Cu(II) Pb(II) and Cd(II) by the addition of rice straw derived biochar to a simulated polluted ultisol. J Haz Mat 229:145–150
Joint FAO/WHO Codex Alimentarius Commission (2018) Report of the 12th Session of the Codex Committee on contaminants in foods. Rome: FAO. Retrieved from http://www.fao.org/news/story/en/item/1143286/icode/
Kalra YP (1995) Determination of pH of soils by different methods: a collaborative study. J AOAC Int 78(2):310–321
Kaminski J, Silva LS, Ceretta CA, dos Santos DR (2007) Acidity and calagme in soils in southern Brazil: historical aspects and future perspectives. (in Portuguese). Top Soil Sci 5:307–332
Komkiene J, Baltrenaite E (2016) Biochar as adsorbent for removal of heavy metal ions [Cadmium(II) Copper(II) Lead(II) Zinc(II)] from aqueous phase. Int J Environ Sci Technol 13:471–482. https://doi.org/10.1007/s13762-015-0873-3
Lahori AH, Guo Z, Zhang Z, Li R, Mahar A, Awasthi MK, Shen F, Sial TA, Kumbhar F, Wang P, Jiang S (2017) Use of biochar as an amendment for remediation of heavy metal-contaminated soils: prospects and challenges. Pedosphere 27:991–1014. https://doi.org/10.1016/S1002-0160(17)60490-9
Laird DA, Fleming P, Davis DD, Horton R, Wang B, Karlen DL (2010) Impact of biochar amendments on the quality of a typical Midwestern agricultural soil. Geoderma 158:443–449. https://doi.org/10.1016/j.geoderma.2010.05.013
Lewis C, Lennon AM, Eudoxie G, Umaharan P (2018) Genetic variation in bioaccumulation and partitioning of cadmium in Theobroma cacao L. Sci Total Environ 640–641:696–703. https://doi.org/10.1016/j.scitotenv.2018.05.365
Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc iron manganese and copper. Soil Sci Soc Am J 42:421–428. https://doi.org/10.2136/sssaj1978.03615995004200030009x
Maddela NR, Kakarla D, García LC, Chakraborty S, Venkateswarlu K, Megharaj M (2020) Cacao-laden cadmium threatens human health and cacao economy: A critical view. Sci Total Environ 720:137645. https://doi.org/10.1016/j.scitotenv.2020.137645
McBride M, Sauve S, Hendershot W (1997) Solubility control of Cu, Zn, Cd and Pb in contaminated soils. Eur J Soil Sci 48:337–346
Mench M, Vangronsveld J, Lepp NW, Edwards R (1998) Physicochemical aspects and efficiency of trace element immobilization by soil amendments. In: Cunningham SD (ed) Vangronsveld J. In-Situ Inactivation and Phytorestoration. Springer Verlag Berlin Heidelberg, Metal-Contaminated Soils, pp 151–182
Meter A, Atkinson RJ, Laliberte B (2019) Cadmium in cacao from Latin America and the Caribbean: A review of research and potential mitigation solutions. Bioversity International Rome. 73, pp ISBN: 978–92–9255–135–3
Moser G, Leuschner C, Hertel D, Hölscher D, Köhler M, Leitner D, Michalzik B, Prihastanti E, Tjitrosemito S, Schwendenmann L (2010) Response of cocoa trees (Theobroma cacao) to a 13-month desiccation period in Sulawesi, Indonesia. Agroforest Syst 79:171–187
Mounicou S, Szpunar J, Lobinski R, Andrey D, Blake CJ (2002) Bioavailability of cadmium and lead in cacao: comparison of extraction procedures prior to size exclusion fast-flow liquid chromatography with inductively coupled plasma mass spectrometric detection (SEC-ICP-MS). J Anal At Spectrom 17(8):880–886. https://doi.org/10.1039/b201639g
Mullins GL, Alley MM, Wysor WG, Phillips SB (2011) Sources of lime for acid soils in Virginia. Virginia Cooperative Extension. http://pubs.ext.vt.edu/452/452-510/452-510_pdf.pdf. Accessed Jan 10 2021
Natale W, Rozane DE, de Medeiros Corrêa MC, Parent LE, de Deus JAL (2020) Chapter 48 - Diagnosis and management of nutrient constraints in guava in: Srivastava AK, Hu CBT-FC (Eds) Elsevier, pp 711–722. https://doi.org/10.1016/B978-0-12-818732-6.00048-4
Niether W, Schneidewind U, Fuchs M, Schneider M, Armengot L (2019) Below- and aboveground production in cocoa monocultures and agroforestry systems. Sci Total Environ 657:558–567. https://doi.org/10.1016/j.scitotenv.2018.12.050
NCSS (2007) Number Cruncher Statistical System for Windows Kaysville Utah USA.
O’Connor D, Peng T, Zhang J, Tsang DCW, Alessi DS, Shen Z, Bolan NS, Hou D (2018) Biochar application for the remediation of heavy metal polluted land: A review of in situ field trials. Sci Total Environ 619–620:815–826. https://doi.org/10.1016/j.scitotenv.2017.11.132
Park JH, Choppala GK, Bolan NS, Chung JW, Chuasavathi T (2011) Biochar reduces the bioavailability and phytotoxicity of heavy metals. Plant Soil 348(1–2):439–451. https://doi.org/10.1007/s11104-011-0948-y
Ramtahal G, Chang Yen I, Ahmad N, Bekele I, Bekele F, Maharaj K (2015) Prediction of soil cadmium bioavailability to cacao (Theobroma cacao L.) using single-step extraction procedures. Commun Soil Sci Plant Anal 46:2585–2594
Ramtahal G, Chang Yen I, Bekele I, Bekele F, Wilson L, Maharaj K, Harrynanan L (2016) Relationships between cadmium in tissues of cacao trees and soils in plantations of Trinidad and Tobago. Food Nutr Sci 07(01):37–43. https://doi.org/10.4236/fns.2016.71005
Ramtahal G, Chang Yen I, Hamid A, Bekele I, Bekele F, Maharaj K, Harrynanan L (2018) The effect of liming on the availability of cadmium in soils and its uptake in cacao (Theobroma cacao L.) in Trinidad and Tobago. Commun Soil Sci Plant Anal 49(19):2456–2464. https://doi.org/10.1080/00103624.2018.1510955
Ramtahal G, Umaharan P, Hanuman A, Davis C, Ali L (2019) The effectiveness of soil amendments biochar and lime in mitigating cadmium bioaccumulation in Theobroma cacao L. Sci Total Eviron 693:133563. https://doi.org/10.1016/j.scitotenv.2019.07.369
Ruysschaert G, Nelissen V, Postma R, Bruun E, O'Toole A, Hammond J, Rödger JM, Hylander L, Kihlberg T, Zwart K, Hauggaard-Nielsen H, Shackley S (2016) Field applications of pure biochar in the North Sea region and across Europe. Biochar in European Soils and Agriculture: Science and Practice. Taylor and Francis Inc, pp 99–135 https://doi.org/10.4324/9781315884462.
Shahid M, Dumat C, Khalid S, Niazi NK, Antunes PMC (2016) Cadmium bioavailability uptake toxicity and detoxification in soil-plant system. Rev Environ Contam Toxicol 241:73–137. https://doi.org/10.1007/398_2016_8
Stafford A, Jeyakumar P, Hedley M, Anderson C (2018) Influence of soil moisture status on soil cadmium phytoavailability and accumulation in plantain (Plantago lanceolata). Soil Syst 2(1):9. https://doi.org/10.3390/soils2010009
Summer ME, Miller WP (1996) Cation exchange capacity and exchange coefficients. In: Sparks DL (ed) Methods of soil analysis. Part 3. Chemical Methods. Soil Science Society ofAmerica, Madison, WI, USA, pp 1201–1229
Sun J, Fan Q, Ma J, Cui L, Quan G, Yan J, Wu L, Hina K, Abdul B, Wang H (2020) Effects of biochar on cadmium (Cd) uptake in vegetables and its natural downward movement in saline-alkali soil. Environ Pollut Bioavailab 32:36–46. https://doi.org/10.1080/26395940.2020.1714487
Tsadilas CD, Karaivazoglou NA, Tsotsolis NC, Stamatiadis S, Samaras V (2005) Cadmium uptake by tobacco as affected by liming N form and year of cultivation. Environ Pollut 134:239–246. https://doi.org/10.1016/j.envpol.2004.08.008
Tlustoš P, Száková J, Hrubý J, Hartman I, Najmanová J, Nedělník J, Pavlíková D, Batysta M (2006) Removal of As Cd Pb and Zn from contaminated soil by high biomass producing plants. Plant Soil Environ 52:413–423
USEPA United States Environmental Protection Agency (2007) SW-846 test method 3051A: microwave assisted acid digestion of sediments sludges soils and oils. https://www.epa.gov/sites/production/files/2015-12/documents/3051a.pdf
Van Zwieten L, Kimber S, Morris S, Chan K, Downie A, Rust J, Joseph S, Cowie A (2010) Effects of biochar from slow pyrolysis of papermill waste on agronomic performance and soil fertility. Plant Soil 327:235–246. https://doi.org/10.1007/s11104-009-0050-x
Vanderschueren R, Argüello D, Blommaert H, Montalvo D, Barraza F, Maurice L, Schreck E, Schulin R, Lewis C, Vazquez JL, Umaharan P, Chavez E, Sarret G, Smolders E (2021) Mitigating the level of cadmium in cacao products: reviewing the transfer of cadmium from soil to chocolate bar. Sci Total Environ 146779. https://doi.org/10.1016/j.scitotenv.2021.146779
Violante A, Cozzolino V, Perelomov L, Caporale A, Pigna M (2010) Mobility and bioavailability of heavy metals and metalloids in soil environments. J Soil Sci Plant Nutr 10(3):268–292. https://doi.org/10.4067/S0718-95162010000100005
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37(1):29–38
WHPA (Western Plant Health Association) (2018) Methods of applying fertilizer. In: Pier J, Barlow D (eds) Western fertilizer handbook (third horticulture edn). Waveland Press Inc., IL USA, pp 231
Wolkowski R, Laboski C (2011) Soil pH and crop response to lime source and tillage. In Proceedings of the 2011 Wisconsin Crop Management Conference January 11–13, pp 38–45
Woldetsadik D, Drechsel P, Keraita B, Marschner B, Itanna F, Gebrekidan H (2016) Effects of biochar and alkaline amendments on cadmium immobilization, selected nutrient and cadmium concentrations of lettuce (Lactuca sativa) in two contrasting soils. Springerplus 5:39. https://doi.org/10.1186/s40064-016-2019-6
Wood GAR, Lass RA (1985) Cocoa. Longmans, New York
World Cacao Foundation (2019) California Proposition 65: What will change for US chocolate lovers and cacao farmers in Latin America? https://www.worldcacaofoundation.org/blog/california-proposition-65-what-will-change-for-us-chocolate-lovers-and-cacao-farmers-in-latin-america/#:~:text=Proposition%2065%20regulates%20the%20presencein%20different%20products%2C%20including%20chocolate.&text=After%20several%20years%20of%20negotiationsCalifornia%2C%20regardless%20of%20its%20origin. Accessed Jan 18 2021
Zug KLM, HuamaníYupanqui HA, Meyberg F, Cierjacks JS, Cierjacks A (2019) Cadmium accumulation in Peruvian cacao (Theobroma cacao L.) and opportunities for mitigation. Water Air Soil Pollut. 230:72. https://doi.org/10.1007/s11270-019-4109-x
Acknowledgements
The authors would like to thank the Joint Cocoa Research Fund (JRF) of the European Cocoa Association (ECA), Chocolates, Biscuits and Confectionery of Europe (CAOBISCO), and the Federation of Cocoa Commerce (FCC) for the financial support of this investigation.
We would also like to acknowledge and thank Mr. Shazam Maharaj for allowing us to conduct this study on his plantation.
Funding
Joint Research Fund (JRF) of the European Cocoa Association (ECA), Chocolates, Biscuits and Confectionery of Europe (CAOBISCO), and the Federation of Cocoa Commerce (FCC).
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Dr. Gideon Ramtahal and Prof. Pathmanathan Umaharan contributed to the study conception and design. Material preparation, data collection and analysis were performed by Ms. Carisa Davis, Mr. Corey roberts, Mr. Anand Hanuman and Mr. Leon Ali. The first draft of the manuscript was written by Dr. Gideon Ramtahal and Prof. Pathmanathan Umaharan and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Ramtahal, G., Umaharan, P., Davis, C. et al. Mitigation of cadmium uptake in Theobroma cacao L: efficacy of soil application methods of hydrated lime and biochar. Plant Soil 477, 281–296 (2022). https://doi.org/10.1007/s11104-022-05422-4
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DOI: https://doi.org/10.1007/s11104-022-05422-4