Crops are the main source of toxic cadmium for humans due to uptake from naturally or anthropogenically polluted soils. Chronic Cd ingestion causes kidney, liver, and skeletal damage along with an increased risk of cancer. Cacao is known to accumulate Cd and may therefore be potentially harmful to human health. Consequently, cocoa production on intensely polluted soils should be avoided. Cocoa products from South America in particular often exceed the limits for Cd, but the factors that drive Cd uptake are as yet poorly studied. In this study, we measured Cd concentrations in defatted cocoa powder from unfermented seeds of 40 different trees on 20 farms in the Huánuco Region, Peru, and associated the Cd levels with the farms’ soil, field management, and nearby vegetation diversity. The mean Cd concentration found in cocoa of the study region was 2.46 mg kg−1 with a range of 0.2–12.56 mg kg−1. The maximum content measured was an order of magnitude higher than the allowed limit of 1.5 mg kg−1 and was the highest reported so far in the literature. Soil Cd content was the most relevant driver of Cd concentration in cacao. In addition, fertilizer use caused significantly higher Cd concentration in cocoa. Higher biodiversity of herbs was positively correlated with Cd contents in cocoa. The study shows that, apart from the known correlation of soil conditions with Cd accumulation in cacao seeds, changes in fertilization and plant composition may be promising measures to counteract Cd contamination in regions with high soil Cd content.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Acebo-Guerrero, Y., Hernández-Rodríguez, A., Heydrich-Pérez, M., El Jaziri, M., & Hernández-Lauzardo, A. (2012). Management of black pod rot in cacao (Theobroma cacao L.): a review. Fruits, 67, 41–48.
Ahenkorah, Y., Halm, B. J., Appiah, M. R., Akrofi, G. S., & Yirenkyi, J. E. K. (1987). Twenty years results from a shade and fertilizer trial on Amazon cacao (Theobroma cacao) in Ghana. Experimental Agriculture, 23, 31–39.
Aikpokpodion, P. E., Lajide, L., & Aiyesanmi, A. F. (2012). Metal fraction in soils collected from selected cocoa plantations in Ogun State, Nigeria. World Applied Science Journal, 20, 628–636.
Amal, A. M., Hossam, S. E.-B., & Mohamed, M. R. (2009). Cadmium stress induced change in some hydrolytic enzymes, free radical formation and ultrastructural disorders in radish plant. Electronic Journal of Environmental, Agricultural and Food Chemistry, 8, 969–983.
Araujo, Q. R., Fernandes, C. A. F., Ribeiro, D. O., Efraim, P., Steinmeier, D., Lieberei, R., Bastide, P., & Araujo, T. G. (2014). Cocoa quality index—a proposal. Food Control, 46, 49–54.
Arévalo-Gardini, E., Arévalo-Hernández, C. O., Baligar, V. C., & He, Z. L. (2017). Heavy metals accumulation in leaves and beans of cacao (Theobrome cacao L.) in major cacao growing regions in Peru. Science of the Total Environment, 605, 792–800.
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. Science of the Total Environment, 649, 120–127.
Bansah, K. J., & Addo, W. K. (2016). Phytoremediation potential of plants grown on reclaimed spoil lands. Ghana Mining Journal, 16, 68–75.
Bates, D. M. (2010). Lme4: mixed-effects modeling with R. Vienna: R Development Core Team.
Bisseleua, D., Hervé, B., & Vidal, S. (2008). Plant biodiversity and vegetation structure in traditional cocoa forest gardens in southern Cameroon under different management. Biodiversity and Conservation, 17, 1821–1835.
Boza, E. J., Motamayor, J. C., Amores, F. M., Cedeño-Amador, S., Tondo, C. L., Livingstone, D. S., Schnell, R. J., & Gutiérrez, O. A. (2014). Genetic characterization of the cacao cultivar CCN 51: its impact and significance on global cacao improvement and production. Journal of the American Society for Horticultural Science, 139, 219–229.
Braun-Blanquet, J. (1964). Pflanzensoziologie: Grundzüge der Vegetationskunde (2nd ed.). Wien: Springer.
CEM (2001). Operational Manual: Mars 5 Microwave Accelerated Reaction System. North Carolina: CEM Corporation.
CEM (2004). Plant Tissue 2: Microwave Sample Preparation Note: XprAG-2 Rev. Date: 6/04. Category: Agricultural.
Chaney, R. L., Malik, M., Li, Y. M., Brown, S. L., Brewer, E. P., Angle, J. S., & Baker, A. J. M. (1997). Phytoremediation of soil metals. Environmental Biotechnology, 8, 279–284.
Chavez, E., He, Z. I., Stoffella, P. J., Mylavarapu, R. S., Li, Y. C., Moyano, B., & Baligar, V. C. (2015). Concentratiom of cadmium in cacao beans and its relationship with soil cadmium in southern Ecuador. Science of the Total Environment, 533, 205–214.
Chen, T., Chang, Q., Clevers, J. G. P. W., & Kooistra, L. (2015). Rapid identification of soil cadmium pollution risk at regional scale based on visible and near-infrared spectroscopy. Environmental Pollution, 206, 217–226.
Cicuzza, D., & Kessler, M. (2011). Conservation value of cacao agroforestry systems for terrestrial herbaceous species in central Sulawesi, Indonesia. Biotropica, 43, 755–762.
Cierjacks, A., Pommeranz, M., Schulz, K., & Almeida-Cortez, J. (2016). Is crop yield related to weed species diversity and biomass in coconut and banana fields in northeastern Brazil? Agriculture, Ecosystem, and Environment, 220, 175–183.
Clough, Y., Faust, H., & Tscharntke, T. (2009a). Cacao boom and bust: sustainability of agroforests and opportunities for biodiversity conservation. Mini-review. Conservation Letters, 2, 197–205.
Clough, Y., Putra, D. D., Pitopang, R., & Tscharntke, T. (2009b). Local and landscape factors determine functional bird diversity in Indonesian cacao agroforestry. Biological Conservation, 142, 1032–1041.
Clough, Y., Barkmann, J., Juhrbandt, J., Kessler, M., Wanger, T. C., Anshary, A., Buchori, D., Cicuzza, D., Darras, K., Putra, D. D., Erasmi, S., Pitopang, R., Schmidt, C., Schulze, C. H., Seidel, D., Steffan-Dewenter, I., Stenchly, K., Vidal, S., Weist, M., Wielgoss, A. C., & Tsharntke, T. (2011). Combining high biodiversity with high yield in tropical agroforests. PNAS, 108, 8311–8316.
European Commission (2014). Commission Regulation (EU) No 488/2014 of 12 May 2014 amending Regulation (EC) No 1881/2006 as regards maximum levels of cadmium in foodstuffs. Official Journal of the European Union, L138, 75–79.
Dudjak, J., Lachman, J., Miholová, D., Kolihová, D., & Pivec, V. (2004). Effect of cadmium on polyphenol content in young barley plants (Hordeum vulgare L.). Plant Soil and Environment, 50, 471–477.
Elwers, S., Zambrano, A., Rhosius, C., & Lieberei, R. (2009). Differences between the content of phenolic compounds in Criollo, Forastero and Trinitario cocoa seeds (Theobroma cacao L.). European Food Research Technologies, 229, 937–948.
European Food Safety Authority (EFSA). (2012). Cadmium dietary exposure in the European population. EFSA Journal, 10, 1–37.
Fauziah, C. I., Rozita, O., Zauyah, S., Anuar, A. R., & Shamshuddin, J. (2001). Heavy metals content in soils of Peninsular Malaysia grown with cocoa and cocoa tissues. Malaysian Journal of Soil Science, 5, 47–58.
Food and Agriculture Organization of the United Nations (FAO), World Health Organization (WHO). (2016). Proposed draft maximum levels for cadmium in chocolate and cocoa-derived products. Rotterdam: Codex Committee on Contaminants in Food, Tenth Session.
Frey, W., & Lösch, R. (2010). Geobotanik: Pflanze und Vegetation in Raum und Zeit (3rd ed.). Heidelberg: Spektrum Akademischer Verlag.
García Carrión, L. F. (2012). Catálogo de Cultivares de Cacao del Perú (3rd ed.). Lima: Ministerio de Agricultura, Dirección General de Competividad Agraria.
Gramlich, A., Tandy, S., Andres, C., Chincheros Paniagua, J., Armengot, L., Schneider, M., & Schulin, R. (2016). Cadmium uptake by cocoa trees in agroforestry and monoculture systems under conventional and organic management. Science of the Total Environment, 580, 677–686.
Gramlich, A., Tandy, S., Gauggel, C., López, M., Perla, D., Gonzales, V., & Schulin, R. (2017). Soil cadmium uptake by cacao in Honduras. Science of the Total Environment, 612, 370–378.
Grant, C. A., Buckley, W. T., Bailey, L. D., & Selles, F. (1996). Cadmium accumulation in crops. Canadian Journal of Plant Science, 78, 1–17.
Greger, M., Kabir, A. H., Landberg, T., Maity, P., & Lindberg, S. (2016). Silicate reduces cadmium uptake into cells of wheat. Environmental Pollution, 211, 90–97.
Groeneveld, J., Tscharntke, T., Moser, G., & Clough, Y. (2010). Experimental evidence for stronger cacao yield limitation by pollination than by plant resources. Perspectives in Plant Ecology, Evolution and Systematics, 12, 183–191.
Hahne, H. C. H., & Kroontje, W. (1973). Significance of pH and chloride concentration on behaviour of heavy metal pollutants: mercury(II), cadmium(II), zinc(II) and lead(II). Journal of Environmental Quality, 2, 444–450.
Hanafi, M. M., & Maria, G. J. (1998). Cadmium and zinc in acid tropical soils: III. Response of cocoa seedlings in a greenhouse experiment. Communications in Soil Science and Plant Analysis, 29, 1949–1960.
He, Q. B., & Singh, B. R. (1994a). Crop uptake of cadmium from phosphorus fertilizers: I. Yield and cadmium content. Water, Air, and Soil Pollution, 74, 251–265.
He, Q. B., & Singh, B. R. (1994b). Crop uptake of cadmium from phosphorus fertilizers: II. Relationship with extractable soil cadmium. Water, Air, and Soil Pollution, 74, 267–280.
Hoenig, M., & de Kersabiec, A.-M. (1996). Sample preparation steps for analysis by atomic spectroscopy methods: present status. Spectrochimica Acta Part B, 51, 1297–1307.
Holm, P. E., Christensen, T. H., Tjell, J. C., & McGrath, S. P. (1995). Heavy metals in the environment: speciation of cadmium and zinc with application to soil solutions. Journal of Environmental Quality, 24, 183–190.
Hoseini, S. M., & Zargari, F. (2013). Cadmium in plants: a review. International Journal of Farming and Allied Science, 2, 2002–2004.
Ji, P., Sun, T., Song, Y., Ackland, M. L., & Liu, Y. (2011). Strategies for enhancing the phytoremediation of cadmium-contaminated agricultural soils by Solanum nigrum L. Environmental Pollution, 159, 762–768.
Jung, M. C., & Thornton, I. (1996). Heavy metal contamination of soils and plants in the vicinity of a lead-zinc mine, Korea. Applied Geochemistry, 11, 53–59.
Kabata-Pendias, A. (2010). Trace elements in soils and plants (4th ed.). Boca Raton: CRC.
Kieck, J. S., Zug, K. L. M., Huamaní Yupanqui, H. A., Gómez Aliaga, R., & Cierjacks, A. (2016). Plant diversity effects on crop yield, pathogen incidence, and secondary metabolism on cacao farms in Peruvian Amazonia. Agriculture, Ecosystem and Environment, 222, 223–234.
Kindt, R., & Coe, R. (2005). Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. Nairobi: ICRAF.
Kirbag Zengin, F., & Munzuroglu, O. (2006). Toxic effects of cadmium (Cd++) on metabolism of sunflower (Helianthus annuus L.) seedlings. Acta Agriculturae Scandinavica Section B-Soil and Plant Science, 56, 224–229.
Kováčik, J., Klejdus, B., Hedbavny, J., Štork, F., & Bačkor, M. (2009). Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamimilla plants. Plant and Soil, 320, 231–242.
Lavid, N., Schwartz, A., Lewinsohn, E., & Tel-Or, E. (2001). Phenols and phenol oxidases are involved in cadmium accumulation in the water plants Nymphoides peltata (Menyanthaceae) and Nymphaeae (Nymphaeaeceae). Planta, 214, 189–195.
Li, L.-Z., Tu, C., Peijnenburg, W. J. G. M., & Luo, Y.-M. (2017). Characteristics of cadmium uptake and membrane transport in roots of intact wheat (Triticum aestivum L.) seedlings. Environmental Pollution, 221, 351–358.
Lieberei, R., & Reisdorff, C. (2012). Nutzpflanzen, 8. Auflage. Stuttgart: Thieme.
Liu, Y., Zhang, C., Zhao, Y., Sun, S., & Liu, Z. (2016). Effects of growing seasons and genotypes on the accumulation of cadmium and mineral nutrients in rice grown in cadmium contaminated soils. Science of the Total Environment, 579, 1282–1288.
Magurran, A. E. (1988). Why diversity? Ecological diversity and its measurement. Berlin: Springer.
McLaughlin, M., & Singh, B. (1995). Cadmium in soils and plants. Norway: Agricultural University of Norway.
Mengel, K., & Kirkby, E. A. (1978). Principles of plant nutrition. Berne: International Potash Institute.
Moser, G., Leuschner, C., Hertel, D., Hölscher, D., Köhler, M., Leitner, D., Michalzik, B., Prihastanti, E., Tjitrosemito, S., & Schwendenmann, L. (2010). Response of cocoa tree (Theobroma cacao) to a 13-month desication period in Sulawesi, Indonesia. Agroforestry Systems, 79, 171–187.
Mounicou, S., Szpunar, J., Lobinski, R., Andrey, D., & Blake, C.-J. (2002a). Bioavailibility of cadmium and lead in cocoa: comparison of extraction procedures prior to size-exclusion fast-flow liquid chromatography with inductively coupled plasma mass spectrometric detection (SEC-ICP-MS). The Royal Society of Chemistry, 17, 880–886.
Mounicou, S., Szunar, J., Andrey, D., Blake, C., & Lobinski, R. (2002b). Development of a sequential enzymolysis approach for the evaluation of the bioaccessibility of Cd and Pb from cocoa. The Royal Society of Chemistry, 127, 1638–1641.
Mounicou, S., Szpunar, J., Andrey, D., Blake, C., & Lobinski, R. (2003). Concentrations and bioavailability of cadmium and lead in cocoa powder and related products. Food Additives and Contaminants, 20, 343–352.
Mullins, G. L., Sommers, L. E., & Barber, S. A. (1986). Modeling the plant uptake of cadmium and zinc from soils treated with sewage sludge. Soil Science Society of America Journal, 50, 1245–1250.
Niemenak, N., Rohsius, C., Elwers, S., Ndoumou, D. O., & Lieberei, R. (2006). Comparative study of different cocoa (Theobroma cacao L.) clones in terms of their phenolic and anthocyanins contents. Journal of Food Composition and Analysis, 19, 612–619.
Ogunlade, M. O., & Agbeniyi, S. O. (2011). Impact of pesticides use on heavy metals pollution in cocoa soils of Cross-River State, Nigeria. African Journal of Agricultural Research, 6, 3725–3728.
Peet, R. K. (1974). The measurement of species diversity. Annual Review of Ecology and Systematics, 5, 285–307.
Pinheiro, J. C., & Bates, D. M. (1995). Mixed-effects models in S and S-Plus. New York: Springer.
Prasad, M. N. V. (1995). Cadmium toxicity and tolerance in vascular plants. Environmental and Experimental Botany, 35, 525–545.
Prugarová, A., & Kovác, M. (1987). Lead and cadmium content in cocoa beans. Food, 31, 635–644.
Purser, W. F. C., & Purser, M. (2008). Metal-mining in Peru, past and present. Austin: Praeger Publishers, University of Texas.
R Development Core Team. (2014). R: a language and environment for statistical computing, version 3.1.2. Vienna: Foundation for Statistical Computing https://www.r-project.org/, 20 April 2017.
Ramtahal, G., Yen, I. C., Seegobin, D., Bekele, I., Bekele, F., Wilson, L., & Harrynanan, L. (2012). Investigation of the effect of mycorrhizal fungi on cadmium accumulation in cacao. Proceedings of the Caribbean Food Crops Society, 48, 147–152.
Ripley, B. (2015). Package MASS. R package version 7 (pp. 3–44). Vienna: R Development Core Team.
Sager, M. (2012). Chocolate and cocoa products as a source of essential elements in nutrition. Nutrition and Food Science, 2, 1–10.
Salt, D. E., Blaylock, M., Kumar, N. P. B. A., Dushenkov, V., Ensley, B. D., Chet, I., & Raskin, I. (1995). Phytoremediation: novel strategy for the removal of toxic metals from environment using plants. Biotechnology, 13, 468–474.
Samedani, B., Juraimi, A. S., Abdullah, S. A. S., Rafii, M. Y., Rahim, A. A., & Anwar, M. P. (2014). Effects of cover crops on weed community and oil palm yield. International Journal of Agricultural Biology, 16, 23–31.
Schroeder, H. A., Nason, M. D. A. P., Tipton, I. H., & Balassa, J. J. (1966). Essential trace metals in man: zinc relation to environmental cadmium. Journal of Chronic Diseases, 20, 179–210.
Schroth, G., Läderach, P., Martinez-Valle, A. I., Bunn, C., & Jassogne, L. (2016). Vulnerability to climate change of cocoa in West Africa: patterns, opportunities and limits to adaption. Science of the Total Environment, 556, 231–241.
Schwendenmann, L., Veldkamp, E., Gerald, M., Hölscher, D., Köhler, M., Clough, Y., Anas, I., Djajakirana, G., Erasmi, S., Hertel, D., Leitner, D., Leuschner, C., Michalzik, B., Propastin, P., Tjoa, A., Tscharntke, T., & van Straaten, O. (2010). Effects of an experimental drought on the functioning of a cacao agroforestry system, Sulawesi, Indonesia. Global Change Biology, 16, 1515–1530.
Smith, R. G., Mortensen, D. A., & Ryan, M. R. (2010). A new hypothesis for the functional role of diversity in mediating resource pools and weed–crop competition in agroecosystems. Weed Research, 50, 37–48.
Soberanis, W., Rios, R., Arévalo, E., Zuniga, L., Cabezas, O., & Krauss, U. (1991). Increased frequency of phytosanitary pod removal in cacao (Theobroma cacao) increases yield economically in eastern Peru. Crop Protection, 18, 677–685.
Stenchly, K., Clough, Y., Buchori, D., & Tscharntke, T. (2011). Spider web guilds in cacao agroforestry—comparing tree, plot and landscape-scale management. Diversity and Distributions, 17, 748–756.
Stenchly, K., Clough, Y., & Tscharntke, T. (2012). Spider species richness in cacao agroforestry systems, comparing vertical strata, local management and distance to forest. Agriculture, Ecosystems and Environment, 149, 189–194.
Stoll, L. (2010). Biochemische Indikatoren für Keimung und Fermentation in Samen von Kakao (Theobroma cacao L.). Doctoral dissertation, Hamburg: Universität Hamburg
Strug, D. T. (1985). The foreign politics of cocaine. Comment on a plan to eradicate the coca leaf in Peru. In Paicini & Franquemont (Eds.), Coca and cocaine. Effect on people and policy in Latin America. Proceedings of the conference: the coca leaf and its derivates—biology, society and policy (pp. 73–88). New York: Cornell University.
Tang, H., Li, T., Yu, H., & Zhang, X. (2016). Cadmium accumulation characteristics and removal potentials of high cadmium accumulating rice line grown in cadmium-contaminated soils. Environmental Science and Pollution Research, 23, 15351–15357.
Thyssen, G. M., Keil, C., Wolff, M., Sperling, M., Kadow, D., Haase, H., & Karst, U. (2018). Bioimaging of the elemental distribution in cocoa beans by means of LA-ICP-TQMS. Journal of Analytical Atomic Spectrometry, 33, 187–194.
Tscharntke, T., Clough, Y., Bhagwat, S. A., Buchori, D., Faust, H., Hertl, D., Hölscher, D., Juhrbandt, J., Kessler, M., Perfecto, I., Scherber, C., Schroth, G., Veldkamp, E., & Wanger, T. C. (2011). Multifunctional shade-tree management in tropical agroforestry landscapes—a review. Journal of Applied Ecology, 48, 619–629.
Tugwell, S., & Branch, G. M. (1989). Differential polyphenolic distribution among tissues in the kelps Ecklonia maxima, Laminaria pallida and Macrocystis angustifolia in relation to plant-defence theory. Journal of Experimental Marine Biology and Ecology, 129, 219–230.
Vaughn, K. C., & Duke, S. O. (1984). Function of polyphenol oxidase in higher plants. Physiologia Plantarum, 60, 106–112.
Villa, J. E. L., Peixoto, R. R. A., & Cadore, S. (2014). Cadmium and lead in chocolates commercialized in Brazil. Journal of Agricultural and Food Chemistry, 62, 8759–8763.
Wagner, G. J. (1993). Accumulation of cadmium in crop plants and its consequences to human health. Advances in Agronomy, 51, 172–212.
Walter, H., & Breckle, S. (2004). Ökologie der Erde, 3. Auflage, Band 2 Spezielle Ökologie der Tropischen und Subtropischen Zonen. München: Elsevier GmbH.
Welz, B., & Sperling, M. (2008). Atomic absorption spectrometry. Third, completely revised edition. Weinheim: Wiley-VCH.
Williams, C. H., & David, D. J. (1976). The accumulation in soil of cadmium residues from phosphate fertilizers and their effect on the cadmium content of plants. Soil Science, 121, 86–93.
World Health Organization (WHO). (2010). Preventing disease through healthy environment. Exposure to cadmium: a major public health concern. Geneva: World Health Organization.
Zhang, D., Gardini, E. A., Motilal, L. A., Baligar, V., Bailey, B., Zuñiga-Cernades, L., Arevalo-Arevalo, C. E., & Meinhardt, L. (2011). Dissecting genetic structure in farmer selections of Theobroma cacao in the Peruvian Amazon: implications for on farm conservation and rehabilitation. Tropical Plant Biology, 4, 106–116.
Zhu, H., Chen, C., Zhu, Q., & Huang, D. (2016). Effects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical China. Environmental Pollution, 219, 99–106.
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A., & Smith, G. M. (2009). Mixed effects models and extensions in ecology with R. New York: Springer.
This study was part of a degree thesis carried out at Universität Hamburg in cooperation with Universidad Nacional Agraria de la Selva (UNAS). Travel expenses were provided by “Hamburglobal.” We thank the team of Alianza Cacao Peru for their support with field analyses. Students from the UNAS helped in the field and the laboratory. At Institute of Plant Science and Microbiology, we thank Thomas Tumforde for assisting with the HPLC analyses of secondary compounds and Detlef Böhm for support in the laboratory. Barbara Rudolph and the working group of Jens Rohwer gave administrative support. Peter Müller and Kelaine Ravdin kindly checked our English.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
About this article
Cite this article
Zug, K.L.M., Huamaní Yupanqui, H.A., Meyberg, F. et al. Cadmium Accumulation in Peruvian Cacao (Theobroma cacao L.) and Opportunities for Mitigation. Water Air Soil Pollut 230, 72 (2019). https://doi.org/10.1007/s11270-019-4109-x
- Heavy metal pollution
- South America
- Food security
- Food chain