Abstract
Because crop uptake of arsenic from soils poses a human health concern, this study examines the effect of plant species, neighborhood, and planting density on arsenic uptake by brassicas grown with companion crops. At a field site contaminated by arsenic and lead, we measured arsenic uptake in arugula (Eruca sativa) and collards (Brassica oleracea var. acephala) grown in arrangements varying in species diversity and density. We further tested the effect of species diversity on arsenic uptake in two greenhouse experiments with arsenic-spiked potting soil, one test using brassicaceous plants with intercropped pairs of arugula, collards, and kale (B. oleracea var. acephala). The other had intercropped pairs of arugula, lettuce (Lactuca sativa), and marigold (Tagetes patula). Arugula in all cropping arrangements accumulated the highest and most variable concentrations of arsenic compared to other species, with neither species diversity in the companion crops nor planting density affecting arsenic uptake. We observed increased phosphorus and sulfur uptake by arugula exposed to soil arsenic in the greenhouse brassica intercropping experiments, a result that may be explained by a biological response to arsenic or competition of arsenate with phosphate and sulfate for adsorption sites in the soil. Arsenic uptake was largely independent of plant-plant facilitation effects sometimes reported for other elements, possibly because of strong buffering of the bioavailable fraction of arsenic in the soils tested.
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Bani, A., Echevarri, G., Zhang, X., Benizri, E., Laubie, B., Morel, J. L., & Simonot, M. O. (2015). The effect of plant density in nickel-phytomining field experiments with Alyssum murale in Albania. Australian Journal Botany, 63, 72–77.
Biedrzycki, M. L., Jilany, T. A., Dudley, S. A., & Bais, H. P. (2010). Root exudates mediate kin recognition in plants. Communicative & Integrative Biology, 3, 28–35.
Boyd, R. S., & Odom, J. W. (1999). Variation in nickel content in the nickel-hyperaccumulating shrub Psychotria douarrei (Rubiaceae) from New Caledonia. Biotropica, 31, 403–410.
Burló, F., Guijarro, I., Carbonell-Barrachina, A. A., Valero, D., & Martínez-Sánchez, F. (1999). Arsenic species: effects on and accumulation by tomato plants. Journal of Agricultural and Food Chemistry, 47, 1247–1253.
Carbonell, A. A., Aarabi, M. A., DeLaune, R. D., Gambrell, R. P., & Patrick, W. H. (1998). Arsenic in wetland vegetation: availability, phytotoxicity, uptake and effects on plant growth and nutrition. Science of The Total Environment, 217, 189–199.
Cattani, I., Capri, E., Boccelli, R., & Del Re, A. A. M. (2009). Assessment of arsenic availability to roots in contaminated Tuscany soils by a diffusion gradient in thin films (DGT) method and uptake by Pteris vittata and Agrostis capillaris. European Journal of Soil Science, 60, 539–548.
Chintakovid, W., Visoottiviseth, P., Khokiattiwong, S., & Lauengsuchonkul, S. (2008). Potential of the hybrid marigolds for arsenic phytoremediation and income generation of remediators in Ron Philbun District, Thailand. Chemosphere, 70, 1532–1537.
Chung, J. Y., Yu, S. D., & Hong, Y. S. (2014). Environmental source of arsenic exposure. Journal of Preventive Medicine and Public Health, 47, 253–257.
De Olivieri, L. K., Melo, C. A., Goveia, D., Lobo, F. A., Hernandez, M. A. A., Fraceto, L. F., & Rosa, A. H. (2015). Adsorption/desorption of arsenic by tropical peat: influence of organic matter, iron and aluminium. Environmental Technology, 36, 149–159.
El-Zohri, M., Odjegba, V., Ma, L., & Rathinasabapathi, B. (2015). Sulfate influx transporters in Arabidopsis thaliana are not involved in arsenate uptake but critical for tissue nutrient status and arsenate tolerance. Planta, 241, 1109–1118.
Finnegan, P. M., & Chen, W. (2012). Arsenic toxicity: the effects on plant metabolism. Frontiers in Physiology, 3, 1–18.
Gomes, M. P., Soares, A. M., & Garcia, Q. S. (2014). Phosphorus and sulfur nutrition modulate antioxidant defenses in Myracrodruom urundeuva plants exposed to arsenic. Journal of Hazardous Materials, 276, 97–104.
Grifoni, M., Schiavon, M., Pezzarossa, B., Petruzzelli, G., & Malagoli, M. (2015). Effects of phosphate and thiosulfate on arsenic accumulation in the species Brassica juncea. Environmental Science and Pollution Research, 22, 2423–2433.
Karimi, N., Ghaderian, S. M., Raab, A., Feldmann, J., & Meharg, A. A. (2009). An arsenic-accumulating, hypertolerant brassica, Isatis capadocica. The New Phytologist, 184, 41–47.
Khan, Z., Midega, C., Pittchar, J., Pickett, J., & Bruce, T. (2011). Push–pull technology: a conservation agriculture approach for integrated management of insect pests, weeds and soil health in Africa. International Journal of Agricultural Sustainability, 9, 162–170.
Kumwimba, M. N., Zeng, X., Bai, L., & Wang, J. (2014). A preliminary study on genetic variation of arsenic concentration in 32 different genotypes of leafy vegetable. Environmental Pollution, 3, 72–87.
Li, X., Mu, Y., Cheng, Y., Liu, X., & Nian, H. (2013). Effects of intercropping sugarcane and soybean on growth, rhizosphere soil microbes, nitrogen and phosphorus availability. Acta Physiologiae Plantarum, 35, 1113–1119.
Lin, L. Y., Yan, X. L., Liao, X. Y., Zhang, Y. X., & Ma, X. (2015). Arsenic accumulation in Panax notoginseng monoculture and intercropping with Pteris vittata. Water, Air, and Soil Pollution, 226, 113. https://doi.org/10.1007/s11270-015-2375-9.
Mallick, S., Kumar, N., Singh, A. P., Sinam, G., Yadav, R. N., & Sinha, S. (2013). Role of sulfate in detoxification of arsenate-induced toxicity in Zea mays L. (SRHM 445): nutrient status and antioxidants. Journal of Plant Interactions, 8, 140–154.
McBride, M. B., Simon, T., Tam, G., & Wharton, S. (2013). Lead and arsenic uptake by leafy vegetables grown on contaminated soils: effects of mineral and organic amendments. Water, Air, and Soil Pollution, 224, 1–10.
McBride, M. B., Shayler, H. A., Russell-Anelli, J. M., Spliethoff, H. M., & Marquez-Bravo, L. G. (2015). Arsenic and lead uptake by vegetable crops grown on an old orchard site amended with compost. Water, Air, and Soil Pollution, 226, 265. https://doi.org/10.1007/s11270-015-2529-9.
Meharg, A. A., & Macnair, M. R. (1991). Uptake, accumulation and translocation of arsenate in arsenate-tolerant and non-tolerant Holcus lanatus L. The New Phytologist, 117, 225–231.
Ngo, L. K., Pinch, B. M., Bennett, W. W., Teasdale, P. R., & Jolley, D. F. (2016). Assessing the uptake of arsenic and antimony from contaminated soil by radish (Raphanus sativus) using DGT and selective extractions. Environmental Pollution, 216, 104–114.
Pickett, J. A., Hamilton, M. L., Hooper, A. M., Khan, Z. R., & Midega, C. A. O. (2010). Companion cropping to manage parasitic plants. Annual Review of Phytopathology, 48, 161–177.
Pigna, M., Cozzolino, V., Giandonato Caporale, A., Mora, M. L., Di Meo, V., Jara, A. A., & Violante, A. (2010). Effects of phosphorus fertilization on arsenic uptake by wheat grown in polluted soils. Journal of Soil Science and Plant Nutrition, 10, 428–442.
Plenchette, C., Clermont-Dauphin, C., Meynard, J. M., & Fortin, J. A. (2005). Managing arbuscular mycorrhizal fungi in cropping systems. Canadian Journal of Plant Science, 85, 31–40.
Puckett, E. E., Serapiglia, M. J., DeLeon, A. M., Long, S., Minocha, R., & Smart, L. B. (2012). Differential expression of genes encoding phosphate transporters contributes to arsenic tolerance and accumulation in shrub willow (Salix spp.) Environmental and Experimental Botany, 75, 248–257.
Purdy, J. J., & Smart, L. B. (2008). Hydroponic screening of shrub willow (Salix spp.) for arsenic tolerance and uptake. International Journal of Phytoremediation, 10, 515–528.
Raab, A., Williams, P. N., Meharg, A., & Feldmann, J. (2007). Uptake and translocation of inorganic and methylated arsenic species by plants. Environment and Chemistry, 4, 197–203.
Rahman, M., Haq, N., & Williams, I. D. (2012). Genetic effect on phytoaccumulation of arsenic in Brassica juncea L. Euphytica, 186, 409–417.
Reid, R., Gridley, K., Kawamata, Y., & Zhu, Y. (2013). Arsenite elicits anomalous sulfur starvation responses in barley. Plant Physiology, 162, 401–409.
Singh, A., & Prasad, P. (2014). Evaluation of potential of Brassica juncea for removal of arsenic from hydroponic solution. International Journal of Current Microbiology Applied Science, 3, 246–252.
Smith, E., Naidu, R., & Alston, A. M. (1998). Arsenic in the soil environment: a review. Advances in Agronomy, 64, 149–195.
Tu, C., & Ma, L. Q. (2005). Effects of arsenic on concentration and distribution of nutrients in the fronds of the arsenic hyperaccumulator Pteris vittata L. Environmental Pollution, 135, 333–340.
Zhao, F. J., Ma, J. F., Meharg, A. A., & McGrath, S. P. (2009). Arsenic uptake and metabolism in plants. The New Phytologist, 181, 777–794.
Acknowledgements
This research was funded by the Atkinson Sustainable Biodiversity Fund, the Toward Sustainability Foundation, the Cornell Sigma Xi Grants in Aid of Research Program (awarded to MPL), and Federal Hatch project NYC-125445. We thank Betsy Leonard for allowing us access to the Dilmun Student Organic Farm property for the field component of this work and Alice Jenkins for the laboratory assistance.
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Lim, M., McBride, M.B. & Kessler, A. Arsenic Bioaccumulation by Eruca sativa Is Unaffected by Intercropping or Plant Density. Water Air Soil Pollut 228, 364 (2017). https://doi.org/10.1007/s11270-017-3544-9
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DOI: https://doi.org/10.1007/s11270-017-3544-9