Abstract
Herein, the cultivation of Phaseolus vulgaris was evaluated in newly reclaimed areas in Abha City, Saudi Arabia, following amendment with different rates of sewage sludge (SS) collected from a nearby municipal wastewater treatment plant. A pot experiment was designed to assess the soil heavy metal (HM) pools, growth, yield and HM uptake by P. vulgaris plants cultivated under different SS amendment rates (0, 10, 20, 30, 40 and 50 g kg−1). SS application was found to significantly change all of the chemical properties of the reclaimed soil (except Fe and Mn). The application of SS caused a gradual significant elevation in the soil organic matter content. The application of SS also led to a meaningful increase in the soil electrical conductivity and the Cd, Co, Cr, Cu, Mo, Ni, Pb and Zn contents. However, the soil pH decreased in reaction to the treatments. However, the measured HMs (except Fe) in the soil mixtures in all treatments after harvesting P. vulgaris plants were below the maximum permissible limits in agricultural soil. Generally, SS application up to 20 g kg−1 caused a significant increase in most of the morphological parameters and biomass of P. vulgaris compared to the plants grown in the control soil, followed by a decreasing trend at SS application rates of 30, 40 and 50 g kg−1. P. vulgaris flower production decreased with an increase in the SS application rate, and fruiting was only successful at rates of 10 and 20 g kg−1. All the HM contents in different tissues of P. vulgaris were meaningfully higher for plants treated with different SS levels matched to those grown in control soil. The highest contents of all of the HMs were documented at 50 g kg−1 SS in all P. vulgaris tissues. However, all HM contents (excluding Fe and Mn in the roots) were within safe limits, with most of the absorbed HMs persisting in roots. The regression analysis showed that P. vulgaris plants have an increasing ability to absorb more HMs with an increase in the SS amendment rate. Calculations of bioaccumulation factor (BAF) showed that the BAF for most investigated HM was < 1. This means that P. vulgaris is an excluder for these HMs. In addition, calculations of the translocation factor (TF) indicated that the capacity of P. vulgaris to translocate HMs from roots to shoots or pods is < 1 for most of the investigated HMs, indicating that the amounts of HMs that persisted in roots were always higher than those that travelled to the stems, leaves or pods. Taken together, our findings suggest that soil application of SS up to 20 g kg−1 can provide a sustainable safe practice for SS disposal and improve P. vulgaris growth and yield, while exerting no environmental threats provided there is no accumulation of HMs to toxic levels in shoots of the grown P. vulgaris plants or in the amended soils.
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References
Abd-Alla MH, Yan F, Schubert S (1999) Effect of sewage sludge application on nodulation, nitrogen fixation, and plant growth of faba bean, soybean and lupin. Angew Bot 73:69–75
Ahmed D, Slima D (2018) Heavy metal accumulation by Corchorus olitorius L. irrigated with wastewater. Environ Sci Pollut Res 25:14996–15005
Allen S (1989) Chemical analysis of ecological materials. Blackwell Scientific Publications, London, p 368
Anonymous (1987) Asir: heritage and civilization. Obeikan Company for Printing and Publishing, Riyadh
Anonymous (2019) Asir agricultural terraces: artificialization of nature and basket of safe food. J Saudi Reg 5:1–2
Antolín MC, Muro I, Sánchez-Díaz M (2010) Application of sewage sludge improves growth, photosynthesis and antioxidant activities of nodulated alfalfa plants under drought conditions. Environ Exp Bot 68:75–82
Aydinalp C, Marinova S (2003) Distribution and forms of heavy metals in some agricultural soils. Pol J Environ Stud 12:629–633
Belaid N, Neel C, Lenain J, Buzier R, Kallel M, Ayoub T, Ayadi A, Bauduc M (2012) Assessment of metal accumulation in calcareous soil and forage crops subjected to long-term irrigation using treated wastewater: case of El Hajeb-Sfax, Tunisia. Agric Ecosyst Environ 158:83–93
Binder DL, Dobermann A, Sander DH, Cassman KG (2002) Biosolids as nitrogen source for irrigated maize and rainfed sorghum. Soil Sci Soc Am J 66:531–542
Branzini A, González RS, Zubillaga M (2012) Absorption and translocation of copper, zinc and chromium by Sesbania virgata. J Environ Manag 102:50–54
Brown S, Leonard P (2004) Recycling of organic carbon in organic wastes is also important for C sequestration in soils. BioCycle 45:25–29
Burzynski M (1987) The influence of lead and cadmium on the absorption and distribution of potassium, calcium, magnesium and iron in cucumber seedlings. Acta Physiol Plant 9:229–238
Chandra R, Yadav S, Mohan D (2008) Effect of distillery sludge on seed germination and growth parameters of green gram (Phaseolus mungo L.). J Hazard Mater 152:431–439
Chowdhury S, Fahmi M (2018) Fuzzy rule-based assessment of runoff for Abha, Saudi Arabia, using the watershed modeling system (WMS) software. Arab J Sci Eng 43:5457–5468
Codex Alimentarius Commission (2011) Joint FAO/WHO food standards programme codex committee on contaminants in foods. In: Proceedings of the FAO/WHO food standards programme fifth session. Hague, The Netherlands
Cornell RM, Schwertmann U (2003) The iron oxides, 2nd edn. Wiley VCH, Weinheim
Dolgen D, Alpaslan MN, Delen N (2007) Agricultural recycling of treatment-plant sludge: a case study for a vegetable-processing factory. J Environ Manag 84:274–281
Dowdy RH, Larson WE, Titrud JM, Latterell JJ (1978) Growth and metal uptake of snap beans growth on sewage sludge amended soil. A four year study. J Environ Qual 7:252–257
Egan M (2013) Biosolids management strategies: An evaluation of energy production as an alternative to land application. Environ Sci Pollut Res 20:4299–4310
Eid EM, Shaltout KH (2016) Bioaccumulation and translocation of heavy metals by nine native plant species grown at a sewage sludge dump site. Int J Phytoremediat 18:1075–1085
Eid EM, Alrumman SA, El-Bebany AF, Fawy KF, Taher MA, Hesham A, El-Shaboury GA, Ahmed MT (2018) The evaluation of sewage sludge application as a fertilizer for broad bean (Faba sativa Bernh.) crops. Food Energy Secur 7:e00142
Eid EM, El-Bebany AF, Taher MA, Alrumman SA, Galal TM, Shaltout KH, Sewelam NA, Ahmed MT (2020a) Heavy metal bioaccumulation, growth characteristics, and yield of Pisum sativum L. grown in agricultural soil-sewage sludge mixtures. Plants 9:1300
Eid EM, Khedher KM, Ayed H, Arshad M, Mouldi A, Shaltout KH, Sewelam NA, Galal TM, El-Bebany AF, Alshehri AMA (2020b) Prediction models based on soil properties for evaluating the heavy metal uptake into Hordeum vulgare L. grown in agricultural soils amended with different rates of sewage sludge. Int J Environ Health Res. https://doi.org/10.1080/09603123.2020.1730771
Farahat EA, Galal TM, Elawa OE, Hassan LM (2017) Health risk assessment and growth characteristics of wheat and maize crops irrigated with contaminated wastewater. Environ Monit Assess 189:535
Frost HL, Ketchum LH (2000) Trace metal concentration in durum wheat from application of sewage sludge and commercial fertilizer. Adv Environ Res 4:347–355
Galal TM (2016) Health hazards and heavy metals accumulation by summer squash (Cucurbita pepo L.) cultivated in contaminated soils. Environ Monit Assess 188:434–445
Garrido S, Campo GMD, Esteller MV, Vaca R, Lugo J (2005) Heavy metals in soil treated with sewage sludge composting, their effect on yield and uptake of broad bean seeds (Vicia faba L.). Water Air Soil Pollut 166:303–319
Gentry HS (1969) Origin of the common bean, Phaseolus vulgaris. Eco Bot 23:55–69
Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, Oxford, p 851
Hao X, Chang C (2003) Does long-term heavy cattle manure applications increase salinity of a clay loam soil in semi-arid southern Alberta? Agric Ecosyst Environ 94:89–103
He ZL, Yang XE, Stoffella PJ (2005) Trace elements in agroecosystems and impacts on the environment. J Trace Elem Med Biol 19:125–140
Hoornweg D, Bhada-Tata P (2012) What a waste: a global review of solid waste management urban development series; knowledge papers no. 15. World Bank, Washington
Huxley E (1999) Dictionary of gardening. Volume 3: L to Q. London: The New Royal Horticultural Society, Macmillan Reference LTD
Jaskulak M, Grobelak A (2019) Cadmium phytotoxicity-biomarkers. In: Hasanuzzaman M, Prasad M, Nahar K (eds) Cadmium tolerance in plants: agronomic, molecular, signaling, and omic approaches. Academic Press, Elsevier, pp 177–191
Jaskulak M, Grobelak A, Grosser A, Vandenbulcke F (2019a) Gene expression, DNA damage and other stress markers in Sinapis alba L. exposed to heavy metals with special reference to sewage sludge application on contaminated sites. Ecotoxicol Environ Safe 181:508–517
Jaskulak M, Rorat A, Grobelak A, Chaabene Z, Kacprzak M, Vandenbulcke F (2019b) Bioaccumulation, antioxidative response, and metallothionein expression in Lupinus luteus L. exposed to heavy metals and silver nanoparticles. Environ Sci Pollut Res 26:16040–16052
Jaskulak M, Grobelak A, Vandenbulcke F (2020) Effects of sewage sludge supplementation on heavy metal accumulation and the expression of ABC transporters in Sinapis alba L. during assisted phytoremediation of contaminated sites. Ecotoxicol Environ Safe 197:110606
Jones AL (1999) Phaseolus bean: post-harvest operations. FAO, Rome, p 24
Kabata-Pendias A (2011) Trace elements in soils and plants. CRC Press, Boca Raton, p 548
Kacprzak M, Neczaj E, Fijałkowski K, Grobelak A, Grosser A, Worwag M, Rorat A, Brattebo H, Almås Å, Singh BR (2017) Sewage sludge disposal strategies for sustainable development. Environ Res 156:39–46
Kalis EJJ, Temminghoff EJM, Town RM, Unsworth ER, Van Riemsdijk WH (2008) Relationship between metal speciation in soil solution and metal adsorption at the root surface of ryegrass. J Environ Qual 37:2221–2231
Kirchmann H, Pilchmayer F, Gerzabek KH (1996) Sulfur balance and sulphur-34 abundance in a long term fertilizer experiment. Soil Sci Soc Am J 60:174–178
Kominko H, Gorazda K, Wzorek Z (2017) The possibility of organo-mineral fertilizer production from sewage sludge. Waste Biomass Valor 8:1781–1791
Koutroubas SD, Antoniadis V, Fotiadis S, Damalas CA (2014) Growth, grain yield and nitrogen use efficiency of Mediterranean wheat in soils amended with municipal sewage sludge. Nutr Cycl Agroecosyst 100:227–243
Krishnamurti GS, Huang PM, Kozak LM (1999) Sorption and desorption kinetics of cadmium from soils: influence of phosphate. Soil Sci 164:888–898
Kumar V, Chopra AK (2012) Fertigation effect of distillery effluent on agronomical practices of Trigonella foenum-graecum L. (Fenugreek). Environ Monit Assess 184:1207–1219
Kumar V, Chopra AK (2014) Accumulation and translocation of metals in soil and different parts of French bean (Phaseolus vulgaris L.) amended with sewage sludge. Bull Environ Contam Toxicol 92:103–108
Larsson EH, Asp H, Bornman JF (2002) Influence prior Cd+2 exposure on the uptake of Cd+2 and other elements in the phytochelatin-deficient mutant, cad1-3, of Arabidopsis thaliana. J Exp Bot 53:447–453
Latare AM, Kumar O, Singh SK, Gupta A (2014) Direct and residual effect of sewage sludge on yield, heavy metals content and soil fertility under rice-wheat system. Ecol Eng 69:17–24
Lee R (2011) The outlook for population growth. Science 333:569–573
Lepp NW (1981) Effect of heavy metal pollution on plants Metals in the environment, vol 2. Springer, Dordrecht, p 258
Li Y, Wang H, Wang H, Yin F, Yang X, Hu Y (2014) Heavy metal pollution in vegetables grown in the vicinity of a multi-metal mining area in Gejiu, China: total concentrations, speciation analysis, and health risk. Environ Sci Pollut Res 21:12569–12582
Luna AS, Gonzaga FB, Werickson FC, Lima ICA (2018) Comparison of different strategies in multivariate regression models for the direct determination of Mn, Cr, and Ni in steel samples using laser-induced breakdown spectroscopy. Spectrochim Acta B 139:20–26
Marinari S, Masciandaro G, Ceccanti B, Grego S (2000) Influence of organic and mineral fertilisers on soil biological and physical properties. Bioresour Technol 72:9–17
Mimura T (1999) Regulation of phosphate transport and homeostasis in plant cells. Int Rev Cytol 191:149–200
Mishra A, Tripathi BD (2008) Heavy metal contamination of soil, and bioaccumulation in vegetables irrigated with treated waste water in the tropical city of Varanasi, India. Toxicol Environ Chem 90:861–871
Nawab J, Li G, Khan S, Sher H, Aamir M, Shamshad I, Khan A, Khan MA (2016) Health risk assessment from contaminated foodstuffs: a field study in chromite mining-affected areas northern Pakistan. Environ Sci Pollut Res 23:12227–12236
Novotná M, Mikeš O, Komprdová K (2015) Development and comparison of regression models for the uptake of metals into various field crops. Environ Pollut 207:357–364
Peng L, Liu W, Su C et al (2012) Effects of different organic residues on rice yield and soil quality. J Mount Sci 9:715–722
Pesci P, Reggiani R (1992) The process of abscisic acid induced proline accumulation and the levels of polyamines and quaternary ammonium compounds in hydrated barley leaves. Physiol Plant 84:134–139
Plaza C, Hernández D, García-Gil JC, Polo A (2004) Microbial activity in pig slurry-amended soils under semiarid conditions. Soil Biol Biochem 36:577–1585
Radford PJ (1967) Growth analysis formulae-their use and abuse. Crop Sci 7:171–175
Ramadan MAE, Al-Ashkar EA (2007) The effect of different fertilizers on the heavy metals in soil and tomato plant. Aus J Basic Appl Sci 1:300–306
Rebah FB, Prévost D, Yezza A, Tyagi RD (2007) Agro-industrial waste materials and wastewater sludge for rhizobial inoculant production: a review. Bioresour Technol 98:3535–3546
Samolada M, Zabaniotou A (2014) Comparative assessment of municipal sewage sludge incineration, gasification and pyrolysis for a sustainable sludge-to-energy management in Greece. Waste Manag 34:411–420
Sawidis T, Breuste J, Mitrovic M, Pavlovic P, Tsigaridas K (2011) Trees as bioindicator of heavy metal pollution in three European cities. Environ Pollut 159:3560–3570
Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50
Sharma B, Sarkar A, Singh P, Singh RP (2017) Agricultural utilization of biosolids: a review on potential effects on soil and plant grown. Waste Manag 64:117–132
Shehata HS, Galal TM (2020) Trace metal concentration in planted cucumber (Cucumis sativus L.) from contaminated soils and its associated health risks. J Verbrauch Lebensm 15:205–217
Singh RP, Agrawal M (2009) Use of sewage sludge as fertilizer supplement for Abelmoschus esculentus plants: physiological, biochemical and growth responses. Int J Environ Waste Manag 3:91–106
Singh RP, Agrawal M (2010a) Biochemical and physiological responses of rice (Oryza sativa L.) grown on different sewage sludge amendments rates. Bull Environ Contam Toxicol 84:606–612
Singh RP, Agrawal M (2010b) Effect of different sewage sludge applications on growth and yield of Vigna radiata L. field crop: Metal uptake by plant. Ecol Eng 36:969–972
Singh S, Saxena R, Pandey K, Bhatt K, Sinha S (2004) Response of antioxidants in sunflower (Helianthus annuus L.) grown on different amendments of tannery sludge: Its metal accumulation potential. Chemosphere 57:1663–1673
Singh RP, Sarkar A, Sengupta C, Singh P, Miranda ARL, Nunes LAPL, Araujo ASF, Melo WJ (2015) Effect of utilization of organic waste as agricultural amendment on soil microbial biomass. Ann Res Rev Biol 7:155–162
Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143
Smith SR (1992) Sewage sludge and refuse composts as peat alternatives for conditioning impoverished soils: effects on the growth response and mineral status of Petunia grandiflora. J Hortic Sci 67:703–716
Smith JL, Papendick RI, Bezdicek DF, Lynch JM (1993) Soil organic matter dynamics and crop residue management. In: Mettin B (ed) Soil microbial ecology. Dekker, New York, pp 65–95
Soil Survey Staff (2014) Keys to soil taxonomy, twelfth edition. U.S. Department of Agriculture, Natural Resources Conservation Service, U.S. Government Printing Office, Washington, DC, p 362
SPSS (2006) SPSS base 15.0 user’s guide. SPSS Inc, Chicago, p 610
Sukreeyapongse O, Holm PE, Strobel BW, Panichsakpatana S, Magid J, Hansen HCB (2002) pH-dependent release of cadmium, copper, and lead from natural and sludge-amended soils. J Environ Qual 31:1901–1909
Tester CF (1990) Organic amendment effects on physical and chemical properties of a sandy soil. Soil Sci Soc Am J 54:827–831
Tindall HD (1978) Commercial vegetable growing. The English Language Book Society and Oxford University Press, Oxford, p 300
Tyagi VK, Lo S-L (2013) Sludge: a waste or renewable source for energy and resources recovery? Renew Sustain Energy Rev 25:708–728
Wang X, Chen T, Ge Y, Jia Y (2008) Studies on land application of sewage sludge and its limiting factors. J Hazard Mater 160:554–558
Wei Y, Liu Y (2005) Effects of sewage sludge compost application on crops and croplandin a3-year field study. Chemosphere 59:1257–1265
Wilke BM (2005) Determination of chemical and physical soil properties. In: Margesin R, Schinner F (eds) Manual for soil analysis—monitoring and assessing soil bioremediation. Springer, Heidelberg, pp 47–95
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
Zhang Q, Hu J, Lee DJ, Chang Y, Lee YJ (2017) Sludge treatment: current research trends. Bioresour Technol 243:1159–1172
Zhao KL, Liu XM, Xu JM, Selim HM (2010) Heavy metal contaminations in a soil-rice system: Identification of spatial dependence in relation to soil properties of paddy fields. J Hazard Mater 181:778–787
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This work was supported by the Deanship of Scientific Research at King Khalid University under Grant Number R.G.P. 1/94/40.
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Eid, E.M., Shaltout, K.H., Alrumman, S.A. et al. Evaluation of newly reclaimed areas in Saudi Arabia for cultivation of the leguminous crop Phaseolus vulgaris under sewage sludge amendment. J Consum Prot Food Saf 16, 153–169 (2021). https://doi.org/10.1007/s00003-020-01311-z
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DOI: https://doi.org/10.1007/s00003-020-01311-z