Sustainable resource management with bone char—challenges and opportunities for enhancing soil health and phosphorus stocks

Abstract

The global annual production of animal by-product (ABP)-derived bone, estimated at 95‒126 million tonnes, presents both an environmental challenge and an opportunity for sustainable resource utilization. We estimate that bone char (BC) could theoretically replace 13‒32% of the global phosphorus (P) fertilizer market. BC, produced through the pyrolysis of animal bones, has emerged as a promising material for use in a range of agricultural applications related to soil fertility and water quality. The conversion of ABP-derived bone into BC through pyrolysis not only eliminates potential human and animal pathogens (e.g., prions, viruses, bacteria), but also creates a valuable resource rich in P, calcium, and magnesium. This review synthesizes current research on the potential applications of BC in agriculture, focusing on its multifunctional role as a slow-release P fertilizer, a carbon (C) storage material, and an effective adsorbent for remediating contaminated soils. Field and laboratory studies demonstrate that BC’s performance is strongly influenced by pyrolysis conditions, with optimal temperatures between 300 and 500 °C for nutrient release applications and above 600–800 °C for enhanced surface area and contaminant remediation. Its hydroxyapatite structure enables gradual P release and potential toxic element (PTE) immobilization, while its porous nature can provide new habitat niches for soil microorganisms and improve soil water retention. In comparison to most conventional inorganic fertilisers, BC can enhance soil fertility by releasing P slowly, thereby improving plant growth and productivity, particularly in acidic soils. The low cost, renewable nature, and ease of regeneration of BC further enhance its appeal as a viable solution for mitigating environmental pollution and promoting sustainable resource management practices. Beyond its established applications, this review identifies critical knowledge gaps, including the need to investigate BC’s long-term impacts on soil health, microbial communities, and greenhouse gas emissions. We also discuss opportunities for optimizing production methods and expanding applications beyond agriculture. Given BC’s potential to address multiple agricultural and environmental challenges, we emphasize the importance of interdisciplinary research to evaluate implementation barriers, including economic viability, social acceptance, and regulatory frameworks.

Graphical Abstract

Keywords

Circular economy / Phosphorus availability / Resource management / Soil fertility / Sustainable agriculture

References

[1] AHDB (2024) Killing-out percentage. Agriculture and Horticulture Development Board, Coventry, UK. https://ahdb.org.uk/knowledge-library/killing-out-percentage#:~:text=Body%20weight,KO%25%20per%2010%20kg%20liveweight. Accessed 1 Feb 2025

[2] Ahmed M, Nigussie A, Addisu S, Belay B, Sato S. Valorization of animal bone into phosphorus biofertilizer: effects of animal species, thermal processing method, and production temperature on phosphorus availability. Soil Sci Plant Nutr. 2021, 67(4): 471-481.

[3] Ali S, Rizwan M, Qayyum MF, Ok YS, Ibrahim M, Riaz M, Arif MS, Hafeez F, Al-Wabel MI, Shahzad AN. Biochar soil amendment on alleviation of drought and salt stress in plants: a critical review. Environ Sci Pollut Res. 2017, 24: 12700-12712.

[4] Alkharabsheh HM, Seleiman MF, Battaglia ML, Shami A, Jalal RS, Alhammad BA, Almutairi AM, Al-Saif KF. Biochar and its broad impacts in soil quality and fertility, nutrient leaching and crop productivity: a review. Agronomy. 2021, 11(5): 993.

[5] Alkurdi SS, Al-Juboori RA, Bundschuh J, Bowtell L, McKnight S. Effect of pyrolysis conditions on bone char characterization and its ability for arsenic and fluoride removal. Environ Pollut. 2020, 262. 114221

[6] Amann A, Zoboli O, Krampe J, Rechberger H, Zessner M, Egle L. Environmental impacts of phosphorus recovery from municipal wastewater. Resour Conserv Recycl. 2018, 130: 127-139.

[7] Amin AEEAZ. Sulfur, Na2-EDTA and their mixture effects on phosphorus release from cow bone char in P-poor sandy soil. Environ Technol Innov. 2020, 17. 100636

[8] Amin AEEAZ. Enhancement of releasing phosphorus from bone char in calcareous sandy soil under applying different levels of water salinity. J Soil Sci Plant Nutr. 2021, 211476-486.

[9] Amin AEEAZ. Effects of pyrolysis temperatures on bone char characterization and its releasing phosphorus in sandy soil. Arch Agron Soil Sci. 2023, 69(2): 304-313.

[10] Amin AEEAZ, Mihoub A. Effect of sulfur-enriched biochar in combination with sulfur-oxidizing bacterium (Thiobacillus spp.) on release and distribution of phosphorus in high calcareous p-fixing soils. J Soil Sci Plant Nutr. 2021, 21(3): 2041-2047.

[11] Atkinson CJ, Fitzgerald JD, Hipps NA. Potential mechanisms for achieving agricultural benefits from biochar application to temperate soils: a review. Plant Soil. 2010, 337: 1-18.

[12] Azeem M, Ali A, Jeyasundar PGA, Bashir S, Hussain Q, Wahid F, Ali EF, Abdelrahman H, Li R, Antoniadis V, Rinklebe J. Effects of sheep bone biochar on soil quality, maize growth, and fractionation and phytoavailability of Cd and Zn in a mining-contaminated soil. Chemosphere. 2021, 282. 131016

[13] Azeem M, Ali A, Jeyasundar PGA, Li Y, Abdelrahman H, Latif A, Li R, Basta N, Li G, Shaheen SM, Rinklebe J. Bone-derived biochar improved soil quality and reduced Cd and Zn phytoavailability in a multi-metal contaminated mining soil. Environ Pollut. 2021, 277. 116800

[14] Azeem M, Shaheen SM, Ali A, Jeyasundar PG, Latif A, Abdelrahman H, Li R, Almazroui M, Niazi NK, Sarmah AK, Li G. Removal of potentially toxic elements from contaminated soil and water using bone char compared to plant-and bone-derived biochars: a review. J Hazard Mater. 2022, 427. 128131

[15] Azeem M, Jeyasundar PGA, Ali A, Riaz L, Khan KS, Hussain Q, Kareem HA, Abbas F, Latif A, Majrashi A, Ali EF. Cow bone-derived biochar enhances microbial biomass and alters bacterial community composition and diversity in a smelter contaminated soil. Environ Res. 2023, 216. 114278

[16] Batjes NH. Total carbon and nitrogen in the soils of the world. Eur J Soil Sci. 2014, 47(2): 151-163.

[17] Bayata A, Mulatu G. Effect of bone char application on soil quality, soil enzyme and in enhancing crop yield in agriculture: a review. Am J Chem Eng. 2024, 13(3): 13-28.

[18] Beauregard MS, Hamel C, St-Arnaud M. Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in alfalfa. Microb Ecol. 2010, 59(2): 379-389.

[19] Bharadwaj AS, Brignon WR, Gould NL, Brown PB, Wu YV. Evaluation of meat and bone meal in practical diets fed to juvenile hybrid striped bass Morone chrysops x M-saxatilis. J World Aqua Soc. 2002, 33: 448-457.

[20] Biswas PP, Liang B, Turner-Walker G, Rathod J, Lee YC, Wang CC, Chang CK. Systematic changes of bone hydroxyapatite along a charring temperature gradient: an integrative study with dissolution behavior. Sci Total Environ. 2021, 766. 142601

[21] Bolan N, Hoang SA, Beiyuan J, Gupta S, Hou D, Karakoti A, Joseph S, Jung S, Kim KH, Kirkham MB, Kua HW. Multifunctional applications of biochar beyond carbon storage. Int Mater Rev. 2022, 67(2): 150-200.

[22] Cantrell KB, Hunt PG, Uchimiya M, Novak JM, Ro KS. Impact of pyrolysis temperature and manure source on physicochemical characteristics of biochar. Bioresour Technol. 2012, 107: 419-428.

[23] Carella F, Seck M, Degli Esposti L, Diadiou H, Maienza A, Baronti S, Vignaroli P, Vaccari FP, Iafisco M, Adamiano A. Thermal conversion of fish bones into fertilizers and biostimulants for plant growth–a low tech valorization process for the development of circular economy in least developed countries. J Environ Chem Eng. 2021, 9(1. 104815

[24] Castillo NAM, Fernández LAG, Thiodjio-Sendja B, Aguilera-Flores MM, Leyva-Ramos R, Reyes-López SY, de León-Martínez LD, Dias JM. Bone char for water treatment and environmental applications: a review. J Anal Appl Pyrolysis. 2023, 175. 106161

[25] Chen SB, Zhu YG, Ma YB, McKay G. Effect of bone char application on Pb bioavailability in a Pb-contaminated soil. Environ Pollut. 2006, 1393): 433-439.

[26] Chen H, Yang X, Wang H, Sarkar B, Shaheen SM, Gielen G, Bolan N, Guo J, Che L, Sun H, Rinklebe J. Animal carcass-and wood-derived biochars improved nutrient bioavailability, enzyme activity, and plant growth in metal-phthalic acid ester co-contaminated soils: a trial for reclamation and improvement of degraded soils. J Environ Manage. 2020, 261. 110246

[27] Christiansen NH, Sørensen P, Labouriau R, Christensen BT, Rubaek GH. Characterizing phosphorus availability in waste products by chemical extractions and plant uptake. J Plant Nutr Soil Sci. 2020, 183(4): 416-428.

[28] Cowie AL, Downie AE, George BH, Singh BP, Van Zwieten L, O'Connell D. Is sustainability certification for biochar the answer to environmental risks?. Pesq Agropec Bras. 2012, 47: 637-648.

[29] Darch T, Dunn RM, Guy A, Hawkins JMB, Ash M, Frimpong KA, Blackwell MSA. Fertilizer produced from abattoir waste can contribute to phosphorus sustainability, and biofortify crops with minerals. PLoS ONE. 2019, 14. e0221647

[30] Das PP, Singh KR, Nagpure G, Mansoori A, Singh RP, Ghazi IA, Kumar A, Singh J. Plant-soil-microbes: a tripartite interaction for nutrient acquisition and better plant growth for sustainable agricultural practices. Environ Res. 2022, 214. 113821

[31] de Castro GF, da Silva IF, da Silva BA, de Matos Oliveira J, Zotarelli L, Tronto J. Sulfuric acid-treated bone char as a recycled source of soluble phosphate fertilizer. Biomass Bioenergy. 2026, 204. 108459

[32] D'Odorico P, Ravi S. Sivanpillai Ramesh, Shroder John F. Chapter 18—Land degradation and environmental change. Hazards and disasters series, biological and environmental hazards, risks, and disasters. 2023, Boston, Elsevier

[33] Doyle JJ. Toxic and essential elements in bone–a review. J Anim Sci. 1979, 49(2): 482-497.

[34] Ducey TF, Collins JC, Ro KS, Woodbury BL, Griffin DD. Hydrothermal carbonization of livestock mortality for the reduction of pathogens and microbially-derived DNA. Front Environ Sci Eng. 2017, 11: 1-8.

[35] Ducousso-Détrez A, Fontaine J, Lounès-Hadj Sahraoui A, Hijri M. Diversity of phosphate chemical forms in soils and their contributions on soil microbial community structure changes. Microorganisms. 2022, 10(3): 609.

[36] El-Naggar A, El-Naggar AH, Shaheen SM, Sarkar B, Chang SX, Tsang DC, Rinklebe J, Ok YS. Biochar composition-dependent impacts on soil nutrient release, carbon mineralization, and potential environmental risk: a review. J Environ Manage. 2019, 241: 458-467.

[37] Enaime G, Baçaoui A, Yaacoubi A, Lübken M. Biochar for wastewater treatment—conversion technologies and applications. Appl Sci. 2020, 10103492.

[38] Etok SE, Valsami-Jones E, Wess TJ, Hiller JC, Maxwell CA, Rogers KD, Manning DA, White ML, Lopez-Capel E, Collins MJ, Buckley M. Structural and chemical changes of thermally treated bone apatite. J Mater Sci. 2007, 42: 9807-9816.

[39] FAO. Statistical yearbook. World food and agriculture. 2023, Rome, Italy, Food and Agriculture Organization of the United Nations.

[40] Field RA, Riley ML, Mello FC, Corbridge JH, Kotula AW. Bone composition in cattle, pigs, sheep and poultry. J Anim Sci. 1974, 393493-499.

[41] Figueiredo MJDFMD, Fernando A, Martins G, Freitas J, Judas F, Figueiredo H. Effect of the calcination temperature on the composition and microstructure of hydroxyapatite derived from human and animal bone. Ceram Int. 2010, 36(8): 2383-2393.

[42] Frišták V, Pipíška M, Soja G, Klokočíková Packová A, Hubeňák M, Kadlečíková M. Agro-environmental benefit and risk of manure-and bone meal-derived pyrogenic carbonaceous materials as soil amendments: availability of PAHs, PTEs, and P. Agronomy. 2019, 9(12): 802.

[43] Fung E, Johnson KI, Li W, Borges W, Chi K, Sharma SK, Madan Y, Sharma PR, Hsiao BS. Study the use of activated carbon and bone char on the performance of gravity sand-bag water filter. Membranes. 2021, 11. 868

[44] Gelardi DL, Li C, Parikh SJ. An emerging environmental concern: biochar-induced dust emissions and their potentially toxic properties. Sci Total Environ. 2019, 678: 813-820.

[45] Ghorbani M, Brown RW, Azarnejad N, Chadwick DR, Loppi S, Jones DL. Bone char outperforms biochar in phosphorus-deficient soils: comparative analysis of soil fertility enhancement and greenhouse gas mitigation. Environ Technol Innov. 2025, 39. 104321

[46] Ghosh PR, Fawcett D, Sharma SB, Poinern GEJ. Progress towards sustainable utilisation and management of food wastes in the global economy. Intern J Food Sci. 2016.

[47] Glæsner N, Hansen HCB, Hu Y, Bekiaris G, Bruun S. Low crystalline apatite in bone char produced at low temperature ameliorates phosphorus-deficient soils. Chemosphere. 2019, 223: 723-730.

[48] Glaser B, Lehr VI. Biochar effects on phosphorus availability in agricultural soils: a meta-analysis. Sci Rep. 2019, 919338.

[49] Glaser B, Haumaier L, Guggenberger G, Zech W. The'terra preta'phenomenon: a model for sustainable agriculture in the humid tropics. Naturwissenschaften. 2001, 88: 37-41.

[50] Grafe M, Kurth JK, Panten K, Raj AD, Baum C, Zimmer D, Leinweber P, Schloter M, Schulz S. Effects of different innovative bone char based P fertilizers on bacteria catalyzing P turnover in agricultural soils. Agric Ecosyst Environ. 2021, 314. 107419

[51] Gruden E, Bukovec P, Zupančič M. Preliminary evaluation of animal bone char as potential metal stabilization agent in metal contaminated soil. Acta Chim Slov. 2017.

[52] Gwenzi W, Chaukura N, Mukome FN, Machado S, Nyamasoka B. Biochar production and applications in sub-Saharan Africa: opportunities, constraints, risks and uncertainties. J Environ Manage. 2015, 150: 250-261.

[53] Gyaneshwar P, Naresh Kumar G, Parekh LJ, Poole PS. Role of soil microorganisms in improving P nutrition of plants. Plant Soil. 2002, 245: 83-93.

[54] Hagemann N, Joseph S, Schmidt HP, Kammann CI, Harter J, Borch T, Young RB, Varga K, Taherymoosavi S, Elliott KW, McKenna A. Organic coating on biochar explains its nutrient retention and stimulation of soil fertility. Nat Commun. 2017, 811089.

[55] Hart A, Ebiundu K, Peretomode E, Onyeaka H, Nwabor OF, Obileke K. Value-added materials recovered from waste bone biomass: technologies and applications. RSC Adv. 2022, 123422302-22330.

[56] Hussain S, Yang J, Hussain J, Sattar A, Ullah S, Hussain I, Rahman SU, Zandi P, Xia X, Zhang L. Mercury fractionation, bioavailability, and the major factors predicting its transfer and accumulation in soil–wheat systems. Sci Total Environ. 2022, 847. 157432

[57] Huyen DT, Long DH, Nguyen HC, Khoa BDD. Investigation of characteristics and application of food waste-derived bone char on plant growth. J Environ Chem Eng. 2024, 12(5. 113446

[58] Irfan M, Chen Q, Yue Y, Pang R, Lin Q, Zhao X, Chen H. Co-production of biochar, bio-oil and syngas from halophyte grass (Achnatherum splendens L.) under three different pyrolysis temperatures. Bioresour Technol. 2016, 211: 457-463.

[59] Jafari M, Tahmoures M, Ehteram M, Ghorbani M, Panahi F. Soil erosion control in drylands. 2022, Cham, Springer.

[60] Jia Y, Siebers N, Panten K, Kruse J. Fate and availability of phosphorus from bone char with and without sulfur modification in soil size fractions after five-year field fertilizations. Soil Tillage Res. 2023, 231. 105720

[61] Jones DL, Cross P, Withers PJ, DeLuca TH, Robinson DA, Quilliam RS, Harris IM, Chadwick DR, Edwards-Jones G. Nutrient stripping: the global disparity between food security and soil nutrient stocks. J Appl Ecol. 2013, 504): 851-862.

[62] Karppinen EM, Stewart KJ, Farrell RE, Siciliano SD. Petroleum hydrocarbon remediation in frozen soil using a meat and bonemeal biochar plus fertilizer. Chemosphere. 2017, 173: 330-339.

[63] Kefalew T, Lami M. Biogas and bio-fertilizer production potential of abattoir waste: implication in sustainable waste management in Shashemene City, Ethiopia. Heliyon. 2021, 7. e08293

[64] Kpomblekoua K, Tabatabai MA. Effect of organic acids on release of phosphorus from phosphate rocks. Soil Sci. 1994, 158: 442-453.

[65] Kruse J, Panten K, Siebers N. The fate of phosphorus from bone char-based fertilizers in soil pools in a 5-year crop rotation. Nutr Cycl Agroecosyst. 2022, 124(2): 263-277.

[66] Kumar M, Goswami R, Patel AK, Srivastava M, Das N. Scenario, perspectives and mechanism of arsenic and fluoride co-occurrence in the groundwater: a review. Chemosphere. 2020, 249. 126126

[67] Lal R. Restoring soil quality to mitigate soil degradation. Sustainability. 2015, 7(5): 5875-5895.

[68] Lamb D, Erskine PD, Parrotta JA. Restoration of degraded tropical forest landscapes. Science. 2005, 310(5754): 1628-1632.

[69] Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D. Biochar effects on soil biota–a review. Soil Biol Biochem. 2011, 43(9): 1812-1836.

[70] Leinweber P. Sauermann U, Klätte M. Pyrolyse von Schlachtknochen–ein attraktiver Ansatz im Phosphorrecycling. InnoSoilPhos. 2017, Bergedorf, Thermopolyphos Steinbeis Edition Stuttgart

[71] Leinweber P, Bathmann U, Buczko U, Douhaire C, Eichler-Löbermann B, Frossard E, Ekardt F, Jarvie H, Krämer I, Kabbe C, Lennartz B. Handling the phosphorus paradox in agriculture and natural ecosystems: scarcity, necessity, and burden of P. Ambio. 2018, 47: 3-19.

[72] Leinweber P, Hagemann P, Kebelmann L, Kebelmann K, Morshedizad M. Ohtake H, Tsuneda S. Bone char as a novel phosphorus fertilizer. Phosphorus recovery and recycling. 2019, Singapore, Springer

[73] Li Z, Wu S, Ye C. Temperature-related changes of bioapatite based on hypermineralized dolphin's bulla. J Raman Spectrosc. 2015, 46(10): 964-968.

[74] Li Z, Wang F, Bai T, Tao J, Guo J, Yang M, Wang S, Hu S. Lead immobilization by geological fluorapatite and fungus Aspergillus niger. J Hazard Mater. 2016, 320: 386-392.

[75] Li S, Barreto V, Li R, Chen G, Hsieh YP. Nitrogen retention of biochar derived from different feedstocks at variable pyrolysis temperatures. J Anal Appl Pyrolysis. 2018, 133: 136-146.

[76] Li J, Wang Y, Zhu C, Xue X, Qian K, Xie X, Wang Y. Hydrogeochemical processes controlling the mobilization and enrichment of fluoride in groundwater of the North China Plain. Sci Total Environ. 2020, 730. 138877

[77] Li Y, Liu J, Han L, Wei B, Liu X. Influence of pyrolysis atmosphere, temperature, and particle size co-regulation on the physicochemical properties of bone char. J Environ Chem Eng. 2023, 11(6. 111357

[78] Li Y, Liu J, Wei B, Zhang X, Liu X, Han L. A comprehensive review of bone char: fabrication procedures, physicochemical properties, and environmental application. Sci Total Environ. 2024.

[79] Liang A, Ma C, Xiao J, Hao Y, Li H, Guo Y, Cao Y, Jia W, Han L, Chen G, Tan Q. Micro/nanoscale bone char alleviates cadmium toxicity and boosts rice growth via positively altering the rhizosphere and endophytic microbial community.. J Hazard Mater. 2023, 454. 131491

[80] Lin SL, Zhang H, Chen WH, Song M, Kwon EE. Low-temperature biochar production from torrefaction for wastewater treatment: a review. Bioresour Technol. 2023, 387. 129588

[81] Ling N, Chen D, Guo H, Wei J, Bai Y, Shen Q, Hu S. Differential responses of soil bacterial communities to long-term N and P inputs in a semi-arid steppe. Geoderma. 2017, 292: 25-33.

[82] Little NG, Mohler CL, Ketterings QM, DiTommaso A. Effects of organic nutrient amendments on weed and crop growth. Weed Sci. 2015, 633): 710-722.

[83] Liu G, Meng J, Huang Y, Dai Z, Tang C, Xu J. Effects of carbide slag, lodestone and biochar on the immobilization, plant uptake and translocation of As and Cd in a contaminated paddy soil. Environ Pollut. 2020, 266. 115194

[84] Liu Y, Luo H, Tie B, Li D, Liu S, Lei M, Du H. The long-term effectiveness of ferromanganese biochar in soil Cd stabilization and reduction of Cd bioaccumulation in rice. Biochar. 2021, 3: 499-509.

[85] Longbottom T, Wahab L, Min K, Jurusik A, Moreland K, Dolui M, Thao T, Gonzales M, Rojas Y, Alvarez J, Malone Z. What's soil got to do with climate change?. GSA Today. 2022, 32(5): 4-10.

[86] MacDonald GK, Bennett EM, Potter PA, Ramankutty N. Agronomic phosphorus imbalances across the world's croplands. Proc Natl Acad Sci U S A. 2011, 108(7): 3086-3091.

[87] Marklein AR, Houlton BZ. Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol. 2012, 193(3): 696-704.

[88] McDowell RW, Pletnyakov P, Haygarth PM. Phosphorus applications adjusted to optimal crop yields can help sustain global phosphorus reserves. Nat Food. 2024, 5: 332-339.

[89] Medellin-Castillo NA, Leyva-Ramos R, Padilla-Ortega E, Perez RO, Flores-Cano JV, Berber-Mendoza MS. Adsorption capacity of bone char for removing fluoride from water solution. Role of hydroxyapatite content, adsorption mechanism and competing anions. J Ind Eng Chem. 2014, 20(6): 4014-4021.

[90] Mei H, Huang W, Wang Y, Xu T, Zhao L, Zhang D, Luo Y, Pan X. One stone two birds: bone char as a cost-effective material for stabilizing multiple heavy metals in soil and promoting crop growth.. Sci Total Environ. 2022, 840. 156163

[91] Mendes GDO, da Silva NMRM, Anastácio TC, Vassilev NB, Ribeiro JIJrda Silva IR, Costa MD. Optimization of A spergillus niger rock phosphate solubilization in solid-state fermentation and use of the resulting product as a P fertilizer. Microb Biotechnol. 2015, 8(6): 930-939.

[92] Mendes KF, de Sousa RN, Takeshita V, Alonso FG, Régo APJ, Tornisielo VL. Cow bone char as a sorbent to increase sorption and decrease mobility of hexazinone, metribuzin, and quinclorac in soil. Geoderma. 2019, 343: 40-49.

[93] Meng L, Chen Y, Tang L, Sun X, Huo H, He Y, Huang Y, Shao Q, Pan S, Li Z. Effects of temperature-related changes on charred bone in soil: from P release to microbial community.. Curr Res Microbial Sci. 2024, 6. 100221

[94] Moreira LC, Rosa GJM, Schaefer DM. Beef production from cull dairy cows: a review from culling to consumption. J Anim Sci. 2021, 99(7. skab192

[95] Morshedizad M, Leinweber P. Leaching of phosphorus and cadmium in soils amended with different bone chars. Clean: Soil, Air, Water. 2017, 458): 1600635.

[96] Morshedizad M, Zimmer D, Leinweber P. Effect of bone chars on phosphorus-cadmium-interactions as evaluated by three extraction procedures. J Plant Nutr Soil Sci. 2016, 1793388-398.

[97] Morshedizad M, Panten K, Klysubun W, Leinweber P. Bone char effects on soil: sequential fractionations and XANES spectroscopy. Soil. 2018, 4(1): 23-35.

[98] Nassar HN, Ismail AR, El-Salamony RA, Aboelazayem O, Abu Amr SA, El-Gendy NS. Animal bone affluence in environmental reclamation: biodiesel production, petro-diesel biodesulfurization and wastewater photo-treatment. Biofuels Bioprod Biorefin. 2021, 15(3): 770-792.

[99] OECD-FAO (2022) OECD-FAO Agricultural Outlook 2022–2031, FAO; OECD;. Rome, Italy; Paris, France. https://policycommons.net/artifacts/2652558/oecd-fao-agricultural-outlook-2022-2031/3675435/. Accessed 09 Apr 2024

[100] Olszta MJ, Cheng X, Jee SS, Kumar R, Kim YY, Kaufman MJ, Douglas EP, Gower LB. Bone structure and formation: a new perspective. Mater Sci Eng R Rep. 2007, 58(3–5): 77-116.

[101] Panten K, Leinweber P. Agronomic evaluation of bone char as phosphorus fertiliser after five years of consecutive application. J Cultivated Plants. 2020.

[102] Panwar NL, Kothari R, Tyagi VV. Thermo chemical conversion of biomass – eco friendly energy routes. Renew Sustain Energy Rev. 2012, 16: 1801-1816.

[103] Patel S, Han J, Gao W. Sorption of 17β-estradiol from aqueous solutions on to bone char derived from waste cattle bones: kinetics and isotherms. J Environ Chem Eng. 2015, 3(3): 1562-1569.

[104] Piccirillo C. Preparation, characterisation and applications of bone char, a food waste-derived sustainable material: a review. J Environ Manage. 2023, 339. 117896

[105] Piccolla CD, Hesterberg D, Muraoka T, Novotny EH. Optimizing pyrolysis conditions for recycling pig bones into phosphate fertilizer. Waste Manag. 2021, 131: 249-257.

[106] Pivato A, Hamad G, Antille DL, Schievano A, Giovanni B, Philipp R, Di MF, Peng W, Stefano C, Lavagnolo MC. Air-polluting emissions from pyrolysis plants: a systematic mapping.. Environments. 2024, 11(7. 149

[107] Postma J, Nijhuis EH, Someus E. Selection of phosphorus solubilizing bacteria with biocontrol potential for growth in phosphorus rich animal bone charcoal. Appl Soil Ecol. 2010, 463): 464-469.

[108] Postma J, Clematis F, Nijhuis EH, Someus E. Efficacy of four phosphate-mobilizing bacteria applied with an animal bone charcoal formulation in controlling Pythium aphanidermatum and Fusarium oxysporum f. sp. radicis lycopersici in tomato. Biol Control. 2013, 67(2): 284-291.

[109] Qian K, Kumar A, Zhang H, Bellmer D, Huhnke R. Recent advances in utilization of biochar. Renew Sustain Energy Rev. 2015, 42: 1055-1064.

[110] Qu J, Wei S, Liu Y, Zhang X, Jiang Z, Tao Y, Zhang G, Zhang B, Wang L, Zhang Y. Effective lead passivation in soil by bone char/CMC-stabilized FeS composite loading with phosphate-solubilizing bacteria. J Hazard Mater. 2022, 423. 127043

[111] Quilliam RS, Glanville HC, Wade SC, Jones DL. Life in the ‘charosphere’–does biochar in agricultural soil provide a significant habitat for microorganisms?. Soil Biol Biochem. 2013, 65: 287-293.

[112] Rafiq MK, Bachmann RT, Rafiq MT, Shang Z, Joseph S, Long R. Influence of pyrolysis temperature on physico-chemical properties of corn stover (Zea mays L.) biochar and feasibility for carbon capture and energy balance. PLoS ONE. 2016, 11(6. e0156894

[113] Rajendran J, Gialanella S, Aswath PB. XANES analysis of dried and calcined bones. Mater Sci Eng, C. 2013, 337): 3968-3979.

[114] Ramanan S, Mkongo G, Zhang Q, Wen H, Mtalo F, Shen J. Assessing the environmental impact of bone char production by in-situ emission monitoring and life cycle assessment. J Clean Prod. 2022, 367. 132974

[115] EU Regulation (2019) Regulation (EC) No 1069/2009 of the European Parliament and of the Council of 21 October 2009 laying down health rules as regards animal by-products and derived products not intended for human consumption and repealing Regulation (EC) No 1774/2002 (Animal by-products Regulation). REGULATION (EC) No 1069/2009 OF THE EUROPEAN PARLIAMENT AND OF THE COUNCIL. 02009R1069-EN-14.12.2019-004.001. http://data.europa.eu/eli/reg/2009/1069/2019-12-14. Accessed June 2024

[116] Rehana MR, Gladis R, Joseph B. Controlled release of nutrients for soil productivity-a review. Curr J Appl Sci Technol. 2022, 41: 34-46.

[117] Reyes-Gasga J, García-García R, Arellano-Jiménez MJ, Sanchez-Pastenes E, Tiznado-Orozco GE, Gil-Chavarria IM, Gomez-Gasga G. Structural and thermal behaviour of human tooth and three synthetic hydroxyapatites from 20 to 600 C. J Phys D Appl Phys. 2008, 41(22. 225407

[118] Rezvani Boroujeni S, Kalbasi M, Asgharzadeh A, Baharlouei J. Evaluating the potential of Halothiobacillus bacteria for sulfur oxidation and biomass production under saline soil. Geomicrobiol J. 2021, 381): 57-65.

[119] Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil. 2009, 321: 305-339.

[120] Robinson JS, Baumann K, Hu Y, Hagemann P, Kebelmann L, Leinweber P. Phosphorus transformations in plant-based and bio-waste materials induced by pyrolysis. Ambio. 2018, 47: 73-82.

[121] Rojas-Mayorga CK, Bonilla-Petriciolet A, Aguayo-Villarreal IA, Hernández-Montoya V, Moreno-Virgen MR, Tovar-Gómez R, Montes-Morán MA. Optimization of pyrolysis conditions and adsorption properties of bone char for fluoride removal from water. J Anal Appl Pyrolysis. 2013, 104: 10-18.

[122] Rojas-Mayorga CK, Silvestre-Albero J, Aguayo-Villarreal IA, Mendoza-Castillo DI, Bonilla-Petriciolet A. A new synthesis route for bone chars using CO₂ atmosphere and their application as fluoride adsorbents. Microporous Mesoporous Mater. 2015, 209: 38-44.

[123] Rojas-Mayorga CK, Mendoza-Castillo DI, Bonilla-Petriciolet A, Silvestre-Albero J. Tailoring the adsorption behavior of bone char for heavy metal removal from aqueous solution. Adsorpt Sci Technol. 2016, 34(6): 368-387.

[124] Saleh ME, El-Refaey AA, El-Damarawy YA. CO₂ emissions and soil organic carbon in calcareous soils as affected by bone char and phosphate rock. Egypt J Soil Sci. 2020, 60: 365-375.

[125] Samavedi S, Whittington AR, Goldstein AS. Calcium phosphate ceramics in bone tissue engineering: a review of properties and their influence on cell behavior. Acta Biomater. 2013, 9(9): 8037-8045.

[126] Santana CA, Piccirillo C, Pereira SIA, Pullar RC, Lima SM, Castro PML. Employment of phosphate solubilising bacteria on fish scales–turning food waste into an available phosphorus source. J Environ Chem Eng. 2019, 7(5. 103403

[127] Scholz RW, Ulrich AE, Eilittä M, Roy A. Sustainable use of phosphorus: a finite resource. Sci Total Environ. 2013, 461: 799-803.

[128] Schwab CV, Hanna M (2019). Master gardeners’ safety precautions for handling, applying, and storing biochar. Iowa State University. https://cenusa.iastate.edu/files/cenusa_2019_023.pdf

[129] Shahid MK, Kim JY, Choi YG. Synthesis of bone char from cattle bones and its application for fluoride removal from the contaminated water. Groundw Sustain Dev. 2019, 8: 324-331.

[130] Shahid S, Imtiaz H, Rashid J, Xu M, Vithanage M, Ahmad M. Uptake, translocation, and nutrient efficiency of nano-bonechar as a plant growth regulator in hydroponics and soil systems. Environ Res. 2024, 251. 118695

[131] Sharma P, Gaur VK, Gupta S, Varjani S, Pandey A, Gnansounou E, You S, Ngo HH, Wong JW. Trends in mitigation of industrial waste: Global health hazards, environmental implications and waste derived economy for environmental sustainability. Sci Total Environ. 2022, 811. 152357

[132] Shen Z, Li Z, Alessi DS. Stabilization-based soil remediation should consider long-term challenges. Front Environ Sci Eng. 2018, 12: 1-3.

[133] Shen Z, Tian D, Zhang X, Tang L, Su M, Zhang L, Li Z, Hu S, Hou D. Mechanisms of biochar assisted immobilization of Pb²⁺ by bioapatite in aqueous solution. Chemosphere. 2018, 190: 260-266.

[134] Siebers N, Leinweber P. Bone char: a clean and renewable phosphorus fertilizer with cadmium immobilization capability. J Environ Qual. 2013, 42: 405-411.

[135] Siebers N, Godlinski F, Leinweber P. The phosphorus fertilizer value of bone char for potatoes, wheat and onions: first results. Landbauforsch Volk. 2012, 62: 59-64

[136] Siebers N, Godlinski F, Leinweber P. Bone char as phosphorus fertilizer involved in cadmium immobilization in lettuce, wheat, and potato cropping. J Plant Nutr Soil Sci. 2014, 177: 75-83.

[137] Sierra I, Ayastuy JL, Gutiérrez-Ortiz MA, Iriarte-Velasco U. A study on the impact of the reaction mechanism of the thermochemical activation of bone char (by pyrolysis and carbonization). J Anal Appl Pyrolysis. 2023, 171. 105973

[138] Simons A, Solomon D, Chibssa W, Blalock G, Lehmann J. Filling the phosphorus fertilizer gap in developing countries. Nat Geosci. 2014, 7: 3-3.

[139] Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB. Stoichiometry of soil enzyme activity at global scale. Ecol Lett. 2008, 1111): 1252-1264.

[140] Soja G, Sörensen A, Drosg B, Gabauer W, Ortner M, Schumergruber A, Dunst G, Meitner D, Guillen-Burrieza E, Pfeifer C. Abattoir residues as nutrient resources: nitrogen recycling with bone chars and biogas digestates. Heliyon. 2023.

[141] Solangi F, Zhu X, Khan S, Rais N, Majeed A, Sabir MA, Iqbal R, Ali S, Hafeez A, Ali B, Ercisli S. The global dilemma of soil legacy phosphorus and its improvement strategies under recent changes in agro-ecosystem sustainability. ACS Omega. 2023, 8: 23271-23282.

[142] Someus E, Pugliese M. Concentrated phosphorus recovery from food grade animal bones. Sustainability. 2018, 10: 2349.

[143] Sorlini S, Palazzini D, Collivignarelli C. Fluoride removal from drinking water in Senegal: laboratory and pilot experimentation on bone char-based treatment. J Water Sanit Hyg Dev. 2011, 1213-223.

[144] Stávková J, Marousek J. Novel sorbent shows promising financial results on P recovery from sludge water. Chemosphere. 2021, 276. 130097

[145] Sun D, Hale L, Kar G, Soolanayakanahally R, Adl S. Phosphorus recovery and reuse by pyrolysis: applications for agriculture and environment. Chemosphere. 2018, 194: 682-691.

[146] Száková J, Stiborová H, Mercl F, Hailegnaw NS, Lhotka M, Derevyankina T, Paul CS, Taisheva A, Brabec M, Tlustoš P. Woodchips biochar versus bone char in a one-year model soil incubation experiment: the importance of soil/char pH alteration on nutrient availability in soil. J Chem Technol Biotechnol. 2023.

[147] Tang L, Shen Z, Duan X, Wang Z, Wu Y, Shao X, Song X, Hu S, Li Z. Evaluating the potential of charred bone as P hotspot assisted by phosphate-solubilizing bacteria. Sci Total Environ. 2019, 696. 133965

[148] Tauqeer HM, Basharat Z, Ramzani PMA, Farhad M, Lewińska K, Turan V, Karczewska A, Khan SA, Faran GE, Iqbal M. Aspergillus niger-mediated release of phosphates from fish bone char reduces Pb phytoavailability in Pb-acid batteries polluted soil, and accumulation in fenugreek. Environ Pollut. 2022, 313. 120064

[149] Turner BL, Wright JS. The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry. 2014, 117: 115-130.

[150] United Nations Convention to Combat Desertification (2022) Global Land Outlook 2: Restoring hope, restoring lands. UNCCD. https://www.pbl.nl/sites/default/files/downloads/pbl-2022-the-global-potential-for-land-restoration-glo2-4816_0.pdf

[151] Vassilev N, Martos E, Mendes G, Martos V, Vassileva M. Biochar of animal origin: a sustainable solution to the global problem of high-grade rock phosphate scarcity?. J Sci Food Agric. 2013, 93(8): 1799-1804.

[152] Vazquez P, Holguin G, Puente ME, Lopez-Cortes A, Bashan Y. Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils. 2000, 30: 460-468.

[153] Wang YS, Dai JG, Wang L, Tsang DC, Poon CS. Influence of lead on stabilization/solidification by ordinary Portland cement and magnesium phosphate cement. Chemosphere. 2018, 190: 90-96.

[154] Wang M, Liu Y, Yao Y, Han L, Liu X. Comparative evaluation of bone chars derived from bovine parts: physicochemical properties and copper sorption behavior. Sci Total Environ. 2020, 700. 134470

[155] Wang X, Li C, Lam CH, Subramanian K, Qin ZH, Mou JH, Jin M, Chopra SS, Singh V, Ok YS, Yan J. Emerging waste valorisation techniques to moderate the hazardous impacts, and their path towards sustainability. J Hazard Mater. 2022, 423. 127023

[156] Warner RD. Review: analysis of the process and drivers for cellular meat production. Animal. 2019, 13: 3041-3058.

[157] Warren GP, Robinson JS, Someus E. Dissolution of phosphorus from animal bone char in 12 soils. Nutr Cycl Agroecosyst. 2009, 84(2): 167-178.

[158] Wickham H. ggplot2: elegant graphics for data analysis. 2016, New York, Springer-Verlag.

[159] Wickham H, François R, Henry L, Müller K (2020) Dplyr: A Grammar of Data Manipulation. R Package Version 0.8.4. https://CRAN.R-project.org/package=dplyr

[160] Wu YH, Zhou J, Yu D, Sun SQ, Luo J, Bing HJ, Sun HY. Phosphorus biogeochemical cycle research in mountainous ecosystems. J Mt Sci. 2013, 10: 43-53.

[161] Yao Q, Li Z, Song Y, Wright SJ, Guo X, Tringe SG, Tfaily MM, Paša-Tolić L, Hazen TC, Turner BL, Mayes MA. Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil. Nat Ecol Evol. 2018, 2(3): 499-509.

[162] Zaharioiu AM, Şandru C, Ionete EI, Marin F, Ionete RE, Soare A, Constantinescu M, Bucura F, Niculescu VC. Eco-friendly alternative disposal through the pyrolysis process of meat and bone meal. Materials. 2022, 15: 6593.

[163] Zendehdel M, Shoshtari-Yeganeh B, Khanmohamadi H, Cruciani G. Removal of fluoride from aqueous solution by adsorption on NaP: HAp nanocomposite using response surface methodology. Process Saf Environ Prot. 2017, 109172-191.

[164] Zhu J, Li M, Whelan M. Phosphorus activators contribute to legacy phosphorus availability in agricultural soils: a review. Sci Total Environ. 2018, 612: 522-537.

[165] Zimmer D, Kruse J, Siebers N, Panten K, Oelschläger C, Warkentin M, Hu Y, Zuin L, Leinweber P. Bone char vs. S-enriched bone char: multi-method characterization of bone chars and their transformation in soil. Sci Total Environ. 2018, 643: 145-156.

[166] Zimmer D, Panten K, Frank M, Springer A, Leinweber P. Sulfur-enriched bone char as alternative P fertilizer: spectroscopic, wet chemical, and yield response evaluation. Agriculture. 2019, 9: 21.

[167] Zwetsloot MJ, Lehmann J, Solomon D. Recycling slaughterhouse waste into fertilizer: how do pyrolysis temperature and biomass additions affect phosphorus availability and chemistry?. J Sci Food Agric. 2015, 952281-288.

[168] Zwetsloot MJ, Lehmann J, Bauerle T, Vanek S, Hestrin R, Nigussie A. Phosphorus availability from bone char in a P-fixing soil influenced by root-mycorrhizae-biochar interactions. Plant Soil. 2016, 408: 95-105.

Funding

Biotechnology and Biological Sciences Research Council(BB/V011596/1)

Programma Operativo Nazionale Ricerca e Competitività(CCI 2014IT16M2OP005)

RIGHTS & PERMISSIONS

The Author(s)