Co-contamination of antibiotics and metals in peri-urban agricultural soils and source identification

Abstract

To identify the dominant sources of contamination in peri-urban land, this study investigated the concentrations and distributions of antibiotics and metals in agricultural soil of this area. An index of landscape development intensity (LDI) was used to characterize the distribution of human disturbance-related land use. The results showed that total antibiotic concentration in the soil reached 395.55 μg/kg and that chlortetracycline was the predominant antibiotic compound, with a relatively high mean concentration of 30.62 μg/kg. In soils, the mean concentrations of Cu, Zn, and Pb were 38.41, 127.88, and 56.61 mg/kg and those of Al, Fe, and K were 83.73, 24.17, and 23.42 g/kg, respectively. A redundancy analysis showed that the landscape pattern in a 300-m buffer zone can well explain the variation in the concentrations of antibiotics and metals (24%, p < 0.05). The LDI in the 300-m buffer zone significantly correlated with the concentrations of total antibiotics and total amounts of Cu and Zn in the soil, suggesting that the risk of soil contamination increases with the intensity of anthropogenic activities. A structural equation modeling analysis indicated that Al, Cu, and Zn could significantly aggravate accumulation of tetracycline antibiotics in the soil, whereas there were only significantly direct paths from Cu to ciprofloxacin and norfloxacin. Overall, the results showed that aggravated co-contamination of antibiotics and metals occurs in agricultural soil under intensive human disturbance.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. Alfaro MA, Gregory PJ, Jarvis SC (2004) Dynamics of potassium leaching on a hillslope grassland soil. J Environ Qual 33:192

    CAS  Google Scholar 

  2. Arhonditsis GB, Stow CA, Steinberg LJ, Kenney MA, Lathrop RC, McBride SJ, Reckhow KH (2006) Exploring ecological patterns with structural equation modeling and Bayesian analysis. Ecol Model 192:385–409

    Google Scholar 

  3. Aristilde L, Marichal C, Miéhé-Brendlé J, Lanson B, Charlet L (2010) Interactions of oxytetracycline with a smectite clay: a spectroscopic study with molecular simulations. Environ Sci Technol 44:7839–7845

    CAS  Google Scholar 

  4. Blanchet G, Libohova Z, Joost S, Rossier N, Schneider A, Jeangros B, Sinaj S (2017) Spatial variability of potassium in agricultural soils of the canton of Fribourg, Switzerland. Geoderma 290:107–121

    CAS  Google Scholar 

  5. Bonzongo JCJ, Donkor AK, Attibayeba A, Gao J (2016) Linking landscape development intensity within watersheds to methyl-mercury accumulation in river sediments. Ambio 45:196–204

    CAS  Google Scholar 

  6. Brown MT, Vivas MB (2005) Landscape development intensity index. Environ Monit Assess 101:289–309

    Google Scholar 

  7. Carneiro M, Colaço B, Colaço J, Faustino-Rocha AI, Colaço A, Lavin S, Oliveira PA (2015) Biomonitoring of metals and metalloids with raptors from Portugal and Spain: a review. Environ Rev 24:63–83

    Google Scholar 

  8. Cassman KG, Bryant DC, Higashi SL, Roberts BA, Kerby TA (1989) Soil potassium balance and cumulative cotton response to annual potassium additions on a vermiculitic soil. Soil Sci Soc Am J 53:805–812

    CAS  Google Scholar 

  9. Chen H, Teng Y, Lu S, Wang Y, Wang J (2015) Contamination features and health risk of soil heavy metals in China. Sci Total Environ 512–513:143–153

    Google Scholar 

  10. Chen TS, Lin HJ (2011) Application of a landscape development intensity index for assessing wetlands in Taiwan. Wetlands 31:745–756

    Google Scholar 

  11. Christou A, Aguera A, Bayona JM, Cytryn E, Fotopoulos V, Lambropoulou D, Manaia CM, Michael C, Revitt M, Schroder P, Fatta-Kassinos D (2017) The potential implications of reclaimed wastewater reuse for irrigation on the agricultural environment: the knowns and unknowns of the fate of antibiotics and antibiotic resistant bacteria and resistance genes—a review. Water Res 123:448–467

    CAS  Google Scholar 

  12. Du LF, Liu WK (2012) Occurrence, fate, and ecotoxicity of antibiotics in agro-ecosystems. A review. Agron Sustain Dev 32:309–327

    CAS  Google Scholar 

  13. Dong Y, Zheng W, Zhou J (2007) Soil geochemical background in Zhejiang (in Chinese). Agro-geological environment survey in Zhejiang. Geological Publishing House, Beijing

    Google Scholar 

  14. Etter A, McAlpine CA, Seabrook L, Wilson KA (2011) Incorporating temporality and biophysical vulnerability to quantify the human spatial footprint on ecosystems. Biol Conserv 144:1585–1594

    Google Scholar 

  15. Ferrey ML, Coreen Hamilton M, Backe WJ, Anderson KE (2018) Pharmaceuticals and other anthropogenic chemicals in atmospheric particulates and precipitation. Sci Total Environ 612:1488–1497

    CAS  Google Scholar 

  16. Gao LH, Shi YL, Li WH, Liu JM, Cai YQ (2015) Occurrence and distribution of antibiotics in urban soil in Beijing and Shanghai, China. Environ Sci Pollut Res 22:11360–11371

    CAS  Google Scholar 

  17. Gao P, Ding Y, Li H, Xagoraraki I (2012) Occurrence of pharmaceuticals in a municipal wastewater treatment plant: mass balance and removal processes. Chemosphere 88:17–24

    CAS  Google Scholar 

  18. Gombert S, Asta J, Seaward MRD (2004) Assessment of lichen diversity by index of atmospheric purity (IAP), index of human impact (IHI) and other environmental factors in an urban area (Grenoble, southeast France). Sci Total Environ 324:183–199

    CAS  Google Scholar 

  19. Guo T, Lou C, Zhai W, Tang X, Hashmi MZ, Murtaza R, Li Y, Liu X, Xu J (2018) Increased occurrence of heavy metals, antibiotics and resistance genes in surface soil after long-term application of manure. Sci Total Environ 635:995–1003

    CAS  Google Scholar 

  20. Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, Briggs JM (2008) Global change and the ecology of cities. Science 319:756–760

    CAS  Google Scholar 

  21. Ho YB, Zakaria MP, Latif PA, Saari N (2014) Occurrence of veterinary antibiotics and progesterone in broiler manure and agricultural soil in Malaysia. Sci Total Environ 488:261–267

    Google Scholar 

  22. Hou J, Wan WN, Mao DQ, Wang C, Mu QH, Qin SY, Luo Y (2015) Occurrence and distribution of sulfonamides, tetracyclines, quinolones, macrolides, and nitrofurans in livestock manure and amended soils of northern China. Environ Sci Pollut Res 22:4545–4554

    CAS  Google Scholar 

  23. Hu W, Wang H, Dong L, Huang B, Borggaard OK, Bruun Hansen HC, He Y, Holm PE (2018) Source identification of heavy metals in peri-urban agricultural soils of southeast China: an integrated approach. Environ Pollut 237:650–661

    CAS  Google Scholar 

  24. Huang Y, Li T, Wu C, He Z, Japenga J, Deng M, Yang X (2015) An integrated approach to assess heavy metal source apportionment in peri-urban agricultural soils. J Hazard Mater 299:540–549

    CAS  Google Scholar 

  25. Jia DA, Zhou DM, Wang YJ, Zhu HW, Chen JL (2008) Adsorption and cosorption of Cu(II) and tetracycline on two soils with different characteristics. Geoderma 146:224–230

    CAS  Google Scholar 

  26. Jia MY, Wang F, Bian YR, Jin X, Song Y, Kengara FO, Xu RK, Jiang X (2013) Effects of pH and metal ions on oxytetracycline sorption to maize-straw-derived biochar. Bioresour Technol 136:87–93

    CAS  Google Scholar 

  27. Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, Goossens H, Laxminarayan R (2018) Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A 115:3463–3470

    Google Scholar 

  28. Kong WD, Zhu YG, Fu BJ, Marschner P, He JZ (2006) The veterinary antibiotic oxytetracycline and Cu influence functional diversity of the soil microbial community. Environ Pollut 143:129–137

    CAS  Google Scholar 

  29. Li C, Chen JY, Wang JH, Ma ZH, Han P, Luan YX, Lu AX (2015a) Occurrence of antibiotics in soils and manures from greenhouse vegetable production bases of Beijing, China and an associated risk assessment. Sci Total Environ 521:101–107

    Google Scholar 

  30. Li J, Zhang HB, Chen YS, Luo YM, Zhang H (2016) Sources identification of antibiotic pollution combining land use information and multivariate statistics. Environ Monit Assess 188:430–442

    Google Scholar 

  31. Li YL, Li YF, Xu ZX, Guan ZM (2015b) Impact of landscape pattern of riparian buffers on water quality in the upper reaches of Huntai River Basin. J Ecol Rural Environ 31:59–68 (in Chinese)

    CAS  Google Scholar 

  32. Liu YJ, Laird DA, Barak P (1997) Release and fixation of ammonium and potassium under long-term fertility management. Soil Sci Soc Am J 61:310–314

    CAS  Google Scholar 

  33. Maas S, Scheifler R, Benslama M, Crini N, Lucot E, Brahmia Z, Benyacoub S, Giraudoux P (2010) Spatial distribution of heavy metal concentrations in urban, suburban and agricultural soils in a Mediterranean city of Algeria. Environ Pollut 158:2294–2301

    CAS  Google Scholar 

  34. MacKay AA, Canterbury B (2005) Oxytetracycline sorption to organic matter by metal-bridging. J Environ Qual 34:1964–1971

    CAS  Google Scholar 

  35. Mader P, Fliessbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697

    CAS  Google Scholar 

  36. Mantovi P, Bonazzi G, Maestri E, Marmiroli N (2003) Accumulation of copper and zinc from liquid manure in agricultural soils and crop plants. Plant Soil 250:249–257

    CAS  Google Scholar 

  37. Margriter SC, Bruland GL, Kudray GM, Lepczyk CA (2014) Using indicators of land-use development intensity to assess the condition of coastal wetlands in Hawai‘i. Landsc Ecol 29:517–528

    Google Scholar 

  38. McLaren TI, Guppy CN, Tighe MK, Forster N, Grave P, Lisle LM, Bennett JW (2012) Rapid, nondestructive total elemental analysis of vertisol soils using portable X-ray fluorescence. Soil Sci Soc Am J 76:1436–1445

    CAS  Google Scholar 

  39. Nicholson FA, Chambers BJ, Williams JR, Unwin RJ (1999) Heavy metal contents of livestock feeds and animal manures in England and Wales. Bioresour Technol 70:23–31

    CAS  Google Scholar 

  40. Nicholson FA, Smith SR, Alloway BJ, Carlton-Smith C, Chambers BJ (2003) An inventory of heavy metals inputs to agricultural soils in England and Wales. Sci Total Environ 311:205–219

    CAS  Google Scholar 

  41. Oliver LM, Lehrter JC, Fisher WS (2011) Relating landscape development intensity to coral reef condition in the watersheds of St. Croix, US Virgin Islands. Mar Ecol Prog Ser 427:293–302

    Google Scholar 

  42. Ostermann A, Gao J, Welp G, Siemens J, Roelcke M, Heimann L, Nieder R, Xue Q, Lin X, Sandhage-Hofmann A, Amelung W (2014) Identification of soil contamination hotspots with veterinary antibiotics using heavy metal concentrations and leaching data—a field study in China. Environ Monit Assess 186:7693–7707

    CAS  Google Scholar 

  43. Pan M, Chu LM (2017) Fate of antibiotics in soil and their uptake by edible crops. Sci Total Environ 599–600:500–512

    Google Scholar 

  44. Pei ZP, Yang S, Li LY, Li CM, Zhang SZ, Shan XQ, Wen B, Guo BY (2014) Effects of copper and aluminum on the adsorption of sulfathiazole and tylosin on peat and soil. Environ Pollut 184:579–585

    CAS  Google Scholar 

  45. Pils JRV, Laird DA (2007) Sorption of tetracycline and chlortetracycline on K- and Ca-saturated soil clays, humic substances, and clay−humic complexes. Environ Sci Technol 41:1928–1933

    CAS  Google Scholar 

  46. Qian M, Wu H, Wang J, Zhang H, Zhang Z, Zhang Y, Lin H, Ma J (2016) Occurrence of trace elements and antibiotics in manure-based fertilizers from the Zhejiang Province of China. Sci Total Environ 559:174–181

    CAS  Google Scholar 

  47. Rahman MM, Shan J, Yang P, Shang X, Xia Y, Yan X (2018) Effects of long-term pig manure application on antibiotics, abundance of antibiotic resistance genes (ARGs), anammox and denitrification rates in paddy soils. Environ Pollut 240:368–377

    CAS  Google Scholar 

  48. Rajmohan N, Prathapar SA, Jayaprakash M, Nagarajan R (2014) Vertical distribution of heavy metals in soil profile in a seasonally waterlogging agriculture field in Eastern Ganges Basin. Environ Monit Assess 186:5411–5427

    CAS  Google Scholar 

  49. Raudsepp-Hearne C, Peterson GD, Bennett EM (2010) Ecosystem service bundles for analyzing tradeoffs in diverse landscapes. Proc Natl Acad Sci U S A 107:5242–5247

    CAS  Google Scholar 

  50. Reiss KC, Hernandez E, Brown MT (2014) Application of the landscape development intensity (LDI) index in wetland mitigation banking. Ecol Model 271:83–89

    Google Scholar 

  51. Riaz L, Mahmood T, Khalid A, Rashid A, Ahmed Siddique MB, Kamal A, Coyne MS (2018) Fluoroquinolones (FQs) in the environment: a review on their abundance, sorption and toxicity in soil. Chemosphere 191:704–720

    CAS  Google Scholar 

  52. Rosolem CA, Steiner F (2017) Effects of soil texture and rates of K input on potassium balance in tropical soil. Eur J Soil Sci 68:658–666

    CAS  Google Scholar 

  53. Seiler C, Berendonk TU (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol 3:399

    Google Scholar 

  54. Sheikhhosseini A, Shirvani M, Shariatmadari H (2013) Competitive sorption of nickel, cadmium, zinc and copper on palygorskite and sepiolite silicate clay minerals. Geoderma 192:249–253

    CAS  Google Scholar 

  55. Simon E, Vidic A, Braun M, Fábián I, Tóthmérész B (2013) Trace element concentrations in soils along urbanization gradients in the city of Wien, Austria. Environ Sci Pollut Res 20:917–924

    CAS  Google Scholar 

  56. Singh S, Kumar M (2006) Heavy metal load of soil, water and vegetables in peri-urban Delhi. Environ Monit Assess 120:79–91

    CAS  Google Scholar 

  57. Sipos P, Németh T, Kis VK, Mohai I (2008) Sorption of copper, zinc and lead on soil mineral phases. Chemosphere 73:461–469

    CAS  Google Scholar 

  58. Song J, Rensing C, Holm PE, Virta M, Brandt KK (2017) Comparison of metals and tetracycline as selective agents for development of tetracycline resistant bacterial communities in agricultural soil. Environ Sci Technol 51:3040–3047

    CAS  Google Scholar 

  59. Stuer-Lauridsen F, Birkved M, Hansen LP, Lutzhoft HCH, Halling-Sorensen B (2000) Environmental risk assessment of human pharmaceuticals in Denmark after normal therapeutic use. Chemosphere 40:783–793

    CAS  Google Scholar 

  60. Sun J, Zeng Q, Tsang DCW, Zhu LZ, Li XD (2017) Antibiotics in the agricultural soils from the Yangtze River Delta, China. Chemosphere 189:301–308

    CAS  Google Scholar 

  61. Tan YY, Guo Y, Gu XY, Gu C (2015) Effects of metal cations and fulvic acid on the adsorption of ciprofloxacin onto goethite. Environ Sci Pollut Res 22:609–617

    CAS  Google Scholar 

  62. Tasho RP, Cho JY (2016) Veterinary antibiotics in animal waste, its distribution in soil and uptake by plants: a review. Sci Total Environ 563:366–376

    Google Scholar 

  63. Teng Y, Wu J, Lu S, Wang Y, Jiao X, Song L (2014) Soil and soil environmental quality monitoring in China: a review. Environ Int 69:177–199

    CAS  Google Scholar 

  64. Ternes TA, Bonerz M, Herrmann N, Teiser B, Andersen HR (2007) Irrigation of treated wastewater in Braunschweig, Germany: an option to remove pharmaceuticals and musk fragrances. Chemosphere 66:894–904

    CAS  Google Scholar 

  65. Tolls J (2001) Sorption of veterinary pharmaceuticals in soils: a review. Environ Sci Technol 35:3397–3406

    CAS  Google Scholar 

  66. Toth G, Hermann T, Da Silva MR, Montanarella L (2016) Heavy metals in agricultural soils of the European Union with implications for food safety. Environ Int 88:299–309

    CAS  Google Scholar 

  67. Violante A, Cozzolino V, Perelomov L, Caporale AG, Pigna M (2010) Mobility and bioavailability of heavy metals and metalloids in soil environments. J Soil Sci Plant Nut 10:268–292

    Google Scholar 

  68. Wang SL, Wang H (2015) Adsorption behavior of antibiotic in soil environment: a critical review. Front Env Sci Eng 9:565–574

    CAS  Google Scholar 

  69. Wong SC, Li XD, Zhang G, Qi SH, Min YS (2002) Heavy metals in agricultural soils of the Pearl River Delta, South China. Environ Pollut 119:33–44

    CAS  Google Scholar 

  70. Wu D, Huang ZT, Yang K, Graham D, Xie B (2015) Relationships between antibiotics and antibiotic resistance gene levels in municipal solid waste leachates in Shanghai, China. Environ Sci Technol 49:4122–4128

    CAS  Google Scholar 

  71. Wu J (1999) Sorption and desorption of copper on soil clay components. J Environ Qual 28:334–338

    CAS  Google Scholar 

  72. Xiang Q, Chen QL, Zhu D, An XL, Yang XR, Su JQ, Qiao M, Zhu YG (2018) Spatial and temporal distribution of antibiotic resistomes in a peri-urban area is associated significantly with anthropogenic activities. Environ Pollut 235:525–533

    CAS  Google Scholar 

  73. Yang Y, Owino AA, Gao Y, Yan X, Xu C, Wang J (2016) Occurrence, composition and risk assessment of antibiotics in soils from Kenya, Africa. Ecotoxicology 25:1194–1201

    CAS  Google Scholar 

  74. Yang Z, Yu T, Hou Q, Xia X, Feng H, Huang C, Wang L, Lv Y, Zhang M (2014) Geochemical evaluation of land quality in China and its applications. J Geochem Explor 139:122–135

    CAS  Google Scholar 

  75. Zhang QQ, Ying GG, Pan CG, Liu YS, Zhao JL (2015) Comprehensive evaluation of antibiotics emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. Environ Sci Technol 49:6772–6782

    CAS  Google Scholar 

  76. Zhang Y, Cai X, Lang X, Qiao X, Li X, Chen J (2012) Insights into aquatic toxicities of the antibiotics oxytetracycline and ciprofloxacin in the presence of metal: complexation versus mixture. Environ Pollut 166:48–56

    CAS  Google Scholar 

  77. Zhang Z, Sun K, Gao B, Zhang G, Liu X, Zhao Y (2011) Adsorption of tetracycline on soil and sediment: effects of pH and the presence of Cu(II). J Hazard Mater 190:856–862

    CAS  Google Scholar 

  78. Zhao FK, Chen LD, Yang L, Fang L, Sun L, Li SJ (2017) Composition and distribution of antibiotics in soils under different land use types in typical peri-urban area of Yangtze River Delta. Environ Sci 38:346–355 (in Chinese)

    Google Scholar 

  79. Zhao F, Chen L, Yang L, Li S, Sun L, Yu X (2018) Distribution, dynamics and determinants of antibiotics in soils in a peri-urban area of Yangtze River Delta, eastern China. Chemosphere 211:261–270

    CAS  Google Scholar 

  80. Zhao Y, Geng J, Wang X, Gu X, Gao S (2011) Tetracycline adsorption on kaolinite: pH, metal cations and humic acid effects. Ecotoxicology 20:1141–1147

    CAS  Google Scholar 

  81. Zheng J, Zhou Z, Wei Y, Chen T, Feng W, Chen H (2018) High-throughput profiling of seasonal variations of antibiotic resistance gene transport in a peri-urban river. Environ Int 114:87–94

    CAS  Google Scholar 

  82. Zheng S, Hu J, Chen K, Yao J, Yu Z, Lin X (2009) Soil microbial activity measured by microcalorimetry in response to long-term fertilization regimes and available phosphorous on heat evolution. Soil Biol Biochem 41:2094–2099

    CAS  Google Scholar 

  83. Zhou X, Qiao M, Wang FH, Zhu YG (2017) Use of commercial organic fertilizer increases the abundance of antibiotic resistance genes and antibiotics in soil. Environ Sci Pollut Res 24:701–710

    CAS  Google Scholar 

  84. Zhu YG, Reid BJ, Meharg AA, Banwart SA, Fu BJ (2017) Optimizing Peri-URban Ecosystems (PURE) to re-couple urban-rural symbiosis. Sci Total Environ 586:1085–1090

    CAS  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation of China (41571130064 and 41701018) and the Youth Innovation Promotion Association, Chinese Academy of Sciences (2018057).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Lei Yang.

Additional information

Responsible editor: Zhihong Xu

Electronic supplementary material

ESM 1

(DOC 67 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhao, F., Yang, L., Chen, L. et al. Co-contamination of antibiotics and metals in peri-urban agricultural soils and source identification. Environ Sci Pollut Res 25, 34063–34075 (2018). https://doi.org/10.1007/s11356-018-3350-y

Download citation

Keywords

  • Landscape development intensity
  • Land use
  • Soil contamination
  • Antibiotics
  • Metals