Skip to main content

Fertilization with Poultry Litter Increases the Abundance of Antibiotic-Resistant Bacteria in Tropical Soil: a Microcosm Study

Abstract

Various antimicrobial agents are used in the poultry industry to treat microbial infections and prevent disease or as growth promoters. As a result, poultry litter (PL) can contain antibiotic residues (AR), antibiotic-resistant bacteria (ARB), and antibiotic resistance genes. Still, PL is used in many countries as a fertilizer and feed supplement for cattle. To evaluate whether usage of PL in agriculture leads to the accumulation of AR and ARB accumulate in the soil, we (i) measured the concentration of monensin, tylosin, ciprofloxacin, oxytetracycline, and chlortetracycline and the abundance of culturable monensin-, tylosin-, and ciprofloxacin-resistant bacteria in 15 commercial PL samples and (ii) exposed soil microcosms to two PL regimes and followed the persistence of PL-associated ARB for 128 days through cultivation on media containing antibiotics. The PL samples analyzed contained high concentrations of monensin (27–95 mg kg−1), tylosin (152–450 mg kg−1), ciprofloxacin (29–101 mg kg−1), and (oxy/chlor)tetracycline (13–87 mg kg−1). Congruently, they included large absolute and relative numbers of bacteria capable of growing on agar plates supplemented with 5 to 50 μg mL−1 monensin (medians, 107–109 CFU g−1, 0.6–45%) or 25 to 50 μg mL−1 tylosin (median, 108 CFU g−1, 14–26%). By contrast, the abundance of bacteria resistant to 25–250 μg mL−1 CP in the PL samples was much lower (median values ranging from 106 to less than 102 CFU g−1, relative abundances, < 0.13%). We observed rapid increments of 1–3 logs in the amount of culturable tylosin- and CP-resistant bacteria in most microcosms upon fertilization (n = 3/4 and n = 5/8, respectively, p < 0.01). Half of these increments were sustained across the experiment (p < 0.05), demonstrating that the introduced ARB can thrive in soil. These results show that fertilization with PL can increase the basal amount of tylosin- and CP-resistant bacteria in the soil. The environmental and sanitary consequences of this finding justify changes in PL’s manufacturing process and a debate on its approved uses in agricultural systems.

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

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

Availability of Data and Material

Original data available from the corresponding author upon request.

References

  1. Armalytė, J., Skerniškytė, J., Bakienė, E., Krasauskas, R., Šiugždinienė, R., Kareivienė, V., Kerzienė, S., Klimienė, I., Sužiedėlienė, E., & Ružauskas, M. (2019). Microbial diversity and antimicrobial resistance profile in microbiota from soils of conventional and organic farming systems. Frontiers in Microbiology, 10, 892.

    Article  Google Scholar 

  2. Battacharyya, R., Ghosh, B. N., Mishra, P. K., Mandal, B., Rao, C. S., Sarkar, D., Das, K., Anil, K. S., Lalitha, M., Hati, K. M., & Franzluebbers, A. J. (2015). Soil degradation in India: Challenges and potential solutions. Sustainability, 7, 3528–3570.

    Article  Google Scholar 

  3. Bich Van, N. T., Phuong-Yen, N. T., Nhung, N. T., Cuong, N. V., Kiet, B. T., Hoang, N. V., Hien, V. B., Chansiripornchai, N., Choisy, M., Ribas, A., Campbell, J., Thwaites, G., & Carrique-Mas, J. (2020). Characterization of viral, bacterial, and parasitic causes of disease in small-scale chicken flocks in the Mekong Delta of Vietnam. Journal of Poultry Science, 99, 783–790.

    Article  Google Scholar 

  4. Bolan, N. S., Szogi, A. A., Chuasavathi, T., Seshadri, B., Rothrock, M. J., & Panneerselvam, P. (2010). Uses and management of poultry litter. World’s Poultry Science Journal, 66, 673–698.

    Article  Google Scholar 

  5. Boovaragamoorthy, G. M., Anbazhagan, M., Piruthiviraj, P., Pugazhendhi, A., Kumar, S. S., Al-Dhabi, N. A., Mohammed Ghilan, A.-K., Arasu, M. V., & Kaliannan, T. (2019). Clinically important microbial diversity and its antibiotic resistance pattern toward various drugs. Journal of Infection and Public Health, 12, 783–788.

    Article  Google Scholar 

  6. Chait, R., Palmer, A. C., Yelin, I., & Kishony, R. (2016). Pervasive selection for and against antibiotic resistance in inhomogeneous multistress environments. Nature Communications, 7, 10333.

    CAS  Article  Google Scholar 

  7. Chee-Sanford, J. C., Mackie, R. I., Koike, S., Krapac, I. G., Lin, Y. F., Yannarell, A. C., Maxwell, S., & Aminov, R. I. (2009). Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. Journal of Environmental Quality, 38, 1086–1108.

    CAS  Article  Google Scholar 

  8. Chen, L. J., Xing, L., & Han, L. J. (2009). Quantitative determination of nutrient content in poultry manure by near infrared spectroscopy based on artificial neural networks. Journal of Poultry Science, 88, 2496–2503.

    CAS  Article  Google Scholar 

  9. Chen, J., Li, J., Zhang, H., Shi, W., & Liu, Y. (2019a). Bacterial heavy-metal and antibiotic resistant genes in a copper tailing dam area in Northern China. Frontiers in Microbiology, 10, 1916.

    Article  Google Scholar 

  10. Chen, Q.-L., An, X.-L., Zheng, B.-X., Gillings, M., Peñuelas, J., Cui, L., Su, J.-Q., & Zhu, Y.-G. (2019b). Loss of soil microbial diversity exacerbates spread of antibiotic resistance. Soil Ecology Letters, 1, 3–13.

    Article  Google Scholar 

  11. Cheng, Z., & Jiang, X. (2014). Microbiological safety of chicken litter or chicken litter-based organic fertilizers: A review. Agriculture, 4, 1–29.

    Article  Google Scholar 

  12. Conde-Cid, M., Núñez Delgado, A., Fernández-Sanjurjo, M. J., Álvarez-Rodríguez, E., Fernández-Calviño, D., & Arias-Estévez, M. (2020). Tetracycline and sulfonamide antibiotics in soil: Presence, fate and environmental risks. Processes, 8, 1479.

    CAS  Article  Google Scholar 

  13. Coufal, C. D., Chavez, C., Niemeyer, P. R., & Carey, J. B. (2006). Measurement of broiler litter production rates and nutrient content using recycled litter. Journal of Poultry Science, 85, 398–403.

    CAS  Article  Google Scholar 

  14. Coyne, L., Arief, R., Benigno, C., Giang, V. N., Huong, L. Q., Jeamsripong, S., Kalpravidh, W., McGrane, J., Padungtod, P., Patrick, I., Schoonman, L., Setyawan, E., Sukarno, A. H., Srisamran, J., Ngoc, P. T., & Rushton, J. (2019). Characterizing antimicrobial use in livestock sector in three south east Asian countries (Indonesia, Thailand, and Vietnam). Antibiotics, 8, 33.

    Article  Google Scholar 

  15. Cycoń, M., Mrozik, A., & Piotrowska-Seget, Z. (2019). Antibiotics in the soil environment – Degradation and their impact on microbial activity and diversity. Frontiers in Microbiology, 10, 338.

    Article  Google Scholar 

  16. Erian, I., & Phillips, C. J. (2017). Public understanding and attitudes towards meat chicken production and relations to consumption. Animals, 7, 20.

    Article  Google Scholar 

  17. Fahrenfeld, N., Knowlton, K., Krometis, L. A., Hession, W. C., Xia, K., Lipscomb, E., Libuit, K., Green, B. L., & Pruden, A. (2014). Effect of manure application on abundance of antibiotic resistance genes and their attenuation rates in soil: Field-scale mass balance approach. Environmental Science and Technology, 48, 2643–2650.

    CAS  Article  Google Scholar 

  18. FAOSTAT. (2020). FAO statistical database. http://www.fao.org/faostat/en/#data/QL . Accessed 15 Sept 2021.

  19. Foust, R. D., Jr., Phillips, M., Hull, K., & Yehorova, D. (2018). Changes in arsenic, copper, iron, manganese, and zinc levels resulting from the application of poultry litter to agricultural soils. Toxics, 6, 28.

    Article  CAS  Google Scholar 

  20. Girardi, C., Greve, J., Lamshöft, M., Fetzer, I., Miltner, A., Schaeffer, A., & Kaestner, M. (2011). Biodegradation of ciprofloxacin in water and soil and its effects on the microbial communities. Journal of Hazardous Materials, 198, 22–30.

    CAS  Article  Google Scholar 

  21. Granados-Chinchilla, F., & Rodriguez, C. (2017). Tetracyclines in food and feedingstuffs: From regulation to analytical methods, bacterial resistance, and environmental and health implications. Journal of Analytical Methods in Chemistry, 2017, 1315497.

    Article  CAS  Google Scholar 

  22. Granados-Chinchilla, F., Sánchez, J., García, F., & Rodríguez, C. (2012). A novel green chemistry method for nonaqueous extraction and high-performance chromatography detection of first, second-, and third-generation tetracyclines, 4-epitetracycline, and tylosin in animal feeds. Journal of Agriculture and Food Chemistry, 60(7121), 7128.

    Google Scholar 

  23. Granados-Chinchilla, F., Arias-Andres, M. J., Montes, F., de Oca, M. L., & Rodríguez, C. (2020). Effect of the veterinary ionophore monensin on the structure and activity of a tropical soil bacterial community. Journal of Environmental Science and Health Part B, 55, 127–134.

    CAS  Article  Google Scholar 

  24. Guo, M., Hu, H.-W., Zhang, Y.-J., Wang, J.-T., Hayden, H., Tang, Y.-Q., & He, J.-Z. (2018). Aerobic composting reduces antibiotic resistance genes in cattle manure and the resistome dissemination in agricultural soils. Science of the Total Environment, 612, 1300–1310.

    Article  CAS  Google Scholar 

  25. Haag, G., Marin, G. H., & Errecalde, J. (2016). Quantification of residual enrofloxacin and ciprofloxacin in feathers of broiler chickens by high-performance liquid chromatography-fluorescence after oral administration. Journal of Advanced Pharmaceutical Technology & Research, 7, 2–5.

    CAS  Article  Google Scholar 

  26. Habib, A., Al Mahdy, S., Islam, F., Paul, T. K., Hossain, S., Hasan, N., & Sikder, M. H. (2017). Efficacy of tylosin and tiamulin against mycoplasmosis in poultry. Research in Agriculture, Livestock and Fisheries, 4, 187–191.

    Article  Google Scholar 

  27. Han, X.-M., Hu, H.-W., Chen, Q.-L., Yang, L.-Y., Li, H.-L., Zhu, Y.-G., Li, X.-Z., & Ma, Y.-B. (2018). Antibiotic resistance genes and associated bacterial communities in agricultural soils amended with different sources of animal manures. Soil Biology and Biochemistry, 126, 91–102.

    CAS  Article  Google Scholar 

  28. Huang, T., Xu, Y., Zeng, J., Zhao, D.-H., Li, L., Liao, X.-P., Liu, Y.-H., & Sun, J. (2016). Low-concentration ciprofloxacin selects plasmid-mediated quinolone resistance encoding genes and affects bacterial taxa in soil containing manure. Frontiers in Microbiology, 7, 1730.

    Google Scholar 

  29. Huang, X., Zheng, J., Tian, S., Liu, C., Liu, L., Wei, L., Fan, H., Zhang, T., Wang, L., Zhu, G., & Xu, K. (2019). Higher temperatures do not always achieve better antibiotic resistance gene removal in anaerobic digestion of swine manure. Applied Environmental Microbiology, 85, e02878-e2918.

    CAS  Google Scholar 

  30. Jordt, H., Stalder, T., Kosterlitz, O., Ponciano, J. M., Top, E. M., & Kerr, B. (2020). Coevolution of host–plasmid pairs facilitates the emergence of novel multidrug resistance. Nature Ecology & Evolution, 4, 863–869. https://doi.org/10.1038/s41559-020-1170-1.

  31. Kang, Y., Gu, X., Hao, Y., & Hu, J. (2016). Autoclave treatment of pig manure does not reduce the risk of transmission and transfer of tetracycline resistance genes in soil: Successive determinations with soil column experiments. Environmental Science and. Pollution Research, 23, 4551–4560.

    CAS  Article  Google Scholar 

  32. Khan, G. J., Khan, R. A., Majeed, I., Siddiqui, F. A., & Khan, S. (2015). Ciprofloxacin: The frequent use in poultry and its consequences on human health. The Professional Medical Journal, 22, 001–005.

    Article  Google Scholar 

  33. Kyakuwaire, M., Olupot, G., Amoding, A., Nkedi-Kizza, P., & Ateendyi-Basambi, T. (2019). How safe is chicken litter for land application as an organic fertilizer?: A review. International Journal of Environmental Research and Public Health, 16, 3521.

    Article  Google Scholar 

  34. Lerner, U., Amram, E., Ayling, R., Mikula, I., Gerchman, I., Harrus, S., Teff, D., Yogev, D., & Lysnyansky, I. (2014). Acquired resistance to 16-membered macrolides tylosin and tilmicosin by Mycoplasma bovis. Veterinary Microbiology, 168, 365–371.

    CAS  Article  Google Scholar 

  35. Ljubojević, D., Velhner, M., Todorović, D., Pajić, M., & Milanov, D. (2016). Tetracycline resistance in Escherichia coli isolates from poultry. Arhiv Veterinarske Medicine, 9, 61–81.

    Google Scholar 

  36. Lopatto, E., Choi, J., Colina, A., Ma, L., Howe, A., & Hinsa-Leasure, S. (2019). Characterizing the soil microbiome and quantifying antibiotic resistance gene dynamics in agricultural soil following swine CAFO manure application. PLoS ONE, 14, e0220770.

    CAS  Article  Google Scholar 

  37. Lorenz, M. G., & Wackernagel, W. (1994). Bacterial gene transfer by natural genetic transformation in the environment. Microbiology Reviews, 58, 563–602.

    CAS  Article  Google Scholar 

  38. Manikandan, M., Chun, S., Kazibwe, Z., Gopal, J., Singh, U. B., & Oh, J-W. (2020). Phenomenal bombardment of antibiotics in poultry: Contemplating the environmental repercussions. International Journal of Environment. Research and Public Health, 17, 5053.

  39. Manyi-Loh, C., Mamphweli, S., Meyer, E., & Okoh, A. (2018). Antibiotic use in agriculture and its consequential resistance in environmental sources: Potential public health implications. Molecules, 23, 795.

    Article  CAS  Google Scholar 

  40. Marchetti, M. L., Buchamer, A., Buldain, D., & Mestorino, N. (2019). Enrofloxacion and ciprofloxacin residues in broiler chicken feathers after enrofloxacin oral administration. ECVE, 4(3), 180–186.

    Google Scholar 

  41. McKinney, C. W., Dungan, R. S., Moore, A., & Leytem, A. (2018). Occurrence and abundance of antibiotics resistance genes in agricultural soil receiving dairy manure. FEMS Microbiology Ecology, 94, 1–9.

    Article  CAS  Google Scholar 

  42. Mottet, A., & Tempio, G. (2017). Global poultry production: Current state and future outlook and challenges. World’s Poultry Science Journal, 73, 245–256.

    Article  Google Scholar 

  43. Nelson, D. W., & Sommers, L. E. (1996). Methods of soil analysis. Part 3. Chemical methods. Soil Science Society of America Book Series, 5, 961–1010.

    Google Scholar 

  44. Noack, S., Chapman, H. D., & Selzer, P. M. (2019). Anticoccidial drugs of the livestock industry. Parasitology Research, 118, 2009–2026.

    Article  Google Scholar 

  45. Nowak, A., Matusiak, K., Borowski, S., Bakula, T., Opaliński, S., Kołacz, R., & Guarowska, B. (2016). Cytotoxicity of odorous compounds from poultry manure. International Journal of Environmental Research and Public Health, 13, 1046.

    Article  CAS  Google Scholar 

  46. Nyakawata, E. Z., Reddy, K. C., & Sistani, K. R. (2001). Tillage, cover cropping, and poultry litter effects on selected soil chemical properties. Soil and Tillage Research, 58, 69–79.

    Article  Google Scholar 

  47. Pan, M., & Chu, L. M. (2017). Transfer of antibiotics from wastewater or animal manure to soil and edible crops. Environment Pollution, 231, 829–836.

    CAS  Article  Google Scholar 

  48. Pereira Leal, R. M., Figueira, R. F., Tornisielo, V. L., & Regitano, J. B. (2012). Occurrence and sorption of fluoroquinolones in poultry litters and soils from São Paulo State, Brazil. Science of the Total Environment, 432, 344–349.

    Article  CAS  Google Scholar 

  49. Pérez-Varela, E., Kyselková, M., Ahmed, E., Sladecek, F. X., Goberna, M., & Elhhottová, D. (2019). Native soil microorganisms hinder the soil enrichment with antibiotic resistance genes following manure applications. Scientific Reports, 9, 6760.

    Article  CAS  Google Scholar 

  50. Peterson, E., & Kaur, P. (2018). Antibiotic resistance mechanisms in bacteria: Relationships between resistance determinants of antibiotic producers, environmental bacteria, and clinical pathogens. Frontiers in Microbiology, 9, 2928.

    Article  Google Scholar 

  51. Qian, X., Gu, J., Sun, W., Wang, X. J., Su, J. Q., & Stedfeld, R. (2018). Diversity, abundance, and persistence of antibiotic resistance genes in various types of animal manure following industrial composting. Journal of Hazardous Materials, 344, 716–722.

    CAS  Article  Google Scholar 

  52. Rodrigues, N. C., Ribeiro, L. A., Brito, M. A., & Martino, J. C. (2004). Chronic copper poisoning in sheep fed with poultry litter and citrus pulp. Ars Veterinaria, 20, 175–179.

    Google Scholar 

  53. Rokka, M., Jestoi, M., & Peltonen, K. (2013). Trace level determination of polyether ionophores in feed. BioMedical Research International, 2013, 151363.

    Article  Google Scholar 

  54. Roth, N., Käsbohrer, A., Mayrhofer, S., Zits, U., Hofacre, C., & Domig, K. J. (2019). The application of antibiotics in broiler production and the resulting antibiotic resistance in Escherichia coli. Poultry Science, 98, 1791–1804.

    CAS  Article  Google Scholar 

  55. Rothrock, M. J., Keen, P. L., Cook, K. L., Durso, L. M., Franklin, A. M., & Dungan, R. S. (2016). How should we be determining background and baseline antibiotic resistance levels in agroecosystem research? Journal of Environmental Quality, 45, 420–431.

    CAS  Article  Google Scholar 

  56. Santos Dalólio, F., Nogueira da Silva, J., Carneiro de Oliveira, A. C., Ferreira Tinôco, I. F., Barbosa, R. C., Resende, M. O., Texeira Albino, L. F., & Texeira Coelho, S. (2017). Poultry litter as biomass energy: A review and future perspectives. Renewable and Sustainable Energy Reviews, 76, 941–949.

    Article  CAS  Google Scholar 

  57. Scott, A., Tien, Y. C., Drury, C. F., Reynolds, W. D., & Top, E. (2018). Enrichment of antibiotic resistance genes in soil receiving composts derived from swine manure, yard wastes, or food wastes, and evidence for multiyear persistence of swine Clostridium spp. Canadian Journal of Microbiology, 64, 201–208.

    CAS  Article  Google Scholar 

  58. Shang, Y., Kumar, S., Oakley, B., & Kim, W. K. (2018). Chicken gut microbiota: Importance and detection technology. Frontiers in Veterinary Science, 5, 254.

    Article  Google Scholar 

  59. Svihus, B., & Itani, K. (2019). Intestinal Passage and its relation to digestive process. Journal of Applied Poultry Research, 28, 546–555.

    CAS  Article  Google Scholar 

  60. Tamminen, M., Virta, M., Fani, R., & Fondi, M. (2012). Large-scale analysis of plasmid relationships through gene-sharing networks. Molecular Biology and Evolution, 29, 1225–1240.

    CAS  Article  Google Scholar 

  61. Tasistro, A. S., Kissel, D. E., & Bush, P. B. (2004). Sampling broiler litter: How many samples are needed? The Journal of Applied Poultry Research, 13, 163–170.

    Article  Google Scholar 

  62. Udikovic-Kolic, N., Wichmann, F., Broderick, N. A., & Handelsman, J. (2014). Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. PNAS, 111, 15202–15207.

    CAS  Article  Google Scholar 

  63. Van Epps, A., & Blaney, L. (2016). Antibiotic residues in animal waste: Occurrence and degradation in conventional agricultural waste: Management practices. Current Pollution Reports, 2, 135–155.

    Article  CAS  Google Scholar 

  64. Von Winterdorff, C. J., Penders, J., van Nierkerk, J. M., Mills, N. D., Majunder, S., van Alphen, L. B., Savelkoul, P. H., & Wolffs, P. F. (2016). Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Frontiers in Microbiology, 7, 173.

    Google Scholar 

  65. Wales, A. D., & Davies, R. H. (2015). Co-Selection of resistance to antibiotics, biocides and heavy metals, and its relevance to foodborne pathogens. Antibiotics, 4, 567–604.

    Article  Google Scholar 

  66. Walsh, F., & Duffy, B. (2013). The culturable soil antibiotic resistome: A community of multi-drug resistant bacteria. PLoS ONE, 8, e65567.

    CAS  Article  Google Scholar 

  67. Wong, A. (2019). Unknown risk on the farm: Does agricultural use of ionophores contribute to the burden of antimicrobial resistance? mSphere, 4, e00433-19.

    Google Scholar 

  68. Xie, W.-Y., Yuan, S.-T., Xu, M.-G., Yang, X.-P., Shen, Q.-R., Zhang, W.-W., Su, J.-Q., & Zhao, & F-J. . (2018). Long-term effects of manure and chemical fertilizers on soil antibiotic resistome. Soil Biology and Biochemistry, 122, 111–119.

    CAS  Article  Google Scholar 

  69. Xiong, W., Sun, Y., Ding, X., Wang, M., & Zeng, Z. (2015). Selective pressure of antibiotics on ARGs and bacterial communities in manure-polluted freshwater-sediment microcosm. Frontiers in Microbiology, 6, 194.

    Google Scholar 

  70. Yang, Q., Zhang, H., Guo, Y., & Tian, T. (2016). Influence of chicken manure fertilization on antibiotic-resistant bacteria in soil and the endophytic bacteria of Pakchoi. International Journal of Environmental Research and Public Health, 13, 662.

    Article  CAS  Google Scholar 

  71. Yang, Y., Ashworth, A. J., Willett, C., Cook, K., Upadyay, A., Owens, P. R., Ricke, S. C., DeBruyn, J. M., & Moore, P. A. (2019). Review of antibiotic resistance, ecology, dissemination, and mitigation in U.S. Broiler Poultry Systems. Frontiers in Microbiology, 10, 2639.

    Article  Google Scholar 

  72. Zhang, R., Gu, J., Wang, X., Li, Y., Zhang, K., Yin, Y., & Zhang, X. (2018). Contributions of the microbial community and environmental variables to antibiotic resistance genes during co-composting with swine manure and cotton stalks. Journal of Hazardous Materials, 358, 82–91.

    CAS  Article  Google Scholar 

  73. Zhu, Y.-G., Zhao, Y., Zhu, D., Gillings, M., Penuelas, J., Ok, Y. S., Capon, A., & Banwart, S. (2019). Soil biota, antimicrobial resistance and planetary health. Environment International, 131, 105059.

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Astrid Leiva and Alfonso García for their help with the references and statistical analysis, respectively.

Funding

There is no external funding to declare. The research was funded by the Vice Rectory Office for Research of the Universidad de Costa Rica (grant number B1038).

Author information

Affiliations

Authors

Corresponding author

Correspondence to César Rodríguez.

Ethics declarations

Ethics Approval

No animal or human assays were performed during this research.

Consent to Participate

Not applicable.

Consent to Publication

Not applicable.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Appendix

Appendix

Table 3 Average composition and chemical analysis of n = 15 poultry litter samples collected at eight Costa Rican farms

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Chaves-Ulate, C., Granados-Chinchilla, F. & Rodríguez, C. Fertilization with Poultry Litter Increases the Abundance of Antibiotic-Resistant Bacteria in Tropical Soil: a Microcosm Study. Water Air Soil Pollut 232, 402 (2021). https://doi.org/10.1007/s11270-021-05347-1

Download citation

Keywords

  • Poultry litter
  • Fertilization
  • Soil
  • Antibiotic residues
  • Antibiotic resistance