Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Dietary condensed tannins in bovine faeces and effects on soil microbial dynamics: are there environmental benefits for cattle production systems?

Gisele M. Fagundes https://orcid.org/0000-0001-9304-6160 A E , Gabriela Benetel B , Mateus M. Carriero B , Ricardo L. M. Sousa B , Kelly C. Santos C , James P. Muir D and Ives C. S. Bueno B
+ Author Affiliations
- Author Affiliations

A Department of Animal Science, Federal University of Roraima, BR-174, Km 12, Boa Vista, RR 69300-000, Brazil.

B Department of Animal Science, University of São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga, SP 13635-900, Brazil.

C Department of Animal Science, Federal Rural University of Pernambuco, Av. Dom Manuel de Medeiros, Recife, PE 52171-900, Brazil.

D Texas A&M AgriLife Research, 1229 North U.S. Highway 281, Stephenville, TX 76401, USA.

E Corresponding author. Email: gisele.fagundes@ufrr.br

Animal Production Science 61(7) 690-697 https://doi.org/10.1071/AN20118
Submitted: 5 March 2020  Accepted: 12 December 2020   Published: 4 February 2021

Abstract

Context: Plant bioactive compounds such as condensed tannins (CT) are seen as an alternative to rumen chemical modulators to mitigate rumen methanogenesis in livestock; however, the presence of CT in ruminant faeces also produces a series of changes in soil microbiomes. Little is known about these effects on soil nutrient dynamics. Therefore, whether CT affect the decomposition process of faecal organic matter, delaying it and consequently increasing soil carbon and nitrogen (N) sequestration, merits study.

Aims: Our study investigated the effects of a diet rich in CT on bovine faecal composition and on subsequent dynamics of a soil microbial population.

Methods: Faeces were analysed from cattle fed the following diets: control (no CT), 1.25% CT, 2.5% CT. In a greenhouse pot experiment over a period of 60 days, faeces from the three dietary treatments were applied to soil and the soil microbial populations were measured against a control with no faeces applied.

Key results: The presence of CT increased the excretion of faecal N and of neutral and acid detergent fibres and lignin, and the higher rate of CT reduced the rate of soil organic matter decomposition. Treatments with dietary CT resulted in greater total numbers of bacteria in the soil than in the no-faeces control and stimulated numbers of Actinobacteria, Proteobacteria (α-Proteobacteria) and Firmicutes.

Conclusions: The study showed that CT alter N recycling and other nutrient inputs in a soil–animal ecosystem by increasing faecal N inputs, delaying organic matter breakdown, and changing soil microbial dynamics.

Implications: The presence of CT in ruminant diets can be beneficial to the soil environment. Sustainable management practices should be encouraged by providing ruminants with feed including high-CT legumes in silvopastoral systems.

Keywords: nutrient cycling, livestock manure, soil microorganisms, sustainability, polyphenol residues.


References

Animut G, Goetsch AL, Puchala R, Patra AK, Sahlu T, Varel VH, Wells J (2008) Methane emission by goats consuming diets with different levels of condensed tannins from lespedeza. Animal Feed Science and Technology 144, 212–227.
Methane emission by goats consuming diets with different levels of condensed tannins from lespedeza.Crossref | GoogleScholarGoogle Scholar |

AOAC (1995) ‘Official methods of analysis.’ 16th edn (Association of Official Analytical Chemists: Arlington, VA, USA)

Bueno ICS, Vitti DMSS, Louvandini H, Abdalla AL (2008) A new approach for in vitro bioassay to measure tannin biological effects based on a gas production technique. Animal Feed Science and Technology 141, 153–170.
A new approach for in vitro bioassay to measure tannin biological effects based on a gas production technique.Crossref | GoogleScholarGoogle Scholar |

Bueno ICS, Brandi RA, Franzolin R, Fagundes GM, Benetel G, Abdalla A, Louvandini H, Muir JP (2015) Comparative in vitro methane production and antimethanogenic effect of tannins in five ruminant species. Animal Feed Science and Technology 205, 1–9.
Comparative in vitro methane production and antimethanogenic effect of tannins in five ruminant species.Crossref | GoogleScholarGoogle Scholar |

Dhanasekaran S, Doherty TM, Kenneth J (2010) Comparison of different standards for real-time PCR-based absolute quantification. Journal of Immunological Methods 354, 34–39.
Comparison of different standards for real-time PCR-based absolute quantification.Crossref | GoogleScholarGoogle Scholar | 20109462PubMed |

Driebe EM, Whitham TG (2000) Cotton wood hybridization affects tannin and nitrogen content of leaf litter and alters decomposition. Oecologia 123, 99–107.
Cotton wood hybridization affects tannin and nitrogen content of leaf litter and alters decomposition.Crossref | GoogleScholarGoogle Scholar | 28308750PubMed |

Eckard RJ, Grainger C, Klein CAM (2010) Options for the abatement of methane and nitrous oxide from ruminant production. Livestock Science 130, 47–56.
Options for the abatement of methane and nitrous oxide from ruminant production.Crossref | GoogleScholarGoogle Scholar |

Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Applied and Environmental Microbiology 71, 4117–4120.
Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays.Crossref | GoogleScholarGoogle Scholar | 16000830PubMed |

Godornes C, Leader BT, Molini BJ, Centurion-Lara A, Lukehart SA (2007) Quantification of rabbit cytokine mRNA by real-time RT-PCR. Cytokine 38, 1
Quantification of rabbit cytokine mRNA by real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 17521914PubMed |

Goldfarb KC, Karaoz U, Handson CA, Santee CA, Bradford MA, Treseder KK, Wallenstein MD, Brodie EL (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Frontiers in Microbiology 2, 94
Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance.Crossref | GoogleScholarGoogle Scholar | 21833332PubMed |

Grainger C, Clarke T, Auldist MJ, Beauchemin KA, Mcginn SM, Waghorn GC, Eckard RJ (2009) Potential use of Acacia mearnsii condensed tannins to reduce methane emissions and nitrogen excretion from grazing dairy cows. Journal of Animal Science 89, 241–251.

Huang Q, Holman DB, Alexander T, Hu T, Jin L, Xu Z, Mcallister TA, Acharya S, Zhao G, Wang Y (2018) Faecal microbiota of lambs fed purple prairie clover (Dalea purpurea Vent.) and alfalfa (Medicago sativa). Archives of Microbiology 200, 137–145.
Faecal microbiota of lambs fed purple prairie clover (Dalea purpurea Vent.) and alfalfa (Medicago sativa).Crossref | GoogleScholarGoogle Scholar | 28864945PubMed |

Jost DI, Joergensen RG, Sundrum A (2013) Effect of cattle faeces with different microbial biomass content on soil properties, gaseous emissions and plant growth. Biology and Fertility of Soils 49, 61–70.
Effect of cattle faeces with different microbial biomass content on soil properties, gaseous emissions and plant growth.Crossref | GoogleScholarGoogle Scholar |

Kalburtji KL, Mosjidis JA, Mamolos AP (1999) Litter dynamics of low and high tannin Sericea lespedeza plants under field conditions. Plant and Soil 208, 271–281.
Litter dynamics of low and high tannin Sericea lespedeza plants under field conditions.Crossref | GoogleScholarGoogle Scholar |

Kraus TEC, Dahlgren RA, Zosozki RJ (2003) Tannins in nutrient dynamics of forest ecosystems: a review. Plant and Soil 256, 41–66.
Tannins in nutrient dynamics of forest ecosystems: a review.Crossref | GoogleScholarGoogle Scholar |

Mertens DR (2002) Gravimetric determination of amylase-treated neutral detergent fiber in feeds with refluxing in beaker or crucibles: collaborative study. Journal of AOAC International 85, 1217–1240.

Min BR, Solaiman S, Sange R, Eun JS (2014) Gastrointestinal bacterial and methanogenic archaea diversity dynamics associated with condensed tannins-containing pine bark diet in goats using 16S rDNA amplicon pyrosequencing. International Journal of Microbiology 2014, 1–11.
Gastrointestinal bacterial and methanogenic archaea diversity dynamics associated with condensed tannins-containing pine bark diet in goats using 16S rDNA amplicon pyrosequencing.Crossref | GoogleScholarGoogle Scholar |

Moreira FMS, Siqueira JO (2006) ‘Microbiologia e bioquímica do solo.’ 2nd edn (Universidade Federal de Lavras: Lavras, MG, Brazil)

Muir JP (2011) The multi-faceted role of condensed tannins in the goat ecosystem. Small Ruminant Research 98, 115–120.
The multi-faceted role of condensed tannins in the goat ecosystem.Crossref | GoogleScholarGoogle Scholar |

Patra AK, Saxena J (2011) Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition. Journal of the Science of Food and Agriculture 91, 24–37.
Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition.Crossref | GoogleScholarGoogle Scholar | 20815041PubMed |

Tahmourespour A, Tabatabaee N, Khalkhali H, Amini I (2016) Tannic acid degradation by Klebsiella strains isolated from goat faeces. Iranian Journal of Microbiology 8, 14

Tedeschi L, Muir JP, Riley DG, Fox DG (2015) The role of ruminant animals in sustainable livestock intensification programs. International Journal of Sustainable Development and World Ecology 22, 452–465.
The role of ruminant animals in sustainable livestock intensification programs.Crossref | GoogleScholarGoogle Scholar |

Terrill TH, Rowan AM, Douglas GB, Barry TN (1992) Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grains. Journal of the Science of Food and Agriculture 58, 321–329.
Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grains.Crossref | GoogleScholarGoogle Scholar |

Terrill TH, Waghorn GC, Woolley DJ, Mcnabb WC, Barry TN (1994) Assay and digestion of 14C-labelled condensed tannins in the gastrointestinal tract of sheep. British Journal of Nutrition 72, 467–477.
Assay and digestion of 14C-labelled condensed tannins in the gastrointestinal tract of sheep.Crossref | GoogleScholarGoogle Scholar |

Winder RS, Lamarche J, Constabel CP, Hamelin RC (2013) The effects of high-tannin leaf litter from transgenic poplars on microbial communities in microcosm soils. Frontiers in Microbiology 4, 290
The effects of high-tannin leaf litter from transgenic poplars on microbial communities in microcosm soils.Crossref | GoogleScholarGoogle Scholar | 24133486PubMed |

Wolfe RM, Terrill TH, Muir JP (2008) Drying method and origin of standard affect condensed tannin (CT) concentrations in perennial herbaceous legumes using simplified butanol-HCl CT analysis. Journal of the Science of Food and Agriculture 88, 1060–1067.
Drying method and origin of standard affect condensed tannin (CT) concentrations in perennial herbaceous legumes using simplified butanol-HCl CT analysis.Crossref | GoogleScholarGoogle Scholar |