Biological effect of tannins from different vegetal origin on microbial and fermentation traits in vitro
R. Rodríguez A B , G. de la Fuente A C , S. Gómez B and M. Fondevila A D
+ Author Affiliations
- Author Affiliations
A Instituto Universitario de Investigación en Ciencias Ambientales, Departamento de Producción Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Miguel Servet 177, 50013 Zaragoza, Spain.
B Instituto de Ciencia Animal, Apto. Postal 24, San José de las Lajas, Mayabeque, Cuba.
C Institute of Biological and Environmental Rural Sciences, Aberystwyth University, SY23 3DD, Aberystwyth, Wales, UK.
D Corresponding author. Email: mfonde@unizar.es
Animal Production Science 54(8) 1039-1046 https://doi.org/10.1071/AN13045
Submitted: 1 February 2013 Accepted: 18 September 2013 Published: 26 November 2013
Abstract
The biological effect of tannins (proportion of the response in different parameters when tannins were inactivated with polyethylene glycol, PEG) as an easy, rapid way to estimate the magnitude of their effect on rumen microbial fermentation, was estimated in vitro for the tropical browse legumes Albizia lebbekoides, Acacia cornigera and Leucaena leucocephala, which differ in their phenolic and tannin content. Samples were incubated in rumen fluid for 24 h in four runs. The inactivation by PEG of tannins from A. lebbekoides increased gas production from 1.62- to 2.83-fold, with this biological effect increasing up to 8 h incubation, then being maintained and increasing after 16 h. In A. cornigera and L. leucocephala, the magnitude of the improvement of gas production was lower (from 1.1- to 1.32-fold and from 1.29- to 1.56-fold) and constant. The inclusion of PEG increased total volatile fatty acids (VFA) concentration (P = 0.019), reduced the molar proportion of acetate (P < 0.001) and increased that of butyrate (P < 0.001) and branched-chain VFA (P < 0.001). Microbial protein mass in A. lebbekoides increased with PEG in a higher extent (P < 0.001) than in L. leucocephala, but it was reduced in A. cornigera. No biological effect was observed on the efficiency of microbial protein synthesis when it was related to VFA concentration (P > 0.10), but when related to the gas produced it was lowest with A. lebbekoides (P = 0.023). The biological effect of tannins, either in total extent or along the incubation period differed according to their origin. Irrespective of their amount or chemical nature, the biological effect gives a direct idea of how tannins affect both the extent and pattern of forages fermentation.
References
Álvarez del Pino MC, Hervás G, Mantecón AR, Giráldez FJ, Frutos P (2005) Comparison of biological and chemical methods, and internal and external standards, for assaying tannins in Spanish shrub species. Journal of the Science of Food and Agriculture 85, 583–590.| Comparison of biological and chemical methods, and internal and external standards, for assaying tannins in Spanish shrub species.Crossref | GoogleScholarGoogle Scholar |
Analytical Software (2008) ‘Statistix 9 for Windows.’ (Analytical Software: Tallahasee, FL)
Andrabi SM, Ritchie MM, Stimson C, Horadagoda A, Hyde M, McNeill DM (2005) In vivo assessment of the ability of condensed tannins to interfere with the digestibility of plant protein in sheep. Animal Feed Science and Technology 122, 13–27.
| In vivo assessment of the ability of condensed tannins to interfere with the digestibility of plant protein in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsVClu7s%3D&md5=053d69125d7807ced7b02c765f3c2907CAS |
Appel HM, Govenor HL, D’Argenzo M, Siska E, Schulz JC (2001) Limitations to Folin assays of foliar phenolics in ecological studies. Journal of Chemical Ecology 27, 761–778.
| Limitations to Folin assays of foliar phenolics in ecological studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvFSrtrw%3D&md5=6d10431af432307017066a49b50aee04CAS | 11446299PubMed |
Baba ASH, Castro FB, Orskov ER (2002) Partitioning of energy and degradability of browse plants in vitro and the implications of blocking the effects of tannin by the addition of polyethylene glycol. Animal Feed Science and Technology 95, 93–104.
| Partitioning of energy and degradability of browse plants in vitro and the implications of blocking the effects of tannin by the addition of polyethylene glycol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpt1agu7w%3D&md5=e8a63de0ca5db4519ef42b12e0922e3fCAS |
Belenguer A, Hervás G, Toral PG, Fondevila M, Frutos P (2011) Is polyethylene glycol innocuous to the rumen bacterial community? A preliminary in vitro study. Animal Production Science 51, 990–995.
| Is polyethylene glycol innocuous to the rumen bacterial community? A preliminary in vitro study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlKrsr3O&md5=b8ef76229f1a53492e974fd43b2c5f89CAS |
Beuvink JMW, Spoelstra SF (1992) Interactions between substrate, fermentation end-products buffering system and gas production upon fermentation of different carbohydrates by mixed rumen microorganisms in vitro. Applied Microbiology and Biotechnology 37, 505–509.
| Interactions between substrate, fermentation end-products buffering system and gas production upon fermentation of different carbohydrates by mixed rumen microorganisms in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsVKqtbw%3D&md5=ac12205d5bd14195c2afbad68c811f91CAS |
Blümmel M, Makkar HPS, Becker K (1997) In vitro gas production: a technique revisited. Journal of Animal Physiology and Animal Nutrition 77, 24–34.
| In vitro gas production: a technique revisited.Crossref | GoogleScholarGoogle Scholar |
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 | 1:CAS:528:DC%2BD1cXhslGktb8%3D&md5=c604f1f9170c0111ebdc6e971f351ec0CAS |
Chaney AL, Marbach EP (1962) Modified reagents for determination of urea and ammonia. Clinical Chemistry 8, 130–132.
Firkins JL, Weiss WP, Piwonka EJ (1992) Quantification of intraruminal recycling of microbial nitrogen using nitrogen-15. Journal of Animal Science 70, 3223–3233.
Frutos P, Hervás G, Giráldez FJ, Mantecón AR (2004) An in vitro study on the ability of polyethylene glycol to inhibit the effect of quebracho tannins and tannic acid on rumen fermentation in sheep, goats, cows, and deer. Australian Journal of Agricultural Research 55, 1125–1132.
| An in vitro study on the ability of polyethylene glycol to inhibit the effect of quebracho tannins and tannic acid on rumen fermentation in sheep, goats, cows, and deer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVantbnE&md5=7b079f054815fd0b0838f088e24ad684CAS |
García GW, Ferguson TV, Neckles FA, Archibald KAE (1996) The nutritive value and forage productivity of Leucaena leucocephala. Animal Feed Science and Technology 60, 29–41.
| The nutritive value and forage productivity of Leucaena leucocephala.Crossref | GoogleScholarGoogle Scholar |
Getachew G, Makkar HPS, Becker K (2000) Effect of polyethylene glycol on in vitro degradability of nitrogen and microbial protein synthesis from tannin-rich browse and herbaceous legumes. The British Journal of Nutrition 84, 73–83.
Getachew G, Makkar HPS, Becker K (2002) Tropical browses: contents of phenolic compounds, in vitro gas production and stoichiometric relationship between short chain fatty acid and in vitro gas production. The Journal of Agricultural Science 139, 341–352.
| Tropical browses: contents of phenolic compounds, in vitro gas production and stoichiometric relationship between short chain fatty acid and in vitro gas production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvFOhtg%3D%3D&md5=f2a8c8d9dd2807157c5f3dfc428af806CAS |
Getachew G, Pitroff W, Putnam DH, Dandekar A, Goyal S, DePeeters EJ (2008) The influence of addition of gallic acid, tannic acid, or quebracho tannins to alfalfa hay on in vitro rumen fermentation and microbial protein synthesis. Animal Feed Science and Technology 140, 444–461.
| The influence of addition of gallic acid, tannic acid, or quebracho tannins to alfalfa hay on in vitro rumen fermentation and microbial protein synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvV2lug%3D%3D&md5=b8b9b52a8156e8cc4950464e835b2f4aCAS |
Guerrero M, Cerrillo-Soto MA, Ramírez RG, Salem AZM, González H (2012) Influence of polyethylene glycol on in vitro gas production profiles and microbial protein synthesis of some shrub species. Animal Feed Science and Technology 176, 32–39.
| Influence of polyethylene glycol on in vitro gas production profiles and microbial protein synthesis of some shrub species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVykt7zI&md5=5235fb8f8f5d9e9de7ff1b193d87283dCAS |
Hsu JT, Fahey GC (1990) Effects of centrifugation speed and freezing on composition of ruminal bacterial samples collected from defaunated sheep. Journal of Dairy Science 73, 149–152.
| Effects of centrifugation speed and freezing on composition of ruminal bacterial samples collected from defaunated sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c7osleruw%3D%3D&md5=e30880e6a434961a54cacd086692ad2dCAS | 1690232PubMed |
Jayanegara A, Leiber F, Kreuzer M (2012) Meta-analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments. Journal of Animal Physiology and Animal Nutrition 96, 365–375.
| Meta-analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xpt12jtbw%3D&md5=affe48a3afde05e6076896200dedc446CAS | 21635574PubMed |
Jones RJ, Palmer B (2000) In vitro digestion studies using 14C-labelled polyethylene glycol (PEG) 4000: comparison of six tanniferous shrub legumes and the grass Panicum maximum. Animal Feed Science and Technology 85, 215–221.
| In vitro digestion studies using 14C-labelled polyethylene glycol (PEG) 4000: comparison of six tanniferous shrub legumes and the grass Panicum maximum.Crossref | GoogleScholarGoogle Scholar |
Jones RJ, Meyer JHF, Bechaz M, Stoltz MA (2000) An approach to screening potential pasture species for condensed tannin activity. Animal Feed Science and Technology 85, 269–277.
| An approach to screening potential pasture species for condensed tannin activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktV2ksbw%3D&md5=ac59fa65175b0ff2b0aa9ed8755794e0CAS |
Kraus TEC, Yu Z, Preston CM, Dahlgren RA, Zasoski RJ (2003) Linking chemical reactivity and protein precipitation to structural characteristics of foliar tannins. Journal of Chemical Ecology 29, 703–730.
| Linking chemical reactivity and protein precipitation to structural characteristics of foliar tannins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitFarsb0%3D&md5=e2b4a5770cbd5cf527405b24e48dd379CAS |
Luchini LD, Broderick GA, Combs DC (1996) Preservation of ruminal microorganisms for in vitro determination of ruminal protein degradation. Journal of Animal Science 74, 1134–1143.
Makkar HPS (2005) In vitro gas methods for evaluation of feeds containing phytochemicals. Animal Feed Science and Technology 123–124, 291–302.
| In vitro gas methods for evaluation of feeds containing phytochemicals.Crossref | GoogleScholarGoogle Scholar |
Makkar HPS, Blummel M, Borowy NK, Becker K (1993) Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. Journal of the Science of Food and Agriculture 61, 161–165.
| Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXksVCms7o%3D&md5=dedcae178faff0c2084bf2f09214a7ecCAS |
Makkar HPS, Blummel M, Becker K (1995) Formation of complexes between polyvinyl pyrrolidone or polyethylene glycol and tannins, and their implications in gas production and true digestibility in in vitro techniques. The British Journal of Nutrition 73, 897–913.
| Formation of complexes between polyvinyl pyrrolidone or polyethylene glycol and tannins, and their implications in gas production and true digestibility in in vitro techniques.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmvVyls78%3D&md5=1e460b9739f095410bfc0b808b320041CAS |
Marinas A, García-González R, Fondevila M (2003) The nutritive value of five pasture species occurring in the summer grazing ranges of the Pyrenees. Animal Science 76, 461–469.
McAllister TA, Bae HD, Jones GA, Cheng KJ (1994) Microbial attachmentand feed digestion in the rumen. Journal of Animal Science 72, 3004–3018.
McSweeney CS, Palmer B, McNeill DM, Krause D (2001) Microbial interactions with tannins: nutritional consequences for ruminants. Animal Feed Science and Technology 91, 83–93.
| Microbial interactions with tannins: nutritional consequences for ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslSms7Y%3D&md5=7d89e3335215b0ca6b5ff4653e386b4cCAS |
Min BR, Barry TN, Attwood GT, McNabb WC (2003) The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Animal Feed Science and Technology 106, 3–19.
| The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtlSmtr0%3D&md5=c7eddc28a39fa9fc977151c4dd112f8aCAS |
Mould FL, Morgan R, Kliem KE, Krystallidou E (2005) A review and simplification of the in vitro incubation medium. Animal Feed Science and Technology 123–124, 155–172.
| A review and simplification of the in vitro incubation medium.Crossref | GoogleScholarGoogle Scholar |
Reed JD (1995) Nutritional toxicology of tannins and related 1 polyphenols in forage legumes. Journal of Animal Science 73, 1516–1528.
Rodríguez R, Mota M, Fondevila M, de la Fuente G (2006) In vitro fermentation of four tropical browse legumes: estimation of the effect of tannins by gas production. In ‘Herbivores – assessment of intake, digestibility and the roles of secondary compounds’. BSAS Occasional Publication No.34. (Eds CJ Sandoval-Castro, JFJ Torres-Acosta, AJ Ayala-Burgos, FDDeB Hovell) pp. 101–107.
Rodríguez R, Mota M, Castrillo C, Fondevila M (2010) In vitro rumen fermentation of the tropical grass Pennisetum purpureum and mixtures with browse legumes: effects of tannin contents. Journal of Animal Physiology and Animal Nutrition 94, 696–705.
| In vitro rumen fermentation of the tropical grass Pennisetum purpureum and mixtures with browse legumes: effects of tannin contents.Crossref | GoogleScholarGoogle Scholar | 20579189PubMed |
Rodríguez R, Britos A, Rodriguez-Romero N, Fondevila M (2011) Effect of plant extracts from several tanniferous browse legumes on in vitro microbial fermentation of the tropical grass Pennisetum purpureum. Animal Feed Science and Technology 168, 188–195.
| Effect of plant extracts from several tanniferous browse legumes on in vitro microbial fermentation of the tropical grass Pennisetum purpureum.Crossref | GoogleScholarGoogle Scholar |
Salem AZM, Robinson PH, El-Adawy MM, Hassan AA (2007) In vitro fermentation and microbial protein synthesis of some browse tree leaves with or without addition of polyethylene glycol. Animal Feed Science and Technology 138, 318–330.
| In vitro fermentation and microbial protein synthesis of some browse tree leaves with or without addition of polyethylene glycol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWkt7zL&md5=b308dffbb3ee4bd0ba99972ebe769baaCAS |
Shelton HM, Brewbaker JL (1994) Leucaena leucacephala – the most widely used forage tree legume. In ‘Forage tree legumes in tropical agriculture’. (Eds RC Gutteridge, HM Shelton) pp. 15–29. (CAB International: Wallingford, UK)
Theodorou MK, Williams BA, Dhanoa MS, McAllan AB, France J (1994) A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Animal Feed Science and Technology 48, 185–197.
| A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds.Crossref | GoogleScholarGoogle Scholar |
Tiemann TT, Avila P, Ramírez G, Lascano CE, Kreuzer M, Hess HD (2008) In vitro ruminal fermentation of tanniniferous tropical plants: plant-specific tannin effects and counteracting efficiency of PEG. Animal Feed Science and Technology 146, 222–241.
| In vitro ruminal fermentation of tanniniferous tropical plants: plant-specific tannin effects and counteracting efficiency of PEG.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFCku7fK&md5=92047e229a79dbfdd3417043cdd3b305CAS |
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.
| Methods for dietary fiber, neutral detergent fiber and nonstarch polysaccharides in relation to animal nutrition.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2FnvVCltA%3D%3D&md5=83605a987aed1cab5024d20cbdabf9b5CAS | 1660498PubMed |
