Mitigating the anti-nutritional effect of polyphenols on in vitro digestibility and fermentation characteristics of browse species in north western Ethiopia

Abstract

Browse species are important sources of forage for livestock in Ethiopia, especially during the dry season, when the quality and quantity of green herbage is limited. However, browse species have anti-nutritional factors, such as polyphenols. This study evaluated the extent to which polyethylene glycol (PEG) can reduce the anti-nutritional effects of polyphenols whose extent is expected to vary depending on the species type and season on the in vitro fermentation of these plant samples. We selected ten browse species commonly used as livestock feed based on their tannin content, and sixty samples of the leaf and twig of these species were collected during the wet and dry seasons. The study was designed as 10 × 2 × 2 factorial arrangement with 10 browse species (Acacia nilotica, Crateva adonsonia, Dombeya torrida, Ekebergia capensis, Ensete ventricosum, Erythrina brucei, Maesa lanceolate, Sesbania sesban, Stereospermum kunthianum, and Terminalia laxiflora), 2 seasons (wet and dry) and 2 states of PEG (with and without PEG). The effects of tannin on the nutritive characteristics were also evaluated by adding PEG as a tannin-binding agent. The chemical composition and in vitro fermentation products of these samples differed significantly (p < 0.001) among browse species. Specifically, total extractable phenol (TEP) ranged from 26.3 to 250.3 g/kg, total extractable tannin (TET) from 22.8 to 210.9 g/kg, and condensed tannin (CT) from 11.1 to 141.3 g/kg, respectively. Season, species, and their interaction have a significant (p < 0.05) effect on the chemical composition and fermentation characteristics of most browse species. The addition of PEG increased gas production (GP), in vitro organic matter digestibility (IVOMD), metabolizable energy (ME) concentration, dry matter degradability (DMD), and volatile fatty acids (VFA), on average, by 76.8%, 47.9%, 42.2%, 21.2%, and 20.2%, respectively. Secondary polyphenols (TEP, TET, CT, and SCT) were significantly (p < 0.001) and negatively correlated with GP, IVOMD, ME, and VFA. Preferable species namely E. ventricosum, S. sesban, M. lanceolata, E. capensis, and A. nilotica were selected for supplementation in terms of their chemical composition, IVOMD, and mitigating effects of PEG on anti-nutritional functions of their secondary compounds. In conclusion, PEG markedly reduced the anti-nutritional effects of polyphenols and improved the in vitro fermentation of browse species harvested in contrasting seasons.

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

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Fig. 1

References

  1. AOAC 1990. Official methods of analysis of the Association of Official Analytical Chemists, The Association.

  2. Arigbede, O., Anele, U., Südekum, K. H., Hummel, J., Oni, A., Olanite, J. & Isah, A. 2012. Effects of species and season on chemical composition and ruminal crude protein and organic matter degradability of some multi-purpose tree species by West African dwarf rams. Journal of animal physiology and animal nutrition, 96, 250-259.

    CAS  PubMed  Google Scholar 

  3. Asfaw, A., Simane, B., Hassen, A. & Bantider, A. 2018. Variability and time series trend analysis of rainfall and temperature in northcentral Ethiopia: A case study in Woleka sub-basin. Weather and climate extremes, 19, 29-41.

    Google Scholar 

  4. Basha, N. A., Scogings, P. F. & Nsahlai, I. V. 2013. Effects of season, browse species and polyethylene glycol addition on gas production kinetics of forages in the subhumid subtropical savannah, South Africa. Journal of the Science of Food and Agriculture, 93, 1338-1348.

    CAS  PubMed  Google Scholar 

  5. BassiriRad, H., Gutschick, V. P. & Lussenhop, J. 2001. Root system adjustments: regulation of plant nutrient uptake and growth responses to elevated CO 2. Oecologia, 126, 305-320.

    PubMed  Google Scholar 

  6. Besharati, M. & Ghezeljeh, E. A. 2017. Effect of adding Polyethylene Glycol and Polyvinyl Pyrrolidon on In Vitro Gas production of Pomegranate seed. Kahramanmaraş Sütçü İmam Üniversitesi Doğa Bilimleri Dergisi, 20, 128-132.

    Google Scholar 

  7. Bouazza, L., Bodas, R., Boufennara, S., Bousseboua, H. & Lopez, S. 2012. Nutritive evaluation of foliage from fodder trees and shrubs characteristic of Algerian arid and semi-arid areas. Journal of animal and feed sciences, 21, 521-536.

    Google Scholar 

  8. Dentinho, M. T. P., Moreira, O. C. & Bessa, R. J. 2018. The use of polyethylene glycol to reduce the anti-nutritional effects of tannins in Cistus ladanifer L. Forest Systems, 27, 04.

    Google Scholar 

  9. Elghandour, M., Salem, A., Gonzalez-Ronquillo, M., Bórquez, J., Gado, H., Odongo, N. & Peñuelas, C. 2013. Effects of exogenous enzymes on in vitro gas production kinetics and ruminal fermentation of four fibrous feeds. Animal Feed Science and Technology, 179, 46-53.

    CAS  Google Scholar 

  10. Espírito-Santo, M. M., Fernandes, G. W., Allain, L. R. & Reis, T. R. 1999. Tannins in Baccharis dracunculifolia (Asteraceae): effects of seasonality, water availability and plant sex. Acta Botanica Brasilica, 13, 167-174.

    Google Scholar 

  11. Frutos, P., Hervas, G., Giráldez, F. J. & Mantecón, A. 2004. Tannins and ruminant nutrition. Spanish Journal of Agricultural Research, 2, 191-202.

    Google Scholar 

  12. Gebrekirstos, A., Mitlöhner, R., Teketay, D. & Worbes, M. 2008. Climate–growth relationships of the dominant tree species from semi-arid savanna woodland in Ethiopia. Trees, 22, 631.

    Google Scholar 

  13. Gemeda, B. S. & Hassen, A. 2015. Effect of tannin and species variation on in vitro digestibility, gas, and methane production of tropical browse plants. Asian-Australasian journal of animal sciences, 28, 188.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Gemiyo, D., Hassen, A., Kocho, T., Birhanu, T., Bassa, Z. & Jimma, A. 2013. Chemical composition and digestibility of major feed resources in mixed farming system of southern Ethiopia. World Applied Sciences Journal, 26, 267-275.

    CAS  Google Scholar 

  15. Gerlach, K., Pries, M. & Südekum, K.-H. 2018. Effect of condensed tannin supplementation on in vivo nutrient digestibilities and energy values of concentrates in sheep. Small Ruminant Research, 161, 57-62.

    Google Scholar 

  16. Getachew, G., Makkar, H. & Becker, K. 2000. Effect of polyethylene glycol on in vitro degradability of nitrogen and microbial protein synthesis from tannin-rich browse and herbaceous legumes. British Journal of Nutrition, 84, 73-83.

    CAS  Google Scholar 

  17. Getachew, G., Makkar, H. & 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.

    CAS  Google Scholar 

  18. Giridhar, K., Prabhu, T., Singh, K. C., Nagabhushan, V., Thirumalesh, T., Rajeshwari, Y. & Umashankar, B. 2018. Nutritional potentialities of some tree leaves based on polyphenols and rumen in vitro gas production. Veterinary world, 11, 1479.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Guerrero, M., Cerrillo-Soto, M., Ramírez, R., Salem, A., González, H. & Juárez-Reyes, A. 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.

    CAS  Google Scholar 

  20. Hernández, S. R., Pérez, J. O., Elghandour, M., Cipriano-Salazar, M., Avila-Morales, B., Camacho-Díaz, L., Salem, A. & Soto, M. C. 2015. Effect of polyethylene glycol on in vitro gas production of some non-leguminous forage trees in tropical region of the south of Mexico. Agroforestry systems, 89, 735-742.

    Google Scholar 

  21. Kamalak, A., Canbolat, O. & Gurbuz, Y. 2005. Comparison between in situ dry matter degradation and in vitro gas production of tannin-containing leaves from four tree species. South African Journal of Animal Science, 35, 233-240.

    Google Scholar 

  22. Kandel, T. P., Sutaryo, S., Møller, H. B., Jørgensen, U. & Lærke, P. E. 2013. Chemical composition and methane yield of reed canary grass as influenced by harvesting time and harvest frequency. Bioresource technology, 130, 659-666.

    CAS  PubMed  Google Scholar 

  23. Kondo, M., Hirano, Y., Kita, K., Jayanegara, A. & Yokota, H. o. 2018. Nutritive evaluation of spent green and black tea leaf silages by in vitro gas production characteristics, ruminal degradability and post-ruminal digestibility assessed with inhibitory activity of their tannins. Animal Science Journal, 89, 1656-1662.

    CAS  PubMed  Google Scholar 

  24. Lamers, J. & Khamzina, A. 2010. Seasonal quality profile and production of foliage from trees grown on degraded cropland in arid Uzbekistan, Central Asia. Journal of animal physiology and animal nutrition, 94, e77-e85.

    CAS  PubMed  Google Scholar 

  25. Makkar, H. 2003. Effects and fate of tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tannin-rich feeds. Small ruminant research, 49, 241-256.

    Google Scholar 

  26. Makkar, H. P., Becker, K., Abel, H. & Szegletti, C. 1995. Degradation of condensed tannins by rumen microbes exposed to quebracho tannins (QT) in rumen simulation technique (RUSITEC) and effects of QT on fermentative processes in the RUSITEC. Journal of the Science of Food and Agriculture, 69, 495-500.

    CAS  Google Scholar 

  27. McDonald, I. 1981. A revised model for the estimation of protein degradability in the rumen. The Journal of Agricultural Science, 96, 251-252.

    CAS  Google Scholar 

  28. Melesse, A., Steingass, H., Schollenberger, M., Holstein, J. & Rodehutscord, M. 2017. Nutrient compositions and in vitro methane production profiles of leaves and whole pods of twelve tropical multipurpose tree species cultivated in Ethiopia. Agroforestry systems, 93, 135-147.

    Google Scholar 

  29. Mengistu, G., Karonen, M., Salminen, J.-P., Hendriks, W. & Pellikaan, W. F. 2017. In vitro fermentation of browse species using goat rumen fluid in relation to browse polyphenol content and composition. Animal Feed Science and Technology, 231, 1-11.

    CAS  Google Scholar 

  30. Menke, K. H. A. S. H. 1988. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Animal research and development, 28, 7-55.

    Google Scholar 

  31. Menke, K., Raab, L., Salewski, A., Steingass, H., Fritz, D. & Schneider, W. 1979. The estimation of the digestibility and metabolizable energy content of ruminant feeding stuffs from the gas production when they are incubated with rumen liquor in vitro. The Journal of Agricultural Science, 93, 217-222.

    CAS  Google Scholar 

  32. Monforte-Briceño, G. E., Sandoval-Castro, C. A., Ramírez-Avilés, L. & Leal, C. M. C. 2005. Defaunating capacity of tropical fodder trees: effects of polyethylene glycol and its relationship to in vitro gas production. Animal Feed Science and Technology, 123, 313-327.

    Google Scholar 

  33. Moss, A. R., Jouany, J.-P. & Newbold, J. Methane production by ruminants: its contribution to global warming. Annales de zootechnie, 2000. EDP Sciences, 231-253.

  34. Nigussie, T., Enyew, H., Tsegaye, A. D., Dagnachew, M., Tsugiyuki, A., Mitsuru, M., Dagnenet, T., Almaw, S. A. & Mesenbet, F. 2018. Effects of land use and sustainable land management practices on runoff and soil loss in the Upper Blue Nile basin, Ethiopia. Science of the total environment.

  35. Ørskov, E. & McDonald, I. 1979. The estimation of protein degradability in the rumen from incubation measurements weighted according to rate of passage. The Journal of Agricultural Science, 92, 499-503.

    Google Scholar 

  36. Osuga, I. M., Wambui, C. C., Abdulrazak, S. A., Ichinohe, T. & Fujihara, T. 2008. Evaluation of nutritive value and palatability by goats and sheep of selected browse foliages from semiarid area of Kenya. Animal Science Journal, 79, 582-589.

    CAS  Google Scholar 

  37. Parissi, Z. M., Abraham, E. M., Roukos, C., Kyriazopoulos, A. P., Petridis, A. & Karameri, E. 2018. Seasonal Quality Assessment of Leaves and Stems of Fodder Ligneous Species. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 46, 426-434.

    CAS  Google Scholar 

  38. Patra, A. K. & Saxena, J. 2009. Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie van Leeuwenhoek, 96, 363-375.

    CAS  PubMed  Google Scholar 

  39. Porter, L. J., Hrstich, L. N. & Chan, B. G. 1985. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry, 25, 223-230.

    Google Scholar 

  40. Ramírez-Restrepo, C., Barry, T., López-Villalobos, N., Kemp, P. & McNabb, W. 2004. Use of Lotus corniculatus containing condensed tannins to increase lamb and wool production under commercial dry land farming conditions without the use of anthelmintics. Animal Feed Science and Technology, 117, 85-105.

    Google Scholar 

  41. Rubanza, C., Shem, M., Otsyina, R., Bakengesa, S., Ichinohe, T. & Fujihara, T. 2005. Polyphenolics and tannins effect on in vitro digestibility of selected Acacia species leaves. Animal Feed Science and Technology, 119, 129-142.

    CAS  Google Scholar 

  42. Salem, A., Salem, M., El-Adawy, M. & Robinson, P. 2006. Nutritive evaluations of some browse tree foliages during the dry season: secondary compounds, feed intake and in vivo digestibility in sheep and goats. Animal Feed Science and Technology, 127, 251-267.

    CAS  Google Scholar 

  43. Salem, A., Robinson, P., El-Adawy, M. & Hassan, A. 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.

    CAS  Google Scholar 

  44. Santos, S. C., Costa, W. F., Batista, F., Santos, L. R., Ferri, P. H., Ferreira, H. D. & Seraphin, J. C. 2006. Seasonal variation in the content of tannins in barks of barbatimão species. Revista Brasileira de Farmacognosia, 16, 552-556.

    CAS  Google Scholar 

  45. SAS 2001. Cary NC, USA: SAS Inst. Inc.

  46. Schofield, P., Mbugua, D. & Pell, A. 2001. Analysis of condensed tannins: a review. Animal feed science and technology, 91, 21-40.

    CAS  Google Scholar 

  47. Shenkute, B., Hassen, A., Assafa, T., Amen, N. & Ebro, A. Identification and nutritive value of potential fodder trees and shrubs in the mid Rift Valley of Ethiopa. 2012. Pakistan Agricultural Scientist’s Forum.

  48. Silanikove, N., Perevolotsky, A. & Provenza, F. D. 2001. Use of tannin-binding chemicals to assay for tannins and their negative postingestive effects in ruminants. Animal Feed Science and Technology, 91, 69-81.

    CAS  Google Scholar 

  49. Singh, B., Sahoo, A., Sharma, R. & Bhat, T. 2005. Effect of polyethylene glycol on gas production parameters and nitrogen disappearance of some tree forages. Animal Feed Science and Technology, 123, 351-364.

    Google Scholar 

  50. Tilley, J. & Terry, R. 1963. A two-stage technique for the in vitro digestion of forage crops. Grass and forage science, 18, 104-111.

    CAS  Google Scholar 

  51. Top, S. M., Preston, C. M., Dukes, J. S. & Tharayil, N. 2017. Climate influences the content and chemical composition of foliar tannins in green and senesced tissues of Quercus rubra. Frontiers in plant science, 8, 423.

    PubMed  PubMed Central  Google Scholar 

  52. Van Soest, P. V., Robertson, J. & Lewis, B. 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of dairy science, 74, 3583-3597.

    PubMed  Google Scholar 

  53. Yayneshet, T., Eik, L. & Moe, S. 2009. Seasonal variations in the chemical composition and dry matter degradability of exclosure forages in the semi-arid region of northern Ethiopia. Animal Feed Science and Technology, 148, 12-33.

    CAS  Google Scholar 

  54. Yisehak, K., De Boever, J. & Janssens, G. 2014. The effect of supplementing leaves of four tannin-rich plant species with polyethylene glycol on digestibility and zootechnical performance of zebu bulls (B os indicus). Journal of animal physiology and animal nutrition, 98, 417-423.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to thank the laboratory staffs of the Arid Land Research Center, Tottori University, and Shimane University as well as the technical staff of Tottori Prefecture Industrial Technology Institute for assisting in the extraction of phenolic compounds and tannins from the leaves of browse species. The first author acknowledges scholarship support from the Japanese Ministry of Education, Culture, Sports, Science, and Technology.

Funding

This research was supported by Science and Technology Research Partnership for Sustainable Development (SATREPS), Grant Number JPMJSA1601, Japan Science and Technology Agency (JST)/Japan International Cooperation Agency (JICA).

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Shigdaf Mekuriaw or Atsushi Tsunekawa.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mekuriaw, S., Tsunekawa, A., Ichinohe, T. et al. Mitigating the anti-nutritional effect of polyphenols on in vitro digestibility and fermentation characteristics of browse species in north western Ethiopia. Trop Anim Health Prod 52, 1287–1298 (2020). https://doi.org/10.1007/s11250-019-02126-3

Download citation

Keywords

  • Dryland
  • In vitro digestibility
  • Polyethylene glycol
  • Season
  • Tannin, Browse species