Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-19T11:13:23.211Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro screening of temperate climate forages from a variety of woody plants for their potential to mitigate ruminal methane and ammonia formation

Published online by Cambridge University Press:  15 November 2018

M. Terranova ,
M. Kreuzer ,
U. Braun  and
A. Schwarm Open the ORCID record for A. Schwarm [Opens in a new window]
M. Terranova
Affiliation:
ETH Zurich, Institute of Agricultural Sciences, Universitaetstrasse 2, 8092 Zurich, Switzerland
M. Kreuzer
Affiliation:
ETH Zurich, Institute of Agricultural Sciences, Universitaetstrasse 2, 8092 Zurich, Switzerland
U. Braun
Affiliation:
Vetsuisse Faculty, University of Zurich, Clinic for Ruminants, 8057 Zurich, Switzerland
A. Schwarm*
Affiliation:
ETH Zurich, Institute of Agricultural Sciences, Universitaetstrasse 2, 8092 Zurich, Switzerland
*
Author for correspondence: A. Schwarm, E-mail: angela.schwarm@usys.ethz.ch
Get access Rights & Permissions [Opens in a new window]

Abstract

Feeding phenol-containing plants to ruminants has the potential to mitigate both methane and ammonia formation. In the present study, mostly woody plants, such as the leaves of trees and shrubs, were tested for their influence on in vitro fermentation. The plants selected grow naturally under temperate climatic conditions, are usually available in bulk and do not directly compete with human food production. The detailed screening included whole plants or parts of different plant species reporting their effects on methane and/or ammonia formation. The plant materials were added at 167 mg/g of total dry matter (DM) to a common total mixed ration and incubated for 24 h with the Hohenheim gas test method. The results from in vitro fermentation were also used to determine the net energy of lactation and utilizable crude protein in the complete diets. Thirteen out of 18 test materials did not impair the organic matter (OM) digestibility of the diet. Ammonia concentrations decreased up to 35% when adding any of the test materials. Methane formation per unit of feed DM and per unit of digestible OM was lowered by 13 of the 18 test materials from 12 to 28% and 5 to 20%, respectively. In conclusion, a number of plant materials tested have the potential to mitigate ruminal ammonia and methane formation without adversely affecting digestibility. The leaves of Betula pendula, Corylus avellana, Ribes nigrum, Vitis vinifera and the aerial part of Geum urbanum were particularly promising in this respect.

Keywords

Fermentationfoliagemethanogenesistannin
Type
Animal Research Paper
Information
The Journal of Agricultural Science , Volume 156 , Issue 7 , September 2018 , pp. 929 - 941
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

AOAC (1997) Official Methods of Analysis. Arlington, VA, USA: Association of Official Analytical Chemists.Google Scholar
Banik, BK, Durmic, Z, Erskine, W, Ghamkhar, K and Revell, C (2013) In vitro ruminal fermentation characteristics and methane production differ in selected key pasture species in Australia. Crop and Pasture Science 64, 935–942.Google Scholar
Bekele, AZ, Clément, C, Kreuzer, M and Soliva, CR (2009) Efficiency of Sesbania sesban and Acacia angustissima in limiting methanogenesis and increasing ruminally available nitrogen in a tropical grass-based diet depends on accession. Animal Production Science 49, 145–153.Google Scholar
Bhatta, R, Uyeno, Y, Tajima, K, Takenaka, A, Yabumoto, Y, Nonaka, I, Enishi, O and Kurihara, M (2009) Difference in the nature of tannins on in vitro ruminal methane and volatile fatty acid production and on methanogenic archaea and protozoal populations. Journal of Dairy Science 92, 5512–5522.Google Scholar
Bodas, R, López, S, Fernández, M, García-González, R, Rodríguez, AB, Wallace, RJ and González, JS (2008) In vitro screening of the potential of numerous plant species as antimethanogenic feed additives for ruminants. Animal Feed Science and Technology 145, 245–258.Google Scholar
Bodas, R, Prieto, N, García-González, R, Andrés, S, Giráldez, FJ and López, S (2012) Manipulation of rumen fermentation and methane production with plant secondary metabolites. Animal Feed Science and Technology 176, 78–93.Google Scholar
Chen, Y, Zhao, Y, Fu, Z-Y, Ma, Z-W, Qian, F-C, Abibuli, A, Yang, B, Abula, R, Xu, X-L and Aniwaer, A (2011) Chemical composition and in vitro ruminal fermentation characteristics of tetraploid black locust (Robinia pseudoacacia L.). Asian Journal of Animal and Veterinary Advances 6, 706–714.Google Scholar
Dijkstra, J, Oenema, O, Van Groenigen, JW, Spek, J, van Vuuren, AM and Bannink, A (2013) Diet effects on urine composition of cattle and N2O emissions. Animal: An International Journal of Animal Bioscience 7(s2), 292–302.Google Scholar
Hristov, AN, Oh, J, Firkins, JL, Dijkstra, J, Kebreab, E, Waghorn, G, Makkar, HPS, Adesogan, AT, Yang, W, Lee, C, Gerber, PJ, Henderson, B and Tricarico, JM (2013) Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options. Journal of Animal Science 91, 5045–5069.Google Scholar
Hummel, J, Südekum, KH, Streich, WJ and Clauss, M (2006) Forage fermentation patterns and their implications for herbivore ingesta retention times. Functional Ecology 20, 989–1002.Google Scholar
Jayanegara, A, Marquardt, S, Kreuzer, M and Leiber, F (2011) Nutrient and energy content, in vitro ruminal fermentation characteristics and methanogenic potential of alpine forage plant species during early summer. Journal of the Science of Food and Agriculture 91, 1863–1870.Google Scholar
Jayanegara, A, Leiber, F and 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.Google Scholar
Kamalak, A (2005). Chemical composition and in vitro dry matter digestibility of leaves of Vitis vinifera. Livestock Research for Ruminal Development 17, Article #3. Available at http://www.lrrd.org/lrrd17/1/kama17003.htmGoogle Scholar
Kumar, R and Singh, M (1984) Tannins: their adverse role in ruminant nutrition. Journal of Agricultural and Food Chemistry 32, 447–453.Google Scholar
Kumarasamy, Y, Cox, PJ, Jaspars, M, Nahar, L and Sarker, SD (2003) Cyanogenic glycosids from Prunus spinosa (Rosaceae). Biochemical Systematics and Ecology 31, 1063–1065.Google Scholar
Macheboeuf, D, Coudert, L, Bergeault, R, Lalière, G and Niderkorn, V (2014) Screening of plants from diversified natural grasslands for their potential to combine high digestibility, and low methane and ammonia production. Animal: An International Journal of Animal Bioscience 8, 1797–1806.Google Scholar
Makkar, HPS (2003) Quantification of Tannins in Tree and Shrub Foliage: A Laboratory Manual. Dordrecht, The Netherlands: Kluwer Academic Publishers.Google Scholar
Marley, CL, Cook, R, Keatinge, R, Barrett, J and Lampkin, NH (2003) The effect of birdsfoot trefoil (Lotus corniculatus) and chicory (Cichorium intybus) on parasite intensities and performance of lambs naturally infected with helminth parasites. Veterinary Parasitology 112, 147–155.Google Scholar
Menke, KH and Steingass, 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
Molan, AL, Attwood, GT, Min, BR and McNabb, WC (2001) The effect of condensed tannins from Lotus pedunculatus and Lotus corniculatus on the growth of proteolytic rumen bacteria in vitro and their possible mode of action. Canadian Journal of Microbiology 47, 626–633.Google Scholar
Niderkorn, V and Macheboeuf, D (2014) Identification of bioactive grassland plants for reducing enteric methane production and rumen proteolysis using in vitro screening assay. Animal Production Science 54, 1805–1809.Google Scholar
Nour, V, Trandafir, I and Cosmulescu, S (2014) Antioxidant capacity, phenolic compounds and minerals content of blackcurrant (Ribes nigrum L.) leaves as influenced by harvesting date and extraction method. Industrial Crops and Products 53, 133–139.Google Scholar
Oliveira, I, Sousa, A, Valentão, P, Andrade, PB, Ferreira, ICFR, Ferreres, F, Bento, A, Seabra, R, Estevinho, L and Pereira, JA (2007) Hazel (Corylus avellana L.) leaves as source of antimicrobial and antioxidative compounds. Food Chemistry 105, 1018–1025.Google Scholar
Palo, RT, Sunnerheim, K and Theander, O (1985) Seasonal variation of phenols, crude protein and cell wall content of birch (Betula pendula Roth.) in relation to ruminant in vitro digestibility. Oecologia 65, 314–318.Google Scholar
Paolini, V, Fouraste, I and Hoste, H (2004) In vitro effects of three woody plant and sainfoin extracts on 3rd-stage larvae and adult worms of three gastrointestinal nematodes. Parasitology 129, 69–77.Google Scholar
Papanastasis, VP, Yiakoulaki, MD, Decandia, M and Dini-Papanastasi, O (2008) Integrating woody species into livestock feeding in the Mediterranean areas of Europe. Animal Feed Science and Technology 140, 1–17.Google Scholar
Peiretti, P, Masoero, G and Tassone, S (2017) Comparison of the nutritive value and fatty acid profile of the green pruning residues of six grapevine (Vitis vinifera L.) cultivars. Livestock Research for Rural Development 29, Article #194. Available at http://www.lrrd.org/lrrd29/10/pier29194.html.Google Scholar
Pinares-Patiño, CS, Ulyatt, MJ, Waghorn, GC, Lassey, KR, Barry, TN, Holmes, CW and Johnson, DE (2003) Methane emission by alpaca and sheep fed on lucerne hay or grazed on pastures of perennial ryegrass/white clover or birdsfoot trefoil. Journal of Agricultural Science, Cambridge 140, 215–226.Google Scholar
Rauha, J-P, Remes, S, Heinonen, M, Hopia, A, Kähkönen, M, Kujala, T, Pihlaja, K, Vuorela, H and Vuorela, P (2000) Antimicrobial effects of Finnish plant extracts containing flavonoids and other phenolic compounds. International Journal of Food Microbiology 56, 3–12.Google Scholar
Sauter, JJ and Wellenkamp, S (1998) Seasonal changes in content of starch, protein and sugars in the twig wood of Salix caprea L. Holzforschung ‒ International Journal of the Biology, Chemistry, Physics, and Technology of Wood 52, 255–262.Google Scholar
Scharenberg, A, Arrigo, Y, Gutzwiller, A, Soliva, CR, Wyss, U, Kreuzer, M and Dohme, F (2007) Palatability in sheep and in vitro nutritional value of dried and ensiled sainfoin (Onobrychis viciifolia) birdfoot trefoil (Lotus corniculatus), and chicory (Cichorium intybus). Archives of Animal Nutrition 61, 481–496.Google Scholar
Selje, N, Hoffmann, EM, Muetzel, S, Ningrat, R, Wallace, RJ and Becker, K (2007) Results of a screening programme to identify plants or plant extracts that inhibit ruminal protein degradation. British Journal of Nutrition 98, 45–53.Google Scholar
Soliva, CR and Hess, HD (2007) Measuring methane emission of ruminants by in vitro and in vivo techniques. In Makkar, HPS and Vercoe, PE (eds), Measuring Methane Production From Ruminants. Dordrecht, The Netherlands: Springer, pp. 15–31.Google Scholar
Steinfeld, H, Gerber, P, Wassenaar, TD, Castel, V, Rosales, M and de Haan, C (2006) Livestock's Long Shadow: Environmental Issues and Options. Rome, Italy: FAO.Google Scholar
Steingass, H and Südekum, K-H (2013) Proteinbewertung beim Wiederkäuer ‒ Grundlagen, analytische Entwicklungen und Perspektiven. Übersichten zur Tierernährung 41, 51–73.Google Scholar
Stickel, F and Seitz, HK (2000) The efficacy and safety of comfrey. Public Health Nutrition 3, 501–508.Google Scholar
Tavendale, MH, Meagher, LP, Park-Ng, ZA, Waghorn, GC and Attwood, GT (2005) Methane production from in vitro incubation of kikuyu grass, lucerne and forages containing condensed tannins. Proceedings of the New Zealand Grassland Association 67, 147–153.Google Scholar
Tiemann, TT, Franco, LH, Peters, M, Frossard, E, Kreuzer, M, Lascano, CE and Hess, H-D (2009) Effect of season, soil type and fertilizer on the biomass production and chemical composition of five tropical shrub legumes with forage potential. Grass and Forage Science 64, 255–265.Google Scholar
Tiemann, TT, Franco, LH, Ramírez, G, Kreuzer, M, Lascano, CE and Hess, H-D (2010) Influence of cultivation site and fertilisation on the properties of condensed tannins and in vitro ruminal nutrient degradation of Calliandra calothyrsus, Flemingia macrophylla and Leucaena leucocephala. Animal Feed Science and Technology 157, 30–40.Google Scholar
Van Soest, PJ, Robertson, JB and 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.Google Scholar
Waghorn, G (2008) Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production ‒ progress and challenges. Animal Feed Science and Technology 147, 116–139.Google Scholar
Wang, S, Terranova, M, Kreuzer, M, Marquardt, S, Eggerschwiler, L and Schwarm, A (2018) Supplementation of pelleted hazel (Corylus avellana) leaves decreases methane and urinary nitrogen emissions by sheep at unchanged forage intake. Scientific Reports 8, Article #5427. doi: https://doi.org/10.1038/s41598-018-23572-3.Google Scholar
Williams, CM, Eun, JS, MacAdam, JW, Young, AJ, Fellner, V and Min, BR (2011) Effect of forage legumes containing condensed tannins on methane and ammonia production in continuous cultures of mixed ruminal microorganisms. Animal Feed Science and Technology 166–167, 364–372.Google Scholar
Woodward, SL, Laboyrie, PJ and Jansen, EBL (2000) Lotus corniculatus and condensed tannins ‒ effects on milk production by dairy cows. Asian-Australasian Journal of Animal Science 13(Supplement), 521–525.Google Scholar
Woodward, SL, Waghorn, GC and Laboyre, P (2004) Condensed tannins in birdsfoot trefoil (Lotus corniculatus) reduced methane emissions from dairy cows. Proceedings of the New Zealand Society of Animal Production 64, 160–164.Google Scholar