Mature herbs as supplements to ruminant diets: effects on in vitro ruminal fermentation and ammonia production
Alexandra N. Kapp-Bitter A B , Uta Dickhoefer C , Michael Kreuzer B and Florian Leiber
A D
+ Author Affiliations
- Author Affiliations
A Department of Livestock Sciences, Research Institute of Organic Agriculture (FiBL), Ackerstrasse 113, 5070 Frick, Switzerland.
B Institute of Agricultural Sciences, ETH Zurich, Universitätstrasse 2, 8092 Zurich, Switzerland.
C Animal Nutrition and Rangeland Management in the Tropics and Subtropics, University of Hohenheim, Schloß Hohenheim 1, 70599 Stuttgart, Germany.
D Corresponding author. Email: florian.leiber@fibl.org
Animal Production Science 61(5) 470-479 https://doi.org/10.1071/AN20323
Submitted: 28 May 2020 Accepted: 20 November 2020 Published: 14 December 2020
Journal Compilation © CSIRO 2021 Open Access CC BY
Abstract
Context: High concentrations of crude protein in ruminant diets may lead to excessive production of ruminal ammonia, which may stress the animal’s metabolism and impact nitrogen efficiency. This may become a problem in zero-concentrate feeding systems when pasture grass is rich in crude protein. Polyphenols such as tannins may protect part of dietary protein from ruminal degradation and thus inhibit ammonia formation.
Aims: The present study screened mature herbs for their potential to mitigate ruminal ammonia formation in cattle, when provided as a supplement to a forage diet.
Methods: Thirty-five temperate-climate, herbaceous meadow plant species (including three legumes) that appear in biodiverse natural and sown pastures were investigated for their effects on ruminal ammonia production. Aboveground material was harvested during ripening of the seeds and analysed for nutrient and phenol concentrations. Net energy and protein absorbable at the duodenum were calculated. Incubations (24 h) with cattle rumen fluid following the in vitro Hohenheim Gas Test protocol were performed to compare the effects of the test plants on ruminal gas and ammonia formation. Test plants replaced one-third of a basal mixture consisting of 57% Lolium perenne L. and 43% Medicago sativa L. (air-dry-matter basis). Results were compared with those obtained with the basal mixture alone.
Key results: According to regression analysis, ammonia concentration after incubation was negatively related to concentrations of total extractable phenols and total tannins in feed mixtures, whereas the relationship was weakly positive with dietary crude protein. In 23 and 19 of the test diets, respectively, in vitro gas production (indicating ruminal organic matter digestibility) and ammonia concentrations in the incubation medium after 24 h were significantly lower than with the basal mixture alone. Incubations containing Galium verum L., Leontodon hispidus L., Lotus corniculatus L., Onobrychis viciifolia Scop., Plantago lanceolata L., Sanguisorba minor Scop. and Scabiosa columbaria L. maintained gas production and estimated in vitro organic matter digestibility while at the same time lowering ammonia concentrations.
Conclusions: Seven mature herbs of a screening of 35 proved to have potential for positive effects on ruminal protein utilisation without impairing fermentation.
Implications: These herbs are of particular interest as dietary supplements for dairy cows grazing protein-rich pastures.
Keywords: condensed tannins, forbs, hydrolysable tannins, plant secondary compounds, protein efficiency.
References
Aboagye IA, Oba M, Koenig KM, Zhao GY, Beauchemin KA (2019) Use of gallic acid and hydrolyzable tannins to reduce methane emission and nitrogen excretion in beef cattle fed a diet containing alfalfa silage. Journal of Animal Science 97, 2230–2244.| Use of gallic acid and hydrolyzable tannins to reduce methane emission and nitrogen excretion in beef cattle fed a diet containing alfalfa silage.Crossref | GoogleScholarGoogle Scholar | 30906949PubMed |
Agroscope (2020) Feeding recommendations for ruminants. [In German] Agroscope, Posieux FR, Switzerland. Available at https://www.agroscope.admin.ch/agroscope/de/home/services/dienste/futtermittel/fuetterungsempfehlungen-wiederkaeuer.html [Accessed 03 December 2020]
Azuhnwi BN, Thomann B, Arrigo Y, Boller B, Hess HD, Kreuzer M, Dohme-Meier F (2012) Ruminal dry matter and crude protein degradation kinetics of five sainfoin (Onobrychis viciifolia Scop) accessions differing in condensed tannin content and obtained from different harvests. Animal Feed Science and Technology 177, 135–143.
| Ruminal dry matter and crude protein degradation kinetics of five sainfoin (Onobrychis viciifolia Scop) accessions differing in condensed tannin content and obtained from different harvests.Crossref | GoogleScholarGoogle Scholar |
Chanthakhoun V, Wanapat M, Berg J, Kang S (2014) Influence of crude protein and energy level on feed intake, ruminal ammonia nitrogen, and methylglyoxal production in swamp buffaloes (Bubalus bubalis). Journal of Animal and Plant Sciences 24, 1716–1723.
Colin-Schoellen O, Jurjanz S, Laurent F (2000) Metabolizable protein supply (APDE) and restricted level of ruminally degradable nitrogen (APDN) in total mixed rations: effect on milk production and composition and on nitrogen utilization by dairy cows. Livestock Production Science 67, 41–53.
| Metabolizable protein supply (APDE) and restricted level of ruminally degradable nitrogen (APDN) in total mixed rations: effect on milk production and composition and on nitrogen utilization by dairy cows.Crossref | GoogleScholarGoogle Scholar |
Dschaak CM, Williams CM, Holt MS, Eun JS, Young AJ, Min BR (2011) Effects of supplementing condensed tannin extract on intake, digestion, ruminal fermentation, and milk production of lactating dairy cows. Journal of Dairy Science 94, 2508–2519.
| Effects of supplementing condensed tannin extract on intake, digestion, ruminal fermentation, and milk production of lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 21524543PubMed |
Frank B, Swensson C (2002) Relationship between content of crude protein in rations for dairy cows and milk yield, concentration of urea in milk and ammonia emissions. Journal of Dairy Science 85, 1829–1838.
| Relationship between content of crude protein in rations for dairy cows and milk yield, concentration of urea in milk and ammonia emissions.Crossref | GoogleScholarGoogle Scholar | 12201534PubMed |
Ghelichkhan M, Eun JS, Christensen RG, Stott RD, MacAdam JW (2018) Urine volume and nitrogen excretion are altered by feeding birdsfoot trefoil compared with alfalfa in lactating dairy cows. Journal of Animal Science 96, 3993–4001.
| Urine volume and nitrogen excretion are altered by feeding birdsfoot trefoil compared with alfalfa in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 29982473PubMed |
Grosse Brinkhaus A, Bee G, Silacci P, Kreuzer M, Dohme-Meier F (2016) Effect of exchanging Onobrychis viciifolia and Lotus corniculatus for Medicago sativa on ruminal fermentation and nitrogen turnover in dairy cows. Journal of Dairy Science 99, 4384–4397.
| Effect of exchanging Onobrychis viciifolia and Lotus corniculatus for Medicago sativa on ruminal fermentation and nitrogen turnover in dairy cows.Crossref | GoogleScholarGoogle Scholar | 26995129PubMed |
Henke A, Dickhoefer U, Westreicher-Kristen E, Knappstein K, Molkentin J, Hasler M, Susenbeth A (2017) Effect of dietary Quebracho tannin extract on feed intake, digestibility, excretion of urinary purine derivatives and milk production in dairy cows. Archives of Animal Nutrition 71, 37–53.
| Effect of dietary Quebracho tannin extract on feed intake, digestibility, excretion of urinary purine derivatives and milk production in dairy cows.Crossref | GoogleScholarGoogle Scholar | 27830586PubMed |
Jayanegara A, Marquardt S, Kreuzer M, 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.
| Nutrient and energy content, in vitro ruminal fermentation characteristics and methanogenic potential of alpine forage plant species during early summer.Crossref | GoogleScholarGoogle Scholar | 21480269PubMed |
Jayanegara A, Marquardt S, Wina E, Kreuzer M, Leiber F (2013) In vitro indications for favourable non-additive effects on ruminal methane mitigation between high-phenolic and high-quality forages. British Journal of Nutrition 109, 615–622.
| In vitro indications for favourable non-additive effects on ruminal methane mitigation between high-phenolic and high-quality forages.Crossref | GoogleScholarGoogle Scholar |
Kälber T, Kreuzer M, Leiber F (2012) Silages containing buckwheat and chicory: quality, digestibility and nitrogen utilisation by lactating cows. Archives of Animal Nutrition 66, 50–65.
| Silages containing buckwheat and chicory: quality, digestibility and nitrogen utilisation by lactating cows.Crossref | GoogleScholarGoogle Scholar | 22397096PubMed |
Kälber T, Kreuzer M, Leiber F (2014) Milk fatty acid composition of dairy cows fed green whole-plant buckwheat, phacelia or chicory in their vegetative and reproductive stage. Animal Feed Science and Technology 193, 71–83.
| Milk fatty acid composition of dairy cows fed green whole-plant buckwheat, phacelia or chicory in their vegetative and reproductive stage.Crossref | GoogleScholarGoogle Scholar |
Kapp-Bitter AN, Dickhoefer U, Suglo E, Baumgartner L, Kreuzer M, Leiber F (2020) Graded supplementation of chestnut tannins to dairy cows fed protein-rich spring pasture: effects on indicators of protein utilization. Journal of Animal and Feed Sciences 29, 97–104.
| Graded supplementation of chestnut tannins to dairy cows fed protein-rich spring pasture: effects on indicators of protein utilization.Crossref | GoogleScholarGoogle Scholar |
Khiaosa-ard R, Zebeli Q (2013) Meta-analysis of the effects of essential oils and their bioactive compounds on rumen fermentation characteristics and feed efficiency in ruminants. Journal of Animal Science 91, 1819–1830.
| Meta-analysis of the effects of essential oils and their bioactive compounds on rumen fermentation characteristics and feed efficiency in ruminants.Crossref | GoogleScholarGoogle Scholar | 23345564PubMed |
Koenig KM, Beauchemin KA, McGinn SM (2018) Feeding condensed tannins to mitigate ammonia emissions from beef feedlot cattle fed high-protein finishing diets containing distillers grains. Journal of Animal Science 96, 4414–4430.
| Feeding condensed tannins to mitigate ammonia emissions from beef feedlot cattle fed high-protein finishing diets containing distillers grains.Crossref | GoogleScholarGoogle Scholar | 30032212PubMed |
Leiber F, Walkenhorst M, Holinger M (2020) The relevance of feed diversity and choice in nutrition of ruminant livestock. Landbauforschung 70, 35–38.
| The relevance of feed diversity and choice in nutrition of ruminant livestock.Crossref | GoogleScholarGoogle Scholar |
Macheboeuf D, Coudert L, Bergeault R, Lalière G, Niderkorn V (2014) Screening of plants from diversified natural grasslands for their potential to combine high digestibility, and low methane and ammonia production. Animal 8, 1797–1806.
| Screening of plants from diversified natural grasslands for their potential to combine high digestibility, and low methane and ammonia production.Crossref | GoogleScholarGoogle Scholar | 25046582PubMed |
Makkar HPS (2003) ‘Quantification of tannins in tree foliage: a laboratory manual.’ (Springer Verlag: Dordrecht, Netherlands)
McSweeney CS, Palmer B, McNeill DM, Krause DO (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 |
Menke KH, 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.
Min BR, Attwood GT, Reilly K, Sun W, Peters JS, Barry TN, McNabb WC (2002) Lotus corniculatus condensed tannins decrease in vivo populations of proteolytic bacteria and affect nitrogen metabolism in the rumen of sheep. Canadian Journal of Microbiology 48, 911–921.
| Lotus corniculatus condensed tannins decrease in vivo populations of proteolytic bacteria and affect nitrogen metabolism in the rumen of sheep.Crossref | GoogleScholarGoogle Scholar | 12489781PubMed |
Mueller-Harvey I (2006) Unravelling the conundrum of tannins in animal nutrition and health. Journal of the Science of Food and Agriculture 86, 2010–2037.
| Unravelling the conundrum of tannins in animal nutrition and health.Crossref | GoogleScholarGoogle Scholar |
Naumann HD, Tedeschi LO, Zeller WE, Huntley NF (2017) The role of condensed tannins in ruminant animal production: advances, limitations and future directions. Revista Brasileira de Zootecnia 46, 929–949.
| The role of condensed tannins in ruminant animal production: advances, limitations and future directions.Crossref | GoogleScholarGoogle Scholar |
Nousiainen J, Shingfield KJ, Huhtanen P (2004) Evaluation of milk urea nitrogen as a diagnostic of protein feeding. Journal of Dairy Science 87, 386–398.
| Evaluation of milk urea nitrogen as a diagnostic of protein feeding.Crossref | GoogleScholarGoogle Scholar | 14762082PubMed |
Pacheco D, Waghorn GC (2008) Dietary nitrogen definitions, digestion, excretion and consequences of excess for grazing ruminants. Proceedings of the New Zealand Grassland Association 70, 107–116.
| Dietary nitrogen definitions, digestion, excretion and consequences of excess for grazing ruminants.Crossref | GoogleScholarGoogle Scholar |
Parker DS, Lomax MA, Seal CJ, Wilton JC (1995) Metabolic implications of ammonia production in the ruminant. The Proceedings of the Nutrition Society 54, 549–563.
| Metabolic implications of ammonia production in the ruminant.Crossref | GoogleScholarGoogle Scholar | 8524901PubMed |
Perez-Maldonado RA, Norton BW, Kerven GL (1995) Factors affecting in vitro formation of tannin-protein complexes. Journal of the Science of Food and Agriculture 69, 291–298.
| Factors affecting in vitro formation of tannin-protein complexes.Crossref | GoogleScholarGoogle Scholar |
Piluzza G, Sulas L, Bullitta S (2014) Tannins in forage plants and their role in animal husbandry and environmental sustainability: a review. Grass and Forage Science 69, 32–48.
| Tannins in forage plants and their role in animal husbandry and environmental sustainability: a review.Crossref | GoogleScholarGoogle Scholar |
Reynolds CK, Kristensen NB (2008) Nitrogen recycling through the gut and the nitrogen economy of ruminants: an asynchronous symbiosis. Journal of Animal Science 86, E293–E305.
| Nitrogen recycling through the gut and the nitrogen economy of ruminants: an asynchronous symbiosis.Crossref | GoogleScholarGoogle Scholar | 17940161PubMed |
Scharenberg A, Kreuzer M, Dohme F (2009) Suitability of sainfoin (Onobrychis viciifolia) hay as a supplement to fresh grass in dairy cows. Asian-Australasian Journal of Animal Sciences 22, 1005–1015.
| Suitability of sainfoin (Onobrychis viciifolia) hay as a supplement to fresh grass in dairy cows.Crossref | GoogleScholarGoogle Scholar |
Sinz S, Kunz C, Liesegang A, Braun U, Marquardt S, Soliva CR, Kreuzer M (2018) In vitro bioactivity of various pure flavonoids in ruminal fermentation, with special reference to methane formation. Czech Journal of Animal Science 63, 293–304.
| In vitro bioactivity of various pure flavonoids in ruminal fermentation, with special reference to methane formation.Crossref | GoogleScholarGoogle Scholar |
Sinz S, Liesegang A, Kreuzer M, Marquardt S (2019a) Do supplements of Acacia mearnsii and grapeseed extracts alone or in combination alleviate metabolic nitrogen load and manure nitrogen emissions of lambs fed a high crude protein diet? Archives of Animal Nutrition 73, 306–323.
| Do supplements of Acacia mearnsii and grapeseed extracts alone or in combination alleviate metabolic nitrogen load and manure nitrogen emissions of lambs fed a high crude protein diet?Crossref | GoogleScholarGoogle Scholar | 31164000PubMed |
Sinz S, Marquardt S, Soliva CR, Braun U, Liesegang A, Kreuzer M (2019b) Phenolic plant extracts are additive in their effects against in vitro ruminal methane and ammonia formation. Asian-Australasian Journal of Animal Sciences 32, 966–976.
| Phenolic plant extracts are additive in their effects against in vitro ruminal methane and ammonia formation.Crossref | GoogleScholarGoogle Scholar | 30744370PubMed |
Stewart EK, Beauchemin KA, Dai X, MacAdam JW, Christensen RG, Villalba JJ (2019) Effect of tannin-containing hays on enteric methane emissions and nitrogen partitioning in beef cattle. Journal of Animal Science 97, 3286–3299.
| Effect of tannin-containing hays on enteric methane emissions and nitrogen partitioning in beef cattle.Crossref | GoogleScholarGoogle Scholar | 31242504PubMed |
Terranova M, Kreuzer M, Braun U, Schwarm A (2018) In vitro screening of temperate climate forages from a variety of woody plants for their potential to mitigate ruminal methane and ammonia formation. The Journal of Agricultural Science 156, 929–941.
| In vitro screening of temperate climate forages from a variety of woody plants for their potential to mitigate ruminal methane and ammonia formation.Crossref | GoogleScholarGoogle Scholar |
Totty VK, Greenwood SL, Bryant RH, Edwards GR (2013) Nitrogen partitioning and milk production of dairy cows grazing simple and diverse pastures. Journal of Dairy Science 96, 141–149.
| Nitrogen partitioning and milk production of dairy cows grazing simple and diverse pastures.Crossref | GoogleScholarGoogle Scholar | 23164232PubMed |
Villalba JJ, Provenza FD, Catanese F, Distel RA (2015) Understanding and manipulating diet choice in grazing animals. Animal Production Science 55, 261–271.
| Understanding and manipulating diet choice in grazing animals.Crossref | GoogleScholarGoogle Scholar |
Waghorn GC, McNabb WC (2003) Consequences of plant phenolic compounds for productivity and health of ruminants. The Proceedings of the Nutrition Society 62, 383–392.
| Consequences of plant phenolic compounds for productivity and health of ruminants.Crossref | GoogleScholarGoogle Scholar | 14506885PubMed |
Yang K, Wei C, Zhao GY, Xu ZW, Lin SX (2017) Effects of dietary supplementing tannic acid in the ration of beef cattle on rumen fermentation, methane emission, microbial flora and nutrient digestibility. Journal of Animal Physiology and Animal Nutrition 101, 302–310.
| Effects of dietary supplementing tannic acid in the ration of beef cattle on rumen fermentation, methane emission, microbial flora and nutrient digestibility.Crossref | GoogleScholarGoogle Scholar | 27272696PubMed |
