Skip to main content

Advertisement

SpringerLink
Log in

Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations

  • Review Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

In the recent years, the exploration of bioactive phytochemicals as natural feed additives has been of great interest among nutritionists and rumen microbiologists to modify the rumen fermentation favorably such as defaunation, inhibition of methanogenesis, improvement in protein metabolism, and increasing conjugated linoleic acid content in ruminant derived foods. Many phytochemicals such as saponins, essential oils, tannins and flavonoids from a wide range of plants have been identified, which have potential values for rumen manipulation and enhancing animal productivity as alternatives to chemical feed additives. However, their effectiveness in ruminant production has not been proved to be consistent and conclusive. This review discusses the effects of phytochemicals such as saponins, tannins and essential oils on the rumen microbial populations, i.e., bacteria, protozoa, fungi and archaea with highlighting molecular diversity of microbial community in the rumen. There are contrasting reports of the effects of these phytoadditives on the rumen fermentation and rumen microbes probably depending upon the interactions among the chemical structures and levels of phytochemicals used, nutrient composition of diets and microbial components in the rumen. The study of chemical structure–activity relationships is required to exploit the phytochemicals for obtaining target responses without adversely affecting beneficial microbial populations. A greater understanding of the modulatory effects of phytochemicals on the rumen microbial populations together with fermentation will allow a better management of the rumen ecosystem and a practical application of this feed additive technology in livestock production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agarwal N, Kamra DN, Chaudhary LC, Patra AK (2006) Effect of Sapindus mukorossi extracts on in vitro methanogenesis and fermentation characteristics in buffalo rumen liquor. J Appl Anim Res 30:1–4

    Google Scholar 

  • Agarwal N, Shekhar C, Kumar R, Chaudhary LC, Kamra DN (2009) Effect of peppermint (Mentha piperita) oil on in vitro methanogenesis and fermentation of feed with buffalo rumen liquor. Anim Feed Sci Technol 148:321–327

    Article  CAS  Google Scholar 

  • Ando S, Nishida T, Ishida M, Hosoda K, Bayaru E (2003) Effect of peppermint feeding on the digestibility, ruminal fermentation and protozoa. Livest Prod Sci 82:245–248

    Article  Google Scholar 

  • Animut G, Goetsch AL, Puchala R, Patra AK, Sahlu T, Varel VH, Wells J (2008) Methane emission by goats consuming different sources of condensed tannins. Anim Feed Sci Technol 144:228–241

    Article  CAS  Google Scholar 

  • Bae HD, McAllister TA, Yanke LJ, Cheng KJ, Muir AD (1993) Effect of condensed tannins on endoglucanase activity and filter paper digestion by Fibrobacter succinogenes S85. Appl Environ Microbiol 59:2132–2138

    CAS  PubMed  Google Scholar 

  • Barile E, Bonanomi G, Antignani V, Zolfaghari B, Sajjadi SE, Scala F, Lanzotti V (2007) Saponins from Allium minutiflorum with antifungal activity. Phytochemistry 68:596–603

    Article  CAS  PubMed  Google Scholar 

  • Benchaar C, Petit HV, Berthiaume R, Ouellet DR, Chiquette J, Chouinard PY (2007) Effects of essential oils on digestion, ruminal fermentation, rumen microbial populations, milk production, and milk composition in dairy cows fed alfalfa silage or corn silage. J Dairy Sci 90:886–897

    CAS  PubMed  Google Scholar 

  • Benchaar C, McAllister TA, Chouinard PY (2008) Digestion, ruminal fermentation, ciliate protozoal populations, and milk production from dairy cows fed cinnamaldehyde, quebracho condensed tannin, or Yucca schidigera saponin extracts. J Dairy Sci 91:4765–4777

    Article  CAS  PubMed  Google Scholar 

  • Busquet M, Calsamiglia S, Ferret A, Carro MD, Kamel C (2005) Effect of garlic oil and four of its compounds on rumen microbial fermentation. J Dairy Sci 88:4393–4404

    CAS  PubMed  Google Scholar 

  • Calsamiglia S, Busquet M, Cardozo PW, Castillejos L, Ferret A (2007) Invited review: essential oils as modifiers of rumen microbial fermentation. J Dairy Sci 90:2580–2595

    Article  CAS  PubMed  Google Scholar 

  • Cardozo PW, Calsamiglia S, Ferret A, Kamel C (2006) Effects of alfalfa extract, anise, capsicum, and a mixture of cinnamaldehyde and eugenol on ruminal fermentation and protein degradation in beef heifers fed a high-concentrate diet. J Anim Sci 84:2801–2808

    Article  CAS  PubMed  Google Scholar 

  • Carulla JE, Kreuzer M, Machmuller A, Hess HD (2005) Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep. Aust J Agric Res 56:961–970

    Article  CAS  Google Scholar 

  • Chiquette J, Cheng KJ, Rode LM, Milligan LP (1989) Effect of tannin content in two isosynthetic strains of birdsfoot trefoil (Lotus corniculatus) on feed digestibility and rumen fluid composition in sheep. Can J Anim Sci 69:1031–1039

    Google Scholar 

  • Duval SM, Newbold CJ, McEwan NR, Graham RC, Wallace RJ (2004) Effect of a specific blend of essential oils on the colonization of substrates by rumen microorganisms. Reprod Nutr Dev 44:35

    Google Scholar 

  • Duval SM, McEwan NR, Graham RC, Wallace RJ, Newbold CJ (2007) Effect of a blend of essential oil compounds on the colonization of starch-rich substrates by bacteria in the rumen. J Appl Microbiol 103:2132–2141

    Article  CAS  PubMed  Google Scholar 

  • Eadie JM, Mann SO, Oxford AE (1956) A survey of physiologically active organic infusoricidal compounds and their soluble derivatives with special reference to their action on the rumen microbial system. J Gen Microbiol 14:122–133

    CAS  PubMed  Google Scholar 

  • Evans JD, Martin SA (2000) Effects of thymol on ruminal micro-organisms. Curr Microbiol 41:336–340

    Article  CAS  PubMed  Google Scholar 

  • Ferme D, Banjac M, Calsamiglia S, Busquet M, Kamel C, Avguštin G (2004) The effects of plant extracts on microbial community structure in a rumen-simulating continuous-culture system as revealed by molecular profiling. Folia Microbiol 49:151–155

    Article  CAS  Google Scholar 

  • Francis G, Kerem Z, Makkar HPS, Becker K (2002) The biological action of saponins in animal systems: a review. Br J Nutr 88:587–605

    Article  CAS  PubMed  Google Scholar 

  • Fraser GR, Chaves AV, Wang Y, McAllister TA, Beauchemin KA, Benchaar C (2007) Assessment of the effects of cinnamon leaf oil on rumen microbial fermentation using two continuous culture systems. J Dairy Sci 90:2315–2328

    Article  CAS  PubMed  Google Scholar 

  • Goel G, Makkar HPS, Becker K (2008a) Effect of Sesbania sesban and Carduus pycnocephalus leaves and fenugreek (Trigonella foenum-graecum L.) seeds and their extracts on partitioning of nutrient from roughage and concentrate based feeds to methane. Anim Feed Sci Technol 147:72–89

    Article  CAS  Google Scholar 

  • Goel G, Makkar HPS, Becker K (2008b) Changes in microbial community structure, methanogenesis and rumen fermentation in response to saponin-rich fractions from different plant materials. J Appl Microbiol 105:770–777

    Article  CAS  PubMed  Google Scholar 

  • Hart KJ, Yanez-Ruiz DR, Duval SM, McEwan NR, Newbold CJ (2008) Plant extracts to manipulate rumen fermentation. Anim Feed Sci Technol 147:8–35

    Article  CAS  Google Scholar 

  • Haslam E (1989) Plant polyphenols. Cambridge University Press, Cambridge

    Google Scholar 

  • Heins Y, Tagari H, Volcani R (1964) Effect of water extracts of carob pods, tannic acid, and their derivatives on the morphology and growth of micro-organisms. Appl Microbiol 12:204–209

    Google Scholar 

  • Hess HD, Monsalve LM, Lascano CE, Carulla JE, Diaz TE, Kreuzer M (2003a) Supplementation of a tropical grass diet with forage legumes and Sapindus saponaria fruits: effects on in vitro ruminal nitrogen turnover and methanogenesis. Aust J Agric Res 54:703–713

    Article  Google Scholar 

  • Hess HD, Kreuzer M, Diaz TE, Lascano CE, Carulla JE, Solvia CR (2003b) Saponin rich tropical fruits affect fermentation and methanogenesis in faunated and defaunated fluid. Anim Feed Sci Technol 109:79–94

    Article  CAS  Google Scholar 

  • Hess HD, Beuret RA, Lotscher M, Hindrichsen IK, Machmüller A, Carulla JE, Lascano CE, Kreuzer M (2004) Ruminal fermentation, methanogenesis and nitrogen utilization of sheep receiving tropical grass hay-concentrate diets offered with Sapindus saponaria fruits and Cratylia argentea foliage. Anim Sci 79:177–189

    Google Scholar 

  • Hristov AN, Mcallister TA, Van Herk FH, Newbold CJ, Cheng KJ (1999) Effect of Yucca schidigera on ruminal fermentation and nutrient digestion in heifer. J Anim Sci 77:2554–2563

    CAS  PubMed  Google Scholar 

  • Hristov AN, Ivan M, Neill L, Mcallister TA (2003) Evaluation of several potential bioactive agents for reducing protozoal activity in vitro. Anim Feed Sci Technol 105:163–184

    Article  CAS  Google Scholar 

  • Hu W-L, Liu J-X, Ye J-A, Wu Y-M, Guo Y-Q (2005) Effect of tea saponin on rumen fermentation in vitro. Anim Feed Sci Technol 120:333–339

    Article  CAS  Google Scholar 

  • Jones GA, McAllister TA, Muir AD, Cheng KJ (1994) Effects of sainfoin (Onobrychis viciifolia Scop.) condensed tannins on growth and proteolysis by four strains of ruminal bacterium. Appl Environ Microbiol 60:1374–1378

    CAS  PubMed  Google Scholar 

  • Kamra DN, Singh R, Agarwal N, Pathak NN (2000) Soapnut (reetha) as natural defaunating agent—its effect on rumen fermentation and in sacco degradability of jowar hay in buffaloes. Buffalo J 16:99–104

    Google Scholar 

  • Kamra DN, Patra AK, Chatterjee PN, Kumar R, Agarwal N, Chaudhary LC (2008) Effect of plant extract on methanogenesis and microbial profile of the rumen of buffalo: a brief overview. Aust J Exp Agric 48:175–178

    Article  CAS  Google Scholar 

  • Lu CD, Jorgensen NA (1987) Alfalfa saponins affect site and extent of nutrient digestion in ruminants. J Nutr 117:919–927

    CAS  PubMed  Google Scholar 

  • Makkar HPS, Blummel M, Becker K (1995) In vitro effects and interaction between tannins and saponins and fate of tannins in the rumen. J Sci Food Agric 69:481–493

    Article  CAS  Google Scholar 

  • Makkar HPS, Sen S, Blummel M, Becker K (1998) Effects of fractions containing saponins from Yucca schidigera, Quillaja saponaria and Acacia auriculoformis on rumen fermentation. J Agric Food Chem 46:4324–4328

    Article  CAS  Google Scholar 

  • McIntosh FM, Williams P, Losa R, Wallace RJ, Beever DA, Newbold CJ (2003) Effects of essential oils on ruminal microorganisms and their protein metabolism. Appl Environ Microbiol 69:5011–5014

    Article  CAS  PubMed  Google Scholar 

  • McMahon LR, Majak W, McAllister TA, Hall JW, Jones GA, Popp JD, Cheng KJ (1999) Effect of sainfoin on in vitro digestion of fresh alfalfa and bloat in steers. Can J Anim Sci 79:203–212

    Article  Google Scholar 

  • McSweeney CS, Palmer B, Bunch R, Krause DO (2001) Effect of the tropical forage calliandra on microbial protein synthesis and ecology in the rumen. J Appl Microbiol 90:78–88

    Article  CAS  PubMed  Google Scholar 

  • Min BR, Attwood GT, McNabb WC, Molan AL, Barry TN (2005) The effect of condensed tannins from Lotus corniculatus on the proteolytic activities and growth of rumen bacteria. Anim Feed Sci Technol 121:45–58

    Article  CAS  Google Scholar 

  • Monforte-Briceno GE, Sandoval-Castro CA, Ramirez-Aviles L, Capetillo-Leal CM (2005) Defaunating capacity of tropical fodder trees: effects of polyethylene glycol and its relationship to in vitro gas production. Anim Feed Sci Technol 123–124:313–327

    Article  CAS  Google Scholar 

  • Muetzel S, Hoffmann EM, Becker K (2003) Supplementation of barley straw with Sesbania pachycarpa leaves in vitro: effects on fermentation variables and rumen microbial concentration structure quantified by ribosomal RNA-targeted probes. Br J Nutr 89:445–453

    Article  CAS  PubMed  Google Scholar 

  • Muhammed S, Stewart CS, Acamovic T (1995) Effects of tannic acid, ellagic acid, gallic acid and catchin on cellulase degradation by the rumen fungus Neocallimastix frontalis strain RE1. Anim Sci 60:550A (Abst)

    Google Scholar 

  • Navas-Camacho A, Laredo MA, Cuesta A, Ortega O, Romero M (1994) Evaluation of tropical tree with high or medium saponins content as dietary alternative to eliminate protozoa from the rumen. Proc Soc Nutr Physiol 3:204

    Google Scholar 

  • Newbold CJ, Hassan SME, Wang J, Ortega ME, Wallace RJ (1997) Influence of foliage from African multipurpose tree on activity of rumen protozoa and bacteria. Br J Nutr 78:237–249

    Article  CAS  PubMed  Google Scholar 

  • Oh HK, Jones MB, Longhurst WM (1967) Effect of various essential oils isolated from Douglasfir needles upon sheep and deer rumen microbial activity. Appl Microbiol 15:777–784

    CAS  PubMed  Google Scholar 

  • Oh HK, Jones MB, Longhurst WM (1968) Comparison of rumen microbial inhibition resulting from various essential oils isolated from relatively unpalatable plant species. Appl Microbiol 16:39–44

    CAS  PubMed  Google Scholar 

  • Ohene-Adjei S, Chaves AV, McAllister TA, Benchaar C, Teather RM, Forster RJ (2008) Evidence of increased diversity of methanogenic archaea with plant extract supplementation. Microb Ecol 56:234–242

    Article  CAS  PubMed  Google Scholar 

  • Okuda T, Mori K, Hatano T (1985) Relationship of the structures of tannins to the binding activities with hemoglobin and methylene blue. Chem Pharm Bull 33:1424–1433

    CAS  PubMed  Google Scholar 

  • Patra AK (2004) Inhibition of ciliate protozoa and stimulation of fiber degrading microbes in the rumen of buffaloes by plant secondary metabolites. Ph.D. thesis, Indian Veterinary Research Institute, Izatnagar

  • Patra AK, Kamra DN, Agarwal N (2006a) Effect of plant extracts on in vitro methanogenesis, enzyme activities and fermentation of feed in rumen liquor of buffalo. Anim Feed Sci Technol 128:276–291

    Article  CAS  Google Scholar 

  • Patra AK, Kamra DN, Agarwal N (2006b) Effect of spices on rumen fermentation, methanogenesis and protozoa counts in in vitro gas production test. Int Cong Series 1293:176–179

    Article  CAS  Google Scholar 

  • Patra AK, Kamra DN, Bhar R, Kumar R, Agarwal N (2008a) Plant secondary metabolites present in Terminalia chebula and Allium sativum reduce methane emission in sheep. Aust J Exp Agric 48:lxx–lxxi

    Google Scholar 

  • Patra AK, Kamra DN, Agarwal N, Chatterjee PN (2008b) Effect of Terminalia chebula and Allium sativum on rumen fermentation, enzyme activities and microbial counts in buffalo. Indian J Anim Nutr 24:251–255

    Google Scholar 

  • Patra AK, Kamra DN, Agarwal N (2008c) Effect of extracts of leaves on rumen methanogenesis, enzyme activities and fermentation in in vitro gas production test. Indian J Anim Sci 78:91–96

    CAS  Google Scholar 

  • Paul SS, Kamra DN, Sastry VRB, Sahu NP, Kumar A (2003) Effect of phenolic monomers on biomass and hydrolytic enzyme activities of an anaerobic fungus isolated from wild nil gai (Baselophus tragocamelus). Lett Appl Microbiol 36:377–381

    Article  CAS  PubMed  Google Scholar 

  • Sakanaka S, Skim M, Taniguchi M, Yamamoto T (1989) Antibacterial substances in Japanese green tea extract against Streptococcus mutans, a cariogenic bacterium. Agric Biol Chem 53:2307–2311

    CAS  Google Scholar 

  • Salawu MB, Acamovic T, Stewart CS, Hovell FD, De B (1999) Effects of feeding quebracho tannin diets, with or without a dietary modifier, on rumen function in sheep. Anim Sci 69:265–274

    CAS  Google Scholar 

  • Salem HB, Nefzaoui A, Salem LB, Tisserand JL, Ben-Salem H, Ben-Salem L (1997) Effect of Acacia cyanophylla Lindl. foliage supply on intake and digestion by sheep fed lucern hay-based diets. Anim Feed Sci Technol 68:101–113

    Article  Google Scholar 

  • Smith AH, Zoetendal EG, Mackie RI (2005) Bacterial mechanisms to overcome inhibitory effects of dietary tannins. Microb Ecol 50:197–205

    Article  CAS  PubMed  Google Scholar 

  • Tagari H, Heins Y, Tamir M, Volcani R (1965) Effect of carob pod extract on cellulolysis, proteolysis, deamination, and protein biosynthesis in an artificial rumen. Appl Microbiol 13:437–442

    CAS  PubMed  Google Scholar 

  • Tavendale MH, Meagher LP, Pacheco D, Walker N, Attwood GT, Sivakumaran S (2005) Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis. Anim Feed Sci Technol 123–124:403–419

    Article  CAS  Google Scholar 

  • Teferedegne B (2000) New perspective on the use of tropical plants to improve ruminant nutrition. Proc Nutr Soc 59:209–214

    CAS  PubMed  Google Scholar 

  • Teferedegne B, McIntosh F, Osuji PO, Odenyo A, Wallace RJ, Newbold CJ (1999) Influence of foliage from different accessions of the sub-tropical leguminous tree, Sesbania sesban, on ruminal protozoa in Ethiopian and Scottish sheep. Anim Feed Sci Technol 78:11–20

    Article  Google Scholar 

  • Valdez FR, Bush LJ, Goetsch AL, Owens FN (1986) Effect of steroidal sapogenins on rumen fermentation and on production of lactating dairy cows. J Dairy Sci 69:1568–1575

    Article  CAS  PubMed  Google Scholar 

  • Waghorn GC, Tavendale MH, Woodfield DR (2002) Methanogenesis in forages fed to sheep. Proc N Z Grassl Assoc 64:167–171

    Google Scholar 

  • Wallace RJ, Arthaud L, Newbold CJ (1994) Influence of Yucca schidigera extract on ruminal ammonia concentration and ruminal micro-organisms. Appl Environ Microbiol 60:1762–1767

    CAS  PubMed  Google Scholar 

  • Wallace RJ, McEwan NR, McIntosh FM, Teferedegne B, Newbold CJ (2002) Natural products as manipulators of rumen fermentation. Asian-Aust J Anim Sci 15:1458–1468

    CAS  Google Scholar 

  • Wang Y, McAllister TA, Newbold CJ, Rode LM, Cheeke PR, Cheng K-J (1998) Effect of Yucca schidigera extract on fermentation and degradation of steroidal saponins in the rumen simulation technique (RUSITEC). Anim Feed Sci Technol 74:143–153

    Article  CAS  Google Scholar 

  • Wang Y, McAllister TA, Yanke LJ, Cheeke PR (2000) Effect of steroidal saponin from Yucca schidigera extract on ruminal microbes. J Appl Microbiol 88:887–896

    Article  CAS  PubMed  Google Scholar 

  • Williams AG, Coleman GS (1992) The rumen protozoa. Springer, Verlag, London

    Google Scholar 

  • Williams YJ, Popovski S, Rea SM, Skillman LC, Toovey AF, Northwood KS, Wright ADG (2009) A vaccine against rumen methanogens can alter the composition of archaeal populations. Appl Environ Microbiol 75:1860–1866

    Article  CAS  PubMed  Google Scholar 

  • Wina E, Muetzel S, Hoffmann E, Makkar HPS, Becker K (2005) Saponins containing methanol extract of Sapindus rarak affect microbial fermentation, microbial activity and microbial community structure in vitro. Anim Feed Sci Technol 121:159–174

    Article  CAS  Google Scholar 

  • Wina E, Muetze S, Becker K (2006) The dynamics of major fibrolytic microbes and enzyme activity in the rumen in response to short- and long-term feeding of Sapindus rarak saponins. J Appl Microbiol 100:114–122

    Article  CAS  PubMed  Google Scholar 

  • Woodward SL, Waghorn GC, Ulyatt MJ, Lassey KR (2001) Early indication that feeding lotus will reduce methane emission from ruminants. Proc N Z Soc Anim Prod 61:23–26

    Google Scholar 

  • Woodward SL, Waghorn GC, Lassey KR, Laboyrie PG (2002) Does feeding sulla (Hedysarum coronarium) reduce methane emission from dairy cows? Proc N Z Soc Anim Prod 62:227–230

    Google Scholar 

  • Zelter SZ, Leory F, Issier JP (1970) Protection of protein in the feed against bacterial deamination in the rumen. I. Studies in vitro: behaviour in the rumen of some protein tanned with tannins from chestnut wood of certain aldehydes (formaldehyde, glutaraldehyde, glyoxal). Ann Biol Anim Biochim Biophys 10:111–122

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Animal Nutrition, Faculty of Veterinary and Animal Sciences, West Bengal University of Animal and Fishery Sciences, 37, K. B. Sarani, Belgachia, Kolkata, India

    Amlan K. Patra

  2. Department of Botany and Microbiology, University of Oklahoma, Norman, OK, USA

    Jyotisna Saxena

Authors
  1. Amlan K. Patra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jyotisna Saxena
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amlan K. Patra.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Patra, A.K., Saxena, J. Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie van Leeuwenhoek 96, 363–375 (2009). https://doi.org/10.1007/s10482-009-9364-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-009-9364-1

Keywords

Search

Navigation