Environmental Science and Pollution Research

, Volume 25, Issue 35, pp 35538–35547 | Cite as

In vitro screening of plants from the Brazilian Caatinga biome for methanogenic potential in ruminant nutrition

  • Brena Santos Oliveira
  • Luiz Gustavo Ribeiro PereiraEmail author
  • Jose Augusto Gomes Azevêdo
  • João Paulo Pacheco Rodrigues
  • Gherman Garcia Leal de Araújo
  • Rogerio Martins Maurício
  • Fernanda Samarini Machado
  • Mariana Magalhães Campos
  • Tássia Ludmila Teles Martins
  • Thierry Ribeiro Tomich
Research Article


Thirty-nine plants naturally found in Brazilian Caatinga semiarid biome were screened using an in vitro fermentability testing focused in apparent organic matter digestibility (aOMD), gas, methane (CH4), and short-chain fatty acid (SCFA) production. Three independent in vitro runs were carried out and plants were classified by CH4 concentration as proportion of gas and per unit of apparent digested organic matter (aDOM). According to its CH4 concentration on produced gas (mL/L), the plants were classified as low (> 110), medium (from 60 to 110), and high (< 60) anti-methanogenic potential. From evaluated plants, 3, 24, and 12 were classified as high, medium, and low anti-methanogenic potential. High anti-methanogenic potential plants Cnidoscolus phillacanthus (CnPh), Chloroleucon foliolosum (ChFo), and Anadenanthera macrocarpa (AnMa) produced 21.3, 34.3, and 35.9 mL CH4/L of gas. Methane concentration for Myracrodruon urundeuva (MyUr) was 61.1 mL/L and classified as medium potential. However, CH4 production per unit of aDOM was similar between MyUr and AnMa (3.35 and 2.68 mL/g, respectively). Molar proportions of acetate and propionate in SCFA produced by ChFo fermentation were 0.02 and 0.78 mmol/mol. Acetate to propionate ratios were 0.79, 0.03, 1.39, and 1.36 for CnPh, ChFo, AnMa, and MyUr, respectively. Greater aOMD were observed for Opuntia sp. and Calotropis procera (632 and 601 g/kg, respectively), which were classified as medium mitigating potential plants. AnMa, ChFo, CnPh, and MyUr are promising anti-methanogenic plants for ruminants. Selecting forages to feed ruminants in Caatinga is a potential strategy for enteric CH4 emission reduction, and our in vitro results can support future research by indicating species to be evaluated in in vivo studies integrating mixed diets with performance, digestibility, and CH4 production, yield, and intensity.

Graphical abstract


Acetate Digestibility In vitro Plant secondary compounds Propionate Greenhouse gas Short-chain fatty acids 



The results of this article is part of “PECUS RumenGases Brazil—conceptual advance in diagnosis and estrategies of mitigating of enteric methane emissions by ruminants in Brazil” research project. The authors are thankful to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES-PVE), Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB), Universidade Federal de São João del-Rei (UFSJ), and Empresa Brasileira de Pesquisa Agropecuária (EMPRAPA) for supporting this research.


  1. Alexandratos N, Bruinsma J (2012) World agriculture towards 2030/2050: the 2012 revision. ESA Working Paper No. 12-03. FAO, RomeGoogle Scholar
  2. AOAC (2005) Official method of analysis, 18th edn. Association of Officiating Analytical Chemists, Washington DCGoogle Scholar
  3. Arruda DM, Ferreira WG, Duque-Brasil R, Schaefer CER (2013) Phytogeographical patterns of dry forests sensu stricto in northern Minas Gerais state, Brazil. An Acad Bras Cienc 85:623–634. CrossRefGoogle Scholar
  4. Bhatta R, Saravanan M, Baruah L, Sampath KT (2012) Nutrient content, in vitro ruminal fermentation characteristics and methane reduction potential of tropical tannin-containing leaves. J Sci Food Agric 92:2929–2935. CrossRefGoogle Scholar
  5. Bodas R, Prieto N, García-González R, Andrés S, Giráldez FJ, López S (2012) Manipulation of rumen fermentation and methane production with plant secondary metabolites. Anim Feed Sci Technol 176:78–93. CrossRefGoogle Scholar
  6. Brito SMO, Coutinho HDM, Talvani A, Coronel C, Barbosa AGR, Vega C, Figueredo FG, Tintino SR, Lima LF, Boligon AA, Athayde ML, Menezes IRA (2015) Analysis of bioactivities and chemical composition of Ziziphus joazeiro Mart. Using HPLC-DAD. Food Chem 186:185–191. CrossRefGoogle Scholar
  7. Cecílio AB, Oliveira P de C, Caldas S et al (2016) Antiviral activity of Myracrodruon urundeuva against rotavirus. Brazilian J Pharmacogn 26:197–202. CrossRefGoogle Scholar
  8. De Azevêdo Silva AM, Da Costa RG, Pereira Filho JM et al (2010) Nutritional value of silk flower hay for lambs. Rev Bras Zootec 39:2739–2743. CrossRefGoogle Scholar
  9. de Carvalho GGP, Rebouças RA, Campos FS, Santos EM, Araújo GGL, Gois GC, de Oliveira JS, Oliveira RL, de A. Rufino LM, Azevedo JAG, Cirne LGA (2017) Intake, digestibility, performance, and feeding behavior of lambs fed diets containing silages of different tropical forage species. Anim Feed Sci Technol 228:140–148. CrossRefGoogle Scholar
  10. de Figueiredo Monteiro CC, Silva de Melo AA, Ferreira MA, de Souza Campos JM, Rodrigues Souza JS, dos Santos Silva ET, de Paula Xavier de Andrade R, da Silva EC (2014) Replacement of wheat bran with spineless cactus (Opuntia ficus indica mill cv Gigante) and urea in the diets of Holstein × Gyr heifers. Trop Anim Health Prod 46:1149–1154. CrossRefGoogle Scholar
  11. de Oliveira-Júnior RG, Ferraz CAA, de Oliveira AP, Araújo CS, Oliveira LFS, Picot L, Rolim LA, Rolim-Neto PJ, Almeida JRGS (2017) Phytochemical and pharmacological aspects of Cnidoscolus pohl species: a systematic review. Phytomedicine 50:137–147. CrossRefGoogle Scholar
  12. Durmic Z, Moate PJ, Jacobs JL, Vadhanabhuti J, Vercoe PE (2016) In vitro fermentability and methane production of some alternative forages in Australia. Anim Prod Sci 56:641. CrossRefGoogle Scholar
  13. Durmic Z, Ramírez-Restrepo CA, Gardiner C, O’Neill CJ, Hussein E, Vercoe PE (2017) Differences in the nutrient concentrations, in vitro methanogenic potential and other fermentative traits of tropical grasses and legumes for beef production systems in northern Australia. J Sci Food Agric 97:4075–4086. CrossRefGoogle Scholar
  14. Fedorah PM, Hrudey SE (1983) A simple apparatus for measuring gas production by methanogenic cultures in serum bottles. Environ Technol Lett 4:425–432. CrossRefGoogle Scholar
  15. Figueredo FG, Ferreira EO, Lucena BFF, Torres CMG, Lucetti DL, Lucetti ECP, Silva JMFL, Santos FAV, Medeiros CR, Oliveira GMM, Colares AV, Costa JGM, Coutinho HDM, Menezes IRA, Silva JCF, Kerntopf MR, Figueiredo PRL, Matias EFF (2013) Modulation of the antibiotic activity by extracts from Amburana cearensis a. C. Smith and Anadenanthera macrocarpa (Benth.) Brenan. Biomed Res Int 2013:1–5. CrossRefGoogle Scholar
  16. Fotius ACA, Ferreira MA, Bispo SV et al (2014) Behavior of sheep fed different sequences of ingredients in a spineless cactus (Nopalea cochenillifera Salm-Dyck) based-diet. Rev Bras Saúde e Produção Anim 15:74–82. CrossRefGoogle Scholar
  17. Garcia F, Vercoe PE, Martinez MJ et al (2018) Essential oils from Lippia turbinata and Tagetes minuta persistently reduce in vitro ruminal methane production in a continuous-culture system. Anim Prod Sci.
  18. Gemeda BS, Hassen A (2015) Effect of tannin and species variation on in vitro digestibility, gas, and methane production of tropical browse plants. Asian-Australasian. J Anim Sci 28:188–199. CrossRefGoogle Scholar
  19. Gomes DI, Detmann E, de Valadares Filho SC, Valadares Filho SC, Fukushima RS, de Souza MA, Valente TNP, Paulino MF, de Queiroz AC (2011) Evaluation of lignin contents in tropical forages using different analytical methods and their correlations with degradation of insoluble fiber. Anim Feed Sci Technol 168:206–222. CrossRefGoogle Scholar
  20. Hatano T, Kira R, Yoshizaki M, Okuda T (1986) Seasonal changes in the tannins of Liquidambar formosana reflecting their biogenesis. Phytochemistry 25:2787–2789. CrossRefGoogle Scholar
  21. Herrero M, Henderson B, Havlík P, Thornton PK, Conant RT, Smith P, Wirsenius S, Hristov AN, Gerber P, Gill M, Butterbach-Bahl K, Valin H, Garnett T, Stehfest E (2016) Greenhouse gas mitigation potentials in the livestock sector. Nat Clim Chang 6:452–461CrossRefGoogle Scholar
  22. Holtshausen L, Chaves AV, Beauchemin KA, McGinn SM, McAllister TA, Odongo NE, Cheeke PR, Benchaar C (2009) Feeding saponin-containing Yucca schidigera and Quillaja saponaria to decrease enteric methane production in dairy cows. J Dairy Sci 92:2809–2821. CrossRefGoogle Scholar
  23. Khanbabaee K, van Ree T (2001) Tannins: classification and definition. Nat Prod Rep 18:641–649. CrossRefGoogle Scholar
  24. Klevenhusen F, Meile L, Kreuzer M, Soliva CR (2011) Effects of monolaurin on ruminal methanogens and selected bacterial species from cattle, as determined with the rumen simulation technique. Anaerobe 17:232–238. CrossRefGoogle Scholar
  25. López S, Makkar HPS, Soliva CR (2010) Screening plants and plant products for methane inhibitors. In: In vitro screening of plant resources for extra-nutritional attributes in ruminants: nuclear and related methodologies. Springer Netherlands, Dordrecht, pp 191–231CrossRefGoogle Scholar
  26. McSweeney CS, Odenyo A, Krause DO (2002) Rumen microbial responses to antinutritive factors in fodder trees and shrub legumes. J Appl Anim Res 21:181–205. CrossRefGoogle Scholar
  27. Meale SJ, Chaves AV, Baah J, McAllister TA (2012) Methane production of different forages in in vitro ruminal fermentation. Asian-Australasian. J Anim Sci 25:86–91. CrossRefGoogle Scholar
  28. Menke KH, Raab L, Salewski A, Steingass H, Fritz D, Schneider W (1979) The estimation of the digestibility and metabolizable energy content of ruminant feedingstuffs from the gas production when they are incubated with rumen liquor in vitro. J Agric Sci 93:217–222. CrossRefGoogle Scholar
  29. Mertens DR, Allen M, Carmany J et al (2002) Gravimetric determination of amylase-treated neutral detergent fiber in feeds with refluxing in beakers or crucibles: collaborative study. J AOAC Int 85:1217–1240Google Scholar
  30. Milliken W (1997) Plants for malaria, plants for fever: medicinal species in Latin America—a bibliographic survey. Royal Botanic Gardens, KewGoogle Scholar
  31. Monteiro JM, Albuquerque UP, Neto EMFL et al (2006) The effects of seasonal climate changes in the Caatinga on tannin levels in Myracrodruon urundeuva (Engl.) Fr. All. and Anadenanthera colubrina (Vell.) Brenan. Rev Bras Farmacogn 16:338–344. CrossRefGoogle Scholar
  32. Mottet A, de Haan C, Falcucci A, Tempio G, Opio C, Gerber P (2017) Livestock: on our plates or eating at our table? A new analysis of the feed/food debate. Glob Food Sec 14:1–8. CrossRefGoogle Scholar
  33. Newbold CJ, de la Fuente G, Belanche A, Ramos-Morales E, McEwan NR (2015) The role of ciliate protozoa in the rumen. Front Microbiol 6.
  34. Oliveira DM, Pimentel LA, Araújo JAS, Rosane MTM, Dantas AFM, Riet-Correa F (2008) Intoxicação por Cnidoscolus phyllacanthus (Euphorbiaceae) em caprinos. Pesqui Vet Bras 28:36–42. CrossRefGoogle Scholar
  35. Oliveira-Filho AT, Cardoso D, Schrire BD, Lewis GP, Pennington RT, Brummer TJ, Rotella J, Lavin M (2013) Stability structures tropical woody plant diversity more than seasonality: insights into the ecology of high legume-succulent-plant biodiversity. South African J Bot 89:42–57. CrossRefGoogle Scholar
  36. Pal K, Patra AK, Sahoo A, Kumawat PK (2015) Evaluation of several tropical tree leaves for methane production potential, degradability and rumen fermentation in vitro. Livest Sci 180:98–105. CrossRefGoogle Scholar
  37. Patra AK, Yu Z (2012) Effects of essential oils on methane production and fermentation by, and abundance and diversity of, rumen microbial populations. Appl Environ Microbiol 78:4271–4280. CrossRefGoogle Scholar
  38. Rocha RP, Melo EC, Radunz LL (2011) Influence of drying process on the quality of medicinal plants: a review. J Med Plants Res 5:7076–7084. CrossRefGoogle Scholar
  39. Sá RA, Gomes FS, Napoleão TH, Santos NDL, Melo CML, Gusmão NB, Coelho LCBB, Paiva PMG, Bieber LW (2009) Antibacterial and antifungal activities of Myracrodruon urundeuva heartwood. Wood Sci Technol 43:85–95. CrossRefGoogle Scholar
  40. Saminathan M, Sieo CC, Abdullah N, Wong CMVL, Ho YW (2015) Effects of condensed tannin fractions of different molecular weights from a Leucaena leucocephala hybrid on in vitro methane production and rumen fermentation. J Sci Food Agric 95:2742–2749. CrossRefGoogle Scholar
  41. Santos MVF d, Lira M de A, Dubeux Junior JCB et al (2010) Potential of Caatinga forage plants in ruminant feeding. Rev Bras Zootec 39:204–215. CrossRefGoogle Scholar
  42. Santos KC, Magalhães ALR, Silva DKA, Araújo GGL, Fagundes GM, Ybarra NG, Abdalla AL (2017) Nutritional potential of forage species found in Brazilian semiarid region. Livest Sci 195:118–124. CrossRefGoogle Scholar
  43. Silva TS, Freire EMX (2010) Abordagem etnobotânica sobre plantas medicinais citadas por populações do entorno de uma unidade de conservação da caatinga do Rio Grande do Norte, Brasil. Rev Bras Plantas Med 12:427–435. CrossRefGoogle Scholar
  44. Silva AM d A, da Costa RG, Pereira Filho JM, Bakke IA, Lôbo KM d S, Lira Filho GE, da Nóbrega GH (2010) Nutritional value of silk flower hay for lambs. Rev Bras Zootec 39:2739–2743. CrossRefGoogle Scholar
  45. Soliva CR, Zeleke AB, Clément C, Hess HD, Fievez V, Kreuzer M (2008) In vitro screening of various tropical foliages, seeds, fruits and medicinal plants for low methane and high ammonia generating potentials in the rumen. Anim Feed Sci Technol 147:53–71. CrossRefGoogle Scholar
  46. Viana GSB, Bandeira MAM, Moura LC, Souza-Filho MVP, Matos FJA, Ribeiro RA (1997) Analgesic and antiinflammatory effects of the tannin fraction from Myracrodruon urundeuva Fr. All. Phyther Res 11:118–122.<118::AID-PTR38>3.0.CO;2-J CrossRefGoogle Scholar
  47. Wyrepkowski CC, Da Costa DLMG, Sinhorin AP et al (2014) Characterization and quantification of the compounds of the ethanolic extract from caesalpinia ferrea stem bark and evaluation of their mutagenic activity. Molecules 19:16039–16057. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Brena Santos Oliveira
    • 1
  • Luiz Gustavo Ribeiro Pereira
    • 2
    Email author
  • Jose Augusto Gomes Azevêdo
    • 1
  • João Paulo Pacheco Rodrigues
    • 3
  • Gherman Garcia Leal de Araújo
    • 4
  • Rogerio Martins Maurício
    • 5
  • Fernanda Samarini Machado
    • 2
  • Mariana Magalhães Campos
    • 2
  • Tássia Ludmila Teles Martins
    • 6
  • Thierry Ribeiro Tomich
    • 2
  1. 1.Department of Agrarian and Environmental SciencesUniversidade Estadual de Santa CruzIlhéusBrazil
  2. 2.Embrapa Gado de LeiteJuiz de ForaBrazil
  3. 3.Institute of Studies of the Humid TropicUniversidade Federal do Sul e Sudeste do ParáXinguaraBrazil
  4. 4.Embrapa SemiáridoPetrolinaBrazil
  5. 5.Bioengineering DepartmentUniversidade Federal de São João Del-ReiSão João Del-ReiBrazil
  6. 6.Department of Animal ScienceUniversidade Federal de Minas GeraisBelo HorizonteBrazil

Personalised recommendations