Effects of black seed oil and Ferula elaeochytris supplementation on ruminal fermentation as tested in vitro with the rumen simulation technique (Rusitec)
F. Klevenhusen A D E , K. Deckardt A E , Ö. Sizmaz B , S. Wimmer A , A. Muro-Reyes C , R. Khiaosa-ard A , R. Chizzola A and Q. Zebeli A
+ Author Affiliations
- Author Affiliations
A Institute of Animal Nutrition and Functional Plant Compounds, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria.
B Department of Animal Nutrition and Nutritional Diseases, Faculty of Veterinary Medicine, Ankara, Turkey.
C Faculty of Veterinary Medicine and Zootechnique, Autonomous University of Zacatecas, Zacatecas, Mexico.
D Corresponding author. Email: fenja.klevenhusen@vetmeduni.ac.at
E F.K. and K.D. contributed equally to this work.
Animal Production Science 55(6) 736-744 https://doi.org/10.1071/AN13332
Submitted: 6 December 2013 Accepted: 13 March 2014 Published: 20 May 2014
Abstract
Plant bioactive compounds are currently viewed as possible feed additives in terms of methane mitigation and improvement of ruminal fermentation. A range of analyses, including the botanical characterisation, chemical composition and in vitro efficiency, have to be conducted before testing the compounds in vivo. Therefore, the aims of this study were (1) to identify the main bioactive components of black seed (Nigella sativa) oil (BO) and of the root powder of Ferula elaeochytris (FE), and (2) to investigate their effects on ruminal fermentation in vitro, when supplemented in different dosages to a diet (1 : 1, forage : concentrate), using the rumen simulation technique (Rusitec). Main compounds of BO were thymoquinone and p-cymene and α-pinene in FE. Supplementation of the diet with BO and FE did not affect concentration of volatile fatty acids but ammonia concentrations decreased with both supplements (P < 0.001). No effects of supplements on protozoal counts were detected but in vitro disappearance of DM and organic matter tended to increase with 50 mg/L FE (P < 0.1), compared with the control.
Additional keywords: essential oils, methane, volatile fatty acids.
References
Adams RP (2007) ‘Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy.’ 4th edn. (Allured Publishing Corporation: Carol Stream, IL)Ahmad A, Husain A, Mujeeb M, Khan SA, Najmi AK, Siddique NA, Damanhouri ZA, Anwar F (2013) A review on therapeutic potential of Nigella sativa: a miracle herb. Asian Pacific Journal of Tropical Biomedicine 3, 337–352.
| A review on therapeutic potential of Nigella sativa: a miracle herb.Crossref | GoogleScholarGoogle Scholar | 23646296PubMed |
AOAC International (1997) AOAC Official Method 973.18, fiber (acid detergent) and lignin (H2SO4) in animal feed, first Action 1973, final Action 1977. In ‘Official methods of analysis of AOAC International’. 16th edn. pp. 28–29. (AOAC International: Arlington, VA)
Başer KHC, Özek T, Demirci B, Kürkçüoğlu M, Aytaç Z, Duman H (2000) Composition of the essential oils of Zosima absinthifolia (Vent.) Link and Ferula elaeochytris Korovin from Turkey. Flavour and Fragrance Journal 15, 371–372.
| Composition of the essential oils of Zosima absinthifolia (Vent.) Link and Ferula elaeochytris Korovin from Turkey.Crossref | GoogleScholarGoogle Scholar |
Beauchemin KA, McGinn SM, Petit HV (2007) Methane abatement strategies for cattle: lipid supplementation of diets. Canadian Journal of Animal Science 87, 431–440.
| Methane abatement strategies for cattle: lipid supplementation of diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSrsbnF&md5=3e7418ad0c9a1f55d00252c262da8160CAS |
Beauchemin KA, Kreuzer M, O’Mara F, McAllister TA (2008) Nutritional management for enteric methane abatement: a review. Australian Journal of Experimental Agriculture 48, 21–27.
| Nutritional management for enteric methane abatement: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVGn&md5=26636171128f28fd501de1857924926bCAS |
Benchaar C, Greathead H (2011) Essential oils and opportunities to mitigate enteric methane emissions from ruminants. Animal Feed Science and Technology 166–167, 338–355.
| Essential oils and opportunities to mitigate enteric methane emissions from ruminants.Crossref | GoogleScholarGoogle Scholar |
Benchaar C, Petit HV, Berthiaume R, Ouellet DR, Chiquette J, Chouinard PY (2007a) 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. Journal of Dairy Science 90, 886–897.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1SmsL4%3D&md5=78c570e609d1a28a6c72360834043918CAS | 17235165PubMed |
Benchaar C, Chaves AV, Fraser GR, Wang Y, Beauchemin KA, McAllister TA (2007b) Effects of essential oils and their components on in vitro rumen microbial fermentation. Canadian Journal of Animal Science 87, 413–419.
| Effects of essential oils and their components on in vitro rumen microbial fermentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSrsbnJ&md5=e5f0c1d1e51a6820b4c71d5647411898CAS |
Benchaar C, Calsamiglia S, Chaves AV, Fraser GR, Colombatto D, McAllister TA, Beauchemin KA (2008) A review of plant-derived essential oils in ruminant nutrition and production. Animal Feed Science and Technology 145, 209–228.
| A review of plant-derived essential oils in ruminant nutrition and production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVKrsLc%3D&md5=788311108a5ba25e28286f8ee2af8e5aCAS |
Broudiscou LP, Cornu A, Rouzeau A (2007) In vitro degradation of 10 mono- and sesquiterpenes of plant origin by caprine rumen micro-organisms. Journal of the Science of Food and Agriculture 87, 1653–1658.
| In vitro degradation of 10 mono- and sesquiterpenes of plant origin by caprine rumen micro-organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntV2ksbg%3D&md5=fc04b9d85f01c3bbf753b12a73d78e09CAS |
Burits M, Bucar F (2000) Antioxidant activity of Nigella sativa essential oil. Phytotherapy Research 14, 323–328.
| Antioxidant activity of Nigella sativa essential oil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsVSqtbY%3D&md5=e72842b8d3dc9a562647cc9a06ebe08bCAS | 10925395PubMed |
Busquet M, Calsamiglia S, Ferret A, Carro MD, Kamel C (2005) Effect of garlic oil and four of its compounds on rumen microbial fermentation. Journal of Dairy Science 88, 4393–4404.
| Effect of garlic oil and four of its compounds on rumen microbial fermentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlSqtr3O&md5=fedede429424ddd67bd3ff388b157967CAS | 16291631PubMed |
Busquet M, Calsamiglia S, Ferret A, Kamel C (2006) Plant extracts affect in vitro rumen microbial fermentation. Journal of Dairy Science 89, 761–771.
| Plant extracts affect in vitro rumen microbial fermentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWrtLk%3D&md5=963ba3b95e3fbd9a024dabd18ff5f571CAS | 16428643PubMed |
Calsamiglia S, Busquet M, Cardozo PW, Castillejos L, Ferret A (2007) Invited review: essential oils as modifiers of rumen microbial fermentation. Journal of Dairy Science 90, 2580–2595.
| Invited review: essential oils as modifiers of rumen microbial fermentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvFOisLg%3D&md5=1aed74b5e3f00c4474ac7a3fef211389CAS | 17517698PubMed |
Canogullari S, Baylan M, Copur G, Sahin A (2009) Effects of dietary Ferula elaeochytris root powder on the growth and reproductive performance of Japanese quail (Coturnix coturnix japonica): it is not recommended in a breeder diet. Archiv fur Geflugelkunde 73, 56–60.
Cardozo PW, Calsamiglia S, Ferret A, Kamel C (2004) Effects of natural plant extracts on ruminal protein degradation and fermentation profiles in continuous culture. Journal of Animal Science 82, 3230–3236.
Cardozo PW, Calsamiglia S, Ferret A, Kamel C (2005) Screening for the effects of natural plant extracts at different pH on in vitro rumen microbial fermentation of a high-concentrate diet for beef cattle. Journal of Animal Science 83, 2572–2579.
Castillejos L, Calsamiglia S, Ferret A (2006) Effect of essential oil active compounds on rumen microbial fermentation and nutrient flow in in vitro systems. Journal of Dairy Science 89, 2649–2658.
| Effect of essential oil active compounds on rumen microbial fermentation and nutrient flow in in vitro systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmsVOltLg%3D&md5=09be1bff05cfb57d310d440aa530a3c6CAS | 16772584PubMed |
Castillejos L, Calsamiglia S, Martín-Tereso J, Ter Wijlen H (2008) In vitro evaluation of effects of ten essential oils at three doses on ruminal fermentation of high concentrate feedlot-type diets. Animal Feed Science and Technology 145, 259–270.
| In vitro evaluation of effects of ten essential oils at three doses on ruminal fermentation of high concentrate feedlot-type diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVKrsbs%3D&md5=78150608faed1f0cea83ee184862112eCAS |
Chaves AV, He ML, Yang WZ, Hristov AN, McAllister TA, Benchaar C (2008) Effects of essential oils on proteolytic, deaminative and methanogenic activities of mixed ruminal bacteria. Canadian Journal of Animal Science 88, 117–122.
| Effects of essential oils on proteolytic, deaminative and methanogenic activities of mixed ruminal bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtFOrsL0%3D&md5=5bdcb21bd4724156d665efd7cbc00dc2CAS |
Crane A, Nelson WO, Brown RE (1957) Effects of D-limonene and α-D-pinene on in vitro carbohydrate dissimilation and methane formation by rumen bacteria. Journal of Dairy Science 40, 1317–1323.
| Effects of D-limonene and α-D-pinene on in vitro carbohydrate dissimilation and methane formation by rumen bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1cXltFartQ%3D%3D&md5=07fba97fc9cf9bf051ab4570e0b21bf0CAS |
Evans JD, Martin SA (2000) Effects of thymol on ruminal microorganisms. Current Microbiology 41, 336–340.
| Effects of thymol on ruminal microorganisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXot1Gis74%3D&md5=76181ebd33956b90eaf711b019c2a0c2CAS | 11014870PubMed |
Flachowsky G, Lebzien C (2012) Effects of phytogenic substances on rumen fermentation and methane emissions: a proposal for a research process. Animal Feed Science and Technology 176, 70–77.
| Effects of phytogenic substances on rumen fermentation and methane emissions: a proposal for a research process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyksbzK&md5=5c831d81a6bf4a57bf0c08b28810b7bbCAS |
Goel G, Makkar HPS, Becker K (2008) Changes in microbial community structure, methanogenesis and rumen fermentation in response to saponin-rich fractions from different plant materials. Journal of Applied Microbiology 105, 770–777.
| Changes in microbial community structure, methanogenesis and rumen fermentation in response to saponin-rich fractions from different plant materials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1amtbnK&md5=4f202ecd7cd153b370c1b78bbbb9c000CAS | 18422554PubMed |
Habeeb AAM, El-Tarabany AA (2012) Effect of Nigella sativa or Curcumin on daily body weight gain, feed intake and some physiological functions in growing Zaraibi goats during hot summer season. Arab Journal of Nuclear Science and Applications 45, 238–249.
Haider V (2004) Untersuchungen zum Verhalten von Monoterpenen im Mageninhalt des Rindes. DVM-thesis, University of Veterinary Medicine, Vienna.
Hart KJ, Yanez-Ruiz DR, Duval SM, McEwan NR, Newbold CJ (2008) Plant extracts to manipulate rumen fermentation. Animal Feed Science and Technology 147, 8–35.
| Plant extracts to manipulate rumen fermentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ejtLzF&md5=db539d9810573eb4c3aae2fd79b44ea1CAS |
Hook SE, Wright A-DG, McBride BW (2010) Methanogens: methane producers of the rumen and mitigation strategies. Archea Article ID 945785, online only.
Jerković I, Mastelić J, Milos M (2001) The impact of both the season of collection and drying on the volatile constituents of Origanum vulgare L. ssp. hirtum grown wild in Croatia. International Journal of Food Science & Technology 36, 649–654.
| The impact of both the season of collection and drying on the volatile constituents of Origanum vulgare L. ssp. hirtum grown wild in Croatia.Crossref | GoogleScholarGoogle Scholar |
Kilic U, Boga M, Gorgulu M, Şahan Z (2011) The effects of different compounds in some essential oils on in vitro gas production. Journal of Animal and Feed Sciences 20, 626–636.
Klevenhusen F, Muro-Reyes A, Khiaosa-ard R, Metzler-Zebeli BU, Zebeli Q (2012) A meta-analysis of the effects of chemical composition of incubated diet and bioactive compounds on in vitro ruminal fermentation. Animal Feed Science and Technology 176, 61–69.
| A meta-analysis of the effects of chemical composition of incubated diet and bioactive compounds on in vitro ruminal fermentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyktLjO&md5=caec03790a01c362030b75aac07ddbadCAS |
Kose EO, Akta Ö, Deniz IG, Sarikürkçü C (2010) Chemical composition, antimicrobial and antioxidant activity of essential oil of endemic Ferula lycia Boiss. Journal of Medicinal Plants Research 4, 1698–1703.
LfL (2011) ‘Bayerische Landesanstalt für Landwirtschaft, Gruber Tabelle zur Fütterung der Milchkühe, Zuchtrinder, Schafe, Ziegen (34. Auflage).’ (Medienhaus Kastner AG: Wolnzach, Germany)
Lila ZA, Mohammed N, Kanda S, Kamada T, Itabashi H (2003) Effect of sarsaponin on ruminal fermentation with particular reference to methane production in vitro. Journal of Dairy Science 86, 3330–3336.
| Effect of sarsaponin on ruminal fermentation with particular reference to methane production in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotFOjtrY%3D&md5=865a032d6ac77a26a7c17c270e211b01CAS | 14594252PubMed |
Macheboeuf D, Morgavi DP, Papon Y, Mousset JL, Arturo-Schaan M (2008) Dose-response effects of essential oils on in vitro fermentation activity of the rumen microbial population. Animal Feed Science and Technology 145, 335–350.
| Dose-response effects of essential oils on in vitro fermentation activity of the rumen microbial population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVKrtrs%3D&md5=f0003bb0ef143a53fb0ed65cb66ff5f5CAS |
Malecky M, Broudiscou LP (2009) Disappearance of nine monoterpenes exposed in vitro to the rumen microflora of dairy goats: effects of inoculum source, redox potential, and vancomycin. Journal of Animal Science 87, 1366–1373.
| Disappearance of nine monoterpenes exposed in vitro to the rumen microflora of dairy goats: effects of inoculum source, redox potential, and vancomycin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFKis7k%3D&md5=16fe0d267f9a4ffee0107b1f7ccc3367CAS | 19098243PubMed |
Malecky M, Broudiscou LP, Schmidely P (2009) Effects of two levels of monoterpene blend on rumen fermentation, terpene and nutrient flows in the duodenum and milk production in dairy goats. Animal Feed Science and Technology 154, 24–35.
| Effects of two levels of monoterpene blend on rumen fermentation, terpene and nutrient flows in the duodenum and milk production in dairy goats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1aisLbN&md5=f841fcb135488e2bc9b4f73bfbe487b5CAS |
McDougall EI (1948) Studies on ruminant saliva. 1. The composition and output of sheep’s saliva. Biochemical Journal 43, 99–109.
McLafferty FW (1989) ‘Registry of mass spectral data.’ 5th edn. (John Wiley & Sons: New York)
Moss AR, Jouany JP, Newbold J (2000) Methane production by ruminants: its contribution to global warming. Annales de Zootechnie 49, 231–253.
| Methane production by ruminants: its contribution to global warming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt12msrk%3D&md5=5c16f7d8f4d5fcbaada5a760b2da87f6CAS |
Oh HK, Sakai T, Jones MB, Longhurst WM (1967) Effect of various essential oils isolated from Douglas fir needles upon sheep and deer rumen microbial activity. Applied and Environmental Microbiology 15, 777–784.
Piras A, Rosab A, Marongiua B, Porceddaa S, Falconieric D, Dessìb MA, Ozcelikd B, Kocae U (2013) Chemical composition and in vitro bioactivity of the volatile and fixed oils of Nigella sativa L. extracted by supercritical carbon dioxide. Industrial Crops and Products 46, 317–323.
| Chemical composition and in vitro bioactivity of the volatile and fixed oils of Nigella sativa L. extracted by supercritical carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltVSit7w%3D&md5=7504ed6180ab5d6da30e3162111003c4CAS |
Poulose AJ, Croteau R (1978) Biosynthesis of aromatic monoterpenes: conversion of γ-terpinene to p-cymene and thymol in Thymus vulgaris L. Archives of Biochemistry and Biophysics 187, 307–314.
| Biosynthesis of aromatic monoterpenes: conversion of γ-terpinene to p-cymene and thymol in Thymus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhs1Kku74%3D&md5=11a353fdb47eed8548e3e874703cca2dCAS | 666313PubMed |
Rasoul-Amini S, Fotooh-Abadi E, Ghasemi Y (2011) Biotransformation of monoterpenes by immobilized microalgae. Journal of Applied Phycology 23, 975–981.
| Biotransformation of monoterpenes by immobilized microalgae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVCrsb7E&md5=800e022f9554aeea0a9fbf689da48cb8CAS |
Russell JB (1998) The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production. Journal of Dairy Science 81, 3222–3230.
| The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVahuw%3D%3D&md5=da22bc2aadb7406092bc4b396bc889fbCAS | 9891267PubMed |
Sahebkar A, Iranshahi M (2010) Biological activities of essential oils from the genus Ferula (Apiaceae). Asian Biomedicine 4, 835–847.
Sahinler S, Sahin A, Gorgulu O (2005) Ferula eleaochytris powder effect in layer diet on feed intake and some egg parameters using a multivariate analysis method for repeated measures. Journal of Applied Animal Research 28, 29–33.
| Ferula eleaochytris powder effect in layer diet on feed intake and some egg parameters using a multivariate analysis method for repeated measures.Crossref | GoogleScholarGoogle Scholar |
Soliva CR, Hess HD (2007) Measuring methane emission of ruminants by in vitro and in vivo techniques. In ‘Measuring methane production from ruminants’. (Eds HPS Makkar, PE Vercoe) pp. 13–15. (Springer: Dordrecht, The Netherlands)
Soliva CR, Meile L, Cieslak A, Kreuzer M, Machmüller A (2004) Rumen simulation technique study on the interactions of dietary lauric and myristic acid supplementation in suppressing ruminal methanogenesis. The British Journal of Nutrition 92, 689–700.
| Rumen simulation technique study on the interactions of dietary lauric and myristic acid supplementation in suppressing ruminal methanogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovFCqsLc%3D&md5=15567164c93911590e40e87242659480CAS | 15522139PubMed |
Soliva CR, Amelchanka SL, Duval SM, Kreuzer M (2011) Ruminal methane inhibition potential of various pure compounds in comparison with garlic oil as determined with a rumen simulation technique (Rusitec). The British Journal of Nutrition 106, 114–122.
| Ruminal methane inhibition potential of various pure compounds in comparison with garlic oil as determined with a rumen simulation technique (Rusitec).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosVOmu7k%3D&md5=b65bffbe4596b1c3a532e1fed5e773eeCAS | 21554814PubMed |
Suter B, Grob K, Pacciarelli B (1997) Determination of fat content and fatty acid composition through 1-min transesterification in the food sample; principles. Zeitschrift für Lebensmittel-Untersuchung und -Forschung A 204, 252–258.
VDLUFA (2007) ‘Methodenbuch: Die Chemische Untersuchung von Futtermitteln. Band III. Handbuch der Landwirtschaftlichen Versuchs- und Untersuchungsmethodik (VDLUFA-Methodenbuch.’ (VDLUFA-Verlag: Darmstadt, Germany)
Wina E, Muetzel S, Becker K (2006) Effects of daily and interval feeding of Sapindus rarak saponins on protozoa, rumen fermentation parameters and digestibility in sheep. Asian-Australasian Journal of Animal Sciences 19, 1580–1587.
