Methane concentration, ruminal fermentation, digestibility, and microbial protein synthesis of beef cattle with the addition of various types of seaweed from West Java-Banten with different levels in the ration (in vitro)

Rahmat Hidayat; Roni Pazla; Asmuddin Natsir; Nurzainah Ginting; Urip Rosani

Keywords:

Abstract

The environmental health of the rumen plays a crucial role in ruminant livestock productivity. One of the byproducts of rumen fermentation is methane gas, which is a significant contributor to greenhouse emissions. The global warming potential of methane is approximately 23 times greater than that of CO₂. Seaweed is recognized as a potential feed additive that can support microbial growth and suppress methane production. This study aimed to investigate the effects of seaweed supplementation on fermentability, digestibility, and methane production in beef cattle through an in vitro approach. A completely randomized factorial design was used, incorporating four different seaweed species at varying supplementation levels, with five replications. The findings demonstrated that the level of seaweed supplementation significantly influenced (p<0.05) fermentability, digestibility, and methane gas concentration. Additionally, the type of seaweed had a notable effect (p<0.05) on digestibility, ammonia concentration, and methane level. Different compounds were identified among the seaweed types via metabolomic analysis. Supplementation with Gracilarian spp., Gelidium spp., and Sargassum spp. improved dry matter digestibility while reducing the ammonia concentration. However, variations in seaweed species did not significantly alter total volatile fatty acid production. Supplementation with Eucheuma spp., Gracilarian spp., and Sargassum spp. lowered the methane concentration. A supplementation level of 15% for Sargassum spp. is suitable for methane mitigation.
References
1. Afzalani, A., Muthalib, R. A., Dianita, R., Hoesni, F., Raguati, R., & Musnandar, E. (2021). Evaluasi suplementasi Indigofera zollingeriana sebagai sumber green protein concentrate terhadap produksi gas metan, Amonia dan sintesis protein mikroba rumen. Jurnal Ilmiah Universitas Batanghari Jambi, 21(3), 1455–1458.
2. Alvarez-Hess, P. S., Jacobs, J. L., Kinley, R. D., Roque, B. M., Neachtain, A. S. O., Chandra, S., & Williams, S. R. O. (2023). Twice daily feeding of canola oil steeped with Asparagopsis armata reduced methane emissions of lactating dairy cows. Animal Feed Science and Technology, 297. https://doi.org/10.1016/j.anifeedsci.2023.115579
3. Andreen, D. M., Billman, E. D., Brito, A. F., & Soder, K. J. (2023). Effect of incremental amounts of Asparagopsis taxiformis on ruminal fermentation and methane production in continuous culture with orchardgrass herbage. Animal Feed Science and Technology, 299. https://doi.org/10.1016/j.anifeedsci.2023.115641
4. AOAC. (2005). Official Methods of Analysis of AOAC International, 18th edition. Gaithersburg (Maryland): AOAC International. https://www.researchgate.net/publication/292783651_AOAC_2005
5. Baek, I. K., Maeng, W. J., Lee, S. H., Lee, H. G., Lee, S. R., Ha, J. K., Lee, S. S., & Hwang, J. H. (2004). Effects of the Brown Seaweed Residues Supplementation on In Vitro Fermentation and Milk Production and Composition of Lactating Dairy Cows. Journal of Animal Science and Technology, 46(3), 373–386. https://doi.org/10.5187/jast.2004.46.3.373
6. Beck, M. R., Al-Marashdeh, O., & Gregorini, P. (2019). Low levels of a seaweed (Ecklonia radiata) extract alter in vitro fermentation products but not in combination with quebracho (Schinopsis quebracho-colorado) tannins. Applied Animal Science, 35(5), 476–481. https://doi.org/10.15232/aas.2019-01892
7. Belanche, A., Jones, E., Parveen, I., & Newbold, C. J. (2016). A metagenomics approach to evaluate the impact of dietary supplementation with Ascophyllum nodosum or Laminaria digitata on rumen function in Rusitec fermenters. Frontiers in Microbiology, 7(MAR). https://doi.org/10.3389/fmicb.2016.00299
8. Cherry, P., Yadav, S., O’Callaghan, C., Popper, Z. A., Ross, R. P., McSorley, E. M., Allsopp, P. J., & Stanton, C. (2016). In-vitro fermentation of whole seaweed and a polysaccharide-rich extract derived from the edible red seaweed Palmaria palmate . Proceedings of the Nutrition Society, 75(OCE2), E57. https://doi.org/10.1017/s0029665116000471
9. Choi, Y., Lee, S. J., Kim, H. S., Eom, J. S., Jo, S. U., Guan, L. L., Seo, J., Kim, H., Lee, S. S., & Lee, S. S. (2021). Effects of seaweed extracts on in vitro rumen fermentation characteristics, methane production, and microbial abundance. Scientific Reports, 11(1). https://doi.org/10.1038/s41598-021-03356-y
10. Conway, E. J., & O’malley, E. (1942). Microdiffusion methods. Ammonia and urea using buffered absorbents (revised methods for ranges greater than 10μg. N). Biochemical Journal, 36(7–9), 655.
11. Cottle, D. J., Nolan, J. V., & Wiedemann, S. G. (2011). Ruminant enteric methane mitigation: A review. Animal Production Science, 51(6), 491–514. https://doi.org/10.1071/AN10163
12. Cruywagen, C. W., Taylor, S., Beya, M. M., & Calitz, T. (2015). The effect of buffering dairy cow diets with limestone, calcareous marine algae, or sodium bicarbonate on ruminal pH profiles, production responses, and rumen fermentation. Journal of Dairy Science, 98(8), 5506–5514. https://doi.org/10.3168/jds.2014-8875
13. Eikanger, K. S., Kjær, S. T., Dörsch, P., Iwaasa, A. D., Alemu, A. W., Schei, I., Pope, P. B., Hagen, L. H., & Kidane, A. (2024). Asparagopsis taxiformis inclusion in grass silage-based diets fed to Norwegian red dairy cows: Effects on ruminal fermentation, milk yield, and enteric methane emission. Livestock Science, 285. https://doi.org/10.1016/j.livsci.2024.105495
14. Fearon, A. L., Felix, A., & Sapra, V. T. (1990). Chemical Composition and In Vitro Dry Matter and Organic Matter Digestibility of Triticale Forage. Journal of Agronomy and Crop Science, 164(4), 262–270. https://doi.org/10.1111/j.1439-037X.1990.tb00816.x
15. Félix, R., Dias, P., Félix, C., Cerqueira, T., Andrade, P. B., Valentão, P., & Lemos, M. F. L. (2021). The biotechnological potential of Asparagopsis armata: What is known of its chemical composition, bioactivities and current market? Algal Research, 60. https://doi.org/10.1016/j.algal.2021.102534
16. Gerber, P. J., Steinfeld, H., Henderson, B., Mottet, A., Opio, C., Dijkman, J., Falcucci, A., & Tempio, G. (2013). Tackling climate change through livestock – A global assessment of emissions and mitigation opportunities.
17. Glasson, C. R. K., Kinley, R. D., de Nys, R., King, N., Adams, S. L., Packer, M. A., Svenson, J., Eason, C. T., & Magnusson, M. (2022). Benefits and risks of including the bromoform containing seaweed Asparagopsis in feed for the reduction of methane production from ruminants. Algal Research, 64. https://doi.org/10.1016/j.algal.2022.102673
18. González-Meza, G. M., Elizondo-Luevano, J. H., Cuellar-Bermudez, S. P., Sosa-Hernández, J. E., Iqbal, H. M. N., Melchor-Martínez, E. M., & Parra-Saldívar, R. (2023). New Perspective for Macroalgae-Based Animal Feeding in the Context of Challenging Sustainable Food Production. Plants, 12(20), 3609.
19. Hamid, S. S., Wakayama, M., Ichihara, K., Sakurai, K., Ashino, Y., Kadowaki, R., Soga, T., & Tomita, M. (2019). Metabolome profiling of various seaweed species discriminates between brown, red, and green algae. Planta, 249, 1921–1947. https://doi.org/10.1007/s00425-019-03134-1
20. Handique, B., Singh, P., Verma, A. K., & Yengkhom, R. (2023). The effect of seaweed formulations on in vitro fermentation, nutrient utilization and growth performance in crossbred calves. Veterinarski Arhiv, 93(5), 513–524. https://doi.org/10.24099/vet.arhiv.1858
21. Hernaman, I., Ayuningsih, B., Ramdani, D., Islami, R. Z., Octaviana, S., Aviana, I., Rahayu, G., Salimah, A. B., Rosani, U., & Budiman, A. (2024). In vitro study of ration containing corncobs soaked by rice hull ash filtrate. Adv. Anim. Vet. Sci, 12(8), 1525–1531.
22. Hernaman, I., Rochana, A., Andayaningsih, P., Suryani, Y., & Ramdhani, M. A. (2015). Evaluation of in Vitro Digestibility of Dried Matter and Organic Matter of Solid Waste of Bioethanol Fermentation from Cassava by Trichoderma Viride and Saccharomyces Cerevisiae. Journal of Asian Scientific Research, 5(11), 513–521. https://doi.org/10.18488/journal.2/2015.5.11/2.11.513.521
23. Hidayah, N., Noviandi, C. T., Astuti, A., & Kustantinah, K. (2023). Chemical composition and in vitro rumen fermentation characteristics of various tropical seaweeds. Journal of Advanced Veterinary and Animal Research, 10(4), 751–762. https://doi.org/10.5455/javar.2023.j731
24. Hindratiningrum, N., Bata, M., & Santosa, S. A. (2011). Produk fermentasi rumen dan produksi protein mikroba sapi lokal yang diberi pakan jerami amoniasi dan beberapa bahan pakan sumber energi. Jurnal Agripet, 11(2), 29–34.
25. Hong, Z. S., Kim, E. J., Jin, Y. C., Lee, J. S., Choi, Y. J., & Lee, H. G. (2015). Effects of supplementing brown seaweed by-products in the diet of Holstein cows during transition on ruminal fermentation, growth performance and endocrine responses. Asian-Australasian Journal of Animal Sciences, 28(9), 1296–1302. https://doi.org/10.5713/ajas.15.0235
26. Hristov, A. N., Callaway, T. R., Lee, C., & Dowd, S. E. (2012). Rumen bacterial, archaeal, and fungal diversity of dairy cows in response to ingestion of lauric or myristic acid. Journal of Animal Science, 90(12), 4449–4457. https://doi.org/10.2527/jas.2011-4624
27. Indugu, N., Narayan, K., Stefenoni, H. A., Hennessy, M. L., Vecchiarelli, B., Bender, J. S., Shah, R., Dai, G., Garapati, S., Yarish, C., Welchez, S. C., Räisänen, S. E., Wasson, D., Lage, C., Melgar, A., Hristov, A. N., & Pitta, D. W. (2024). Microbiome-informed study of the mechanistic basis of methane inhibition by Asparagopsis taxiformis in dairy cattle. MBio, 15(8), e00782-24. https://doi.org/10.1128/mbio.00782-24
28. Kannan, G., Terrill, T. H., Kouakou, B., & Lee, J. H. (2019). Dietary brown seaweed extract supplementation in small ruminants. In Medicinal Plants: From Farm to Pharmacy (pp. 291–312). Springer International Publishing. https://doi.org/10.1007/978-3-030-31269-5_13
29. Kinley, R. D., & Fredeen, A. H. (2015). In vitro evaluation of feeding North Atlantic stormtoss seaweeds on ruminal digestion. Journal of Applied Phycology, 27(6), 2387–2393. https://doi.org/10.1007/s10811-014-0487-z
30. Kinley, R. D., Vucko, M. J., Machado, L., & Tomkins, N. W. (2016). In Vitro Evaluation of the Antimethanogenic Potency and Effects on Fermentation of Individual and Combinations of Marine Macroalgae. American Journal of Plant Sciences, 07(14), 2038–2054. https://doi.org/10.4236/ajps.2016.714184
31. Knapp, J. R., Laur, G. L., Vadas, P. A., Weiss, W. P., & Tricarico, J. M. (2014). Invited review: Enteric methane in dairy cattle production: Quantifying the opportunities and impact of reducing emissions. Journal of Dairy Science, 97(6), 3231–3261. https://doi.org/10.3168/jds.2013-7234
32. Leelavathi, M. S., Vani, S., Centre, E., & Road, M. (2015). Comparitive Analysis of Phytochemical Compounds of Marine Algae Isolated From Gulf of Mannar. World Journal of Pharmacy and Pharmaceutical Sciences, 4(05), 640–654.
33. Lopez-Santamarina, A., Sinisterra-Loaiza, L., Mondragón-Portocarrero, A., Ortiz-Viedma, J., Cardelle-Cobas, A., Abuín, C. M. F., & Cepeda, A. (2023). Potential prebiotic effect of two Atlantic whole brown seaweeds, Saccharina japonica and Undaria pinnatifida, using in vitro simulation of distal colonic fermentation. Frontiers in Nutrition, 10, 1170392. https://doi.org/10.3389/fnut.2023.1170392
34. Maia, M. R. G., Fonseca, A. J. M., Oliveira, H. M., Mendonça, C., & Cabrita, A. R. J. (2016). The potential role of seaweeds in the natural manipulation of rumen fermentation and methane production. Scientific Reports, 6(1), 32321. https://doi.org/10.1038/srep32321
35. Mansuit, H., Samsuri, M. D. C., Sipaut, C. S., Yee, C. F., Yasir, S. M., & Mansa, R. (2015). Effect of varying acid hydrolysis condition in Gracilaria Sp. fermentation using Sasad. IOP Conference Series: Materials Science and Engineering, 78(1), 12004. https://doi.org/10.1088/1757-899X/78/1/012004
36. Maranatha, G., Fattah, S., Sobang, Y. U. L., Yunus, M., & Henuk, Y. L. (2020). Digestibility of dry matter and organic matter and the in vitro rumen parameters of complete feed from fermented corn cobs and moringa (Moringa oleifera) leaves meal. IOP Conference Series: Earth and Environmental Science, 454(1), 12062. https://doi.org/10.1088/1755-1315/454/1/012062
37. Markham, R. (1942). A steam distillation apparatus suitable for micro-Kjeldahl analysis. Biochemical Journal, 36(10–12), 790.
38. Matthews, C., Crispie, F., Lewis, E., Reid, M., O’Toole, P. W., & Cotter, P. D. (2019). The rumen microbiome: a crucial consideration when optimising milk and meat production and nitrogen utilisation efficiency. In Gut Microbes (Vol. 10, Issue 2, pp. 115–132). https://doi.org/10.1080/19490976.2018.1505176
39. Mihaila, A. A., Glasson, C. R. K., Lawton, R., Muetzel, S., Molano, G., & Magnusson, M. (2022). New temperate seaweed targets for mitigation of ruminant methane emissions: an in vitro assessment. Applied Phycology, 3(1), 274–284. https://doi.org/10.1080/26388081.2022.2059700
40. Narvaez-Izquiedo, J., Fonseca-De La Hoz, J., Kannan, G., & Bohorquez-Herrera, J. (2024). Use of macroalgae as a nutritional supplement for sustainable production of ruminants: A systematic review and an insight on the Colombian Caribbean region. Algal Research, 77. https://doi.org/10.1016/j.algal.2023.103359
41. Özkan Gülzari, Ş., Lind, V., Aasen, I. M., & Steinshamn, H. (2019). Effect of supplementing sheep diets with macroalgae species on in vivo nutrient digestibility, rumen fermentation and blood amino acid profile. Animal, 13(12), 2792–2801. https://doi.org/10.1017/S1751731119001502
42. Plummer, D. T. (1978). An introduction to practical biochemistry. (No Title).
43. Pramono, A., Hadi, R. F., Sutrisno, J., & Cahyadi, M. (2019). The Effect of Protected Soybean Oil and Soybean Groats Base on in Vitro Dry Matter Digestibility, in Vitro Organic Matter Digestibility in the Rumen and Post Rumen. IOP Conference Series: Earth and Environmental Science, 347(1), 12016. https://doi.org/10.1088/1755-1315/347/1/012016
44. Qori’ah, A., Surono, S., & Sutrisno, S. (2016). Sintesis protein mikroba dan aktivitas selulolitik akibat penambahan level zeolit sumber nitrogen slow release pada glukosa murni secara in vitro. Jurnal Ilmu-Ilmu Peternakan (Indonesian Journal of Animal Science), 26(2), 1–7.
45. Ramadan, G., Fouda, W. A., Ellamie, A. M., & Ibrahim, W. M. (2020). Dietary supplementation of Sargassum latifolium modulates thermo-respiratory response, inflammation, and oxidative stress in bacterial endotoxin-challenged male Barki sheep. Environmental Science and Pollution Research, 27(27), 33863–33871. https://doi.org/10.1007/s11356-020-09568-5
46. Rira, M., Morgavi, D. P., Archimède, H., Marie-Magdeleine, C., Popova, M., Bousseboua, H., & Doreau, M. (2015). Potential of tannin-rich plants for modulating ruminal microbes and ruminal fermentation in sheep. Journal of Animal Science, 93(1), 334–347. https://doi.org/10.2527/jas.2014-7961
47. Rosani, U., Hernaman, I., Hidayat, R., & Hidayat, D. (2024). Fermentability, digestibility, and gas production of Garut sheep fed maize straw silage-based rationsnbalanced with rice bran and rice husks (in vitro). Journal of Animal and Feed Sciences. https://doi.org/10.22358/jafs/190441/2024
48. Roskam, E., Kirwan, S. F., Kenny, D. A., O’Donnell, C., O’Flaherty, V., Hayes, M., & Waters, S. M. (2022a). Effect of brown and green seaweeds on diet digestibility, ruminal fermentation patterns and enteric methane emissions using the rumen simulation technique. Frontiers in Animal Science, 3. https://doi.org/10.3389/fanim.2022.1021631
49. Roskam, E., Kirwan, S. F., Kenny, D. A., O’Donnell, C., O’Flaherty, V., Hayes, M., & Waters, S. M. (2022b). Effect of brown and green seaweeds on diet digestibility, ruminal fermentation patterns and enteric methane emissions using the rumen simulation technique. Frontiers in Animal Science, 3. https://doi.org/10.3389/fanim.2022.1021631
50. Saravanan, K., Duraisamy, S., Ramasamy, G., Kumarasamy, A., & Balakrishnan, S. (2018). Evaluation of the saccharification and fermentation process of two different seaweeds for an ecofriendly bioethanol production. Biocatalysis and Agricultural Biotechnology, 14, 444–449. https://doi.org/10.1016/j.bcab.2018.03.017
51. Shannon, E., Conlon, M., & Hayes, M. (2022a). The Prebiotic Effect of Australian Seaweeds on Commensal Bacteria and Short Chain Fatty Acid Production in a Simulated Gut Model. Nutrients, 14(10), 2163. https://doi.org/10.3390/nu14102163
52. Shannon, E., Conlon, M., & Hayes, M. (2022b). The Prebiotic Effect of Australian Seaweeds on Commensal Bacteria and Short Chain Fatty Acid Production in a Simulated Gut Model. Nutrients, 14(10), 2163. https://doi.org/10.3390/nu14102163
53. Shen, S., Yang, W., Li, L., Zhu, Y., Yang, Y., Ni, H., Jiang, Z., & Zheng, M. (2023). In vitro fermentation of seaweed polysaccharides and tea polyphenol blends by human intestinal flora and their effects on intestinal inflammation. Food and Function, 14(2), 1133–1147. https://doi.org/10.1039/d2fo03390a
54. Subbiah, V., Ebrahimi, F., Agar, O. T., Dunshea, F. R., Barrow, C. J., & Suleria, H. A. R. (2024). Author Correction: In vitro digestion and colonic fermentation of phenolic compounds and their antioxidant potential in Australian beach-cast seaweeds (Scientific Reports, (2024), 14, 1, (4335), 10.1038/s41598-024-54312-5). Scientific Reports, 14(1), 4335. https://doi.org/10.1038/s41598-024-56269-x
55. Subbiah, V., Xie, C., Dunshea, F. R., Barrow, C. J., & Suleria, H. A. R. (2023). The quest for phenolic compounds from seaweed: Nutrition, biological activities and applications. Food Reviews International, 39(8), 5786–5813.
56. Sun, J., Zhao, G., & Li, M. M. (2023). USING NUTRITIONAL STRATEGIES TO MITIGATE RUMINAL METHANE EMISSIONS FROM RUMINANTS. Frontiers of Agricultural Science and Engineering, 10(3), 390–402. https://doi.org/10.15302/J-FASE-2023504
57. Tayyab, U., Novoa-Garrido, M., Roleda, M. Y., Lind, V., & Weisbjerg, M. R. (2016). Ruminal and intestinal protein degradability of various seaweed species measured in situ in dairy cows. Animal Feed Science and Technology, 213, 44–54. https://doi.org/10.1016/j.anifeedsci.2016.01.003
58. Terry, S. A., Coates, T., Gruninger, R., Abbott, D. W., & Beauchemin, K. A. (2023). Evaluation of the red seaweed Mazzaella japonica as a feed additive for beef cattle. Frontiers in Animal Science, 4. https://doi.org/10.3389/fanim.2023.1181768
59. Terry, S. A., Garcia, V., & Beauchemin, K. A. (2023). Assessing the methane mitigation potential of Canadian red seaweeds using in vitro batch culture. Canadian Journal of Animal Science, 103(4), 394–405. https://doi.org/10.1139/cjas-2023-0063
60. Terry, S. A., Krüger, A. M., Lima, P. M. T., Gruninger, R. J., Abbott, D. W., & Beauchemin, K. A. (2023). Evaluation of Rumen Fermentation and Microbial Adaptation to Three Red Seaweeds Using the Rumen Simulation Technique. Animals, 13(10), 1643. https://doi.org/10.3390/ani13101643
61. Theodorou, M. K., Williams, B. A., Dhanoa, M. S., McAllan, A. B., & France, J. (1994). A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Animal Feed Science and Technology, 48(3–4), 185–197.
62. Tilley, J. M. A., & Terry, R. A. (1969). The relationship between the soluble constituents of herbage and their dry‐matter digestibility. Grass and Forage Science, 24(4), 290–295.
63. Wasson, D. E., Stefenoni, H., Cueva, S. F., Lage, C., Räisänen, S. E., Melgar, A., Fetter, M., Hennessy, M., Narayan, K., Indugu, N., Pitta, D., Yarish, C., & Hristov, A. N. (2023). Screening macroalgae for mitigation of enteric methane in vitro. Scientific Reports, 13(1), 9835. https://doi.org/10.1038/s41598-023-36359-y
64. Wasson, D. E., Yarish, C., & Hristov, A. N. (2022). Enteric methane mitigation through Asparagopsis taxiformis supplementation and potential algal alternatives. Frontiers in Animal Science, 3. https://doi.org/10.3389/fanim.2022.999338
65. Widiawati, Y., & Hikmawan, D. (2021). Enteric methane mitigation by using seaweed Eucheuma cottonii. IOP Conference Series: Earth and Environmental Science, 788(1). https://doi.org/10.1088/1755-1315/788/1/012152
66. Yanza, Y. R., Szumacher-Strabel, M., Bryszak, M., Gao, M., Kolodziejski, P., Stochmal, A., Slusarczyk, S., Patra, A. K., & Cieslak, A. (2018). Coleus amboinicus (Lour.) leaves as a modulator of ruminal methanogenesis and biohydrogenation in vitro1. Journal of Animal Science, 96(11), 4868–4881. https://doi.org/10.1093/jas/sky321

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How to cite

Hidayat, R., Roni Pazla, Asmuddin Natsir, Nurzainah Ginting, & Rosani, U. (2025). Methane concentration, ruminal fermentation, digestibility, and microbial protein synthesis of beef cattle with the addition of various types of seaweed from West Java-Banten with different levels in the ration (in vitro). Journal of Animal Behaviour and Biometeorology, (| Accepted Articles). Retrieved from https://malque.pub/ojs/index.php/jabb/article/view/7416

[1] Afzalani, A., Muthalib, R. A., Dianita, R., Hoesni, F., Raguati, R., & Musnandar, E. (2021). Evaluasi suplementasi Indigofera zollingeriana sebagai sumber green protein concentrate terhadap produksi gas metan, Amonia dan sintesis protein mikroba rumen. Jurnal Ilmiah Universitas Batanghari Jambi, 21(3), 1455–1458.

[2] Alvarez-Hess, P. S., Jacobs, J. L., Kinley, R. D., Roque, B. M., Neachtain, A. S. O., Chandra, S., & Williams, S. R. O. (2023). Twice daily feeding of canola oil steeped with Asparagopsis armata reduced methane emissions of lactating dairy cows. Animal Feed Science and Technology, 297. https://doi.org/10.1016/j.anifeedsci.2023.115579

[3] Andreen, D. M., Billman, E. D., Brito, A. F., & Soder, K. J. (2023). Effect of incremental amounts of Asparagopsis taxiformis on ruminal fermentation and methane production in continuous culture with orchardgrass herbage. Animal Feed Science and Technology, 299. https://doi.org/10.1016/j.anifeedsci.2023.115641

[4] AOAC. (2005). Official Methods of Analysis of AOAC International, 18th edition. Gaithersburg (Maryland): AOAC International. https://www.researchgate.net/publication/292783651_AOAC_2005

[5] Baek, I. K., Maeng, W. J., Lee, S. H., Lee, H. G., Lee, S. R., Ha, J. K., Lee, S. S., & Hwang, J. H. (2004). Effects of the Brown Seaweed Residues Supplementation on In Vitro Fermentation and Milk Production and Composition of Lactating Dairy Cows. Journal of Animal Science and Technology, 46(3), 373–386. https://doi.org/10.5187/jast.2004.46.3.373

[6] Beck, M. R., Al-Marashdeh, O., & Gregorini, P. (2019). Low levels of a seaweed (Ecklonia radiata) extract alter in vitro fermentation products but not in combination with quebracho (Schinopsis quebracho-colorado) tannins. Applied Animal Science, 35(5), 476–481. https://doi.org/10.15232/aas.2019-01892

[7] Belanche, A., Jones, E., Parveen, I., & Newbold, C. J. (2016). A metagenomics approach to evaluate the impact of dietary supplementation with Ascophyllum nodosum or Laminaria digitata on rumen function in Rusitec fermenters. Frontiers in Microbiology, 7(MAR). https://doi.org/10.3389/fmicb.2016.00299

[8] Cherry, P., Yadav, S., O’Callaghan, C., Popper, Z. A., Ross, R. P., McSorley, E. M., Allsopp, P. J., & Stanton, C. (2016). In-vitro fermentation of whole seaweed and a polysaccharide-rich extract derived from the edible red seaweed Palmaria palmate . Proceedings of the Nutrition Society, 75(OCE2), E57. https://doi.org/10.1017/s0029665116000471

[9] Choi, Y., Lee, S. J., Kim, H. S., Eom, J. S., Jo, S. U., Guan, L. L., Seo, J., Kim, H., Lee, S. S., & Lee, S. S. (2021). Effects of seaweed extracts on in vitro rumen fermentation characteristics, methane production, and microbial abundance. Scientific Reports, 11(1). https://doi.org/10.1038/s41598-021-03356-y

[10] Conway, E. J., & O’malley, E. (1942). Microdiffusion methods. Ammonia and urea using buffered absorbents (revised methods for ranges greater than 10μg. N). Biochemical Journal, 36(7–9), 655.

[11] Cottle, D. J., Nolan, J. V., & Wiedemann, S. G. (2011). Ruminant enteric methane mitigation: A review. Animal Production Science, 51(6), 491–514. https://doi.org/10.1071/AN10163

[12] Cruywagen, C. W., Taylor, S., Beya, M. M., & Calitz, T. (2015). The effect of buffering dairy cow diets with limestone, calcareous marine algae, or sodium bicarbonate on ruminal pH profiles, production responses, and rumen fermentation. Journal of Dairy Science, 98(8), 5506–5514. https://doi.org/10.3168/jds.2014-8875

[13] Eikanger, K. S., Kjær, S. T., Dörsch, P., Iwaasa, A. D., Alemu, A. W., Schei, I., Pope, P. B., Hagen, L. H., & Kidane, A. (2024). Asparagopsis taxiformis inclusion in grass silage-based diets fed to Norwegian red dairy cows: Effects on ruminal fermentation, milk yield, and enteric methane emission. Livestock Science, 285. https://doi.org/10.1016/j.livsci.2024.105495

[14] Fearon, A. L., Felix, A., & Sapra, V. T. (1990). Chemical Composition and In Vitro Dry Matter and Organic Matter Digestibility of Triticale Forage. Journal of Agronomy and Crop Science, 164(4), 262–270. https://doi.org/10.1111/j.1439-037X.1990.tb00816.x

[15] Félix, R., Dias, P., Félix, C., Cerqueira, T., Andrade, P. B., Valentão, P., & Lemos, M. F. L. (2021). The biotechnological potential of Asparagopsis armata: What is known of its chemical composition, bioactivities and current market? Algal Research, 60. https://doi.org/10.1016/j.algal.2021.102534

[16] Gerber, P. J., Steinfeld, H., Henderson, B., Mottet, A., Opio, C., Dijkman, J., Falcucci, A., & Tempio, G. (2013). Tackling climate change through livestock – A global assessment of emissions and mitigation opportunities.

[17] Glasson, C. R. K., Kinley, R. D., de Nys, R., King, N., Adams, S. L., Packer, M. A., Svenson, J., Eason, C. T., & Magnusson, M. (2022). Benefits and risks of including the bromoform containing seaweed Asparagopsis in feed for the reduction of methane production from ruminants. Algal Research, 64. https://doi.org/10.1016/j.algal.2022.102673

[18] González-Meza, G. M., Elizondo-Luevano, J. H., Cuellar-Bermudez, S. P., Sosa-Hernández, J. E., Iqbal, H. M. N., Melchor-Martínez, E. M., & Parra-Saldívar, R. (2023). New Perspective for Macroalgae-Based Animal Feeding in the Context of Challenging Sustainable Food Production. Plants, 12(20), 3609.

[19] Hamid, S. S., Wakayama, M., Ichihara, K., Sakurai, K., Ashino, Y., Kadowaki, R., Soga, T., & Tomita, M. (2019). Metabolome profiling of various seaweed species discriminates between brown, red, and green algae. Planta, 249, 1921–1947. https://doi.org/10.1007/s00425-019-03134-1

[20] Handique, B., Singh, P., Verma, A. K., & Yengkhom, R. (2023). The effect of seaweed formulations on in vitro fermentation, nutrient utilization and growth performance in crossbred calves. Veterinarski Arhiv, 93(5), 513–524. https://doi.org/10.24099/vet.arhiv.1858

[21] Hernaman, I., Ayuningsih, B., Ramdani, D., Islami, R. Z., Octaviana, S., Aviana, I., Rahayu, G., Salimah, A. B., Rosani, U., & Budiman, A. (2024). In vitro study of ration containing corncobs soaked by rice hull ash filtrate. Adv. Anim. Vet. Sci, 12(8), 1525–1531.

[22] Hernaman, I., Rochana, A., Andayaningsih, P., Suryani, Y., & Ramdhani, M. A. (2015). Evaluation of in Vitro Digestibility of Dried Matter and Organic Matter of Solid Waste of Bioethanol Fermentation from Cassava by Trichoderma Viride and Saccharomyces Cerevisiae. Journal of Asian Scientific Research, 5(11), 513–521. https://doi.org/10.18488/journal.2/2015.5.11/2.11.513.521

[23] Hidayah, N., Noviandi, C. T., Astuti, A., & Kustantinah, K. (2023). Chemical composition and in vitro rumen fermentation characteristics of various tropical seaweeds. Journal of Advanced Veterinary and Animal Research, 10(4), 751–762. https://doi.org/10.5455/javar.2023.j731

[24] Hindratiningrum, N., Bata, M., & Santosa, S. A. (2011). Produk fermentasi rumen dan produksi protein mikroba sapi lokal yang diberi pakan jerami amoniasi dan beberapa bahan pakan sumber energi. Jurnal Agripet, 11(2), 29–34.

[25] Hong, Z. S., Kim, E. J., Jin, Y. C., Lee, J. S., Choi, Y. J., & Lee, H. G. (2015). Effects of supplementing brown seaweed by-products in the diet of Holstein cows during transition on ruminal fermentation, growth performance and endocrine responses. Asian-Australasian Journal of Animal Sciences, 28(9), 1296–1302. https://doi.org/10.5713/ajas.15.0235

[26] Hristov, A. N., Callaway, T. R., Lee, C., & Dowd, S. E. (2012). Rumen bacterial, archaeal, and fungal diversity of dairy cows in response to ingestion of lauric or myristic acid. Journal of Animal Science, 90(12), 4449–4457. https://doi.org/10.2527/jas.2011-4624

[27] Indugu, N., Narayan, K., Stefenoni, H. A., Hennessy, M. L., Vecchiarelli, B., Bender, J. S., Shah, R., Dai, G., Garapati, S., Yarish, C., Welchez, S. C., Räisänen, S. E., Wasson, D., Lage, C., Melgar, A., Hristov, A. N., & Pitta, D. W. (2024). Microbiome-informed study of the mechanistic basis of methane inhibition by Asparagopsis taxiformis in dairy cattle. MBio, 15(8), e00782-24. https://doi.org/10.1128/mbio.00782-24

[28] Kannan, G., Terrill, T. H., Kouakou, B., & Lee, J. H. (2019). Dietary brown seaweed extract supplementation in small ruminants. In Medicinal Plants: From Farm to Pharmacy (pp. 291–312). Springer International Publishing. https://doi.org/10.1007/978-3-030-31269-5_13

[29] Kinley, R. D., & Fredeen, A. H. (2015). In vitro evaluation of feeding North Atlantic stormtoss seaweeds on ruminal digestion. Journal of Applied Phycology, 27(6), 2387–2393. https://doi.org/10.1007/s10811-014-0487-z

[30] Kinley, R. D., Vucko, M. J., Machado, L., & Tomkins, N. W. (2016). <i>In Vitro</i> Evaluation of the Antimethanogenic Potency and Effects on Fermentation of Individual and Combinations of Marine Macroalgae. American Journal of Plant Sciences, 07(14), 2038–2054. https://doi.org/10.4236/ajps.2016.714184

[31] Knapp, J. R., Laur, G. L., Vadas, P. A., Weiss, W. P., & Tricarico, J. M. (2014). Invited review: Enteric methane in dairy cattle production: Quantifying the opportunities and impact of reducing emissions. Journal of Dairy Science, 97(6), 3231–3261. https://doi.org/10.3168/jds.2013-7234

[32] Leelavathi, M. S., Vani, S., Centre, E., & Road, M. (2015). Comparitive Analysis of Phytochemical Compounds of Marine Algae Isolated From Gulf of Mannar. World Journal of Pharmacy and Pharmaceutical Sciences, 4(05), 640–654.

[33] Lopez-Santamarina, A., Sinisterra-Loaiza, L., Mondragón-Portocarrero, A., Ortiz-Viedma, J., Cardelle-Cobas, A., Abuín, C. M. F., & Cepeda, A. (2023). Potential prebiotic effect of two Atlantic whole brown seaweeds, Saccharina japonica and Undaria pinnatifida, using in vitro simulation of distal colonic fermentation. Frontiers in Nutrition, 10, 1170392. https://doi.org/10.3389/fnut.2023.1170392

[34] Maia, M. R. G., Fonseca, A. J. M., Oliveira, H. M., Mendonça, C., & Cabrita, A. R. J. (2016). The potential role of seaweeds in the natural manipulation of rumen fermentation and methane production. Scientific Reports, 6(1), 32321. https://doi.org/10.1038/srep32321

[35] Mansuit, H., Samsuri, M. D. C., Sipaut, C. S., Yee, C. F., Yasir, S. M., & Mansa, R. (2015). Effect of varying acid hydrolysis condition in Gracilaria Sp. fermentation using Sasad. IOP Conference Series: Materials Science and Engineering, 78(1), 12004. https://doi.org/10.1088/1757-899X/78/1/012004

[36] Maranatha, G., Fattah, S., Sobang, Y. U. L., Yunus, M., & Henuk, Y. L. (2020). Digestibility of dry matter and organic matter and the in vitro rumen parameters of complete feed from fermented corn cobs and moringa (Moringa oleifera) leaves meal. IOP Conference Series: Earth and Environmental Science, 454(1), 12062. https://doi.org/10.1088/1755-1315/454/1/012062

[37] Markham, R. (1942). A steam distillation apparatus suitable for micro-Kjeldahl analysis. Biochemical Journal, 36(10–12), 790.

[38] Matthews, C., Crispie, F., Lewis, E., Reid, M., O’Toole, P. W., & Cotter, P. D. (2019). The rumen microbiome: a crucial consideration when optimising milk and meat production and nitrogen utilisation efficiency. In Gut Microbes (Vol. 10, Issue 2, pp. 115–132). https://doi.org/10.1080/19490976.2018.1505176

[39] Mihaila, A. A., Glasson, C. R. K., Lawton, R., Muetzel, S., Molano, G., & Magnusson, M. (2022). New temperate seaweed targets for mitigation of ruminant methane emissions: an in vitro assessment. Applied Phycology, 3(1), 274–284. https://doi.org/10.1080/26388081.2022.2059700

[40] Narvaez-Izquiedo, J., Fonseca-De La Hoz, J., Kannan, G., & Bohorquez-Herrera, J. (2024). Use of macroalgae as a nutritional supplement for sustainable production of ruminants: A systematic review and an insight on the Colombian Caribbean region. Algal Research, 77. https://doi.org/10.1016/j.algal.2023.103359

[41] Özkan Gülzari, Ş., Lind, V., Aasen, I. M., & Steinshamn, H. (2019). Effect of supplementing sheep diets with macroalgae species on in vivo nutrient digestibility, rumen fermentation and blood amino acid profile. Animal, 13(12), 2792–2801. https://doi.org/10.1017/S1751731119001502

[42] Plummer, D. T. (1978). An introduction to practical biochemistry. (No Title).

[43] Pramono, A., Hadi, R. F., Sutrisno, J., & Cahyadi, M. (2019). The Effect of Protected Soybean Oil and Soybean Groats Base on in Vitro Dry Matter Digestibility, in Vitro Organic Matter Digestibility in the Rumen and Post Rumen. IOP Conference Series: Earth and Environmental Science, 347(1), 12016. https://doi.org/10.1088/1755-1315/347/1/012016

[44] Qori’ah, A., Surono, S., & Sutrisno, S. (2016). Sintesis protein mikroba dan aktivitas selulolitik akibat penambahan level zeolit sumber nitrogen slow release pada glukosa murni secara in vitro. Jurnal Ilmu-Ilmu Peternakan (Indonesian Journal of Animal Science), 26(2), 1–7.

[45] Ramadan, G., Fouda, W. A., Ellamie, A. M., & Ibrahim, W. M. (2020). Dietary supplementation of Sargassum latifolium modulates thermo-respiratory response, inflammation, and oxidative stress in bacterial endotoxin-challenged male Barki sheep. Environmental Science and Pollution Research, 27(27), 33863–33871. https://doi.org/10.1007/s11356-020-09568-5

[46] Rira, M., Morgavi, D. P., Archimède, H., Marie-Magdeleine, C., Popova, M., Bousseboua, H., & Doreau, M. (2015). Potential of tannin-rich plants for modulating ruminal microbes and ruminal fermentation in sheep. Journal of Animal Science, 93(1), 334–347. https://doi.org/10.2527/jas.2014-7961

[47] Rosani, U., Hernaman, I., Hidayat, R., & Hidayat, D. (2024). Fermentability, digestibility, and gas production of Garut sheep fed maize straw silage-based rationsnbalanced with rice bran and rice husks (in vitro). Journal of Animal and Feed Sciences. https://doi.org/10.22358/jafs/190441/2024

[48] Roskam, E., Kirwan, S. F., Kenny, D. A., O’Donnell, C., O’Flaherty, V., Hayes, M., & Waters, S. M. (2022a). Effect of brown and green seaweeds on diet digestibility, ruminal fermentation patterns and enteric methane emissions using the rumen simulation technique. Frontiers in Animal Science, 3. https://doi.org/10.3389/fanim.2022.1021631

[49] Roskam, E., Kirwan, S. F., Kenny, D. A., O’Donnell, C., O’Flaherty, V., Hayes, M., & Waters, S. M. (2022b). Effect of brown and green seaweeds on diet digestibility, ruminal fermentation patterns and enteric methane emissions using the rumen simulation technique. Frontiers in Animal Science, 3. https://doi.org/10.3389/fanim.2022.1021631

[50] Saravanan, K., Duraisamy, S., Ramasamy, G., Kumarasamy, A., & Balakrishnan, S. (2018). Evaluation of the saccharification and fermentation process of two different seaweeds for an ecofriendly bioethanol production. Biocatalysis and Agricultural Biotechnology, 14, 444–449. https://doi.org/10.1016/j.bcab.2018.03.017

[51] Shannon, E., Conlon, M., & Hayes, M. (2022a). The Prebiotic Effect of Australian Seaweeds on Commensal Bacteria and Short Chain Fatty Acid Production in a Simulated Gut Model. Nutrients, 14(10), 2163. https://doi.org/10.3390/nu14102163

[52] Shannon, E., Conlon, M., & Hayes, M. (2022b). The Prebiotic Effect of Australian Seaweeds on Commensal Bacteria and Short Chain Fatty Acid Production in a Simulated Gut Model. Nutrients, 14(10), 2163. https://doi.org/10.3390/nu14102163

[53] Shen, S., Yang, W., Li, L., Zhu, Y., Yang, Y., Ni, H., Jiang, Z., & Zheng, M. (2023). In vitro fermentation of seaweed polysaccharides and tea polyphenol blends by human intestinal flora and their effects on intestinal inflammation. Food and Function, 14(2), 1133–1147. https://doi.org/10.1039/d2fo03390a

[54] Subbiah, V., Ebrahimi, F., Agar, O. T., Dunshea, F. R., Barrow, C. J., & Suleria, H. A. R. (2024). Author Correction: In vitro digestion and colonic fermentation of phenolic compounds and their antioxidant potential in Australian beach-cast seaweeds (Scientific Reports, (2024), 14, 1, (4335), 10.1038/s41598-024-54312-5). Scientific Reports, 14(1), 4335. https://doi.org/10.1038/s41598-024-56269-x

[55] Subbiah, V., Xie, C., Dunshea, F. R., Barrow, C. J., & Suleria, H. A. R. (2023). The quest for phenolic compounds from seaweed: Nutrition, biological activities and applications. Food Reviews International, 39(8), 5786–5813.

[56] Sun, J., Zhao, G., & Li, M. M. (2023). USING NUTRITIONAL STRATEGIES TO MITIGATE RUMINAL METHANE EMISSIONS FROM RUMINANTS. Frontiers of Agricultural Science and Engineering, 10(3), 390–402. https://doi.org/10.15302/J-FASE-2023504

[57] Tayyab, U., Novoa-Garrido, M., Roleda, M. Y., Lind, V., & Weisbjerg, M. R. (2016). Ruminal and intestinal protein degradability of various seaweed species measured in situ in dairy cows. Animal Feed Science and Technology, 213, 44–54. https://doi.org/10.1016/j.anifeedsci.2016.01.003

[58] Terry, S. A., Coates, T., Gruninger, R., Abbott, D. W., & Beauchemin, K. A. (2023). Evaluation of the red seaweed Mazzaella japonica as a feed additive for beef cattle. Frontiers in Animal Science, 4. https://doi.org/10.3389/fanim.2023.1181768

[59] Terry, S. A., Garcia, V., & Beauchemin, K. A. (2023). Assessing the methane mitigation potential of Canadian red seaweeds using in vitro batch culture. Canadian Journal of Animal Science, 103(4), 394–405. https://doi.org/10.1139/cjas-2023-0063

[60] Terry, S. A., Krüger, A. M., Lima, P. M. T., Gruninger, R. J., Abbott, D. W., & Beauchemin, K. A. (2023). Evaluation of Rumen Fermentation and Microbial Adaptation to Three Red Seaweeds Using the Rumen Simulation Technique. Animals, 13(10), 1643. https://doi.org/10.3390/ani13101643

[61] Theodorou, M. K., Williams, B. A., Dhanoa, M. S., McAllan, A. B., & France, J. (1994). A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Animal Feed Science and Technology, 48(3–4), 185–197.

[62] Tilley, J. M. A., & Terry, R. A. (1969). The relationship between the soluble constituents of herbage and their dry‐matter digestibility. Grass and Forage Science, 24(4), 290–295.

[63] Wasson, D. E., Stefenoni, H., Cueva, S. F., Lage, C., Räisänen, S. E., Melgar, A., Fetter, M., Hennessy, M., Narayan, K., Indugu, N., Pitta, D., Yarish, C., & Hristov, A. N. (2023). Screening macroalgae for mitigation of enteric methane in vitro. Scientific Reports, 13(1), 9835. https://doi.org/10.1038/s41598-023-36359-y

[64] Wasson, D. E., Yarish, C., & Hristov, A. N. (2022). Enteric methane mitigation through Asparagopsis taxiformis supplementation and potential algal alternatives. Frontiers in Animal Science, 3. https://doi.org/10.3389/fanim.2022.999338

[65] Widiawati, Y., & Hikmawan, D. (2021). Enteric methane mitigation by using seaweed Eucheuma cottonii. IOP Conference Series: Earth and Environmental Science, 788(1). https://doi.org/10.1088/1755-1315/788/1/012152

[66] Yanza, Y. R., Szumacher-Strabel, M., Bryszak, M., Gao, M., Kolodziejski, P., Stochmal, A., Slusarczyk, S., Patra, A. K., & Cieslak, A. (2018). Coleus amboinicus (Lour.) leaves as a modulator of ruminal methanogenesis and biohydrogenation in vitro1. Journal of Animal Science, 96(11), 4868–4881. https://doi.org/10.1093/jas/sky321

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