Skip to main content

Ensilage and anaerobic digestion of Sargassum muticum

Abstract

The brown seaweed Sargassum muticum is an invasive species to the coasts of the British Isles, mainland Europe and North America. Attempts at its eradication and control have generally not been successful, although time-consuming and costly. Commercial exploration of this biomass for fuel could encourage its harvesting and control. Anaerobic digestion (AD) has been suggested as one of the most promising methods of exploiting algae for biofuel. The harvesting of S. muticum is seasonal; thus, there will be a need to preserve and store seaweed to supply a year-round anaerobic digestion process. Ensiling is widely used in terrestrial agriculture, but there has been little research on ensiling seaweed. The aims of this research were to: a) study the effect of ensiling on the biomethane potential of S. muticum, b) effect of size reduction prior to ensilage on leachate and other losses during ensiling and c) examine the mass balance and energy losses of ensiling S. muticum. Ensiling was found to be an effective, low energy loss method of preserving seaweed with energy loss from the biomass due to ensiling <8 % of the higher heating value of seaweed feedstock. Ensiling results in losses of salt from the biomass and the virtual total loss of organic sulphur. Size reduction of seaweed prior to ensilage reduced leachate and energy loss from the biomass. Ensiling had no significant effect on methane yield. However, methane yields from S. muticum are low ≤0.11 L CH4 g−1 volatile solid (VS) at ~25 % of the theoretical maximum. Further research is needed to establish the reasons for the recalcitrance of S. muticum, but the C:N ratio of S. muticum is low (8:1), and co-digestion with a low nitrogen content substrate such as crude glycerol may be a potential method of improving methane yield.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  • Adams JMM, Ross AB, Anastasakis K, Hodgson EM, Gallagher JA, Jones JM, Donnison IS (2011) Seasonal variation in the chemical composition of the bioenergy feedstock Laminaria digitata for thermochemical conversion. Bioresour Technol 102:226–234

    CAS  Article  PubMed  Google Scholar 

  • Allen E, Wall DM, Herrmann C, Murphy JD (2014) Investigation of the optimal percentage of green seaweed that may be co-digested with dairy slurry to produce gaseous biofuel. Bioresour Technol 170:436–444

    CAS  Article  PubMed  Google Scholar 

  • Allen E, Wall DM, Herrmann C, Xia A, Murphy JD (2015) What is the gross energy yield of third generation gaseous biofuel sourced from seaweed? Energy 81:352–360

    CAS  Article  Google Scholar 

  • Alvarado-Morales M, Boldrin A, Karakashev DB, Holdt SL, Angelidaki I, Astrup T (2013) Life cycle assessment of biofuel production from brown seaweed in Nordic conditions. Bioresour Technol 129:92–99

    CAS  Article  PubMed  Google Scholar 

  • Anastasakis K, Ross AB (2011) Hydrothermal liquefaction of the brown macro-alga Laminaria saccharina: effect of reaction conditions on product distribution and composition. Bioresour Technol 102:4876–4883

  • Ashbell G, Weinberg ZG (2005) Silage production and utilization. FAO, Bet Dagan, Israel

  • Astals S, Musenze RS, Bai X, Tannock S, Tait S, Pratt S, Jensen PD (2015) Anaerobic co-digestion of pig manure and algae: Impact of intracellular algal products recovery on co-digestion performance. Bioresour Technol 181:97–104

    CAS  Article  PubMed  Google Scholar 

  • Bae DY, Ang PO, Boo SM (2013) Mitochondrial cox3 and trnW-I sequence diversity of Sargassum muticum. Aquat Bot 104:220–223

    CAS  Article  Google Scholar 

  • Banks C, Zhang Y (2010) Optimising inputs and outputs from anaerobic digestion processes - Technical Report. Defra, Southampton

  • Black WAP (1955) The preservation of seaweed by ensiling and bactericides. J Sci Food Agric 6:14–23

    CAS  Article  Google Scholar 

  • Bruton T, Lyons H, Lerat Y, Stanley M, Rasmussen MB (2009) A review of the potential of marine algae as a source of biofuel in Ireland. Sustainable Energy Ireland, Dublin

    Google Scholar 

  • BSI (2009a) Solid biofuels—determination of ash content

    Google Scholar 

  • BSI (2009b) Determination of moisture content. Oven dry method. Total moisture. Simplified method

  • BSI (2010) Determination of the gross heat of combustion (calorific value)

    Google Scholar 

  • Buswell AM, Mueller HF (1952) Mechanism of methane fermentation. Indu Eng Chem 44:550–552

    CAS  Article  Google Scholar 

  • CABI (2011) Sargassum muticum. In: Invasive species compendium. CAB International, Wallingford

    Google Scholar 

  • Charmley E, Savoie P, McRae KB, Lu X (1999) Effect of maceration at mowing on silage conservation, voluntary intake, digestibility and growth rate of steers fed precision chopped or round bale silages. Can J Anim Sci 79:195–202

    Article  Google Scholar 

  • Chen H, Zhou D, Luo G, Zhang S, Chen J (2015) Macroalgae for biofuels production: progress and perspectives. Renew Sust Energy Rev 47:427–437

    CAS  Article  Google Scholar 

  • Cook EJ, Jenkins S, Maggs C, Minchin D, Mineur F, Nall C, Sewell J (2013) Impacts of climate change on non-native species. MCCIP Sci Rev 2013:155–166. doi:10.14465/2013.arc17.155-166

  • Critchley AT, Farnham WF, Morrell SL (1986) An account of the attempted control of an introduced marine alga, Sargassum muticum, in southern England. Biol Cons 35:313–332

    Article  Google Scholar 

  • Davison DM (2009) Sargassum muticum in Scotland 2008: a review of information, issues and implications, Commissioned Report No.324 (ROAME No. R07AC707)., Scottish Natural Heritage

  • Dewar WA, McDonald P (1961) Determination of dry matter in silage by distillation with toluene. J Sci Food Agric 12:790–795

    CAS  Article  Google Scholar 

  • Driehuis F, van Wikselaar PG (2000) The occurrence and prevention of ethanol fermentation in high-dry-matter grass silage. J Sci Food Agric 80:711–718

    CAS  Article  Google Scholar 

  • Edwards M, Haniffy D, Heesch S, Hernandez-Kantun J, Moniz M, Queguineur B, Ratcliff J, Soler-Vila A, Wan A (2014) Macroalgae fact-sheets. Ryan Institute, NUI, Galway

  • Engelen A, Santos R (2009) Which demographic traits determine population growth in the invasive brown seaweed Sargassum muticum? J Ecol 97:675–684

    Article  Google Scholar 

  • European Environment Agency (EEA) (2003) Winter surface concentrations of nitrates in sea water. EEA. http://www.eea.europa.eu/data-and-maps/figures/winter-surface-concentrations-of-nitrates-in-sea-water. Accessed 15 Dec 2015.

  • Fistarol GO, Salomon PS, Rosato M, Garcia-Blairsy Reina G (2012) Production of methane using microalgae biomass from a wastewater treatment plant. Curr Top Biotech 7:51–60

    CAS  Google Scholar 

  • Gerardi MH (2003) The microbiology of anaerobic digesters. Wastewater microbiology series. Wiley-Interscience, Hoboken, N.J

  • Gibson CE (2011) Northern Ireland State of the Seas Report. Agri-Food and Biosciences Institute, Belfast

  • Golueke CG, Oswald WJ, Gotaas HB (1957) Anaerobic digestion of algae. Appl Microbiol 5:47–55

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gorham J, Lewey SA (1984) Seasonal changes in the chemical composition of Sargassum muticum. Mar Biol 80:103–107

    CAS  Article  Google Scholar 

  • Heaven S, Milledge J, Zhang Y (2011) Comments on ‘Anaerobic digestion of microalgae as a necessary step to make microalgal biodiesel sustainable’. Biotechnol Adv 29:164–167

    CAS  Article  PubMed  Google Scholar 

  • Herrmann C, FitzGerald J, O'Shea R, Xia A, O'Kiely P, Murphy JD (2015) Ensiling of seaweed for a seaweed biofuel industry. Bioresour Technol 196:301–313

    CAS  Article  PubMed  Google Scholar 

  • Hierholtzer A, Akunna JC (2012) Modelling sodium inhibition on the anaerobic digestion process. Wat Sci Technol 66:1565–1573

    CAS  Article  Google Scholar 

  • IFRF. International Flame Research Foundation (2004) Online Combustion Handbook. Method from Combustion File 24

    Google Scholar 

  • Jard G, Marfaing H, Carrere H, Delgenes JP, Steyer JP, Dumas C (2013) French Brittany macroalgae screening: composition and methane potential for potential alternative sources of energy and products. Bioresour Technol 144:492–498

    CAS  Article  PubMed  Google Scholar 

  • Jones DIH, Jones R (1995) The effect of crop characteristics and ensiling methodology on grass silage effluent production. J Agr Eng Res 60:73–81

    Article  Google Scholar 

  • Kent Wildlife Trust (2006) Have you seen you seen these species on the shores around Kent or Sussex? http://www.pevensey-bay.co.uk/resources/pdf/BAR%20Have%20you%20seen%20these.pdf. Accessed 29 April 2014

  • Kohler B, Diepolder M, Ostertag J, Thurner S, Spiekers H (2013) Dry matter losses of grass, lucerne and maize silages in bunker silos. Ag Food Sci 22:145–150

    Google Scholar 

  • Kreuger E, Nges IA, Bjornsson L (2011) Ensiling of crops for biogas production: effects on methane yield and total solids determination. Biotech Biofuels 4. doi:10.1186/1754-6834-4-44

  • Lahtinen S, Ouwehand A, Salminen S, Av W (eds) (2012) Lactic acid bacteria: microbiological and functional aspects, Fourth edn. CRC, Boca Rotan

  • Lefebvre O, Moletta R (2006) Treatment of organic pollution in industrial saline wastewater: a literature review. Water Res 40:3671–3682

    CAS  Article  PubMed  Google Scholar 

  • Liu F, Pang SJ, Gao SQ, Shan TF (2013) Intraspecific genetic analysis, gamete release performance, and growth of Sargassum muticum (Fucales, Phaeophyta) from China. Chin J Ocean Limnol 31:1268–1275

    CAS  Article  Google Scholar 

  • Lodeiro P, Cordero B, Grille Z, Herrero R, de Vicente MES (2004) Physicochemical studies of cadmium(II) biosorption by the invasive alga in Europe, Sargassum muticum. Biotech Bioeng 88:237–247

    CAS  Article  Google Scholar 

  • Medway Swale Estuary Partnership (ND) In The Water. http://www.msep.org.uk/invasive-species-in-the-water.php. Accessed 22 April 2014

  • Merrill AL, Watts BK (1955) Energy values of foods: Basis & Duration. Slight revised February 1973 Agricultural Handbook 74. US Department of Agriculture, Washington, DC

  • Milledge J, Nielsen B, Bailey D (2015a) High-value products from macroalgae: the potential uses of the invasive brown seaweed, Sargassum muticum. Rev Environ Sci Biotechnol. doi:10.1007/s11157-015-9381-7

    Google Scholar 

  • Milledge JJ (2010) The potential yield of microalgal oil. Biofuels Int 4(44):45

    Google Scholar 

  • Milledge JJ, Heaven S (2014) Methods of energy extraction from microalgal biomass: a review. Rev Environ Sci Biotechnol 13:301–320 d

    CAS  Article  Google Scholar 

  • Milledge JJ, Heaven S (2015) Energy balance of biogas production from microalgae: development of an energy and mass balance model. Curr Biotechnol 4:554–567

    CAS  Article  Google Scholar 

  • Milledge JJ, Smith B, Dyer P, Harvey P (2014) Macroalgae-derived biofuel: a review of methods of energy extraction from seaweed biomass. Energies 7:7194–7222

    CAS  Article  Google Scholar 

  • Milledge JJ, Staple A, Harvey P (2015b) Slow pyrolysis as a method for the destruction of Japanese wireweed, Sargassum muticum. Env Nat Resour Res 5:28–36

    Google Scholar 

  • Milledge JJ, Temukum KN, Ratana A, Nielsen BV, Harvey P (2015c) Anaerobic digestion (AD) of novel wastes. Paper presented at the 3rd Faculty of Engineering & Science Research Symposium University of Greenwich, 16/09/2015. https://www.researchgate.net/profile/John_Milledge/publications

  • Muller CE (2009) Long-stemmed vs. cut haylage in bales—effects on fermentation, aerobic storage stability, equine eating behaviour and characteristics of equine faeces. Anim Feed Sci Technol 152:307–321

    Article  Google Scholar 

  • Murphy F, Devlin G, Deverell R, McDonnell K (2013) Biofuel production in Ireland—an approach to 2020 targets with a focus on algal biomass. Energies 6:6391–6412

    Article  Google Scholar 

  • Nallathambi Gunaseelan V (1997) Anaerobic digestion of biomass for methane production: a review. Biomass Bioenergy 13:83–114

    Article  Google Scholar 

  • Neureiter M, dos Santos JTP, Perez Lopez C, Pichler H, Kirchmayr R, Braun R (2005) Effect of silage preparation on methane yields from whole crop maize silages. Paper presented at the IWA 4th International Symposium on Anaerobic Digestion of Solid Wastes Copenhagen, http://www.cropgen.soton.ac.uk/publications/8%20Other/Copenhagen/Oth_Copenhagen4_Neureiter.pdf

  • Nguyen H, Heaven S, Banks C (2014) Energy potential from the anaerobic digestion of food waste in municipal solid waste stream of urban areas in Vietnam. Int J Energy Environ Eng 5:365–374

    CAS  Article  Google Scholar 

  • Oliveira JV, Alves MM, Costa JC (2015) Optimization of biogas production from Sargassum sp. using a design of experiments to assess the co-digestion with glycerol and waste frying oil. Bioresour Technol 175:480–485

    CAS  Article  PubMed  Google Scholar 

  • Oude Elferink SJWH, Driehuis F, Gottschal JC, Spoelstra SF (1999) Silage fermentation processes and their manipulation. Paper presented at the FAO Electronic Conference on Tropical Silage, http://www.fao.org/docrep/005/x8486e/x8486e09.htm

  • Pagliaro M, Rossi M (2008) The future of glycerol: new uses of a versatile raw material. Royal Society of Chemistry, Cambridge

    Google Scholar 

  • Pearson D (1973) Laboratory techniques in food analysis. Butterworth, London

    Google Scholar 

  • Persson SPE, Bartlett HD, Branding AE, Regan RW (1979) Agricultural anaerobic digesters. Bulletin 827, Pennsylvania State University, http://extension.psu.edu/natural-resources/energy/waste-to-energy/resources/biogas/projects/bulletin-827.pdf

  • Peu P, Picard S, Diara A, Girault R, Béline F, Bridoux G, Dabert P (2012) Prediction of hydrogen sulphide production during anaerobic digestion of organic substrates. Bioresour Technol 121:419–424

    CAS  Article  PubMed  Google Scholar 

  • Porter MG, Murray RS (2001) The volatility of components of grass silage on oven drying and the inter-relationship between dry-matter content estimated by different analytical methods. Grass Forage Sci 56:405–411

    CAS  Article  Google Scholar 

  • Rittmann BE, McCarty PL (2001) Environmental biotechnology: principles and applications. McGraw-Hill, Singapore

    Google Scholar 

  • Ross AB, Jones JM, Kubacki ML, Bridgeman T (2008) Classification of macroalgae as fuel and its thermochemical behaviour. Bioresour Technol 99:6494–6504

    CAS  Article  PubMed  Google Scholar 

  • Shinya Y, Yukihiko M (eds) (2008) The Asian biomass handbook—a guide for biomass production and utilization. The Japan Institute of Energy, Tokyo

  • Skoog DA (2004) Fundamentals of analytical chemistry. 8th ed., International student ed edn. Thomson/Brooks/Cole, London

  • Soto M, Vazquez MA, de Vega A, Vilarino JM, Fernandez G, de Vicente ME (2015) Methane potential and anaerobic treatment feasibility of Sargassum muticum. Bioresour Technol 189:53–61

    CAS  Article  PubMed  Google Scholar 

  • Sutherland A, Varela J (2014) Comparison of various microbial inocula for the efficient anaerobic digestion of Laminaria hyperborea. BMC Biotech 14:7

    Article  Google Scholar 

  • Symons GE, Buswell AM (1933) The methane fermentation of carbohydrates. J Amer Chem Soc 55:2028–2036

    CAS  Article  Google Scholar 

  • Tanniou A, Vandanjon L, Gonçalves O, Kervarec N, Stiger-Pouvreau V (2015) Rapid geographical differentiation of the European spread brown macroalga Sargassum muticum using HRMAS NMR and fourier-transform infrared spectroscopy. Talanta 132:451-456

  • The River Stour (Kent) Internal Drainage Board (2012) Minutes of Board Meeting. http://www.riverstouridb.org.uk/documents/minutes081112.pdf

  • Tsapekos P, Kougias PG, Angelidaki I (2105) Biogas production from ensiled meadow grass; effect of mechanical pretreatments and rapid determination of substrate biodegradability via physicochemical methods. Bioresour Technology doi:http://dx.doi.org/10.1016/j.biortech.2015.02.025

  • Uchida M, Miyoshi T (2013) Algal fermentation—the seed for a new fermentation industry of foods and related products. Jap Agric Res Quart 47:53–63

    CAS  Article  Google Scholar 

  • Wakeman KD, Erving L, Riekkola-Vanhanen ML, Puhakka JA (2010) Silage supports sulfate reduction in the treatment of metals- and sulfate-containing waste waters. Water Res 44:4932–4939

    CAS  Article  PubMed  Google Scholar 

  • Wei N, Quarterman J, Jin YS (2013) Marine macroalgae: an untapped resource for producing fuels and chemicals. Trends Biotech 31:70–77

    CAS  Article  Google Scholar 

  • Wernberg T, Thomsen MS, Staehr PA, Pedersen MF (2001) Comparative phenology of Sargassum muticum and Halidrys siliquosa (Phaeophyceae: Fucales) in Limfjorden, Denmark. Bot Mar 44:31–39

    Article  Google Scholar 

  • Williams FE, Eschen R, Harris A, Djeddour DH, Pratt CF, Shaw RS, Varia S, Lamontagne-Godwin JD, Thomas SE (2010) The economic cost of invasive non-native species on Great Britain. CABI, Wallingford

    Google Scholar 

  • Wout R, Greenwell H, Davies D, Theodorou M (2013) Methods of ensiling algae, ensiled algae and uses of ensiled algae. PCT Patent WO2013045931-A1,

  • Yang EJ, Ham YM, Lee WJ, Lee NH, Hyun CG (2013) Anti-inflammatory effects of apo-9′-fucoxanthinone from the brown alga, Sargassum muticum. J Pharm Sci 21:62. doi:10.1186/2008-2231-21-62

    CAS  Google Scholar 

  • Zafren SY, Panov AA (1978) Glycosides during ensiling. Biol Bull Acad Sci the USSR 5:360–362

    CAS  Google Scholar 

  • Zhao FJ, Liu FL, Liu JD, Ang PO, Duan DL (2008) Genetic structure analysis of natural Sargassum muticum (Fucales, Phaeophyta) populations using RAPD and ISSR markers. J Appl Phycol 20:191–198

    CAS  Article  Google Scholar 

  • Zhou D, Zhang L, Zhang S, Fu H, Chen J (2010) Hydrothermal liquefaction of macroalgae Enteromorpha prolifera to bio-oil. Energy Fuels 24:4054–4061

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the EPSRC project number EP/K014900/1 (MacroBioCrude: Developing an Integrated Supply and Processing Pipeline for the Sustained Production of Ensiled Macroalgae-derived Hydrocarbon Fuels) and the University of Greenwich. The authors would also like to acknowledge Mr Willie McKnight, North East Kent Scientific Coastal Advisory Group, for the collection of seaweed samples; the assistance of colleagues at the University of Greenwich: Mrs Devyani Amin and Dr Alan Staple and Smurfit Kappa Townsend Hook Paper Makers for the provision of the inoculum.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John J. Milledge.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Milledge, J.J., Harvey, P.J. Ensilage and anaerobic digestion of Sargassum muticum . J Appl Phycol 28, 3021–3030 (2016). https://doi.org/10.1007/s10811-016-0804-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-016-0804-9

Keywords

  • Sargassum muticum
  • Phaeophyta
  • Anaerobic digestion
  • Ensilage
  • Invasive species
  • Algae
  • Macroalgae
  • Japanese wireweed