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A review of multiple biostimulant and bioeffector benefits of AMPEP, an extract of the brown alga Ascophyllum nodosum, as applied to the enhanced cultivation and micropropagation of the commercially important red algal carrageenophyte Kappaphycus alvarezii and its selected cultivars

  • 6th Congress of the International Society for Applied Phycology
  • Published:
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Abstract

Commercially manufactured extracts of a variety of seaweeds have been used extensively for several decades for the relief of abiotic and biotic stresses for (terrestrial) agricultural crops and horticulture, to improve yield and quality. However, the use of seaweed extracts for their beneficial properties, as applied to marine macroalgae, only began in the mid to late 2000s. Kappaphycus alvarezii is an important red seaweed on the coasts of tropical to sub-tropical waters, mainly because of the various applications of kappa carrageenan, which is the major industrial colloid extracted from this extensively cultivated biomass. Cultivation of this seaweed has brought economic benefits to tens of thousands of seaweed farmers in Southeast Asia and other minor producing countries. Recently, Ascophyllum (aka. Acadian) Marine Plant Extract Powder (AMPEP), a commercial seaweed extract from the brown intertidal, macroalga A. nodosum was used in steps taken during the micropropagation and field cultivation of K. alvarezii. The reasons for utilizing this treatment included addressing the current problems facing the industry, such as decreased productivity, loss of vigor and diminished crop quality. This was brought about by shortages in the availability of good quality propagules (seedlings) and also disease and endo-epiphyte infestations, which affected the ability to grow and harvest saleable biomass, thus decreasing the income, and therefore the interest and participation of the potential seaweed farmers (based on the factor of repetitive, “drudge” labor and their derived income per unit effort). This paper reviews studies on Kappaphycus including the use of AMPEP specifically and also some alternative extracts to mitigate both biotic and abiotic stressors, using examples from micropropagation, field cultivation, endophyte mitigation and impacts on the resulting carrageenan qualities. Taken together, this body of evidence provides proof of concept and very promising results which may lead to further studies more specifically to identify the modes of action and the metabolic pathways by which the complex AMPEP extract might improve stress tolerances in K. alvarezii in order to obtain higher productivity and enhanced quality characteristics (i.e., exposure to increasing surface seawater temperature, salinity fluctuations and photo-inhibitory irradiance as well as attacks by pathogenic and opportunistic organisms).

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References

  • Adnan H, Porse H (1987) Culture of Eucheuma cottonii and Eucheuma spinosum in Indonesia. Hydrobiologia 151/152:355–358

    Google Scholar 

  • Ali MM, Sani MZB, Hi KK, SMd Y, Critchley AT, Hurtado AQ (2017a) The comparative efficiency of a brown algal-derived biostimulant extract (AMPEP), with and without supplemented PGRs: the induction of direct, axis shoots as applied to the propagation of vegetative seedlings for the successful mass cultivation of three commercial strains of Kappaphycus in Sabah, Malaysia. J Appl Phycol. https://doi.org/10.1007/s10811-017-1366-1

    Google Scholar 

  • Ali MM, Yashir S, Critchley AT, Hurtado AQ (2017b) Impacts of Ascophyllum Marine Plant Extract Powder (AMPEP) on the growth, incidence of the endophyte Neosiphonia apiculata and associated carrageenan quality of three, commercial cultivars of Kappaphycus. J Appl Phycol. https://doi.org/10.1007/s10811-017-1312-2

    Google Scholar 

  • Arthur GD, Stirk WA, van Staden J (2003) Effect of a seaweed concentrate on the growth and yield of three varieties of Capsicum annuum. S Afr J Bot 69:207–211

    Google Scholar 

  • Ask E (1999) Cottonii and spinosum cultivation handbook. FMC Food Ingredients Division, Philadelphia 52pp

    Google Scholar 

  • Ateweberhan M, Rougier A, Rakotomahazo C (2015) Influence of environmental factors and farming technique on growth and health of farmed Kappaphycus alvarezii (cottonii) in southwest Madagascar. J Appl Phycol 27:923–934

    Google Scholar 

  • Babu S, Rengasamy R (2012) Effect of Kappaphycus alvarezii SLF treatment on seed germination, growth and development of seedling in some crop plants. J Acad Ind Res 1:186–195

    Google Scholar 

  • Belda M, Sanchez D, Bover E, Prieto B, Padrón C, Cejalvo D, Lloris JM (2016) Extraction of polyphenols in Himanthalia elongata and determination by high performance liquid chromatography with diode array detector prior to its potential use against oxidative stress. J Chromatogr B 1033-1043:334–341

    Google Scholar 

  • Bernardon-Mery A, Joubert J-M, Hoareau A (2013) Laminarin used against apple scab. Phytoma 662:4

  • Bhattacharyya D, Zamani M, Pramod B, Prithiviraj R (2015) Seaweed extracts as biostimulants in horticulture. Sci Hortic 196:39–48

    Google Scholar 

  • Bixler HJ, Porse H (2011) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321–335

    Google Scholar 

  • Blunden G, Jenkins T, Liu YW (1996) Enhanced leaf chlorophyll levels in plants treated with seaweed extract. J Appl Phycol 8:535–543

    CAS  Google Scholar 

  • Borlongan IAG, Tibubos KR, Yunque DAT, Hurtado AQ, Critchley AT (2011) Impact of AMPEP on the growth and occurrence of epiphytic Neosiphonia infestation on two varieties of commercially cultivated Kappaphycus alvarezii grown at different depths in the Philippines. J Appl Phycol 23:615–621

    Google Scholar 

  • Buschmann AH, Camus C, Infante J, Neori A, Israel Á, Hernández-González MC, Pereda SV, Gomez-Pinchetti J-L, Golberg A, Tadmor-Shalev N, Critchley AT (2017) Seaweed production: overview of the global state of exploitation, farming and emerging research activity. Eur J Phycol 52:391–406

    Google Scholar 

  • Campbell R, Hotchkiss S (2017) Carrageenan industry market overview. In: Hurtado AQ, Critchley AT, Neish IC (eds) Tropical seaweed farming trends, problems and opportunities: focus on spinosum and cottonii of commerce. Springer, Dodrecht, pp 193–205

    Google Scholar 

  • Catarino MD, Silva AMS, Cardosa SM (2017) Fucaceae: a source of bioactive phlorotannins. Int J Mol Sci 18(6). doi:https://doi.org/10.3390/ijms18061327

  • Coronado AS, Dionisio Sese ML (2014) Antimicrobial property of crude ethanolic extract from Sargassum crassifolium J.G. Agardh. Asian J Microbiol Biotechnol Environ Sci 16:471–474

    Google Scholar 

  • Cottier-Cook EJ, Nagabhatla N, Badis Y, Campbell ML, Chopin T, Dai W, Fang J, He P, Hewitt CL, Kim GH, Huo Y, Jiang Z, Kema G, Li X, Liu F, Liu H, Liu Y, Lu Q, Luo Q, MaoY MFE, Rebours C, Shen H, Stentiford GD, Yarish C, Wu H, Yang X, Zhang J, Zhou Y, CMM G (2016) Safeguarding the future of the global seaweed aquaculture industry. UNU-INWEH and SAMS, South Hamilton, 12 pp

    Google Scholar 

  • Craigie J (2011) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371–393

    CAS  Google Scholar 

  • Craigie JS, MacKinnon SL, Walter JA (2007) Liquid seaweed extracts identified using 1H NMR profiles. J Appl Phycol 20:665–671

    Google Scholar 

  • Critchley AT, Largo D, Wee W, Bleicher L’honneur G, Hurtado AQ, Schubert J (2004) A preliminary summary on Kappaphycus farming and the impact of epiphytes. Jpn J Phycol (Supplement) 52:231–232

    Google Scholar 

  • Crouch IJ, van Staden J (1992) Effect of seaweed concentrate on the establishment and yield of greenhouse tomato plants. J Appl Phycol 4:291–296

    Google Scholar 

  • Crouch IJ, van Staden J (1993) Evidence for the presence of plant growth regulators in commercial seaweed products. Plant Growth Regul 13:21–29

    CAS  Google Scholar 

  • Doty MS (1973) Farming the red seaweed, Eucheuma, for carrageenans. Micron 9:59–73

    Google Scholar 

  • Doty MS (1985) Eucheuma alvarezii sp. novum (Gigartinales, Rhodophyta) from Malaysia. In: Abbott IA, Norris JN (eds) Taxonomy of economic seaweeds: with reference to some Pacific and Caribbean species. California Sea Grant College Program, La Jolla, pp 37–45

    Google Scholar 

  • Doty MS, Alvarez VB (1981) Eucheuma farm productivity. Int Seaweed Symp 8:688–691

    Google Scholar 

  • Doty MS, Norris JN (1985) Eucheuma species (Solieriaceae, Rhodophyta) that are major sources of carrageenan. In: Abbott IA, Norris JN (eds) Taxonomy of economic seaweeds: with reference to some Pacific and Caribbean species. California Sea Grant College Program, La Jolla, pp 47–61

    Google Scholar 

  • Dring M (2006) Stress resistance and disease resistance in seaweeds: the role of reactive oxygen metabolism. Adv Bot Res 43:175–207

    CAS  Google Scholar 

  • du Jardin P (2015) Plant biostimulants: definition, concept, main categories and regulation. Sci Hortic 196:3–14

    Google Scholar 

  • Esserti S, Smaili A, Rifai LA, Koussa T, Makroum K, Belfaiza M, Kabil EM, Faize L, Burgos L, Alburquerque N, Faize M (2017a) Protective effect of three brown seaweed extracts against fungal and bacterial diseases of tomato. J Appl Phycol 29:1081–1093

    CAS  Google Scholar 

  • Esserti S, Faize M, Rifai LA, Smaili A, Belfaiza M, Alburquerque N, Burgos L, Koussa T, Makroum K (2017b) Media derived from brown seaweeds Cystoseira myriophylloides and Fucus spiralis for in vitro plant tissue culture. Plant Cell Tissue Organ Cult 128:437–446

    CAS  Google Scholar 

  • Esserti S, Smaili A, Makroum K, Belfaiza M, Rifai LA, Koussa T, Kasmi I, Faize M (2018) Priming of Nicotiana benthamiana antioxidant defences using brown seaweed extracts. J Phytopathol 166:86–94

    CAS  Google Scholar 

  • Fan D, Hodges DM, Zhang JZ, Kirby CW, Ji XH, Locke SJ, Critchley AT, Prithiviraj B (2011) Commercial extract of the brown seaweed Ascophyllum nodosum enhances phenolic antioxidant content of spinach (Spinacia oleracea L.) which protects Caenorhabditis elegans against oxidative and thermal stress. Food Chem 124:195–202

    CAS  Google Scholar 

  • Garcia-Vaquero M, Rajaura G, O’Doherty JV, Sweeney T (2016) Polysaccharides from macroalgae: recent advances, innovative technologies and challenges in extraction and purification. Food Res Int 99:1011–1020

    PubMed  Google Scholar 

  • Goes HG, Reis RP (2011) An initial comparison of tubular netting versus tie-tie methods of cultivation for Kappaphycus alvarezii (Rhodophyta, Solieriaceae) on the south coast of Rio de Janeiro State, Brazil. J Appl Phycol 23:607–613

    Google Scholar 

  • Góes HG, Reis RP (2012) Temporal variation of the growth, carrageenan yield and quality of Kappaphycus alvarezii (Rhodophyta, Gigartinales) cultivated at Sepetiba Bay, southeastern Brazilian coast. J Appl Phycol 24:173–180

    Google Scholar 

  • Goñi O, Fort A, Quille P, McKeown PC, Spillane C, O’Connell SO (2016) Comparative transcriptome analysis of two Ascophyllum nodosum extract biostimulants: same seaweed but different. J Agric Food Chem 64:2980–2989

    PubMed  Google Scholar 

  • Guan J, Liang L, Mao S (2017) Applications of carrageenan in advanced drug delivery. In: Venkatesan J, Anil S, Kim SK (eds) Seaweed polysaccharides, isolation, biological and biomedical applications. Elsevier, Amsterdam, pp 283–298

    Google Scholar 

  • Hayashi L, Oliveira EC, Bleicher-L'honneur G, Boulenguer P, Pereira RTL, von Seckendorff R, Shimoda VT, Leflamand A, Vallée P, Critchley AT (2007) The effects of selected cultivation conditions on the carrageenan characteristics of Kappaphycus alvarezii (Rhodophyta, Solieriaceae) in Ubatuba Bay, São Paulo, Brazil. J Appl Phycol 19:505–511

    CAS  Google Scholar 

  • Hayashi L, Yokoya NS, Kikuchi DM, Oliveira EC (2008) Callus induction and micropropagation improved by colchicines and phytoregulators in Kappaphycus alvarezii (Rhodophyta, Solieriaceae). J Appl Phycol 20:653–659

    Google Scholar 

  • Hayashi L, Bulboa C, Kradolfer P, Soriano G, Robledo D (2014) Cultivation of red seaweeds: a Latin American perspective. J Appl Phycol 26:719–727

    Google Scholar 

  • Hayashi L, Reis RP, Alves dos Santos AA, Castelar B, Robledo D, de Vega GB, Msuya FE, Eswaran K, Yasir S, Ali MJ, Hurtado AQ (2017) The cultivation of Kappaphycus and Eucheuma in tropical and sub-tropical waters. In: Hurtado AQ, Critchley AT, Neish IC (eds) Tropical seaweed farming trends, problems and opportunities: focus on spinosum and cottonii of commerce. Springer, Dordrecht, pp 55–90

    Google Scholar 

  • Hotchkiss S, Brooks M, Campbell R, Philip K, Trius A (2016) The use of carrageenan in food. In: Pereira L (ed) Carrageenans: sources and extraction methods, Molecular Structure, Bioactive Properties and Health Effects. Nova Science Publications Inc., New York

  • Hung LD, Hori K, Nang HQ, Kha T, Hoa LT (2009) Seasonal changes in growth rate, carrageenan yield and lectin content in the red alga Kappaphycus alvarezii cultivated in Camranh Bay, Vietnam. J Appl Phycol 21:265–272

    CAS  Google Scholar 

  • Hurtado AQ, Critchley AT, Trespoey A, Bleicher-L’honneur G (2006) Occurrence of Polysiphonia epiphytes in Kappaphycus farms at Calaguas Is. Camarines Norte, Philippines. J Appl Phycol 18:301–306

    Google Scholar 

  • Hurtado AQ, Yunque DA, Tibubos KT, Critchley AT (2009) Use of Acadian marine plant extract powder from Ascophyllum nodosum in tissue culture of Kappaphycus varieties. J Appl Phycol 21:633–639

    Google Scholar 

  • Hurtado AQ, Joe M, Sanares RC, Fan D, Prithiviraj B, Critchley AT (2012) Investigation of the application of Acadian Marine Plant Extract Powder (AMPEP) to enhance the growth, phenolic content, free radical scavenging, and iron chelating activities of Kappaphycus Doty (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 24:601–611

    CAS  Google Scholar 

  • Hurtado AQ, Gerung GS, Critchley AT YS (2014a) Cultivation of tropical red seaweeds in the BIMP-EAGA region. J Appl Phycol 26:702–718

    Google Scholar 

  • Hurtado AQ, Neish IC, Critchley AT (2014b) Farm productivity of seaweed carrageenan farming in the ASEAN countries. Paper presented at the International Seaweed Congress, 19–21 Nov 2014, Waterfront Hotel, Cebu

  • Hurtado AQ, Neish IC, Critchley AT (2015) Developments in production technology of Kappaphycus in the Philippines: more than four decades of farming. J Appl Phycol 27:1945–1961

    CAS  Google Scholar 

  • Jayaraman J, Norrie J, Punja ZK (2011) Commercial extract from the brown seaweed Ascophyllum nodosum reduces fungal diseases in greenhouse cucumber. J Appl Phycol 23:353–361

    Google Scholar 

  • Kadam SU, O’Donnell CP, Rai DK, Hossain MB, Burgess CM, Walsh D, Tiwari BK (2015) Laminarin from Irish brown seaweeds Ascophyllum nodosum and Laminaria hyperborea: ultrasound assisted extraction, characterization and bioactivity. Mar Drugs 13:4270–4280

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kapilkumar I, Vitkin E, Robin A, Yakhini Z, Mishori D, Golberg A (2017) Macroalgal biorefinery from Kappaphycus alvarezii: conversion modeling and performance prediction for India and the Philippines as examples. Bioenerg Res. https://doi.org/10.1007/s12155-017-9874-z

    Google Scholar 

  • Klarzynski O, Plesse B, Joubert J, Yvin JC, Kopp M, Kloareg B, Fritig B (2000) Linear β -1,3 glucans are elicitors of defense responses in Tobacco-France. Plant Physiol 124:1027–1037

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar G, Sahoo D (2011) Effect of seaweed liquid extract on growth and yield of Triticum aestivum var. Pusa Gold. J Appl Phycol 23:251–255

    Google Scholar 

  • Kumar M, Reddy CRK, Jha B (2013) The ameliorating effect of Acadian marine plant extract against ionic liquids-induced oxidative stress and DNA damage in marine macroalga Ulva lactuca. J Appl Phycol 25:369–378

    CAS  Google Scholar 

  • Kumari R, Kaur I, Bhatnagar A (2011) Effect of aqueous extract of Sargassum johnstonii Setchell on growth, yield and quality of Lycopersicon esculentum Mill. J Appl Phycol 23:623–633

    Google Scholar 

  • Largo DB (2002) Recent development in seaweed diseases. In: Hurtado AQ, Guanzon NG Jr, de Castro-Mallare TR, Luhan MRJ (eds). Proc Nat Seaweed Planning Workshop. Tigbauan, Iloilo, pp 35–42

  • Le Lann K, Surget G, Couteau C, Coiffard L, Cérantola S, Gaillard F, Larnicol M, Zubia M, Guérard F, Poupart N, Stiger-Pouvreau V (2016) Sunscreen, antioxidant, and bactericide capacities of phlorotannins from the brown macroalga Halidrys siliquosa. J Appl Phycol 28:3547–3559

    Google Scholar 

  • Leclerc M, Caldwell CD, Lada RR, Norrie J (2006) Effect of plant growth regulators on propagule formation in Hemerocallis spp. and Hosta spp. Hortscience 41:651–653

    CAS  Google Scholar 

  • Lötze E, Hoffman E (2016) Nutrient composition and content of various biological active compounds of three South African-based commercial seaweed biostimulants. J Appl Phycol 28:1379–1386

    Google Scholar 

  • Loureiro RR, Reis RP, Critchley AT (2010) In vitro cultivation of three Kappaphycus alvarezii (Rhodophyta, Areschougiaceae) variants (green, red and brown) exposed to a commercial extract of the brown alga Ascophyllum nodosum (Fucaceae, Ochrophyta). J Appl Phycol 22:101–104

    Google Scholar 

  • Loureiro RR, Reis RP, Berrogain FD, Critchley AT (2012) Extract powder from the brown alga Ascophyllum nodosum (Linnaeus) Le Jolis (AMPEP): a ‘vaccine-like; effect on Kappaphycus alvarezii (Doty) Doty ex P.C. Silva. J Appl Phycol 24:427–432

    Google Scholar 

  • Loureiro RR, Reis R, Marroig R (2014a) Effect of the commercial extract of the brown alga Ascophyllum nodosum Mont. on Kappaphycus alvarezii (Doty) Doty ex P.C. Silva in situ submitted to lethal temperatures. J Appl Phycol 26:629–634

    Google Scholar 

  • Loureiro RR, Reis RP, Berrogain FD, Critchley AT (2014b) Effects of a commercial extract of the brown alga Ascophyllum nodosum on the biomass production of Kappaphycus alvarezii (Doty) Doty ex P.C. Silva and its carrageenan yield and gel quality cultivated in Brazil. J Appl Phycol 26:763–768

    Google Scholar 

  • Loureiro RR, Hurtado AQ, Critchley AT (2017) Impacts of AMPEP on epiphytes and diseases in Kappaphycus and Eucheuma cultivation. In: Hurtado AQ, Critchley AT, Neish IC (eds) Tropical seaweed farming trends, problems and opportunities: focus on spinosum and cottonii of commerce. Springer, Dodrecht, pp 111–119

    Google Scholar 

  • Luhan MRJ, Mateo JP (2017) Clonal production of Kappaphycus alvarezii (Doty) Doty in vitro. J Appl Phycol 29:2339–2344

    CAS  Google Scholar 

  • MacKinnon SL, Hiltz D, Ugarte R, Craft CA (2010) Improved methods of analysis for betaines in Ascophyllum nodosum and its commercial seaweed extracts. J Appl Phycol 22:489–494

    Google Scholar 

  • Mancuso S, Azzarello E, Mugnai S, Briand X (2006) Marine bioactive substances (IPA extract) improve foliar ion uptake and water stress tolerance in potted Vitis vinifera plants. Adv Hortic Sci 20:156–161

    Google Scholar 

  • Markets and Markets (2016) Hydrocolloids market global forecast by type (gelatin, xanthan, carrageenan, alginate, agar, pectin, guar, locust bean, gum arabic, and CMC), function (thickener, stabilizer, gelling, fat replacer, and coating), source, application, and by region—Global forecast to 2020 Markets and Markets, February 2016

  • Marroig RG, Loureiro RR, Reis RP (2016) The effect of Ascophyllum nodosum (Ochrophyta) extract powder on the epibiosis of Kappaphycus alvarezii (Rhodophyta) commercially cultivated on floating rafts. J Appl Phycol 28:2471–2477

    Google Scholar 

  • Martynenko A, Shotton K, Astatkie T, Petrash G, Fowler C, Neily W, Critchley AT (2016) Thermal imaging of soybean response to drought stress: the effect of Ascophyllum nodosum seaweed extract. SpringerPlus 5:1393

    PubMed  PubMed Central  Google Scholar 

  • Mendoza WG, Montaño NE, Ganzon-Fortes ET, Villanueva RD (2002) Chemical and gelling profile of ice-ice infected carrageenan from Kappaphycus striatum (Schmitz) Doty ‘sacol’ strain (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 14:409–418

    CAS  Google Scholar 

  • Mireya R, Vigen-Calleros G, Ruiz-López M, Zañudo-Hernández J, Délano-Frier JP, Sánchez-Hernández C, Hernández-Herrera A (2014) Extracts from green and brown seaweeds protect tomato (Solanum lycopersicum) against the necrotrophic fungus Alternaria solani. J Appl Phycol 26:1607–1614

    Google Scholar 

  • Moreira R, Sineiro J, Chenlo F, Arufe S, Díaz-Varela D (2017) Aqueous extracts of Ascophyllum nodosum obtained by ultrasound-assisted extraction: effects of drying temperature of seaweed on the properties of extracts. J Appl Phycol 29:3191–3200

    CAS  Google Scholar 

  • Msuya FE, Buriyo A, Omar I, Pascal B, Narrain K, Ravina JJM, Mrabu E, Wakibia JG (2014) Cultivation and utilisation of red seaweeds in the Western Indian Ocean (WIO) region. J Appl Phycol 26:699–705

    CAS  Google Scholar 

  • Neish IC, Suryanarayan S (2017) Development of eucheumatoid seaweed value-chains through carrageenan and beyond. In: Hurtado AQ, Critchley AT, Neish IC (eds) Tropical seaweed farming trends, problems and opportunities: focus on spinosum and cottonii of commerce. Springer, Dordrecht, pp 173–192

    Google Scholar 

  • Neves FAS, Simioni C, Bouzon ZL, Hayashi L (2015) Effects of spindle inhibitors and phytoregulators on the micropropagation of Kappaphycus alvarezii (Rhodophyta, Gigartinales). J Appl Phycol 27:437–445

    CAS  Google Scholar 

  • Olivares-Molina A, Fernández K (2016) Comparison of different extraction techniques for obtaining extracts from brown seaweeds and their potential effects as angiotensin I-converting enzyme (ACE) inhibitors. J Appl Phycol 28:1295–1302

    CAS  Google Scholar 

  • Ortiz-Tena JG, Shieder D, Sieber V (2017) Carrageenan and more: biorefinery approaches with special references to the processing of Kappaphycus. In: Hurtado AQ, Critchley AT, Neish IC (eds) Tropical seaweed farming trends, problems and opportunities: focus on spinosum and cottonii of commerce. Springer, Dordrecht, pp 155–164

    Google Scholar 

  • Pang T, Liu J, Liu Q, Zhang L, Lin W (2012) Impacts of glyphosate on photosynthetic behaviors in Kappaphycus alvarezii and Neosiphonia savatieri detected by JIP-test. J Appl Phycol 24:467–473

    CAS  Google Scholar 

  • Pang T, Liu J, Liu Q, Li H, Li J (2015) Observations on pests and diseases affecting a eucheumatoid farm in China. J Appl Phycol 27:1975–1984

    Google Scholar 

  • Parker HS (1974) The culture of the red algal genus Eucheuma in the Philippines. Aquaculture 3:425–439

    Google Scholar 

  • Pereira L, Soares F, Freitas AC, Duarte AC, Ribeiro-Claro P (2017) Extraction, characterization and uses of carrageenan. In: Sudha PN (ed) Industrial applications of marine biopolymers. CRC Press, Boca Raton, pp 37–90

    Google Scholar 

  • Porse H, Rudolph B (2017) The seaweed hydrocolloid industry: 2016 updates, requirements, and outlook. J Appl Phycol 29:2187–2200

    Google Scholar 

  • Pramanick B, Brahmachari K, Ghosh A, Zodape ST (2014) Foliar nutrient management through Kappaphycus and Gracilaria saps in rice-potato-green gram crop sequence. J Sci Ind Res 73:613–617

    Google Scholar 

  • Raimundo S, Pattathil S, Eberhard S, Hahn MG, Popper ZA (2017) β-1,3-glucans are components of brown seaweed (Phaeophyceae) cell walls. Protoplasma 254:997–1016. https://doi.org/10.3389/fpls.2017.01362

  • Rayirath P, Jithesh MN, Farid A, Khan W, Palanisamy R, Hankins SD, Critchley AT, Prithiviraj B (2008) Rapid bioassays to evaluate the plant growth promoting activity of Ascophyllum nodosum (L.) Le Jol. using a model plant, Arabidopsis thaliana (L.) Heynh. J Appl Phycol 20:423–429

    Google Scholar 

  • Rayirath P, Benkel B, Hodges DM, Allan-Wojtas P, MacKinnon S, Critchley AT, Prithiviraj B (2009) Lipophilic components of the brown seaweed, Ascophyllum nodosum, enhance freezing tolerance in Arabidopsis thaliana. Planta 230:135–147

    CAS  PubMed  Google Scholar 

  • Rayorath PM, Khan W, Palanisamy R, MacKinnon SL, Stefanova R, Hankins SD, Critchley AT, Prithiviraj B (2008a) Extracts of the brown seaweed Ascophyllum nodosum induce gibberellic acid (GA3)-independent amylase activity in barley. J Plant Growth Regul 27:370–379

    CAS  Google Scholar 

  • Rayorath PM, Narayanan JM, Farid A, Khan W, Palanisamy R, Hankins SD, Critchley AT, Prithiviraj B (2008b) Rapid bioassays to evaluate the plant growth promoting activity of Ascophyllum nodosum (L.) Le Jol. using a model plant, Arabidopsis thaliana. J Appl Phycol 20:423–429

    CAS  Google Scholar 

  • Robertson-Andersson DV, Leitao D, Bolton JJ, Anderson RJ, Njobeni A, Ruck K (2006) Can kelp extract (Kekpak®) be useful in seaweed mariculture? J Appl Phycol 18:315–321

    Google Scholar 

  • Robledo D, Gasca-Leyva E, Fraga J (2013) Social and economic dimensions of carrageenan seaweed farming in Mexico. In: Valderrama D, Cai J, Hishamunda N, Ridler N (eds) Social and economic dimensions of carrageenan seaweed farming. Fish aqua tech paper 580. FAO, Rome, pp 185–204

    Google Scholar 

  • Sangha JS, Kandasamy S, Khan W, Singh Bahia W, Singh RP, Critchley AT, Prithiviraj B (2015) λ-carrageenan suppresses tomato chlorotic dwarf viroid (TCDVd) replication and symptom expression in tomatoes. Mar Drugs 13:2875–2889

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santaniello A, Scartazza A, Gresta F, Loreta E, Iasone A, Di Tommaso D, Piaggesi A, Perata P (2017) Ascophyllum nodosum seaweed extract alleviates drought stress in Arabidopsis by affecting photosynthetic performance and related gene expression. Protoplasma 254:997–1016

    Google Scholar 

  • Sharma N, Chauhan RS, Sood H (2015) Seaweed extract as a novel elicitor and medium for mass propagation and picroside-I production in an endangered medicinal herb Picrorhiza kurroa. Plant Cell Tissue Organ Cult 122:57–65

    Google Scholar 

  • Sharma L, Banerjee M, Malik GC, Gopalakrishnan VAK, Zodape ST, Arup Ghosh A (2017) Sustainable agro-technology for enhancement of rice production in the red and lateritic soils using seaweed based biostimulants. J Clean Prod 149:968–975

    CAS  Google Scholar 

  • Shekhar Sharma HS, Fleming C, Selby C, Rao JR, Martin T (2014) Plant biostimulants: a review on the processing of macroalgae and use of extracts for crop management to reduce abiotic and biotic stresses. J Appl Phycol 26:465–490

    Google Scholar 

  • Shi P, Geng S, Feng T, Wu H (2017) Effects of Ascophyllum nodosum extract on growth and antioxidant defense systems of two freshwater microalgae. J Appl Phycol. https://doi.org/10.1007/s10811-017-1287-z

    Google Scholar 

  • Shukla PS, Shotton K, Norman E, Neily W, Critchley AT, Prithiviraj B (2017) Seaweed extract improves drought tolerance of soybean by regulating stress-response genes. AoB Plants 10:10

    Google Scholar 

  • Singh S, Singh MK, Pal SK, Trivedi K, Yesuraj D, Singh CS, Vijay Anand KG, Chandramohan M, Patidar R, Kubavat D, Zodape ST, Ghosh A (2016) Sustainable enhancement in yield and quality of rain-fed maize through Gracilaria edulis and Kappaphycus alvarezii seaweed sap. J Appl Phycol 28:2099–2112

    CAS  Google Scholar 

  • Sivanandhan S, Selvaraj N, Ganapathi A, Manickavasagam M (2014) Improved production of withanolides in shoot suspension culture of Withania somnifera (L.) Dunal by seaweed extracts. Plant Cell Tissue Organ Cult 119:221–225

    Google Scholar 

  • Spann TM, Little HA (2011) Applications of a commercial extract of the brown seaweed Ascophyllum nodosum increases drought tolerance in container-grown ‘Hamlin’ Sweet Orange nursery trees. Hort Sci 46:577–582

    Google Scholar 

  • Stadnik J, de Freitas MB (2014) Algal polysaccharides as sources of plant resistance inducers. Trop Plant Pathol 39:111–118

    Google Scholar 

  • Tibubos K, Hurtado AQ, Critchley AT (2017) Direct formation of axes in new plantlets of Kappaphycus alvarezii (Doty) Doty, as influenced by the use of AMPEP K+, spindle inhibitors and plant growth hormones. J Appl Phycol 29:2345–2349

    CAS  Google Scholar 

  • Trivedi K, Vijay Anand KG, Kubavat D, Patidar R, Ghosh A (2017) Drought alleviatory potential of Kappaphycus seaweed extract and the role of the quaternary ammonium compounds as its constituents towards imparting drought tolerance in Zea mays L. J Appl Phycol. https://doi.org/10.1007/s10811-017-1375-0

    Google Scholar 

  • Trono GC, Valdestamon RG (1994) New aspects in the ecology and culture of Kappaphycus and Eucheuma. Korean J Phycol 9:205–216

    Google Scholar 

  • Tsiresy G, Preux J, Lavitra T, Dubois P, Lepoint G, Eeckhaut I (2016) Phenology of farmed seaweed Kappaphycus alvarezii infestation by the parasitic epiphyte Polysiphonia sp. in Madagascar. J Appl Phycol 28:2903–2914

    Google Scholar 

  • Urbani S, Ziosi V, MacKinnon S, Henderson D, Ratcliffe J, Manda A, Pirondi A (2016) Testing the bioactivity of kelp extracts developed via chemical and physical separation techniques using bioassays. Acta Hortic 1148:109–114

  • USDA (2016) https://www.ams.usda.gov/sites/default/files/media/Aquatic%20Plant%20Extract%20Tech%20Review.pdf. Accessed Jan 2018

  • Uyenco FR (1977) Microbiological studies of diseased Eucheuma sp. and other seaweeds. Nat Seaweeds Symp. Metro Manila, Philippines

  • Uyenco FR, Saniel LS, Jacinto GS (1981) The ‘ice-ice’ problem in seaweed farming. Proc Int Seaweed Symp 10:625–630

    Google Scholar 

  • Vairappan CS (2006) Seasonal occurrences of epiphytic algae on the commercially cultivated red alga Kappaphycus alvarezii (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 18:611–617

    Google Scholar 

  • Vairappan CS, Chung CS, Hurtado AQ, Msuya FE, Bleicher L’honneur G, Critchley AT (2008) Distribution and symptoms of epiphyte infection in major carrageenophyte-producing farms. J Appl Phycol 20:477–483

    Google Scholar 

  • Valderrama D, Cai J, Hishamunda N, Ridler N (2013) Social and economic dimensions of carrageenan seaweed farming. Fish Aqua Tech Paper 580. FAO, Rome

    Google Scholar 

  • Van Oosten MJ, Pepe O, De Pascale S, Silletti S, Maggio A (2017) The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants. Chem Biol Technol Agric 4:5

    Google Scholar 

  • Wally OSD, Critchley AT, Hiltz D, Craigie JS, Han X, Zaharia LI, Abrams SR, Prithiviraj B (2013) Regulation of phytohormone bio-synthesis and accumulation in Arabidopsis following treatment with commercial extract from the marine macroalga Ascophyllum nodosum. J Plant Growth Regul 32:324–339

    CAS  Google Scholar 

  • Yong WTL, Ting SH, Yong YS, Thien VY, Wong SH, Chin WL, Rodrigues KF, Anton A (2014) Optimization of culture conditions for the direct regeneration of Kappaphycus alvarezii (Rhodophyta, Solieriaceae). J Appl Phycol 26:1597–1606

    CAS  Google Scholar 

  • Yunque DAT, Tibubos KR, Hurtado AQ, Critchley AT (2011) Optimization of culture conditions for tissue culture production of young plantlets of carrageenophyte Kappaphycus. J Appl Phycol 23:433–438

    Google Scholar 

  • Zhang XZ, Ervin EH (2004) Cytokinin-containing seaweed and humic acid extracts associated with creeping bentgrass leaf cytokinins and drought resistance. Crop Sci 44:1737–1745

    CAS  Google Scholar 

  • Zhang XZ, Ervin EH (2008) Impact of seaweed extract-based cytokinins and zeatin riboside on creeping bentgrass heat tolerance. Crop Sci 48:364–370

    Google Scholar 

  • Zodape ST, Mukhopagyay S, Eswaran K, Reddy MP, Chikara J (2010) Enhanced yield and nutritional quality in green gram (Phaseolus radiata L) treated with seaweed (Kappaphycus alvarezii) extract. J Sci Ind Res 69:468–471

    CAS  Google Scholar 

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Acknowledgments

The senior author would like to thank ASL, Canada for the continued donations of AMPEP samples provided in order to conduct these studies. The authors are most grateful to the constructive feedback of two anonymous reviewers and also to Lynn Cornish for the final version.

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Authors and Affiliations

  1. Integrated Services for the Development of Aquaculture and Fisheries (ISDA) Inc., MacArthur Highway, Tabuc Suba, Jaro, 5000, Iloilo City, Philippines

    Anicia Q. Hurtado

  2. Verschuren Centre for Sustainability in Energy and the Environment, Cape Breton University, Sydney, Nova Scotia, B1P 6L2, Canada

    Alan T. Critchley

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  1. Anicia Q. Hurtado
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Correspondence to Anicia Q. Hurtado.

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Hurtado, A.Q., Critchley, A.T. A review of multiple biostimulant and bioeffector benefits of AMPEP, an extract of the brown alga Ascophyllum nodosum, as applied to the enhanced cultivation and micropropagation of the commercially important red algal carrageenophyte Kappaphycus alvarezii and its selected cultivars. J Appl Phycol 30, 2859–2873 (2018). https://doi.org/10.1007/s10811-018-1407-4

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