Skip to main content
Log in

Allelopathy in macroalgae: Ecological principles, research opportunities and pitfalls reviewed

  • Review
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Macroalgae are a vast source of bioactive metabolites, some of which are produced as a defence against competing and/or fouling species, i.e., allelochemicals. As both the occurrence of allelopathy in seaweed and its underlying mechanisms are understudied, we summarised the current knowledge on this phenomenon, as well as elucidate opportunities and challenges in this emerging field. We mark out which biotic and environmental factors govern the stability and durability of allelopathic interactions, and which of them might confound conclusions on the absence/presence of allelopathy in macroalgae. We compiled information of the taxonomic position of 138 putative allelopathic species of brown, green, and red seaweeds, as well as the identity of the compounds they produce. Additionally, we characterise which physiological processed are likely targeted by aquatic allelochemicals. In summary, this work updates our understanding of the occurrence of allelopathy in seaweed on a global scale as well as their allelochemicals affecting competitors, providing recommendations for future research on this topic.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Abdul Malik SA, Bedoux G, Robledo D, García-Maldonado J, Freile-Pelegrín Y, Bourgougnon N (2020) Chemical defense against microfouling by allelopathic active metabolites of Halymenia floresii (Rhodophyta). J Appl Phycol 32:2673–2687

    CAS  Google Scholar 

  • Accoroni S, Percopo I, Cerino F, Romagnoli T, Pichierri S, Perrone C, Totti C (2015) Allelopathic interactions between the hab dinoflagellate Ostreopsis cf. ovata and macroalgae. Harmful Algae 49:147–155

    Google Scholar 

  • Aina O, Bakare OO, Daniel AI, Gokul A, Beukes DR, Fadaka AO, Keyster M et al (2022) Seaweed-derived phenolic compounds in growth promotion and stress alleviation in plants. Life 12:1548

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Alamsjah M, Hirao S, Ishibashi F, Fujita Y (2005) Isolation and Structure Determination of algicidal compounds from Ulva fasciata. Biosci Biotechnol Biochem 69:2186–2192

    CAS  PubMed  Google Scholar 

  • Alamsjah M, Hirao S, Ishibashi F, Oda T, Fujita Y (2008) Algicidal activity of polyunsaturated fatty acids derived from Ulva fasciata and U. pertusa (Ulvaceae, Chlorophyta) on phytoplankton. J Appl Phycol 20:713–720

  • Andras T, Alexander T, Gahlena A, Parry R, Fernandez F, Kubanek J, Wang MD, Hay ME et al (2012) Seaweed allelopathy against coral: Surface distribution of a seaweed secondary metabolite by imaging mass spectrometry. J Chem Ecol 38:1203–1214

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baird AH, Morse ANC (2004) Induction of metamorphosis in larvae of the brooding corals Acropora palifera and Stylophora pistillata. Mar Freshw Res 55:469–472

    Google Scholar 

  • Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: An examination of future possibilities. J Exp Bot 55:1607–1621

    CAS  PubMed  Google Scholar 

  • Bambaranda BVASM, Sasaki N, Chirapart A, Salin KR, Tsusaka TW (2019) Optimization of macroalgal density and salinity for nutrient removal by Caulerpa lentillifera from aquaculture effluent. Processes 7:303

    CAS  Google Scholar 

  • Bazes A, Silkina A, Douzenel P, Faÿ F, Kervarec N, Morin D, Berge J-P, Bourgougnon N (2009) Investigation of the antifouling constituents from the brown alga Sargassum muticum (Yendo) Fensholt. J Appl Phycol 21:395–403

    CAS  Google Scholar 

  • Ben Gharbia H, Kéfi-Daly Yahia O, Cecchi P, Masseret E, Amzil Z, Herve F, Rovillon G, Nouri H, M’Rabet C, Couet D, Triki HZ, Laabir M (2017) New insights on the species-specific allelopathic interactions between macrophytes and marine HAB dinoflagellates. PLoS One 12:e0187963

    PubMed  PubMed Central  Google Scholar 

  • Benitt C, Young CS, Sylvers LH, Gobler CJ (2022) Inhibition of harmful algal blooms caused by Aureococcus anophagefferens (Pelagophyceae) using native (Gracilaria tikvahiae) and invasive (Dasysiphonia japonica) red seaweeds from North America. J Appl Phycol 34:965–983

    CAS  Google Scholar 

  • Björk M, Axelsson L, Beer S (2004) Why is Ulva intestinalis the only macroalga inhabiting isolated rockpools along the Swedish Atlantic coast? Mar Ecol Prog Ser 284:109–116

  • Blum U (1999) Designing laboratory plant debris-soil bioassays: some reflections. In: Dakshini Inderjit KMM, Foy CL (eds) Principles and practices in plant ecology: allelochemical interactions. CRC Press, Boca Raton, pp 17–23

  • Bonaldo RM, Hay ME (2014) Seaweed-coral interactions: variance in seaweed allelopathy, coral susceptibility, and potential effects on coral resilience. PLoS One 9:e85786

  • Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VG (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90:1478–1484

    PubMed  Google Scholar 

  • Budzałek G, Śliwińska-Wilczewska S, Wiśniewska K, Wochna A, Bubak I, Latała A, Wiktor J (2021) Macroalgal defense against competitors and herbivores. Int J Mol Sci 22:7865

    PubMed  PubMed Central  Google Scholar 

  • Cade-Menun B, Paytan A (2010) Nutrient temperature and light stress alter phosphorus and carbon forms in culture-grown algae. Mar Chem 121:27–36

    CAS  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:2075–2075

    Google Scholar 

  • Carl C, de Nys R, Paul NA (2014) The seeding and cultivation of a tropical species of filamentous Ulva for algal biomass production. PLoS One 9:e98700

    PubMed  PubMed Central  ADS  Google Scholar 

  • Carpenter RC (1990) Competition among marine macroalgae: a physiological perspective. J Phycol 26:6–12

    Google Scholar 

  • Chadwick NE, Morrow KM (2011) Competition among sessile organisms on coral reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 347–371

  • Chambers LD, Stokes KR, Walsh FC, Wood RJK (2006) Modern approaches to marine antifouling coatings. Surf Coat Technol 201:3642–3652

    CAS  Google Scholar 

  • Cotas J, Leandro A, Monteiro P, Pacheco D, Figueirinha A, Gonçalves AMM, da Silva GJ, Pereira L (2020) Seaweed phenolics: From extraction to applications. Mar Drugs 18:384

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clements CS, Burns AS, Stewart FJ, Hay ME (2020) Seaweed-coral competition in the field: effects on coral growth, photosynthesis and microbiomes require direct contact. Proc R Soc B 287:20200366

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defence patterns in relation to defence theories. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 228–241

    Google Scholar 

  • da Gama BA, Pereira RC, Carvalho AG, Coutinho R, Yoneshigue-Valentin Y (2002) The effects of seaweed secondary metabolites on biofouling. Biofouling 18:13–20

    Google Scholar 

  • da Gama B, Plouguerné E, Pereira R (2014) The antifouling defence mechanisms of marine macroalgae. Adv Bot Res 71:413–440

    Google Scholar 

  • Dayton PK (1971) Competition, disturbance, and community organization: The provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–389

    Google Scholar 

  • De Nys R, Coll JC, Price IR (1991) Chemically mediated interactions between the red alga Plocamium hamatum (Rhodophyta) and the octocoral Sinularia cruciata (Alcyonacea). Mar Biol 108:315–320

    Google Scholar 

  • De Nys R, Leya T, Maximilien R, Afsar A, Nair P, Steinberg P (1996) The need for standardised broad scale bioassay testing: A case study using the red alga Laurencia rigida. Biofouling 10:213–224

    PubMed  Google Scholar 

  • De’ath G, Fabricius K, Sweatman H, Puotinen M (2012) The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci 109:17995-17999

  • Del Monaco C, Hay M, Gartrell P, Mumby P, Diaz-Pulido G (2017) Effects of ocean acidification on the potency of macroalgal allelopathy to a common coral. Sci Rep 7:41053

  • Denboh T, Suzuki M, Mizuno Y, Ichimura T (1997) Suppression of Laminaria sporelings by allelochemicals from coralline red algae. Bot Mar 40:249–256

  • Dixon J, Schroeter SC, Kastendiek J (1981) Effects of the encrusting bryozoan Membranipora membranacea on the loss of blades and fronds by the giant kelp Macrocystis pyrifera (Laminariales). J Phycol 17:341–345

    Google Scholar 

  • Dworjanyn SA, de Nys R, Steinberg PD (1999) Localisation and surface quantification of secondary metabolites in the red alga Delisea pulchra. Mar Biol 133:727–736

    CAS  Google Scholar 

  • Dworjanyn S, de Nys R, Steinberg PD (2006) Chemically mediated antifouling in the red alga Delisea pulchra. Mar Ecol Prog Ser 318:153–163

    CAS  ADS  Google Scholar 

  • El-Darier S, Metwally A, Nasser A, Taha H (2021) Biointerference relationship between the macroalga Ulva lactuca and two green microalgae. Egypt J Aquat Res 47:163–169

    Google Scholar 

  • Erhard D (2006) Allelopathy in aquatic environments. In: Reigosa MJ, Pedrol N, Gonzalez L (eds.) Allelopathy: a physiological process with ecological implications. Springer, Dordrecht, pp 433±450

  • Feldmann J, Feldmann G (1950) Les “corps en cerise” des Laurencia obtusa (Huds) Lamour. C R Acad Sci Paris Ser D 231:1335–1337

  • Fong J, Lim Z, Bauman A, Valiyaveettil S, Liao L, Yip Z, Todd P (2019) Allelopathic effects of macroalgae on Pocillopora acuta coral larvae. Mar Environ Res 151:104745

    CAS  PubMed  Google Scholar 

  • Friedlander M, Gonen Y, Kashman Y, Beer S (1996) Gracilaria conferta and its epiphytes: 3. Allelopathic inhibition of the red seaweed by Ulva cf. lactuca. J Appl Phycol 8:21–25

  • Fu M, Cao S, Li J, Zhao S, Liu J, Zhuang M, Qin Y, Gao S, Sun Y, Kim JK, Zhang J, He P (2022) Controlling the main source of green tides in the Yellow Sea through the method of biological competition. Mar Pollut Bull 177:113561

    CAS  PubMed  Google Scholar 

  • Gao Z, Xu D, Meng C, Zhang X, Wang Y, Li D et al (2014) The green tide-forming macroalga Ulva linza outcompetes the red macroalga Gracilaria lemaneiformis via allelopathy and fast nutrients uptake. Aquat Ecol 48:53–62

    CAS  Google Scholar 

  • Getachew M, Getachew P, Cho J, Choi J, Hong Y (2017) The phaeophyte Hizikia fusiformis extracts suppress rhizoid and blade formation in seaweeds. Bot Sci 95:830

    Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  PubMed  Google Scholar 

  • Gomes M, Garcia Q, Barreto L, Pimenta L, Matheus M, Figueredo C (2017) Allelopathy: An overview from micro- to macroscopic organisms, from cells to environments, and the perspectives in a climate-changing world. Biologia 72:113–129

    Google Scholar 

  • Gonzalez MA, Goff LJ (1989) The red algal epiphytes Microcladia coulteri and M. californica (Rhodophyceae, Ceramiaceae). J Phycol 25:558–567

    Google Scholar 

  • Green-Gavrielidis L, MacKechnie F, Thornber C, Gomez-Chiarri M (2018) Bloom-forming macroalgae (Ulva spp.) inhibit the growth of co-occurring macroalgae and decrease eastern oyster larval survival. Mar Ecol Prog Ser 595:27–37

    CAS  ADS  Google Scholar 

  • Gross EM (2003) Allelopathy of aquatic autotrophs. Crit Rev Plant Sci 22:313–339

    Google Scholar 

  • Hansen P (2002) Effect of high pH on the growth and survival of marine phytoplankton: implications for species succession. Aquat Microb Ecol 28:279–288

    Google Scholar 

  • Harlin M, Rice E (1987) Allelochemistry in marine macroalgae. Crit Rev Plant Sci 5:237–249

    CAS  Google Scholar 

  • Hellio C, Simon-Colin C, Clare A, Deslandes E (2004) Isethionic acid and floridoside isolated from the red alga, Grateloupia turuturu, inhibit settlement of Balanus amphitrite cyprid larvae. Biofouling 20:139–145

    CAS  PubMed  Google Scholar 

  • Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642

    PubMed  Google Scholar 

  • Hutchinson GE (1975) A Treatise on Limnology. Vol. III. Limnological Botany, John Wiley & Sons, New York

  • Imai I, Fujimaru D, Nishigaki T (2002) Co-culture of fish with macroalgae and associated bacteria: A possible mitigation strategy for noxious red tides in enclosed coastal sea. Fish Sci 68:493–496

    Google Scholar 

  • Imai I, Fujimaru D, Nishigaki T, Kurosaki M, Sugita H (2006) Algicidal bacteria isolated from the surface of seaweeds from the coast of Osaka Bay in the Seto Inland Sea, Japan. Afr J Mar Sci 28:319–323

    Google Scholar 

  • Inaba T, Hori T, Aizawa H, Ogata A, Habe H (2017) Architecture, component, and microbiome of biofilm involved in the fouling of membrane bioreactors. NPJ Biofilms Microbiomes 3:5

    PubMed  PubMed Central  Google Scholar 

  • Inaba N, Kodama I, Nagai S, Shiraishi T, Matsuno K, Yamaguchi A, Imai I (2020) Distribution of harmful algal growth-limiting bacteria on artificially introduced Ulva and natural macroalgal beds. Appl Sci 10:5658

    CAS  Google Scholar 

  • Inderjit, Wardle DA, Karban R, Callaway RM (2011) The ecosystem and evolutionary contexts of allelopathy. Trends Ecol Evol 26:655-662

  • International Allelopathy Society (IAS) (1996) First World Congress on Allelopathy : A Science for the Future: Book of Abstracts. SAI (University of Cadiz), Cadiz, Spain, p 278

  • Jackson JBC, Donovan MK, Cramer KL, Lam VV (2014) Status and Trends of Caribbean Coral Reefs: 1970–2012. Global Coral Reef Monitoring Network, IUCN, Gland, Switzerland

  • Jeong JH, Jin HJ, Sohn CH et al (2000) Algicidal activity of the seaweed Corallina pilulifera against red tide microalgae. J Appl Phycol 12:37–43

    Google Scholar 

  • Jin Q, Dong S (2003) Comparative studies on the allelopathic effects of two different strains of Ulva pertusa on Heterosigma akashiwo and Alexandrium tamarense. J Exp Mar Biol Ecol 293:41–55

    Google Scholar 

  • Jin Q, Dong S, Wang C (2005) Allelopathic growth inhibition of Prorocentrum micans (Dinophyta) by Ulva pertusa and Ulva linza (Chlorophyta) in laboratory cultures. Eur J Phycol 40:31–37

    Google Scholar 

  • Jin Q, Wu H, Zhang X, Ke Z (2016) Influence of non-nutrient environmental factors on Ulva pertusa’s inhibitory effects on Heterosigma akashiwo growth. J Mar Biol Assoc UK 96:1041–1052

    Google Scholar 

  • Kabera JN, Semana E, Mussa AR, He X (2014) Plant secondary metabolites: Biosynthesis, classification, function and pharmacological properties. J Pharm Pharmacol 2:377–392

    Google Scholar 

  • Kakisawa H, Asari F, Kusumi T, Toma T, Sakurai T, Oohusa T et al (1988) An allelopathic fatty acid from the brown alga Cladosiphon okamuranus. Phytochemistry 27:731–735

    CAS  Google Scholar 

  • Kim MJ, Choi JS, Kang SE et al (2004) Multiple allelopathic activity of the crustose coralline alga Lithophyllum yessoense against settlement and germination of seaweed spores. J Appl Phycol 16:175–179

    Google Scholar 

  • Koivikko R, Eranen JK, Loponen J, Jormalainen V (2008) Variation of phlorotannins among three populations of Fucus vesiculosus as revealed by HPLC and colorimetric quantification. J Chem Ecol 34:57–64

    CAS  PubMed  Google Scholar 

  • Kuffner I, Walters L, Becerro M, Paul V, Ritson-Williams R, Beach K (2006) Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar Ecol Prog Ser 323:107–117

    ADS  Google Scholar 

  • Lane AL, Nyadong L, Galhena AS, Shearer TL, Stout EP, Parry RM, Kwasnik M, Wang MD, Hay ME, Fernandez FM, Kubanek J (2009) Desorption electrospray ionization mass spectrometry reveals surface-mediated antifungal chemical defense of a tropical seaweed. Proc Natl Acad Sci USA 106:7314–7319

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Legrand C, Rengefors K, Fistarol G, Granéli E (2003) Allelopathy in phytoplankton - biochemical, ecological and evolutionary aspects. Phycologia 42:406–419

    Google Scholar 

  • Longo GO, Hay ME (2017) Seaweed allelopathy to corals: Are active compounds on, or in, seaweeds? Coral Reefs 36:247–253

    ADS  Google Scholar 

  • Lourenço-Lopes C, Garcia-Oliveira P, Carpena M, Fraga-Corral M, Jimenez-Lopez C, Pereira AG, Prieto MA, Simal-Gandara J (2020) Scientific approaches on extraction, purification and stability for the commercialization of fucoxanthin recovered from brown algae. Foods 9:1113

    PubMed  PubMed Central  Google Scholar 

  • Lu H, Xie H, Gong Y, Wang Q, Yang Y (2011) Secondary metabolites from the seaweed Gracilaria lemaneiformis and their allelopathic effects on Skeletonema costatum. Biochem Syst Ecol 39:397–400

    CAS  Google Scholar 

  • Lv M, Yuan M, Wang Y, Tang X, Zhao Y (2021) Allelopathic effects of Ulva linza on marine phytoplankton and identification of the allelochemicals. Environ Sci Pollut Res 28:45714–45723

    CAS  Google Scholar 

  • Macίas FA, Galindo JLG, Garcίa-Dίaz MD, Galindo JCG (2008) Allelopathic agents from aquatic ecosystems: potential biopesticides models. Phytochem Rev 7:155–178

  • Maggi E, Bulleri F, Bertocci I, Benedetti-Cecchi L (2012) Competitive ability of macroalgal canopies overwhelms the effects of variable regimes of disturbance. Mar Ecol Progr Ser 465:99–109

    ADS  Google Scholar 

  • Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51:139–144

    PubMed  Google Scholar 

  • Ma Z, Wu M, Lin L, Thring RW, Yu H, Zhang X, Zhao M (2017) Allelopathic interactions between the macroalga Hizikia fusiformis (Harvey) and the harmful blooms-forming dinoflagellate Karenia mikimotoi. Harmful Algae 65:19–26

    PubMed  Google Scholar 

  • McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417

    ADS  Google Scholar 

  • Miller MW (1998) Coral/seaweed competition and the control of reef community structure within and between latitudes. Oceanogr Mar Biol 36:65–96

    Google Scholar 

  • Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097

  • Molisch H (1937) Der Einfluss einer Pflanze auf die Andere, Allelopathie. Gustav Fischer,  Jena 

    Google Scholar 

  • Muller CH (1969) Allelopathy as a factor in ecological process. Vegetatio 18:348–353

    Google Scholar 

  • Muzell Trezzi M, Vidal RA, Balbinot Junior AA, Von Hertwig Bittencourt H, Da Silva Souza Filho AP (2016) Allelopathy: Driving mechanisms governing its activity in agriculture. J Plant Interact 11:53-60

  • Nabivailo YV, Skriptsova AV, Titlyanov EA (2014) The interspecific relationships of seaweeds and their role in the formation of communities of Ahnfeltia tobuchiensis (Kanno et Matsubara, 1932) Makienko, 1970 (Rhodophyta). Russ J Mar Biol 40:344–353

    CAS  Google Scholar 

  • Nagayama K, Shibata T, Fujimoto K, Honjo T, Nakamura T (2003) Algicidal effect of phlorotannins from the brown alga Ecklonia kurome on red tide microalgae. Aquaculture 218:601–611

    CAS  Google Scholar 

  • Nakai S, Hosomi M, OkadaM Murakami A (1996) Control of algal growth by macrophytes and macrophyte-extracted bioactive compounds. Water Sci Technol 34:227–235

    CAS  Google Scholar 

  • Nakai S, Inoue Y, Hosomi M, Murakami A (2000) Myriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa. Water Res 34:3026–3032

    CAS  Google Scholar 

  • Nan C, Zhang H, Lin S, Zhao G, Liu X (2008) Allelopathic effects of Ulva lactuca on selected species of harmful bloom-forming microalgae in laboratory cultures. Aquat Bot 89:9–15

    Google Scholar 

  • Nan C, Zhang H, Zhao G (2004) Allelopathic interactions between the macroalga Ulva pertusa and eight microalgal species. J Sea Res 52:259–268

    Google Scholar 

  • Nelson T, Lee D, Smith B (2003) Are “green tides” harmful algal blooms? Toxic properties of water-soluble extracts from two bloom-forming macroalgae, Ulva fenestrata and Ulvaria obscura (Ulvophyceae). J Phycol 39:874–879

    CAS  Google Scholar 

  • Neori A, Chopin T, Troell M, Buschmann A, Kraemer G, Halling C et al (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231:361–391

    Google Scholar 

  • Nyadong L, Hohenstein EG, Galhena A, Lane AL, Kubanek J, Sherrill CD, Fernández FM (2009) Reactive desorption electrospray ionization mass spectrometry (DESI-MS) of natural products of a marine alga. Anal Bioanal Chem 394:245–254

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nylund G, Cervin G, Persson F, Hermansson M, Steinberg P, Pavia H (2008) Seaweed defence against bacteria: a poly-brominated 2-heptanone from the red alga Bonnemaisonia hamifera inhibits bacterial colonisation. Mar Ecol Prog Ser 369:39–50

    CAS  ADS  Google Scholar 

  • Nylund G, Gribben P, de Nys R (2007) Surface chemistry versus whole-cell extracts: antifouling tests with seaweed metabolites. Mar Ecol Prog Ser 329:73–84

  • Nylund GM, Pavia H (2003) Inhibitory effects of red algal extracts on larval settlement of the barnacle Balanus improvisus. Mar Biol 143:875–882

    Google Scholar 

  • Nylund GM, Persson F, Lindegarth M, Cervin G, Hermans-son M, Pavia H (2010) The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defence. FEMS Microbiol Ecol 71:84–93

    CAS  PubMed  Google Scholar 

  • Oh M, Lee S, Jin D, Hong Y, Jin H (2009) Isolation of algicidal compounds from the red alga Corallina pilulifera against red tide microalgae. J Appl Phycol 22:453–458

    Google Scholar 

  • Othmani A, Bunet R, Bonnefont J, Briand J, Culioli G (2016) Settlement inhibition of marine biofilm bacteria and barnacle larvae by compounds isolated from the Mediterranean brown alga Taonia atomaria. J Appl Phycol 28:1975–1986

    CAS  Google Scholar 

  • Paine RT (1990) Benthic macroalgal competition: complications and consequences. J Phycol 26:12–17

    Google Scholar 

  • Pansch C, Cerda O, Lenz M, Wahl M, Thiel M (2009) Consequences of light reduction for anti-herbivore defense and bioactivity against mussels in four seaweed species from northern-central Chile. Mar Ecol Prog Ser 381:83–97

    ADS  Google Scholar 

  • Paradas WC, Salgado LT, Sudatti DB, Crapez MA, Fujii MT, Coutinho R et al (2010) Induction of halogenated vesicle transport in cells of the red seaweed Laurencia obtusa. Biofouling 26:277–286

    PubMed  Google Scholar 

  • Paradas WC, Tavares Salgado L, Pereira RC, Hellio C, Atella GC, de Lima Moreira D, do Carmo AP, Soares AR, Menezes Amado-Filho G (2016) A novel antifouling defense strategy from red seaweed: Exocytosis and deposition of fatty acid derivatives at the cell wall surface. Plant Cell Physiol 57:1008-1019

  • Patil V, Abate R, Yang Y, Zhang J, Lin H, Chen C, Liang J, Sun L, Li X, Gao Y (2020) Allelopathic effect of Pyropia haitanensis (Rhodophyta) on the bloom-forming Skeletonema costatum (Bacillariophyta). J Appl Phycol 32:1275–1286

    CAS  Google Scholar 

  • Paul N, Cole L, de Nys R, Steinberg P (2006) Ultrastructure of the gland cells of the red alga Asparagopsis armata (Bonnemaisoniaceae). J Phycol 42:637–645

    Google Scholar 

  • Pereira RC, da Gama BA, Teixeira VL, Yoneshigue-Valentin Y (2003) Ecological roles of natural products of the Brazilian red seaweed Laurencia obtusa. Braz J Biol 63:665–672

    CAS  PubMed  Google Scholar 

  • Pereira RC, Soares AR, Teixeira VL, Villaça RC, da Gama BAP (2004) Variation on chemical defenses against herbivory in southwestern Atlantic Stypopodium zonale (Phaeophyta). Bot Mar 47:202–208

  • Pezzolesi L, Accoroni S, Rindi F, Samorì C, Totti C, Pistocchi R (2021) Survey of the allelopathic potential of Mediterranean macroalgae: production of long-chain polyunsaturated aldehydes (PUAs). Phytochemistry 189:112826

    CAS  PubMed  Google Scholar 

  • Plouguerné E, Cesconetto C, Cruz C, Pereira R, da Gama B (2012) Within-thallus variation in polyphenolic content and antifouling activity in Sargassum vulgare. J Appl Phycol 24:1629–1635

    Google Scholar 

  • Plouguerné E, Hellio C, Cesconetto C, Thabard M, Mason K, Véron B, Pereira RC, da Gama BAP (2010) Antifouling activity as a function of population variation in Sargassum vulgare from the littoral of Rio de Janeiro (Brazil). J Appl Phycol 22:717–724

    Google Scholar 

  • Qian H, Xu X, Chen W, Jiang H, Jin Y, Liu W, Fu Z (2009) Allelochemical stress causes oxidative damage and inhibition of photosynthesis in Chlorella vulgaris. Chemosphere 75:368–375

    CAS  PubMed  ADS  Google Scholar 

  • Ralph P (2000) Herbicide toxicity of Halophila ovalis assessed by chlorophyll a fluorescence. Aquat Bot 66:141–152

    CAS  Google Scholar 

  • Raniello R, Mollo E, Lorenti M, Gavagnin M, Buia MC (2007) Phytotoxic activity of caulerpenyne from the Mediterranean invasive variety of Caulerpa racemosa: a potential allelochemical. Biol Invasions 9:3

    Google Scholar 

  • Rasher D, Hay M (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci 107:9683–9688

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Rasher D, Hay M (2014) Competition induces allelopathy but suppresses growth and anti-herbivore defence in a chemically rich seaweed. Proc R Soc B Biol Sci 281:20132615

    Google Scholar 

  • Rasher D, Stout E, Engel S, Kubanek J, Hay M (2011) Macroalgal terpenes function as allelopathic agents against reef corals. Proc Natl Acad Sci 108:17726–17731

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Reis VM, Oliveira LS, Passos RM, Viana NB, Mermelstein C, Sant’anna C, Pereira RC, Paradas WC, Thompson FL, Amado-Filho GM, Salgado LT (2013) Traffic of secondary metabolites to cell surface in the red alga Laurencia dendroidea depends on a two-step transport by the cytoskeleton. PLoS One 8:e63929

    PubMed  PubMed Central  ADS  Google Scholar 

  • Reyes-Contreras M, Kazandjian A, Ballantine D (2016). Identification of compounds of allelopathic extracts from two species of Metapeyssonnelia (Rhodophyta) growing on the hydrocoral, Millepora complanata, in Puerto Rico. Gulf Caribbean Res 27

  • Rice EL (1984) Allelopathy, 2nd edn. Academic Press, New York, p 422

  • Rickert E, Karsten U, Pohnert G, Wahl M (2015) Seasonal fluctuations in chemical defenses against macrofouling in Fucus vesiculosus and Fucus serratus from the Baltic Sea. Biofouling 31:363–377

    CAS  PubMed  Google Scholar 

  • Rickert E, Lenz M, Barboza F, Gorb S, Wahl M (2016) Seasonally fluctuating chemical microfouling control in Fucus vesiculosus and Fucus serratus from the Baltic Sea. Mar Biol 163:203

  • Rogers CS, Miller J (2006) Permanent ‘phase shifts’ or reversible declines in coral cover? Lack of recovery of two coral reefs in St. John, US Virgin Islands. Mar Ecol Prog Ser 306:103–114

    ADS  Google Scholar 

  • Saha M, Wahl M (2013) Seasonal variation in the antifouling defence of the temperate brown alga Fucus vesiculosus. Biofouling 29:661–668

    CAS  PubMed  Google Scholar 

  • Salgado LT, Viana NB, Andrade LR, Leal RN, da Gama BA, Attias M, Pereira RC, Amado Filho GM (2008) Intra-cellular storage, transport and exocytosis of halogenated compounds in marine red alga Laurencia obtusa. J Struct Biol 162:345–355

    CAS  PubMed  Google Scholar 

  • Schmitt T, Hay M, Lindquist N (1995) Constrains on chemically mediated coevolution: multiple functions of seaweed secondary metabolites. Ecology 76:107–123

    Google Scholar 

  • Schoenwaelder MEA (2002) The occurrence and cellular significance of physodes in brown algae. Phycologia 41:125–139

    Google Scholar 

  • Shitan N (2016) Secondary metabolites in plants: transport and self-tolerance mechanisms. Biosci Biotechnol Biochem 80:1283–1293

    CAS  PubMed  Google Scholar 

  • Slattery M, Lesser M (2014) Allelopathy in the tropical alga Lobophora variegata (Phaeophyceae): mechanistic basis for a phase shift on mesophotic coral reefs? J Phycol 50:493–505

    PubMed  Google Scholar 

  • Śliwińska-Wilczewska S, Wiśniewska K, Konarzewska Z, Cieszyńska A, Barreiro Felpeto A, Lewandowska A, Latała A (2021) The current state of knowledge on taxonomy, modulating factors, ecological roles, and mode of action of phytoplankton allelochemicals. Sci Total Environ 773:145681

    PubMed  ADS  Google Scholar 

  • Sousa WP (1979) Disturbance in marine intertidal boulder fields: The nonequilibrium maintenance of species diversity. Ecology 60:1225

    Google Scholar 

  • Steinberg P, De Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621–629

    CAS  Google Scholar 

  • Sudatti D, Rodrigues S, Coutinho R, da Gama B, Salgado L, Amado Filho G, Pereira R (2008) Transport and defensive role of elatol at the surface of the red seaweed Laurencia obtusa (Ceramiales, Rhodophyta). J Phycol 44:584–591

    PubMed  Google Scholar 

  • Sun X, Xia YM, Xu NJ (2012) Allelopathic effects of Enteromorpha intestinalis (Ulvaceae, Chlorophyta) on Prorocentrum micans (Prorocentraceae, Dinophyta). Allelopath J 30:299–310

    Google Scholar 

  • Sun Yy, Zhou J, Han X, Zhang N, Yang Z, Zhang X (2021b) Several natural products isolated from a red alga Gracilaria lemaneiformis and its evaluation of antialgal activity against six common red tide microalgae. Environ Sci Pollut Res 28:22409–22426

    CAS  Google Scholar 

  • Svensson J, Nylund G, Cervin G, Toth G, Pavia H (2013) Novel chemical weapon of an exotic macroalga inhibits recruitment of native competitors in the invaded range. J Ecol 101:140–148

    CAS  Google Scholar 

  • Sylvers L, Gobler C (2021) Mitigation of harmful algal blooms caused by Alexandrium catenella and reduction in saxitoxin accumulation in bivalves using cultivable seaweeds. Harmful Algae 105:102056

    CAS  PubMed  Google Scholar 

  • Tang Y, Gobler C (2011) The green macroalga, Ulva lactuca, inhibits the growth of seven common harmful algal bloom species via allelopathy. Harmful Algae 10:480–488

    Google Scholar 

  • Tang YZ, Kang Y, Berry D, Gobler CJ (2015) The ability of the red macroalga, Porphyra purpurea (Rhodophyceae) to inhibit the proliferation of seven common harmful microalgae. J Appl Phycol 27:531–544

    CAS  Google Scholar 

  • Valenti T, James S, Lahousse M, Schug K, Roelke D, Grover J, Brooks B (2010) A mechanistic explanation for pH-dependent ambient aquatic toxicity of Prymnesium parvum carter. Toxicon 55:990–998

    CAS  PubMed  Google Scholar 

  • Vallim MA, De Paula JC, Pereira RC, Teixeira VL (2005) The diterpenes from dictyotacean marine brown algae in the tropical Atlantic American region. Biochem Syst Ecol 33:1–16

    CAS  Google Scholar 

  • Vermeij M, Dailer M, Smith C (2011) Crustose coralline algae can suppress macroalgal growth and recruitment on Hawaiian coral reefs. Mar Ecol Prog Ser 422:1–7

    ADS  Google Scholar 

  • Vyvyan J (2002) Allelochemicals as leads for new herbicides and agrochemicals. Tetrahedron 58:1631–1646

    CAS  Google Scholar 

  • Wang R, Feng L, Tang X, Wang J, Dong S et al (2012) Allelopathic growth inhibition of Heterosigma akashiwo by the three Ulva spcieces (Ulva pertusa, Ulva linza, Enteromorpha intestinalis) under laboratory conditions. Acta Oceanol Sin 31:138–144

    CAS  Google Scholar 

  • Wang R, Tang X (2016) Allelopathic effects of macroalga Corallina pilulifera on the red-tide forming alga Heterosigma akashiwo under laboratory conditions. Chin J Ocean Limnol 34 314–321

  • Wang RJ, Xiao H, Zhang PY, Qu L, Cai HJ, Tang X (2006) Comparative studies on the allelopathic effects of Ulva Pertusa Kjellml, Corallina pilulifera Postl et Ruprl, and Sargassum thunbergii Mertl O. Kuntze on Skeletonema costatum (Grev.) Cleve. J Integr Plant Biol 48:1415−1423

  • Wang R, Xiao H, Zhang P, Qu L, Cai H, Tang X (2007) Allelopathic effects of Ulva pertusa, Corallina pilulifera and Sargassum thunbergii on the growth of the dinoflagellates Heterosigma akashiwo and Alexandrium tamarense. J Appl Phycol 19:109–121

    PubMed  Google Scholar 

  • Wang S, Wang G, Weinberger F, Bian D, Nakaoka M, Lenz M (2017a) Anti-epiphyte defences in the red seaweed Gracilaria vermiculophylla: non-native algae are better defended than their native conspecifics. J Ecol 105:445–457

    CAS  Google Scholar 

  • Wang R, Wang Y, Zhou J, Sun J, Tang X (2013) Algicidal activity of Ulva pertusa and Ulva prolifera on Prorocentrum donghaiense under laboratory conditions. Afr J Microbiol Res 7:4389–4396

    Google Scholar 

  • Wang S, Weinberger F, Xiao L, Nakaoka M, Wang G, Krueger-Hadfield S, Sotka EE, Bin D, Lenz M (2017b) In situ common garden assays demonstrate increased defense against natural fouling in non-native populations of the red seaweed Gracilaria vermiculophylla. Mar Biol 164

  • White LF, Shurin JB (2011) Density dependent effects of an exotic marine macroalga on native community diversity. J Exp Mar Biol Ecol 405:111–119

    Google Scholar 

  • Wu JT, Chiang YR, Huang WY, Jane WN (2006) Cytotoxic effects of free fatty acids on phytoplankton algae and cyanobacteria. Aquat Toxicol 80:338–345

    CAS  PubMed  Google Scholar 

  • Xu D, Gao Z, Zhang X, Fan X, Wang Y, Li D, Wang W, Zhuang Z, Ye N (2012) Allelopathic interactions between the opportunistic species Ulva prolifera and the native macroalga Gracilaria lichevides. PLoS One 7:e33648

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Xu W, Tan L, Guo X, Wang J (2020) Isolation of anti-algal substances from Cylindrotheca closterium and their inhibition activity on bloom-forming Prorocentrum donghaiense. Ecotoxicol Environ Saf 190:110180

    CAS  PubMed  Google Scholar 

  • Ye C, Liao H, Yang Y (2014) Allelopathic inhibition of photosynthesis in the red tide-causing marine alga, Scrippsiella trochoidea (Pyrrophyta), by the dried macroalga, Gracilaria lemaneiformis (Rhodophyta). J Sea Res 90:10–15

    Google Scholar 

  • Young DN, Howard BM, Fenical W (1980) Subcellular localization of brominated secondary metabolites in the red alga Laurencia snyderae. J Phycol 16:182–185

    CAS  Google Scholar 

  • Zhang JH, Huo YZ, Zhang ZL, Yu KF, He Q, Zhang LH, Yang LL, Xu R, He PM (2013) Variations of morphology and photosynthetic performances of Ulva prolifera during the whole green tide blooming process in the Yellow Sea. Mar Environ Res 92:35–42

    CAS  PubMed  Google Scholar 

  • Zhang Y, Xu N, Li Y (2021) Effect of the Extracts of Sargassum fusiforme on Red Tide Microalgae in East China Sea. Front Mar Sci 8:628095

Download references

Author information

Authors and Affiliations

Authors

Contributions

Ilias Semmouri: Data collection, data analysis, Writing—Original Draft, Review & Editing; Colin Janssen: Supervision, Writing—Review & Editing; Jana Asselman: Supervision, Writing—Review & Editing.

Corresponding author

Correspondence to Ilias Semmouri.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 73 KB)

Supplementary file2 (DOCX 336 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Semmouri, I., Janssen, C.R. & Asselman, J. Allelopathy in macroalgae: Ecological principles, research opportunities and pitfalls reviewed. J Appl Phycol 36, 441–458 (2024). https://doi.org/10.1007/s10811-023-03110-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-023-03110-z

Keywords

Navigation