Seaweed Extracts as Potential Novel Bioherbicides or Bioherbicide Sources

As highlighted earlier, minimal research efforts have been put into studying the use of seaweed extracts as potential bioherbicides or bioherbicide sources (Table 1). A study by Brain et al. (Reference Brain, Lines, Booth, Ansell, Faulkner and Fenical1977), which did not directly explore seaweed bioherbicide potential, demonstrated the possibility that seaweed extracts could possess such phytotoxic properties. In this study, seaweed extracts were reported to enhance the herbicidal effects of a synthetic chemical herbicide, an auxin-type compound called mecoprop (also known as methylchlorophenoxypropionic acid or MCPP), when in combination with the herbicide. One possible mechanism suggested in the study for the increased herbicidal activity was that certain seaweed bioactive compounds such as polysaccharides and cytokinins interacted with the herbicide, facilitating the absorption of the herbicide and further disruption of metabolism within the plant. This resulted in a shorter/faster weed kill time compared with when mecoprop was used alone (Brain et al. Reference Brain, Lines, Booth, Ansell, Faulkner and Fenical1977).

In an earlier study, four crude extracts of the Brazilian red seaweed [Plocamium brasiliense (Greville) M. Howe & W.R. Taylor] were obtained using organic solvents of increasing polarity; n-hexane, dichloromethane, ethyl acetate, and ethanol/water (7:3) (Fonseca et al. Reference Ortiz-Ramírez, Cavalcanti, Ramos and Teixeira2012). These extracts, prepared to a concentration of 1% (w/v) were evaluated for any phototoxic activities against two pasture weed species, shameplant (Mimosa pudica L.) and sicklepod [Senna obtusifolia (L.) Irwin & Barneby]. It was observed that the dichloromethane extract produced the strongest inhibition of seed germination by 35.0% and 14.0%, radicle elongation by 52.0% and 41.7%, and hypocotyl development by 17.1% and 25.5%, respectively, in M. pudica and S. obtusifolia (Fonseca et al. Reference Ortiz-Ramírez, Cavalcanti, Ramos and Teixeira2012). Previous work carried out by the same research group on the chemotaxonomic analysis of the Brazilian red seaweed and, more specifically, the fractionation of the dichloromethane seaweed extract, revealed richness in halogenated monoterpenes (Ferreira et al. Reference Ferreira, Amaro, Cavalcanti, de Rezende, Galvão da Silva, Barbosa, de Palmer Paixão and Teixeira2010; Vasconcelos et al. Reference Vasconcelos, Ferreira, Pereira, Cavalcanti and Teixeira2010). Fonseca et al. (Reference Ortiz-Ramírez, Cavalcanti, Ramos and Teixeira2012) suggested that the halogenated monoterpenes were likely responsible for or played a key role in the phytotoxic activities displayed by the extract.

In a recent study, in which a phytotoxic screen of a range of seaweed extracts were tested against lettuce (Lactuca sativa L.) seeds, the ethyl acetate extract of two Rhodophyta species, Mastocarpus stellatus (Stackhouse) Guiry (MEE) and Porphyra dioica J. Brodie & L.M. Irvine (PEE) were found to be most active in reducing lettuce seedling growth (Chukwuma et al. Reference Chukwuma, Tan, Hughes, McLoughlin, O’Toole and McCarthy2023). In pre- and postplant emergence assays in lab trials, the phytotoxicities of both extracts were further evaluated against the broad-leaf weed white clover (Trifolium repens L.) and the grass Italian ryegrass [Lolium perenne L. ssp. multiflorum (Lam.) Husnot]. Preplant emergence phytotoxic activities displayed by both active red seaweed extracts at a concentration of 5 mg ml⁻¹ included a significant decrease in germination speed, significant inhibition of seed germination, and early seedling growth (Figure 2A and 2B). In the postplant emergence assay, overall plant growth was inhibited, and chlorosis of plant leaves, suspected to occur as a result of the inhibition of synthesis or enhanced degradation of leaf pigments, was also observed (Chukwuma et al. Reference Chukwuma, Tan, Hughes, McLoughlin, O’Toole and McCarthy2023; Figure 2C).

Figure 2. In vitro pre- and postplant emergence phytotoxicities of crude extracts of two red seaweeds (MEE and PEE). (A) Seed germination percentage in extract-treated and control plates over a 5-d period. (B, i and C, i) Solvent control plates; (B, ii and C, ii) MEE-treated plates; (B, iii and C, iii) PEE-treated plates. (Adapted from Chukwuma et al. Reference Chukwuma, Tan, Hughes, McLoughlin, O’Toole and McCarthy2023.)

Several recent studies have attributed phytotoxic properties to various phenolic compounds (Espinosa-Colín et al. Reference Espinosa-Colín, Hernandez-Caballero, Infante, Gago, García-Muñoz and Sosa2023; Facenda et al. Reference Facenda, Real, Galán-Pérez, Gámiz and Celis2023; Feitoza et al. Reference Feitoza, Lima, Oliveira, Oliveira, Moraes, Oliveira, Carvalho and Da Cunha2018; Galán-Pérez et al. Reference Galán-Pérez, Gámiz and Celis2021; Pardo-Muras et al. Reference Pardo-Muras, Puig, Souto and Pedrol2020, Reference Pardo-Muras, Puig and Pedrol2022), in addition to their well-known antioxidant properties (Zeb Reference Zeb2020). In the study by Chukwuma et al. (Reference Chukwuma, Tan, Hughes, McLoughlin, O’Toole and McCarthy2023), it was observed that the active red seaweed extracts (MEE and PEE) demonstrated significant levels of water-insoluble phenolic compounds, including phenolic acids and flavonoids. However, it was unlikely that the phenolics were solely responsible or played a major role in the observed phytotoxic activities, as the n-hexane extracts of the same red seaweeds, which also contained significant amounts of water-insoluble phenolics, displayed no inhibitory activities in the phytotoxic screen.

In another study by Haniffa et al. (Reference Haniffa, Ranjith, Dharmaratne, Yasin Mohammad and Choudhary2021), it was reported that among 16 aqueous seaweed extracts (comprising red, brown, and green species) screened for allelopathic inhibitory activity on lettuce seeds at a concentration of 1,000 ppm, 7 of the extracts produced significant inhibitory effects on lettuce seed germination and radicle growth. The extracts of Laurencia heteroclada Harvey, Caulerpa racemosa (Forsskål) J. Agardh, and Caulerpa sertularioides (S. G. Gmelin) M. Howe exhibited the strongest inhibition of lettuce seed germination, resulting in germination percentages of 17.5%, 25%, and 18%, respectively, values significantly lower than the distilled water control (85.0%). The extract of C. racemosa produced the strongest plant growth inhibitory effect, resulting in the smallest mean radicle length of 0.63 ± 0.197 cm, which was also significantly smaller than the control (3.33 ± 0.172 cm) (Haniffa et al. Reference Haniffa, Ranjith, Dharmaratne, Yasin Mohammad and Choudhary2021). Having produced the most significant inhibition on seed germination, bioactive compounds present in the active red seaweed (L. heteroclada) extract were further isolated and identified to include nonaromatic cuparane, algoane, caulerpin, cholesterol, and a new brominated nonaromatic isolaurene-type sesquiterpene. However, only algoane showed moderate activities against lettuce seed germination and radicle growth, when the pure compounds (solvated in methanol and prepared to a concentration of 1,000 ppm) were individually tested for phytotoxic activities. It was suggested that two or more components of the active aqueous red seaweed extract acted in synergy or were required to elicit the phytotoxic effects observed (Haniffa et al. Reference Haniffa, Ranjith, Dharmaratne, Yasin Mohammad and Choudhary2021).

Several different classes of natural products or secondary metabolites derived particularly from plants or microbes have been associated with varying phytotoxic activities (Table 2). Seaweeds have been shown to be a rich source of these bioactive compounds, as well as being prolific producers of more diverse and complex biomolecules (Gómez-Guzmán et al. Reference Gómez-Guzmán, Rodríguez-Nogales, Algieri and Gálvez2018; Gunathilake et al. Reference Gunathilake, Akanbi, Suleria, Nalder, Francis and Barrow2022; Salehi et al. Reference Salehi, Sharifi-Rad, Seca, Pinto, Michalak, Trincone, Mishra, Nigam, Zam and Martins2019; Santos et al. Reference Santos, Félix, Pais, Rocha and Silvestre2019). This indicates that further exploration into establishing seaweed phytotoxic potential and an increased effort in the development or formulation of seaweed-derived bioherbicides would likely yield desirable/positive outcomes.

Table 2. Some bioactive compounds derived from plant or microbes associated with phytotoxic properties.

Variability in Chemical Composition

Seaweeds are morphologically complex organisms with diverse chemical compositions that vary greatly depending on factors such as seaweed species, location of habitat, and environmental conditions. These factors could influence variable extraction yields, which might indicate an alteration in the availability or concentrations of the desired bioactive compound(s), and could in turn lead to reduction or loss of efficacy (Afonso et al. Reference Afonso, Correia, Freitas, Baptista, Neves and Mouga2021; Aroyehun et al. Reference Aroyehun, Palaniveloo, Ghazali, Rizman-Idid and Abdul Razak2019; Arunkumar and Sivakumar Reference Arunkumar and Sivakumar2012; Marinho-Soriano et al. Reference Marinho-Soriano, Fonseca, Carneiro and Moreira2006; Sanz et al. Reference Sanz, Torres, Domínguez, Pinto, Costa and Guedes2023; Tan et al. Reference Tan, O’Sullivan, Prieto, Gardiner, Lawlor, Leonard, Duggan, McLoughlin and Hughes2012). Thus, it is challenging to standardize the extraction process and ensure consistent bioherbicide formulations with predictable concentrations of the desired bioactive compounds. This is why the application of natural product discovery strategies such as bioactivity-guided isolation or fractionation-driven bioassay (Duke et al. Reference Duke, Dayan, Romagni and Rimando2000), which aid the isolation and identification of the responsible bioactive compound(s) in such active extracts, is an important step in the research and development process. However, in many cases, desired activity is often lost or greatly diminished when the diversity and complexity of molecules in crude extracts are simplified to yield individual compounds (Duke et al. Reference Duke, Dayan, Romagni and Rimando2000).

Regulatory Approval

The regulatory approval process for bioherbicides as with all other biopesticides can be time-consuming, capital intensive, and high risk (Marrone Reference Marrone2024). Seaweed extracts or their bioactive compounds for potential use as bioherbicides would need to undergo rigorous ecotoxicological testing for safety or undesired environmental impact before obtaining regulatory approval for commercial use. As natural compounds, they are expected to be eco-friendly and have a shorter half-life than synthetic chemical herbicides (Cordeau et al. Reference Cordeau, Triolet, Wayman, Steinberg and Guillemin2016; Duke et al. Reference Duke, Dayan, Romagni and Rimando2000). However, such natural phytotoxins that could potentially be derived from seaweeds may not be completely harmless to other non-target life forms, including mammals (Cordeau et al. Reference Cordeau, Triolet, Wayman, Steinberg and Guillemin2016), and their spectrum of biological activity should be carefully evaluated (Duke et al. Reference Duke, Dayan, Romagni and Rimando2000). In fact, natural compounds have been noted to be some of the most potent mammalian toxins (Duke et al. Reference Duke, Dayan, Romagni and Rimando2000). Interestingly, the red seaweed species especially, are known to produce bioactive compounds usually associated with halogen atoms (Sudatti et al. Reference Sudatti, Duarte, Soares, Salgado and Pereira2020). For example, Asparagopsis taxiformis (Delile) Trevisan and Asparagopsis armata Harvey are two Rhodophyta species known for the production of the bromoform (CHBr₃), an antimethanogenic compound that is currently being considered a potential ecotoxicological risk and could have other damaging effects in the environment, such as ozone layer depletion (Glasson et al. Reference Glasson, Kinley, de Nys, King, Adams, Packer, Svenson, Eason and Magnusson2022; Jia et al. Reference Jia, Quack, Kinley, Pisso and Tegtmeier2022). It is important to note that the presence of a halogen substitute in the structure of synthetic herbicides has aided their increased persistence (half-life) and environmentally toxic properties (Soltys et al. Reference Soltys, Krasuska, Bogatek and Gniazdowsk2013).

Formulation and Stability

Developing stable and effective formulations of bioherbicides from seaweeds can be challenging. Appropriate formulation techniques such as encapsulation, emulsification, or the addition of adjuvants (Ash Reference Ash2010; Cordeau et al. Reference Cordeau, Triolet, Wayman, Steinberg and Guillemin2016; Hallett Reference Hallett2005; Marrone Reference Marrone2019; Roberts et al. Reference Roberts, Florentine, Fernando and Tennakoon2022; Seiber et al. Reference Seiber, Coats, Duke and Gross2014; Campos et al. Reference Campos, Ratko, Bidyarani, Takeshita and Fraceto2023) may be required to enhance the solubility, stability/shelf-life, and efficacy of the specific bioactive compound against target weeds, and to protect it from adverse environmental conditions. There are reports that have shown inconsistency or failure of potential bioherbicides to replicate in field or greenhouse studies the phytotoxic activities previously displayed in vitro (in lab trials), possibly due to soil conditions/microbial activities or other environmental conditions (Travaini et al. Reference Travaini, Sosa, Ceccarelli, Walter, Cantrell, Carrillo, Dayan, Meepagala and Duke2016). Hence, conducting tests that yield positive results from mimicking real-world situations is needed. Such reduction or loss of efficacy could be a consequence of poor formulation, which could affect certain properties of the natural compounds or enhance their biodegradation in the field (or soil) after application (Chuah et al. Reference Chuah, Tan and Ismail2013; Facenda et al. Reference Facenda, Real, Galán-Pérez, Gámiz and Celis2023; Galán-Pérez et al. Reference Galán-Pérez, Gámiz and Celis2021). Poor storage of the extractable materials or the crude extracts generated from them has also been shown to affect stability as well as efficacy of the bioactive compounds they contain (Laher et al. Reference Laher, Aremu, Van Staden and Finnie2013; Srivastava et al. Reference Srivastava, Akoh, Yi, Fischer and Krewer2007; Stafford et al. Reference Stafford, Jäger and van Staden2005). This is due to the occurrence of reactions (influenced by storage conditions) that could chemically modify the bioactive compounds, thereby altering their composition or concentration.

Cost and Scalability

Another challenge is the cost of seaweed extraction, formulation, and production. In general, marketing/commercialization cost of bioherbicides is relatively high compared with cheaper and already commercially available synthetic herbicides (Ash Reference Ash2010; Stefanski et al. Reference Stefanski, Camargo, Scapini, Bonatto, Venturin, Weirich, Ulkovski, Carezia, Ulrich, Michelon, Soares, Mathiensen, Fongaro, Mossi and Treichel2020). There is no doubt that the research and development of seaweed-derived bioherbicides through to commercialization would be highly capital intensive, as previously noted for other bioherbicides/biopesticides in the market (Marrone Reference Marrone2019, Reference Marrone2024). Moreover, large-scale seaweed farming, harvesting, and processing is labor intensive and requires significant investment in infrastructure and equipment. This could be disincentivizing or affect the profitability of producing such seaweed-derived bioherbicides on a commercial scale (Soltys et al. Reference Soltys, Krasuska, Bogatek and Gniazdowsk2013). Hence, cost-effective and scalable seaweed production methods need to be developed (Kite-Powell et al. Reference Kite-Powell, Ask, Augyte, Bailey, Decker, Goudey, Grebe, Li, Lindell, Manganelli, Marty-Rivera, Ng, Roberson, Stekoll, Umanzor and Yarish2022) to make bioherbicides that could be potentially derived from seaweeds commercially viable and sustainable. This is why relevant support through increasing available government or private sector funding to universities and research institutions and more investments in start-ups involved in the area of bioherbicide formulation or development would be key for any progress to be made (Marrone Reference Marrone2024).

Environmental Considerations

Continuous large-scale seaweed harvesting to sustain production could have potential environmental or ecological impacts on biodiversity and on the marine environment as a whole. Although, the allelochemicals derived from seaweeds are generally considered environmentally friendly alternatives to chemical herbicides, careful monitoring and mitigation measures need to be in place to ensure sustainable and environmentally responsible production practices. The development of seaweed aquaculture production systems is a vital approach to recovery or replacement of such depleted seaweeds (García-Poza et al. Reference García-Poza, Leandro, Cotas, Cotas, Marques, Pereira and Gonçalves2020; Kim et al. Reference Kim, Yarish, Hwang, Park and Kim2017). Additionally, new techniques, including synthetic biology, molecular biology, genomics, metabolomics, among others (Marrone Reference Marrone2024; Soltys et al. Reference Soltys, Krasuska, Bogatek and Gniazdowsk2013), are important tools that have been applied to identify genes of interest in order to engineer fast-growing organisms in the lab to yield such phytotoxic compounds with reduced/no environmental considerations.

Weed Spectrum and Efficacy

The efficacy of seaweed extracts or the specific bioactive compound(s) as a bioherbicide may vary depending on the type of weeds targeted (Chukwuma et al. Reference Chukwuma, Tan, Hughes, McLoughlin, O’Toole and McCarthy2023), and they may not be very effective against a wide range of weed species. This could be as a result of the yield of extract obtained or, more specifically, the concentration of responsible bioactive compound(s) present in the seaweed extract, which may be low (requiring excessive extraction). Thus, their phytotoxicities may be short-lived and lack long-term impact. As such, further research is needed to identify the active compounds and determine the spectrum of weeds that can be effectively controlled by seaweed-derived bioherbicides.