Introduction
The occurrence of weed species and their damaging effects on the environment, including crop and forest plantations, is a global challenge that has resulted in huge losses to practitioners as well as other stakeholders in the agricultural and forestry sectors.
The use of synthetic herbicides, which have dominated the pesticide market for several years, has been the main protocol for tackling the damaging effects of invasive plant or weed species (Qu et al. Reference Qu, He, Yang, Lin, Yang, Wu, Li and Yang2021). Globally, glyphosate, a commercially available broad-spectrum and systemic postemergence herbicide (Tataridas et al. Reference Tataridas, Kanatas, Chatzigeorgiou, Zannopoulos and Travlos2022), has to date been the most effective and widely used synthetic chemical treatment for the control and management of weed species (Kanissery et al. Reference Kanissery, Gairhe, Kadyampakeni, Batuman and Alferez2019; Wynn and Webb Reference Wynn and Webb2022). The economic losses that would be experienced by European Union (EU) farmers in the production of some major crops, including wheat (Triticum aestivum L.), potatoes (Solanum tuberosum L.), and grapes (Vitis vinifera L.), without the use of glyphosate are estimated at 24 billion kg (worth €10.5 billion), 10.4 billion kg (worth €2 billion), and 4.7 billion kg (worth €4.2 billion), respectively (Wynn and Webb Reference Wynn and Webb2022). However, there are problems associated with the use of synthetic herbicides, which includes non-target specificity as well as their nonbiodegradable nature, making them potentially hazardous to the environment and its inhabitants (Kanissery et al. Reference Kanissery, Gairhe, Kadyampakeni, Batuman and Alferez2019). An attempt to tackle their non–target specific nature, through the establishment of transgenic herbicide-resistant (HR) crops (Chahal et al. Reference Chahal, Varanasi, Jugulam and Jhala2017), still has its limitations (Green and Owen Reference Green and Owen2011), as this intervention has aided the evolution and widespread nature of extremely problematic HR weeds in the environment (Duke Reference Duke2011).
Approval for the use of glyphosate in the EU was recently renewed for 10 yr (Commission Implementing Regulation [EU] 2023/2660 of November 28, 2023), following a report by the European Food Safety Authority (EFSA) that revealed its active ingredient as showing no critical areas of concern with respect to endangering human and environmental health (Álvarez et al. Reference Álvarez, Arena, Auteri, Binaglia, Castoldi, Chiusolo, Crivellente, Egsmose, Fait, Ferilli, Gouliarmou, Nogareda, Ippolito, Istace and Jarrah2023). However, EU biosecurity measures and sustainable development goals (Tataridas et al. Reference Tataridas, Kanatas, Chatzigeorgiou, Zannopoulos and Travlos2022) are continually emphasizing the rational use of synthetic herbicides and the incorporation of natural herbicides (Álvarez-Rodríguez et al. Reference Álvarez-Rodríguez, Spinozzi, Sánchez-Moreiras, López-González, Ferrati, Lucchini, Maggi, Petrelli and Araniti2023). Hence, there is a serious drive to identify eco-friendly and sustainably viable bioherbicides as natural alternatives for replacing or augmenting synthetic chemical herbicides.
Seaweeds are very important natural resources highly abundant along the Irish coastline and other coastlines across the world, with potential that is yet untapped or not fully exploited. The harsh competitive marine environment they thrive in, which constitutes several biotic and abiotic stressors (Hu et al. Reference Hu, Duan, Lopez-Bautista, Hu and Fraser2016), stimulates them to synthesize and host a wide array of bioactive molecules (Cikoš et al. Reference Cikoš, Jurin, Čož-Rakovac, Gašo-Sokač, Jokić and Jerković2021; Salehi et al. Reference Salehi, Sharifi-Rad, Seca, Pinto, Michalak, Trincone, Mishra, Nigam, Zam and Martins2019) for adaptation and survival. These metabolites have given seaweeds and algae in general huge relevance, making them vital tools for natural product research applicable in several fields of study, including agriculture and forestry (Machado et al. Reference Machado, Santos Filho and Pavarini2019).
Studies on the possible use of seaweed extracts as novel bioherbicide sources is a relatively new area with very limited literature in this space (Chukwuma et al. Reference Chukwuma, Tan, Hughes, McLoughlin, O’Toole and McCarthy2023; Fonseca et al. Reference Ortiz-Ramírez, Cavalcanti, Ramos and Teixeira2012; Haniffa et al. Reference Haniffa, Ranjith, Dharmaratne, Yasin Mohammad and Choudhary2021; Rifana Reference Rifana2019). It may be that using seaweeds for weed suppression is contrary to popular belief, because from ancient times farmers have utilized seaweeds as organic matter (fertilizers or fertilizer supplements) for the enhancement of yields of different crops (Taylor et al. Reference Taylor, Harker and Robertson1993). Additionally, seaweeds are known to be very rich in micro- and macro-elements as well as other plant growth stimulatory molecules (Ali et al. Reference Ali, Ramsubhag and Jayaraman2021; Arioli et al. Reference Arioli, Mattner and Winberg2015; du Jardin Reference du Jardin2015). As such, researchers have focused more on the beneficial effects of seaweed extracts on plant growth and development, either as a biofertilizer or plant biostimulant (Ali et al. Reference Ali, Ramsubhag and Jayaraman2021; Crouch and Van Staden Reference Crouch and Van Staden1992; Godlewska et al. Reference Godlewska, Michalak, Tuhy and Chojnacka2016; Hassan et al. Reference Hassan, Ashour, Soliman, Hassanien, Alsanie, Gaber and Elshobary2021; Hernández-Herrera et al. Reference Hernández-Herrera, Santacruz-Ruvalcaba, Ruiz-López, Norrie and Hernández-Carmona2014; Vasantharaja et al. Reference Vasantharaja, Abraham, Inbakandan, Thirugnanasambandam, Senthilvelan, Jabeen and Prakash2019), as opposed to their plant growth inhibitory properties. Nevertheless, as seaweeds are prolific producers of diverse and complex secondary metabolites such as polysaccharides, pigments, phenols, alkaloids, terpenes, among others (Arioli et al. Reference Arioli, Mattner and Winberg2015), some of which are halogenated (Güven et al. Reference Güven, Percot and Sezik2010; Salehi et al. Reference Salehi, Sharifi-Rad, Seca, Pinto, Michalak, Trincone, Mishra, Nigam, Zam and Martins2019), they have shown a wide spectrum of biological properties, including phytotoxicity (Chukwuma et al. Reference Chukwuma, Tan, Hughes, McLoughlin, O’Toole and McCarthy2023; Fonseca et al. Reference Ortiz-Ramírez, Cavalcanti, Ramos and Teixeira2012; Haniffa et al. Reference Haniffa, Ranjith, Dharmaratne, Yasin Mohammad and Choudhary2021). Interestingly, several studies have reported terpenoids/terpenes, phenolics, fatty acids and steroids as groups of bioactive compounds associated with phytotoxic activities (Araniti et al. Reference Araniti, Lupini, Sunseri and Abenavoli2017; Espinosa-Colín et al. Reference Espinosa-Colín, Hernandez-Caballero, Infante, Gago, García-Muñoz and Sosa2023; Feitoza et al. Reference Feitoza, Lima, Oliveira, Oliveira, Moraes, Oliveira, Carvalho and Da Cunha2018; Pardo-Muras et al. Reference Pardo-Muras, Puig, Souto and Pedrol2020, Reference Pardo-Muras, Puig and Pedrol2022). Seaweeds are known to produce these bioactive compounds (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), which points to their capacity to serve as rich natural sources for novel bioherbicide formulation/development. This is also supported by several reports that have uncovered the allelopathic inhibitory effects of seaweeds on the same or other seaweed species, as well as other varying organisms occurring within the natural environment (Andras et al. Reference Andras, Alexander, Gahlena, Parry, Fernandez, Kubanek, Wang and Hay2012; Rasher and Hay Reference Rasher and Hay2010; Rasher et al. Reference Rasher, Stout, Engel, Kubanek and Hay2011; Sudatti et al. Reference Sudatti, Duarte, Soares, Salgado and Pereira2020; Vieira et al. Reference Vieira, Thomas, Culioli, Genta-Jouve, Houlbreque, Gaubert, De Clerck and Payri2016; Ye and Zhang Reference Ye and Zhang2013).
This review covers the use or application of seaweeds as biopesticides for sustainable agricultural/forestry pest management and focuses more specifically on their phytotoxic capabilities, which are indicative of their potential to be used as rich natural sources for novel bioherbicide development. Challenges to the development of bioherbicides from seaweeds and a potential path forward for the development of this research area are also discussed.
Seaweeds as Biopesticides for Sustainable Agricultural/Forestry Pest Management
The control of pests (including weed species) and diseases highly destructive to plants (crops and trees alike), remains a global issue. The use of chemically synthesized pesticides, which are known to persist in the environment, eventually accumulating and causing toxicities to the inhabitants (Buch et al. Reference Buch, Brown, Niva, Sautter and Sousa2013; Chagnon et al. Reference Chagnon, Kreutzweiser, Mitchell, Morrissey, Noome and Van Der Sluijs2015), is gradually being phased out. However, they will continue to remain a priority in controlling plant pests and diseases until better or low-risk alternatives are readily available. Currently, synthetic chemical pesticides are now either being augmented or totally replaced with biological control agents (which are living organisms, e.g., microbes, natural enemies/predators, plant-incorporated protectants) or natural products (bio-derived compounds), popularly known as biopesticides (Copping and Menn Reference Copping and Menn2000; Seiber et al. Reference Seiber, Coats, Duke and Gross2014).
The use of biopesticides rather than synthetic chemical pesticides is constantly gaining popularity around the globe because of their safety for non-target organisms and the environment in general and the relative ease of registering a biopesticide, especially in the United States (Copping and Menn Reference Copping and Menn2000). According to DunhamTrimmer (2019), North America and Europe are regions with the largest share, with over 60% of the total global biopesticide market (Figure 1). The Latin American market was forecast to grow faster than any other region, possibly because climatic conditions and other environmental factors within the region seems more favorable for the application or use of biopesticides (Figure 1).
Research into the pesticidal properties of seaweeds will continue to remain relevant to the fields of agriculture and forestry (Machado et al. Reference Machado, Santos Filho and Pavarini2019; O’Keeffe et al. Reference O’Keeffe, Hughes, McLoughlin, Tan and McCarthy2019b). Owing to the versatility of natural compounds present in seaweeds, there is no doubt that they are viable tools to help advance research in areas concerned with sustainable integrated pest management (IPM). The main aim of IPM is to drastically reduce or completely prevent the damaging effects of plant pests and diseases. The use of seaweed as a novel biopesticide encompasses biocidal properties. These properties include bioinsecticidal (Chanthini et al. Reference Chanthini, Senthil-Nathan, Stanley-Raja, Karthi, Sivanesh, Ramasubramanian, Abdel-Megeed, El Maghraby, Ghaith, Alwahibi, Elshikh and Hunter2021; Saber et al. Reference Saber, Hamed, Abdel-Rahim and Cantonati2018), biobactericidal/biofungicidal (Esserti et al. Reference Esserti, Smaili, Rifai, Koussa, Makroum, Belfaiza, Kabil, Faize, Burgos, Alburquerque and Faize2017, Reference Esserti, Smaili, Makroum, Belfaiza, Rifai, Koussa, Kasmi and Faize2018; O’Keeffe et al. Reference O’Keeffe, Hughes, McLoughlin, Tan and McCarthy2019a), bionematicidal (Ngala et al. Reference Ngala, Valdes, dos Santos, Perry and Wesemael2016; Sultana et al. Reference Sultana, Baloch, Ara, Ehteshamul-Haque, Tariq and Athar2011), as well as bioherbicidal (Chukwuma et al. Reference Chukwuma, Tan, Hughes, McLoughlin, O’Toole and McCarthy2023; Fonseca et al. Reference Ortiz-Ramírez, Cavalcanti, Ramos and Teixeira2012; Haniffa et al. Reference Haniffa, Ranjith, Dharmaratne, Yasin Mohammad and Choudhary2021) activities. Another group of biopesticides, known as biostimulants or biofertilizers, primarily protect plants by stimulating their growth and immunity against pests and diseases (Ali et al. Reference Ali, Ramsubhag and Jayaraman2021; du Jardin Reference du Jardin2015).
There are clearly more studies in the literature that have revealed the biobactericidal or biofungicidal activities of seaweed extracts in comparison to those that have demonstrated other biopesticide properties. Unfortunately, studies on seaweed bioherbicidal activities, which is the focus of this review and will be discussed in detail later, has the least research output available in literature (Table 1), showing the need to increase research efforts in this novel area.
Bioherbicides
Bioherbicides, which are often called biopesticides, are important tools for integrated weed management. There are two major types of bioherbicides, some of which are already commercially available: (1) natural products or allelochemicals derived from plants or other natural sources, commonly referred to as biochemical bioherbicides; and (2) microbial bioherbicides, or more specifically fungal bioherbicides, also referred to as mycoherbicides (Kalia and Mudhar Reference Kalia, Mudhar, Singh, Parmar and Kuhad2011).
Mycoherbicides are quite popular due to their ability to target host plants specifically and their easy application and production. Under standard laboratory conditions, these microbes are easily cultured and do not require highly specific nutrients for growth and mass production (Kalia and Mudhar Reference Kalia, Mudhar, Singh, Parmar and Kuhad2011). Biochemical bioherbicides are also gaining popularity, because they are eco-friendly and target specific (Roberts et al. Reference Roberts, Florentine, Fernando and Tennakoon2022). Biochemical bioherbicides use a variety of mechanisms/modes of action to unleash phytotoxic activities against weed species (Duke et al. Reference Duke, Pan, Bajsa-Hirschel and Boyette2022; Seiber et al. Reference Seiber, Coats, Duke and Gross2014). On the other hand, mycoherbicides have a basic mechanism of control that involves the invasion of vascular tissues once in contact with the host plant (Kalia and Mudhar Reference Kalia, Mudhar, Singh, Parmar and Kuhad2011; Roberts et al. Reference Roberts, Florentine, Fernando and Tennakoon2022). Additionally, microbial bioherbicides must first multiply and may have to compete with other microbes within the environment (Willoughby et al. Reference Willoughby, Seier, Stokes, Thomas and Varia2014). Hence, their spread and action is usually too slow (Duke et al. Reference Duke, Pan, Bajsa-Hirschel and Boyette2022), and this could reduce their effectiveness as a biocontrol treatment (Willoughby et al. Reference Willoughby, Seier, Stokes, Thomas and Varia2014). Moreover, if they spread successfully, the microbes can become native to the treated area, such that further application may not be needed, thereby, becoming a disincentive for commercialization (Duke et al. Reference Duke, Pan, Bajsa-Hirschel and Boyette2022). Kalia and Mudhar (Reference Kalia, Mudhar, Singh, Parmar and Kuhad2011) reported that under field conditions, mortality of weed plants caused by mycoherbicides was around 25% less compared with mycoherbicidal activity under laboratory conditions.
In light of this, the direct use of allelochemicals such as those that could be derived from seaweeds may possibly yield quicker herbicidal effects, as potent as or even more potent than those of synthetic herbicides. Furthermore, the tendency of natural compounds utilizing multiple mode(s) of action could help suppress or counteract the emergence of HR weed species (Duke et al. Reference Duke, Pan, Bajsa-Hirschel and Boyette2022; Seiber et al. Reference Seiber, Coats, Duke and Gross2014).
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).
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.
The Current Bioherbicide Market and Possible Constraints to the Development of Seaweed-derived Bioherbicides
Progress made on the identification and development (or formulation) of new bioherbicides has been quite slow, and there is a long way to go before they significantly impact the market as compared with the other biopesticides (bioinsecticides, biobactericides/biofungicides, and bionematicides) (Marrone Reference Marrone2024; Seiber et al. Reference Seiber, Coats, Duke and Gross2014). This might be partly due to the availability of glyphosate, a synthetic herbicide that has dominated the herbicide market for many years. This significantly reduces the overall value of the market and in turn results in a relatively reduced effort in the discovery of bioherbicides (Duke et al. Reference Duke, Pan, Bajsa-Hirschel and Boyette2022). It might also be in part due to the inconsistency in the performance of “potential” bioherbicides under field conditions, and as such, few have achieved long-term commercial success (Cordeau et al. Reference Cordeau, Triolet, Wayman, Steinberg and Guillemin2016).
Bioherbicides were first commercially available in the 1980s (Cordeau et al. Reference Cordeau, Triolet, Wayman, Steinberg and Guillemin2016). Although, the number of biopesticides has increased globally since then, bioherbicides still occupy an insignificant share, just 1% of the total market share of all biopesticides (DunhamTrimmer 2018; Marrone Reference Marrone2024). In 2016, it was reported that there were about 15 duly registered bioherbicides available in the market (Cordeau et al. Reference Cordeau, Triolet, Wayman, Steinberg and Guillemin2016). However, due to recent advances in the field of bioherbicide development, the number has increased to 23, most of which are commercially available in the United States, Canada, Australia, and Asia, with only 1 in Africa, while 2 are available in Europe: 1 in Belgium and 1 in France (Roberts et al. Reference Roberts, Florentine, Fernando and Tennakoon2022). Addition of about seven new bioherbicides to the market between the years 2016 and 2022 is relatively slow progress, again indicating the need to intensify research efforts in this area. However, in a recent review, Marrone (Reference Marrone2024) reported about 11 companies developing new bioherbicides, mostly based on metabolites, and some new innovative biotechnologies such as RNA interference (RNAi) and peptides; 3 of these companies (Bioprodex, Biohelp, and the Toothpick Project) have products already commercially available. It should be noted that the majority of these commercially available bioherbicides were derived from plants or are microbial-based. Therefore, it is envisioned that as seaweeds are abundant natural resources, further exploration into their use as potentially novel bioherbicide sources would greatly boost or enhance bioherbicide development and help increase available options.
As with any potential source of bioactive compounds, there are some limitations or challenges worth mentioning that could impede the development or formulation of bioherbicides from seaweeds. Some of them are described in the following sections.
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.
Prospects/Path Forward
Bioherbicides are very important tools for sustainable agricultural or forestry practices. Expansion of their role in integrated pest (weed) management necessitates an increased effort in searching for new potential bioherbicides and assessing their efficacy in the field (Cordeau et al. Reference Cordeau, Triolet, Wayman, Steinberg and Guillemin2016). Undoubtedly, natural compounds used as insecticides or fungicides with new molecular targets have gained more acceptance and achieved more commercial successes compared with those used as bioherbicides (Duke et al. Reference Duke, Pan, Bajsa-Hirschel and Boyette2022). However, bioherbicides such as those that could be derived from seaweeds have high potential impact and would likely gain traction in the market in the coming years. This is owing to the fact that 40% of the chemical pesticide market is currently herbicides (Marrone Reference Marrone2024). Moreover, no new synthetic herbicide with a significant mode(s) of action has been introduced or commercialized in the last 20 to 30 yr (Marrone Reference Marrone2024; Qu et al. Reference Qu, He, Yang, Lin, Yang, Wu, Li and Yang2021; Seiber et al. Reference Seiber, Coats, Duke and Gross2014), and with many being banned from use, there is room within the market for the rapid development and growth of bioherbicides. Unlike synthetic herbicides, natural compounds (or phytotoxins) have been shown to have several molecular targets or utilize multiple modes of action, indicating that they have potential to help cope with or eventually overcome the growing population of HR weeds (Dayan et al. Reference Dayan, Owens, Watson, Asolkar and Boddy2015; Duke et al. Reference Duke, Dayan, Romagni and Rimando2000, Reference Duke, Pan, Bajsa-Hirschel and Boyette2022; Seiber et al. Reference Seiber, Coats, Duke and Gross2014). The potential of natural compounds for having longer persistence and stronger potency than living microbes (easily constrained by environmental factors), positions them as more exciting and promising tools to explore as new bioherbicide options (Marrone Reference Marrone2024).
Therefore, the versatility and quantity of secondary metabolites noted to be present in seaweeds make them a preferred, sustainably viable option to explore as potentially novel bioherbicide sources to help increase the number of effective solutions available in the bioherbicide world market today. A report by the International Market Analysis and Research Consulting (IMARC) group forecast a compound annual growth rate of 12.8% for the global bioherbicide market between the years 2023 and 2028 (IMARC n.d.). This means that by 2028, the market is expected to reach a value of US$5 billion compared with its value as of 2022, which stood at US$2.4 billion (IMARC n.d.). This anticipated increase in the value of the market size of bioherbicides could be easily attained or surpassed through intensifying research and development efforts in areas exploring the use of seaweeds as potential bioherbicide sources.
Seaweeds are abundant natural resources along coastlines across the globe that have diverse chemical composition and bioactive properties. Reports on different seaweed species using allelochemicals to compete with one another and other varying organisms (An et al. Reference An, Wang, Li, Tian and Hu2008; Andras et al. Reference Andras, Alexander, Gahlena, Parry, Fernandez, Kubanek, Wang and Hay2012; Rasher and Hay Reference Rasher and Hay2010; Rasher et al. Reference Rasher, Stout, Engel, Kubanek and Hay2011; Sudatti et al. Reference Sudatti, Duarte, Soares, Salgado and Pereira2020; Vieira et al. Reference Vieira, Thomas, Culioli, Genta-Jouve, Houlbreque, Gaubert, De Clerck and Payri2016; Ye and Zhang Reference Ye and Zhang2013) signifies great potential for their use as bioherbicide sources. However, the limitations and challenges highlighted need to be addressed. According to Ash (Reference Ash2010), the major constraints to bioherbicide development and commercialization could be overcome by synergizing and providing a clear path in the processes involving scientific research and the business (product development and marketing) aspects of it, such that intellectual property is shared equitably among all parties involved. Most importantly, research, development, and regulations are required to overcome these constraints. This would help in harnessing and maximizing the full potential of deriving bioherbicides from seaweeds for use as novel, sustainable, and environmentally friendly alternatives to synthetic herbicides, and to increase available effective bioherbicides.
Acknowledgments
The authors would like to thank South East Technological University (SETU) and Irish Forestry Unit Trust Management Limited (IForUT) for funding this research. SETU PhD Co-fund Scholarship Programme, reference no. WIT_PhDCofund_2019_004. The authors declare no competing interests.