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INTRODUCTION
Crop pathogens and pests are responsible for massive agricultural losses worldwide (Roy et al., 2022). Moreover, the continuous and increasing use of synthetic chemical products to control these issues represents a constant risk to human health and the environment (Shkula et al., 2021). In developing countries such as Ecuador, agriculture has been regarded as an enemy of the environment due to the lack of strict regulations regarding the use of harmful active ingredients. Meanwhile, in continents like Europe, efforts are already underway to suppress the use of agrochemicals, as is the case of the From farm to fork strategy, which, within its objectives for 2023, aims to reduce the use of pesticides and synthetic fertilizers. In this vein, sustainable agricultural practices will merit novel and environmentally friendly compounds that foster plant immunity against pathogens (European Comission et al., 2020).
It is known that plants respond to pathogen attacks in two main ways: acquired or induced systemic resistance (Shukla et al., 2021). At present, some researchers are focusing their attention on sustainable induced biotic resistance strategies by means of natural elicitors (Patel et al., 2018; Shukla et al., 2021; Roy et al., 2022). Incorporating them in the production of various crops entails a broad range of positive responses in the plant-soil system. According to Agarwal et al. (2021), algae extracts, which are rich in biomolecules, act as bio-elicitors to improve plants’ tolerance to diseases. Agarwal et al. (2021) suggest that the extracts from a diversity of algae stimulate defense mechanism at the physiological, biochemical, and molecular levels, regulating signaling pathways, oxidative stress homeostasis, and the expression of defensive genes and enzymes. In addition, they modulate the rhizosphere microbiota, reinforcing protection against pathogens. Ali et al. (2021) posit that the efficacy of these extracts is due to a complex mixture of organic and inorganic substances, not to individual components, highlighting the importance of the interaction between an extract’s diverse components.
In Spain and the United States, there are leading companies in the production of algae-based biostimulants and bio-fertilizers. These companies possess substantial evidence regarding algae extracts and their antiviral, antibacterial, or antifungal properties, making them promising substitutes for enhancing plant defenses (Roy et al., 2022). In this vein, stimulating plant immunity using seaweed extracts could be a feasible strategy for naturally increasing immunity while aiming to reduce the use of pesticides in agricultural countries (Shukla et al., 2021). In addition, it represents an opportunity for the development of new industries.
Seaweeds are classified into three major groups: Chlorophytes (green), Phaeophytes (brown), and Rhodophytes (red). These marine organisms are relatively abundant in the coastal zone of Ecuador, a country with a coastal continental profile of 2860 km (Jiménez and Torres, 2023), where Salinas Bay and the Gulf of Guayaquil have recorded the greatest diversity of species (Jiménez and Torres, 2023; Valverde-Balladares and Armas, 2023). With the purpose of promoting innovative alternatives for the current issues with agrochemicals, this literature review aimed to synthesize the biotechnological potential of macroalgae within the Ecuadorian agricultural sector, focusing on the cultivation of Kappaphycus alvarezii (Doty) Doty ex PCSilva 1996 (Solieriaceae), Acanthophora spicifera (M. Vahl) Børgesen 1910 (Rhodomelaceae), and Hypnea spinella (C. Agardh) Kützing 1847 (Cystocloniaceae) as part of a sustainable option for the development of products related to improving the quality of the crops grown in the country.
Methodological search strategy
For this review, the Google Scholar, PubMed, ScienceDirect, SciELO, and Springer databases were used to collect relevant articles. The key terms employed (in Spanish) included “Metabolites in Kappaphycus alvarezii, Acanthophora spicifera, and Hypnea spinella”, “agrochemicals in Ecuadorian crops”, and “sap from K. alvarezii, A. spicifera, and H. spinella”. The research questions that motivated this article were what are the bioactive compounds present in macroalgae that can be used to improve the quality of crops in agricultural countries? and what are the metabolites present in K. alvarezii, A. spicifera, and H. spinella that have potential biopesticidal, biofertilizer, or biostimulant properties? The search was limited to research articles published in English and Spanish during the 2002-2023 period. The findings from the last two decades helped to elaborate a table and discuss advancements with a national focus for the utilization of the aforementioned macroalgae in crops which use agrochemicals at unacceptable concentrations.
Overview of macroalgae
Seaweeds are one of the main components of primary producers (Ali et al., 2021) and play a significant role in the marine ecosystem. They serve as food for a wide variety of organisms, from fish to marine mammals. They also contribute to the formation of coral reefs and the protection of coastlines against erosion (Murugaiyan, 2020). Their cultivation aligns with the principles of sustainable production, as they can mitigate about 200 million tons of CO2/year (FAO, 2022) without the need for freshwater or competition for land regarding food production (Rudke et al., 2020). Seaweeds can reduce nitrogen and phosphorus concentrations in aquatic systems, acting as a natural source of these elements (FAO, 2022).
Macroalgae contain a wide range of chemical compounds, highlighting polysaccharides, amino acids, enzymes, polyphenols, phlorotannins, plant pigments, unsaturated fatty acids, sterols, osmoprotectants, antimicrobial compounds, and plant hormones (Agarwal et al., 2021). However, these bioactive compounds can vary due to factors such as the species, harvest location, season, environmental conditions, and extraction method (Matos et al., 2021; Lema Ch. et al., 2023). The polyphenols and polysaccharides that characterize algae can act as elicitors at low concentrations, inducing immunity against plant pathogens by recognizing molecular patterns associated with them, which can bind to recognition receptors on the plant cell membrane. Their binding to the receptor on the plant cell membrane leads to the activation of signaling events that trigger a defense response (Shukla et al., 2021). The presence of these bioactive compounds has sparked the interest of various agrochemical companies for the production of commercial biostimulants using algae biomass. In addition, these compounds can be mixed into agricultural formulations containing urea, humic acids, potassium sulfate, and ammonium phosphate for plant growth and development (Flórez-Jalixto et al., 2021).
In the littoral of Ecuador, a total of 345 species of algae have been identified, out of which 13.9 % correspond to Chlorophyta, 14.4 % to Phaeophyta, and 77.7 % to Rhodophyta (Valverde-Balladares and Armas, 2023). Each group contains a diversity of secondary metabolites that confer multiple properties used commercially for various purposes, including agriculture (Illera-Vives et al., 2020). Within the group of red algae in Ecuador, Kappaphycus alvarezii, Acanthophora spicifera, and Hypnea spinella are underutilized at the local level, as they primarily provide profit as phycocolloids, but they are characterized by several additional metabolites of biotechnological interest (Table 1). Most of their production is concentrated in the province of Santa Elena, on the Ecuadorian Pacific coast, and is destined for the United States, Europe, and Asia.
Table 1 Bioactive compounds from K. alvarezii, A. spicifera, and H. spinella. GAE: equivalent gallic acid, DPPH: 2,2-diphenyl-1-picrylhydrazyl. Ps: dry weight, Pf: fresh or wet weight, -: not reported.
Despite its favorable tropical climatic conditions and extensive coastal areas, Ecuador is still in the early stages of development regarding algae production and cultivation. This is reflected in its absence among the major global algae producers (Cai et al., 2021). In 2019, the global seaweed production reached 35.8 million tons, with the participation of 49 countries and territories (Cai et al., 2021). Asia concentrates 97 % of the global production, whereas, in America and Europe, there is a predominance of wild harvesting. In contrast, cultivation is the main method in Asia, Africa, and Oceania (Cai, 2021).
The nascent algae production in Ecuador can be attributed to its short history regarding the controlled cultivation of this resource. However, the country has the potential to perform this activity, as indicated by the FAO report titled Algae and microalgae: An overview to unlock their potential in the development of global aquaculture, which mentions Ecuadorian production of the genera Kappaphycus and Eucheuma, albeit with a global percentage of less than 0.01 % (Cai et al., 2021).
According to Jiménez and Torres (2023) , Ecuador has appropriate conditions to expand its diversification of aquaculture, with a greater focus on macroalgae cultivation, especially in the province of Santa Elena., In their research, they identify at least 10 locations along the Ecuadorian coast, spread across five provinces, that meet the oceanographic, environmental, biological, and social characteristics for establishing new macroalgae marine farms (Figure 1).
Figure 1 Coastal provinces of Ecuador with suitable oceanographic parameters for macroalgae cultivation according to Jiménez and Torres (2023) . Santa Rosa, Salinas - main cultivation area for K. alvarezii. Other sectors within the province of Santa Elena with floating systems for macroalgal cultivation.
Works such as Montúfar-Romero et al. (2023) demonstrate that the growth of the macroalgae K. alvarezii in Ecuador exceeds previous studies conducted in other tropical and subtropical regions. The daily growth rate obtained in that study was 15.2 % g.day-1, surpassing previous data on both the Atlantic and Asia. The geographical characteristics and favorable conditions for macroalgae growth in Ecuador, together with promising results from studies such as Jiménez and Torres (2023) and Montúfar-Romero et al. (2023), show an encouraging landscape for the development of macroalgae cultivation in the country.
Effect of applying macroalgae-based biostimulants in different crops
According to the Foreign Trade Bulletin (2023), Ecuador’s fruit exports have increased in recent years. In 2022, the value of Ecuador’s fruit exports was $1.2 billion. This growth is due to several factors, including the increasing demand for Ecuadorian fruits in international markets, improvements in the quality of Ecuadorian fruits, and the expansion of fruit production in Ecuador.
The use of macroalgae in sustainable agriculture is a practice that is gaining popularity in Ecuador. The Ecuadorian government is supporting the advancement of this practice, as it offers an opportunity to enhance the sustainability of agriculture in the country. Therefore, it is important to consider the suitability and nutritional richness of the waste from red macroalgae for use in sustainable agriculture in Ecuador.
Kappaphycus, Laminaria, Ascophyllum, Enteromorpha, Sargassum, and Ulva are the macroalgae genera most commonly used worldwide for the manufacture of plant biostimulants in the form of liquid concentrate and soluble powder (Cai et al., 2021; Pandya and Mehta, 2023). Their organic matrix is generally complex, composed of trace elements, minerals (Table 2), amino acids, lipids, carbohydrates, and promoting hormones (auxins, cytokinins, gibberellins, and betaines), which are responsible for elicitor and phyto-stimulatory activities (Mondal et al., 2015; Michalak et al., 2016). Other macroalgae genera are also used in the manufacture of biostimulants, such as Porphyra, Codium, Gracilaria, and Chlorella (Khan et al., 2009).
Table 2 Mineral nutrient content (mg/100 g Dw) of macroalgae used to formulate biostimulants. Na: sodium, K: potassium, Ca: calcium, Mg: magnesium, P: phosphorus, S: sulfur, Fe: iron, Zn: zinc, Mn: manganese, -: not reported.
Algae-based extracts have been tested on different crops common in Ecuadorian agriculture, demonstrating their potential even with small doses. Due to their nutrient content, algae-based extracts have shown plants to provide improved flower setting, biomass yield, seed germination, and fruit production, as well as enhanced post-harvest shelf life in various crops, which acquire greater resistance to different phytopathogens (Mantri et al., 2017). Roy et al. (2022) studied the impact of the foliar application of K. alvarezii sap on rice previously infected with the bacterial blight disease. In their study, they showed that crops treated with extracts had lower levels of disease severity and produced higher yields as a result of increased plant antibacterial defenses. In another experiment aimed at evaluating the effect of four bioformulations of K. alvarezii on banana crops during the vegetative and flowering stages, it was observed that foliar application at a dose of 1 mL/L significantly improved cluster weight by 25.24 % with respect to the water control (Ravi et al., 2018). Similarly, other researchers have used K. alvarezii sap as a seaweed biofertilizer to promote the growth, yield, and improvement of potatoes and tomatoes (Pramanick et al., 2017). It has been recorded that the influence of two red seaweed species, K. alvarezii with S. wightii and A. spicifera with S. vulgare, contributes to mitigating bacterial spot and early blight disease while improving crop growth characteristics, such as height, the number of leaves, chlorophyll content, and yield, when applied as foliar spray on tomatoes (Ali et al., 2022; Vaghela et al., 2023). Spraying Gracilaria spp. with a 15 % dose of fertilizers on rice reported increased growth and improved grain and straw yields (Layek et al., 2018).
The benefits associated with the use of extracts from different algae in crops support various authors’ claims (Hassan et al., 2021) that position algae extract biostimulants as one of the best sustainable promoters of biological growth (Table 3). This assertion is reinforced by the market presence of over 15 commercial products whose results are backed by rigorous scientific studies (Illera-Vives et al., 2020).
Action mechanism algae extract-based biostimulants
Roy et al. (2022) evaluated two commercial formulations of K. alvarezii and demonstrated that their foliar application, before or after infection, induces a superior antibacterial defensive response in comparison with untreated plants. The treated plants accumulated higher levels of salicylic acid, a key defensive hormone, and exhibited a greater expression of associated immune genes. In addition, the treatments with the extract increased the endogenous levels of jasmonic acid and cytokinin, accompanied by a greater expression of their corresponding sensitive genes. These results suggest that K. alvarezii extract has a significant potential to enhance plant defenses against bacterial pathogens.
On the other hand, Patel et al. (2018) evaluated the impact of K. alvarezii sap on three commercially important varieties of durum wheat under saline and drought stress during vegetative and reproductive phases. Under saline stress conditions, the plants treated with the sap showed a lower Na+/K+ ratio and a higher Ca2+ content. Moreover, the sap mitigated cell membrane damage by maintaining a higher water content in the tissue and reducing electrolyte leakage and malondialdehyde content. Reactive oxygen species, superoxide, and peroxide levels were also significantly reduced in the treatment based on K. alvarezii. Osmoprotectants such as total proteins, proline, amino acids, and soluble sugars increased with the application of K. alvarezii sap both under and in the absence of stress conditions. Phytohormones (abscisic acid, cytokinin, and auxin) were significantly regulated with the application of the sap, and they significantly improved the yield by increasing the number of spikes and grains (Figure 2).
According to Samuels et al. (2022), seaweed extracts exert their beneficial effects on plants through three main mechanisms: a better nutrient acquisition, the inhibition of chlorophyll degradation, and the triggering of defense responses. The application of seaweed extracts stimulates the production of auxins, gibberellins, and cytokinins, improving the uptake of essential nutrients such as N, P, K, Fe, and Zn. Seaweed extracts, rich in betaines and glycine betaine, protect plant cells from abiotic stress by preserving chlorophyll, complex proteins, antioxidant enzymes, and the photosystem II. The polysaccharides from algal cell walls (ulvans, laminarins, carrageenans) act as triggers for plant defense responses. Resistance mechanisms against pathogens are induced by the accumulation of pathogenesis-related proteins, enzymes such as chitinases and glucanases, and phenolic molecules. Other authors suggest that seaweed extracts with a high content of indole-3-acetic acid, like Ascophyllum nodosum and Laminaria spp. are effective in promoting root morphological traits in maize (Rouphael and Colla, 2020).
Seaweed extract formulations: emerging trends and techniques
At present, most commercial seaweed extract products are elaborated from brown algae such as Ascophyllum nodosum, Fucus, Laminaria, Sargassum, and Turbinaria spp. (Mukherjee and Patel, 2020). However, red algae extracts from K. alvarezii, A. spicifera, and H. spinella show promise in replacing a variety of synthetic agrochemical molecules (Figure 3), as they contain a diversity of macronutrients, micronutrients, and amino acids that are underutilized in this field (Murillo Carvajal and Romo González, 2021). These nutrients can help plants to grow and develop healthily, which may reduce the need for chemical fertilizers. These extracts are a natural source of phosphorus and potassium, among other nutrients essential for plant growth (Table 2). These algal extracts can help plants to absorb nitrogen and phosphorus from the soil and translocate it from the root to the shoot in a more efficient manner, which can reduce the need for synthetic nitrogenous and phosphate fertilizers (Pérez-Madruga et al., 2020). They could also contribute to reducing water pollution by nitrates.
Algal extracts contain phytohormones that help plants bloom and bear fruit more efficiently by acting as hormonal growth regulators, which can increase crop yields (Murillo Carvajal and Romo González, 2021). Formulations with these phytohormones can reduce environmental pollution by synthetic hormonal growth regulators. Concurrently, phytohormones can help plants to defend against pests and diseases by acting as secondary metabolites (Udayan et al., 2018). These phytohormones can act as natural insecticides, fungicides, and nematicides. Due to the defenses they provide, they can help to reduce the need for synthetic organochlorine and organophosphate pesticides. This can aid in protecting birds and other wildlife from exposure to these toxic pesticides.
Furthermore, these bioactive extracts condition the soil with organic matter, improving its structure, trace element content, minerals, growth regulators, vitamins, and other metabolites. To a lesser extent, they could enhance soil hydration, favoring the development of beneficial microorganisms (Flórez-Jalixto et al., 2021). Their phenolic compounds have the potential to promote crop growth and develop defense mechanisms, and they counteract oxidative stress (Roy et al., 2022). Consequently, they are candidates to replace a variety of synthetic molecules to address issues of compaction, water retention, or salinity.
Extraction methods
There are various methods for extracting the active principles of algae, which are based on achieving cell rupture to release the components of interest. New extraction methods include acid and alkaline hydrolysis, cell disruption under pressure, fermentation, and enzyme-assisted extraction (Flórez-Jalixto et al., 2021). Recent technologies in biomolecule extraction equipment reduce times thanks to alternations between pressure, temperatures, and solvents. Green alternative extraction methods have been developed, such as those with pressurized liquid, subcritical water, and supercritical fluid, as well as microwave- and ultrasound-assisted extraction using different solvents (acetone, ethanol, methanol, 2-propanol, and water), including alternative solvents such as ionic liquids (Rudke et al., 2020). As research in this field continues, it is likely that algae extracts will become even more common in agriculture, and that traditional extraction methods will be updated by innovative technologies.
Proposals for Ecuador
Algal extracts are a natural and sustainable alternative to synthetic agrochemicals. They are safe and can help farmers to improve the productivity of their crops at more accessible costs (Sithamparanathan et al., 2019). The use of seaweed as biostimulants is a growing sector in various parts of the world, including Latin America (González-Giro et al., 2018). Improvements in the growth and productivity of various crops in different countries, following the application of seaweed extracts from K. alvarezii and A. spicifera, have been encouragingly documented, and their applicability in more economically important crops continues to be researched. There is still a scarcity of data and studies that adequately document the application potential of H. spinella.
Ecuador has experience in cultivating native and exotic macroalgae such as A. spicifera and K. alvarezii (Jiménez and Torres, 2023). This practice offers a promising alternative to improve the immunity and stress resistance of crops of national and international commercial interest, in addition to reducing the use of synthetic chemical inputs. Developing this market in Ecuador would pave the way to the creation of new industries that leverage the bioactive compounds of macroalgae. However, to advance in this field, more in-depth research is required which covers extraction procedures, total chemical analysis, the influence of origin on components, and the effect of seasonality, among other factors. The richness in minerals, vitamins, bioactive substances, proteins, and lipids with antibacterial, antiviral, and antifungal properties provides an optimistic future for their use as raw materials for extracting bioactive components for agricultural bioformulations.
Currently, the successful implementation of the commercial cultivation of K. alvarezii in Ecuador has demonstrated that scientific innovations can benefit coastal rural populations lacking alternative economic opportunities. The biotechnological exploitation of A. spicifera could help mitigate its invasiveness on the Ecuadorian coasts. Finally, the chemical analysis of H. spinella would allow exploring its potential for synergistic utilization in combination with the aforementioned algae.
On the other hand, continuous advancement in both agricultural methods and the development of integrated products is crucial to attract investments. The rural economy will not only be bolstered by the commercial cultivation of algae, but also through the use of liquid and solid bioformulations derived from algae biomass (Mantri et al., 2017). Furthermore, their utilization would mark the beginning of the development of parallel industries that exploit their other by-products.
Given the existing information, Ecuador should leverage the implementation of this agroecological alternative in its transition towards a green agriculture, as seaweed extracts contain nearly all primary and secondary nutrients for plants. This merits government efforts for holistic planning in the implementation of seaweed cultivation projects that enable commercial activity with a high degree of confidence and efficiency, which will lead to an improvement in the local coastal economy. The geographical expansion of commercial agriculture is inevitable in the foreseeable future, but the current government is expected to increase R + D funding and encourage external or private investment for agriculture in deep and offshore waters, along with continuous environmental and social assessment.
CONCLUSIONS
Red macroalgae, particularly K. alvarezii, A. spicifera, and H. spinella, exhibit significant biotechnological potential for application in sustainable agriculture in Ecuador. These marine organisms, widely distributed along the country’s coastal region, contain a diversity of bioactive compounds such as polysaccharides, amino acids, enzymes, polyphenols, plant pigments, and hormones, which provides them with elicitor and phyto-stimulator properties. The inclusion of extracts from these macroalgae in agricultural production has evidenced positive impacts, enhancing plant disease resistance, activating defense mechanisms, modulating soil microbiota, and bolstering crop yield and quality. Moreover, the cultivation of macroalgae is a sustainable practice that does not require fresh water or competition for land, and it can mitigate carbon dioxide (CO2) emissions through increased biomass (carbon assimilation during growth). Ecuador has favorable climatic and oceanographic conditions for the development of macroalgae cultivation, especially in the province of Santa Elena, which represents a significant opportunity to diversify aquaculture and promote sustainable agriculture in the country.
Therefore, promoting research and development on technologies aimed at the cultivation and processing of red macroalgae in Ecuador is recommended, with a focus on the species K. alvarezii, A. spicifera, and H. spinella. These research efforts should cover the optimization of cultivation conditions, the thorough characterization of the bioactive compounds present in these macroalgae, and the rigorous evaluation of their effectiveness in various agricultural crops. Furthermore, academic institutions, research centers, and entities in the agricultural sector are called upon to collaborate in an interdisciplinary manner to facilitate the transfer of knowledge and technologies specialized in this emerging field. It is also important to develop policies and regulations that encourage the use of macroalgae-based biostimulants as a sustainable alternative to synthetic agrochemicals, in line with international trends towards a more ecological agriculture. Finally, it is advisable to educate farmers about the multiple benefits offered by macroalgae biostimulants and actively promote their integration into everyday agricultural practices. This will significantly contribute to the sustainability and competitiveness of the Ecuadorian agricultural sector on the global stage.
