Abstract
Presently, the world is using eco-friendly products to limit pollution in soil, air, water, and marine environments and to mitigate rapid climate change according to the sustainable development goals of the United Nations Development Programme. As a result, most countries attempt to produce environmentally friendly herbicides, fertilizers, and pesticides from plants, algae (e.g., Cladophora glomerata, Laurencia pinnata, Plocamium cartilagineum, Polcamium spp.) or animal manure. Plants, such as Anethum sowa, Thymus vulgaris, Foeniculum vulgare, Syzygium aromaticum, Pinus sylvestris, Citrus spp., Piper spp. and Mentha spicata, are ecofriendly sources of essential oils, containing safe components, which can resist harmful pests. This review evaluates the common plants and algae used for extracting biopesticides, geographical distribution, target pests, mode of action, and commercial viability.
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Introduction
The world’s population is increasing tremendously and is expected to reach 8.5 billion by 2030. Conversely, food will decrease due to various reasons including harmful pests (Desa, 2011) and land for agriculture becoming less (Jhala et al., 2020). Annually, many crops are spoiled by an estimated 67,000 pests like fungi, weeds, bacteria, and insects (Agrios, 2005; Meena & Mishra, 2020). Using plants and algae for controlling pests is not new and is a traditional method (Choi et al., 2004). Biopesticides, originating from natural products (plant, algae, fungi) are eco-friendly, less toxic, and have less resistance build-up among insects and pathogens (Regnault-Roger et al., 2012). Biopesticides are effective because they have specific targets, and inhibit or kill harmful pests without negative effects on humans and beneficial organisms. Pests are a major factor in the declining yield of crops, which influence economies and feed populations (Sinha & Biswas, 2011).
Biopesticides are biodegradable and promote eco-friendly environments (Mazid et al., 2011). Safe plant and algae biopesticides are commercially available (Alam et al., 2002). In the United States of America, almost 200 biopesticides are used against harmful pests (Kumar & Singh, 2015), while in India 2.89% of the total market are biopesticides, which are increasingly used (Thakore, 2006). Biopesticides mainly derived from plants and algae have gained attention and publicity due to potentially healthier benefits in agriculture and for human health (Gupta & Dikshit, 2010). It possesses antifungal, antibacterial, antivirus, and insecticidal biopesticides (Akinbode & Ikotun, 2008; Hao et al., 2021; Harlapur et al., 2010; Yasmin et al., 2008).
Plant-based pesticides are commonly derived from herbs and plant-based pesticides are known as herbal pesticides (Pal et al., 2013). Almost 6000 plant species are used as insecticides (Dimetry et al., 1993). Different forms of algae are potential biopesticides. Microalgae are a microscopic group of algae that have bioactive compounds, which are effective against harmful organisms (Costa et al., 2019). Interest and awareness are increasing to use medicinal plants and algae for controlling and inhibiting plant diseases caused by pests. For this purpose, almost 2400 plant species have been screened for potential phytoactivity (Khafagi & Dewedar, 2000).
In this review we will discuss both biopesticides active against plant pathogens and biopesticides active against insect pests.
Assessment of plants as biopesticide
Plant derived pesticides are obtained from leaves, roots, barks, seeds, fruits and bulbs. The plant parts are dried and bioactive compounds extracted (Chougule & Andoji, 2016). Different parts of plants are used for making biopesticides and extracts taken for assessing potential activity. (Ahmad et al., 2009). For example, cinnamon essential oil extract from cinnamon bark showed antifungal activity against Phytophthora colocasiae which causes acute decline, and up to 100% crop loss. The main component of the oil is cinnamaldehyde. At 0.625 mg/mL, the maximum inhibition of mycelial growth, zoospore germination, and sporulation of the fungus were observed, whereas leaf necrosis due to phytotoxicity was 100% at 1.25 mg/mL (Hong et al., 2021).
Essential oils can be used as biopesticide alternatives to monocrotophos. The eugenol derivative, 4-allyl-2-methoxy-1-(4-trifluoromethyl-benzyloxy)-benzene with a feeding deterrent index (FDI) of 54.14% and the thymol derivative, 2-isopropyl-4-methyl-2-(4-nitrobenzyl) oxy) benzene with an FDI of 53.88% are extracted from clove and thyme essential oils respectively. Both showed as antifeedant agents against the fourth instar larvae of Spodoptera littoralis through oral administration for 14 days. This study revealed that the ether compound was more effective than the ester compound regardless of the essential oil (Yan et al., 2021). Commercially available herbaceous plant Nepeta cataria extracts are effective repellents against mites, mosquitoes and cockroaches. The essential oil and hydrosol from Cuminum cyminum (cumin) seeds, characterized by γ-terpinene-7-al (34.95%), cumin aldehydes (26.48%), and α-terpinene-7-al (12.77%), were evaluated against second-stage juvenile (J2s) root-knot nematodes Meloidogyne incognita and M. javanica in the soil. The motility, hatching, and survival of J2s was affected after immersion in the essential oil at 1000 and 2000 μL/L. The lowest numbers of hatched J2s were recorded. More than 70% of paralyzed J2s were recorded after immersion for 48 h, which increased to more than 90% after 96 h (Pardavella et al., 2021).
Azadirichta indica L., Thuja orientalis L., Nicotiana tabacum L., Nicotiana rustica L., and Melia azedarach L. aqueous and powder extracts are used as alternatives to synthetic insecticides for the control of C. maculatus in stored pulses. Their toxicity was evaluated under specific conditions at concentrations of 0.50%, 1%, 1.5%, 2%, 2.5%, and 3%, and the following was the most effective biopesticide, N. tabacum, A. indica, and M. azedarach. The mortality rate of C. maculatus was significantly higher with all aqueous phytochemicals and all N. tabacum concentrations as well as powdered A. indica. T. orientalis recorded lower mortalities with the least number of phytochemicals (Akbar & Khan, 2021). Azadirachtin, a component of NeemAzal, is a plant-based insecticide, which is bio-efficient and biodegradable. Azadirachtin suppresses sugar beet moths (Scrobipalpa ocellatella) by reducing feeding, delays in larval and nymphal development, incomplete ecdysis, sterile eggs, deformed pupae and adults, and reduced fecundity. The optimal period to spray azadirachtin was 5–6 days after the moth deposited eggs, and concentrations of 2 and 2.5-ml L–1 had a substantial impact on S. ocellatella mortality. Thus, defined concentrations of a sugar beet moth insecticide applied at the end of the growing season significantly reduced crop loss (Allahvaisi et al., 2021). The Asteraceae family of plants are used as botanical pesticides as they have effective chemicals for killing and controlling harmful fungi. Bioactive compounds include alkaloids, terpenoids and flavonoids (Ferreira et al., 2013). Tarchonanthus camphorats is capable of killing and inhibiting many bacteria (Sunder et al., 2011). Current trends are towards the extraction and use of plant materials for pest control (Villaverde et al., 2016) (Fig. 1).
Assessment of algae as eco-friendly biopesticides
Marine macro-algae (seaweed), are present on the seafloor attached to rocks or boulders, floating over the seawater, or sometimes drifting to shore. Seaweeds are found in the inter-tidal zones of tropical to temperate to cold waters (Coppejans et al., 2009). More than 10.000 species of macro-algae are known. Seaweeds are categorized into three main groups i.e., red (Rhodophyta), brown (Ochrophyta), and green (Chlorophyta), based on pigmentation, morphological, and anatomical features (Guiry & Guiry, 2017). Seaweeds have been used as food, forage, fertilizer, medicine, and other therapeutic applications benefiting human health (Blunden, 1993; Smit, 2004). Marine algae synthesize and emit bioactive compounds as a defence mechanism, which have been identified and isolated (Perez et al., 2016). More than 2700 natural products have been reported. The secondary metabolites belong to terpenoids, alkaloids, phenols, esters, triglycerides, hydrocarbons, isoprenoids, alcohols, fatty alcohols, steroids, and waxy constituents. The largest variety of natural products has been reported from the red algae (Rhodophyta) mainly from genus Laurencia (Ioannou & Roussis, 2009). Laurencia is a complex genus comprising 383 species, of which 209 are taxonomically accepted (Cassano et al., 2019). The newly discovered Laurencia karachiana from Pakistan also possess insecticidal potential (Bibi et al., 2021) enriched with alcohols, fatty acids, sesquiterpenes, diterpenes, and steroids (Bibi et al., 2020).
The insecticidal potential of seaweeds is described (Table 1). Chemical composition analysis of seaweed extracts revealed that halogenated compounds such as triterpenoids and lipophilic compounds such as fatty acids are involved in insecticidal activity (Gressler et al., 2009). Oil-based compounds penetrate insects’ bodies through cuticles and respiratory tracts and cause cellular and haemolymph acidosis, which leads to death (Sugiura et al., 2008). Fucus spiralis brown algae essential oil has an insecticidal effect against the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae) (Gressler et al., 2009). Insecticidal efficiency was tested on the pupae and adults using different concentrations of F. spiralis essential oils. The activity of the essential oils against adults was higher, with an LD50 and an LD90 of 0.239 and 2.467 ppm, respectively (Boutjagualt et al., 2022). Gas chromatography–mass spectrometry revealed the presence of borneol (13.13%), hentriacontane (6.13%), bornyl salicylate (5.48%), docosane (6.93%), octacosane (5.62%), heptacosane (7.22%), and limonene (4.9%), which made up the essential oil (Boutjagualt et al., 2022).
Widespread distribution of seaweeds can be utilized as an alternative approach to develop eco-friendly pesticides and repellents against mosquito species (Bibi et al., 2020). Further volatile compounds that are synthesized by seaweeds for their defence against herbivores and predators induce feeding deterrents and toxic effects against agricultural pests (Rovirosa et al., 2013). These antifeedants can be isolated and applied against harmful sap sucking pests and stored grain commodities. Thus, huge biomass of seaweeds, enriched with potential bioactive compounds, is wasted every year along the shore and is the most alternative and safe source of biopesticides that can replace harmful synthetic pesticides.
Mechanism of action of biopesticides
Despite the variety of phytochemical pesticides, the mode of action of all compounds is unknown (Singh, 2017). Plants’ bioactive compounds have different actions that may be physical or biological towards plant pathogens, insects, nematodes, and interactions depending on the type of compound and the pathogen (Grdiša and Kristina 2013; Aioub et al., 2022).
Mode of action of biopesticides
Plant extracts are lethal or toxic and affect the physiological activities of insect pests like preventing feeding and decreasing oviposition (Chengala & Singh, 2017). Antifeedant plant extracts prevent feeding by making the meal taste bad and the larvae die of starvation. Examples include M. alternifolia oil on Helicoverpa armigera (Liao et al., 2017); Gliricidium sepium methanol extract against coffee Mealybugs (Planococcus citri Risso) (Nukmal et al., 2017); and Polyalthia longifolia (methanol extract), Polyalthia longifolia (petroleum ether), Limonia acidissima (methanol) against Spodoptera litura (Arora, 2017). The eco-friendly essential oil of Ageratina adenophora has an antifeedant activity of 87.46% against Plutella xylostella (L.) (Mayanglambam et al., 2022).
Botanical pesticides have a toxic effect on insects infesting stored products by poisoning the mitochondrion, resulting in electron transport chain disruption and energy production inhibition (Stevenson et al., 2017). The crude phenolic compounds (methanolic extract) of Acorus calamus poisons the tobacco cutworm (Spodoptera litura) larvae and affect the hormonal balance by decreasing carboxylesterase, which affects the neurotransmitter acetylcholine (Wiwattanawanichakun et al., 2022). Essential oils from Mentha arvensis are highly toxic and penetrate the thick, hard exoskeleton, leading to disorders in the biological systems of Sitophilus granaries (Renoz et al., 2022). Thaumastocoris peregrinus is controlled by toxic essential oil from Eugenia uniflora (L.), which affects the hatching and increases the mortality of adults and nymphs (Stenger et al., 2021).
Botanical insecticides harm the pathogen by decreasing or inhibiting its stages of development (Isman, 2017). Essential oils of Teucrium quadrifarium and Boenninghausenia albiflora have growth inhibitor properties against Spilarctia obliqua, causing morphological and physiological effects, leading to a decrease in larval and pupal weight and increased mortality (Tandon & Mittal, 2018). Plant extracts from Lantana camara, Catharanthus roseus, Coleus amboinicus, Curcuma longa, and Alpinia pyramidata provide toxicity, growth regulator properties, and antifeedant activity towards Plutella xylostella Linn diamondback moth (2nd larval instar) (Javier et al., 2019).
Extracted plant metabolites like alcohols, terpenes, alkaloids, phenols and tannins inhibit fungal growth by inhibiting spore germination and development of mycelia, or by degenerating hypha and mycelia (Yoon et al., 2013). The pathogenic fungus Valsa mali was affected by wood tar (EC50 ranged from 69.54 to 92.81 μg/mL), leading to hyphal breaks, increased cell membrane permeability, and unbalanced enzyme production related to the decrease in pectinase and related genes. (Chen et al., 2022). A series of Michael-type amino derivatives were prepared from xanthatin, a secondary metabolite extract from Xanthium strumarium, with antifungal activity and inhibition of mycelium growth on C. mandshurica and spore germination against F. solani (Zhi et al., 2022). Uvaria grandiflora extract (zeylenone) inhibited growth of cucumber powdery mildew, and sporangium formation of Phytophthora capsica by destroying the cell wall structure and energy metabolism. Also, zeylenone was toxic to normal cell lines (He et al., 2021).
Similarly, botanical pesticide exposure affects bacterial growth especially Gram-negative organisms through its effect on cellular metabolism like protein synthesis (Djeussi et al., 2013). Pesticide exposure causes microbial death by increasing plasma membrane permeability (Khan et al., 2009). For example, hydroalcoholic extract from Larrea tridentata provides bactericidal activity to multidrug-resistant bacteria like Pseudomonas syringae, Michiganensis, Clavibacter michiganensis sbsp., especially Xanthomonas campestris (Morales-ubaldo et al., 2021). Parthenolide from Magnolia grandiflora Linn causes cell death in Xanthomonas oryzae pv. oryzae (Xoo) by accumulation of reactive oxygen species, decreased glutathione reductase and increased glutathione peroxidase activity (Xu et al., 2018).
Plant extracts with nematocidal activity inhibits egg hatching and reduces nematode populations (Abd El-Aal et al., 2021; Eldeeb et al., 2022). For example, methanolic extracts of Anaphalis virgata and Anaphalis nepalensis were tested against root-knot nematodes (Ismail et al., 2021). Extract of W. indica roots provide high nematocidal activity towards J2 of M. incognita by three isolated compounds i.e., waltherione C, 5′-methoxywaltherione A and waltherione A (Jang et al., 2019).
Some phytochemicals inhibit viral infection by inducing host resistance (Montanha & Moellerke, 2004), inhibiting virus penetration and virus replication (Rajasekaran et al., 2013). Benzosuberene compound extracted from Cedrus deodara oils inhibit self-assembly of tobacco mosaic virus (Sharma et al., 2021). The liberation of nucleic acids of watermelon mosaic virus is blocked by Thuja orientalis extract, leading to inhibition of multiplication (Elbeshehy et al., 2015).
Nano-biopesticides
Nanopesticides are nanostructures with two to three dimensions between 1 to 200 nm, used to carry agrochemical ingredients. Nano-biopesticides are appealing because of their small size, high surface-area-to-volume ratio, stability, increased effectiveness, improved solubility, mobility, and importantly low toxicity (Fig. 2) (Lade et al., 2019). Toxins released into the food chain by chemical pesticides sprayed directly on plants can cause environmental problems. Pesticides that contain nanoparticle formulations, such as micelles and nano-composites, lower the risk of environmental and health problems (Aioub et al., 2022). Clay-based nanotubes similarly transmit chemical insecticides (Sasson et al., 2007). Nano-biopesticides, like nano-fertilizers, are packaged in carriers that allow for the controlled release of active ingredients to achieve the intended effects in each environment.
The addition of nano-biopesticides to biopolymers improves stiffness, penetrability, crystallinity, thermal stability, solubility, and biodegradability (Manjunatha et al., 2016).
Nano-biopesticides comprising nano-materials that are applied to soils, results in the establishment of mutualistic bacteria that boost plant growth (Lu et al., 2010). Toxicity can be caused by silver-based nanoparticle coatings, which can be reversed by biocompatible coatings, improving the likelihood of seed germination in plants. Nano-emulsions, nano-encapsulates, nano-containers, and nano-cages have recently been described as nano-pesticide delivery strategies for plant protection with various capabilities (Bouwmeester et al., 2009; Hazafa et al., 2022). Cationic polymers may adhere to polyanionic surfaces of bacteria, rupture cell membranes, and kill pests. Biopesticides, such as nano-biopesticides, can be used on plants to reduce microbial resistance, but chemicals applied directly to plants are unable to suppress a wide spectrum of bacterial growth (Li et al., 2019). Long amino acid chains including tertiary ammonium groups can be found in nanoparticles. Depending on their structure, these groups may combat a variety of pests and ailments including bacteria (Hazafa et al., 2022; Ng et al., 2014), because of their strong activity in a range of environmental and chemical conditions. Many polymers with this property have been discovered and studied. For example, amphiphilic copolymers, functionalized cationic polycarbonates, poly(amidoamines), polyethylenimine, poly (methyl methacrylates), amino celluloses and chlorinated cellulose acetates are available commercially (Ng et al., 2014).
Plants containing nano-emulsions of essential oils can be employed to reduce insect larval infections. Nano-emulsions from Tagetes minuta, Ageratum conyzoides, and Achillea fragrantissima are used to inhibit the growth of Callosobruchus maculatus. The nano-emulsions can be used in fumigation to kill or restrict the formation of eggs and larvae, with treatment ranging from 16.1–40.5 μL/L and 4.5–243 μL/L, respectively (Nenaah et al., 2015). Encapsulation of essential oils can be accomplished with nanoparticles made of liposomes and solid lipids. Inverse gelation and oil emulsion can be used to encapsulate essential oils (Lopez et al., 2012). Encapsulation in liposomes is beneficial against bacteria because the cell membrane is protected from the impact of essential oils (Sherry et al., 2013). However, many forms of nanoparticles are employed for pest control. Microparticles are also employed to keep the effects of essential oils stable. Encapsulation of carvacrol with the cell wall of Saccharomyces cerevisiae was conducted with a diameter of 0.5 mL to control the larvae of Rhipicephalus microplus with LC50 of 0.71 mg/mL. Saccharomyces cerevisiae cell wall appears to be beneficial in preserving the low volatility of encapsulated carvacrol, which retains acaricidal action for up to 60 h (Da Silva et al., 2017).
Commercial applications of biopesticides derived from plants and algae
Commercially made pesticides derived from higher plants and algae are biodegradable and eco-friendly. Compounds extracted from biological origins contain chemicals like terpenes, alkaloids, quinines, aldehydes, amino acids, saccharides, and flavonoids. These compounds are ecologically important as they are used commercially for antifeedant, nematicide, insecticide and fungicide products (Souto et al., 2021). From 1939 to 1962, the world focused on synthetic pesticides like 1,1,1-trichloro-2-propanol and 2-bis(4-chlorophenyl)-ethane (Jarman & Ballschmiter, 2012). As these chemicals are harmful and remain in contaminated soil, water and air for long periods and have adverse environmental effects (Multigner et al., 2010).
Formation of commercial biopesticides with algae is simple and low cost, as different varieties of microalgae can be obtained through wastewater (Ranglová et al., 2021). Duckweed (Lemna minor), water hyacinth (Eichhornia crassipes) and filamentous algae (Lyngbya wollei) produce allelopathic compounds that have potential commercial chemical application to inhibit the growth of pests (Fu et al., 2020). Biopesticides are evaluated and checked with the same regulations and rules as synthetic pesticides. Products from plants and algae are required to be prepared in safe environments according to strict guidelines before registration (Wang et al., 2000). It is believed that the commercial market of biopesticides will completely replace the market of synthetic pesticides by 2050 (Damalas, 2018) (Table 2).
Conclusion and future prospective
Synthetic pesticides’ quick action makes them the first line of treatment, but their large-scale use has resulted in environmental hazards and the development of resistance. Therefore, environmentally safe plant products with fungicidal and insecticidal properties are a potential alternative. They can be as effective as conventional pesticides when applied as part of an integrated pest management strategy, especially for crops such as fruits, vegetables, nuts, and flowers. Application of chemical pesticides leads to the destruction of beneficial microorganisms and residues may accumulate. Bioactive compounds present in plants and algae have pesticidal effects. Biopesticides derived from them are eco-friendly, safe and beneficial for the environment. Therefore, development of eco-friendly plant and algal-based pesticides is needed for pest management with minimal environmental impact. Biopesticides along with fewer application constraints, enhanced resistance management potential, and environmental safety make them more efficient. This supports the United Nations Development Program's 2030–2050 objectives, with the preservation of the global climate, which protects life on land and in water. Thus, a clean environment is secured where with adequate food for every human being, a reduction in poverty, and enhanced scientific and cultural development.
Data availability
Data available on request.
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Acknowledgements
The authors are thankful to Miss/ Yathreb M. Hashim for her preliminary literature searches about the mode of action of biopesticides, and Miss/ Nouran A. El-shershaby for paraphrasing some parts of the preliminary manuscript.
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Open access funding provided by The Science, Technology & Innovation Funding Authority (STDF) in cooperation with The Egyptian Knowledge Bank (EKB).
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Ahmed A.A. Aioub: Collected and summarized the results and revise the final manuscript.
Soumya Ghosh: participated in writing the manuscript. The authors read and approved the final manuscript.
Ammar AL-Farga: Collected and summarized the results and revise the final manuscript.
Abdullah M. Elwakeele; conducted a systematic literature review and wrote the primary manuscript.
Allah Nawaz Khan: conducted a systematic literature review and wrote the primary manuscript.
Rabia Bibi: conducted a systematic literature review.
Soumya Ghosh: participated in writing the manuscript. The authors read and approved the final manuscript.
Asma Nawaz: participated in writing the manuscript. The authors read and approved the final manuscript.
Naglaa T. Sherif: participated in writing the manuscript. The authors read and approved the final manuscript.
Sohaila A. Elmasry: participated in writing the manuscript and References.
Esraa E. Ammar: Collected and summarized the results, design graphics, and revise the final manuscript.
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Aioub, A.A.A., Ghosh, S., AL-Farga, A. et al. Back to the origins: biopesticides as promising alternatives to conventional agrochemicals. Eur J Plant Pathol (2024). https://doi.org/10.1007/s10658-024-02865-6
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DOI: https://doi.org/10.1007/s10658-024-02865-6