Insecticidal and Nematicidal Contributions of Mexican Flora in the Search for Safer Biopesticides.

Plant metabolites have been used for many years to control pests in animals and to protect crops. Here, we reviewed the available literature, looking for the species of Mexican flora for which extracts and metabolites have shown activity against pest insects and parasitic nematodes of agricultural importance, as well as against nematodes that parasitize domestic cattle. From 1996 to 2018, the search for novel and eco-friendly biopesticides has resulted in the identification of 114 species belonging to 36 botanical families of Mexican plants with reported biological effects on 20 insect species and seven nematode species. Most plant species with detected pesticide properties belong to the families Asteraceae, Fabaceae, and Lamiaceae. Eighty-six metabolites have been identified as pesticidal active principles, and most have been terpenoids. Therefore, the continuation and intensification of this area of research is very important to contribute to the generation of new products that will provide alternatives to conventional pesticide agents. In addition, future studies will contribute to the recognition and dissemination of the importance of propagating plant species for their conservation and sustainable use.

1. Introduction

Pest control in the agricultural sector requires a greater number of alternative products that meet food safety, sustainability, and environmental care requirements. One of the strategies used to obtain new natural agents for protecting crops and domestic animals is the exploration of a diversity of plants and their metabolites [1,2]. Natural products with pesticidal properties have been demonstrated to be an important source of compounds which are used as raw materials in the development of new protective agents, both in their natural form or as semisynthetic derivatives exhibiting better effects. In addition, the chemical structures of the active components of natural products have guided the synthesis of other active compounds [3]. The exploration and use of natural products are currently increasing, with a greater focus on identifying metabolites for use in the treatment of human diseases, including parasistism and plant diseases, as well as products for use in pest control in the agricultural sector [4,5,6,7,8,9].

The biotic wealth of Mexico, which includes large tropical zones, is widely recognized as being among the greatest in the world, with Mexico harbouring an estimated 23,314 species of native vascular plants, approximately 49.8% of which are endemic [10]. Nevertheless, the amount of biodiversity prospecting for natural products in Mexico is low, and as in other countries, it has primarily focused on the search for products to control diseases or plagues that affect humans [11,12,13]. With respect to agricultural applications, most studies have focused on identifying antimicrobial agents rather than insecticides, nematicides, and herbicides [5,13,14,15]. Regarding plants with insecticidal properties, the results of previous studies have identified 24 Mexican plant species with pesticidal potentials that are used in different regions of the country, many of which have been identified as medicinal plants by ethnobotanical antecedents [16]. In contrast, few botanical prospecting studies have been performed to identify plants with activities against phyto and zoonematode pests. Worldwide, few plant extracts have been shown to have an acaricidal activity, three of which are from Mexican flora and were tested on Rhipicephalus microplus, and only seven pure natural compounds have been identified as active principles [17]. Undoubtedly, Tagetes erecta (Asteraceae), a native plant of Mesoamerica, is currently recognized as one of the most promising plant species given its diverse biological activities against human and plant pathogens as well as against multiple pests [9,18].

Therefore, this work reviews the Mexican flora with extracts or secondary metabolites that have shown biological activity against pest insects or parasitic nematodes. Some plant species that were introduced to Mexico, such as Allium sativum, Azadirachta indica, and Ricinus communis, among others, are also discussed. The information was compiled from all of the electronic databases available at the institution, which included Google Scholar, SciFinder, PubMed, Redylac, Scopus, and Science Direct, among others.

2. Insecticidal Compounds and Plant Extracts

Research on natural products for controlling pest insects that affect plants has led to the identification of 85 plant species with extracts and metabolites that are effective against at least one of the evaluated targets. These plants belong to 26 botanical families, predominantly Asteraceae (31%), Lamiaceae (14%), Meliaceae (7%), Annonaceae (6%), Chenopodiaceae (6%), Fabaceae (5%), and Rutaceae (5%), with the rest belonging to the families Acanthaceae, Anacardiaceae, Asparagaceae, Bignoniaceae, Brassicaceae, Burseraceae, Cactaceae, Caricaceae, Convolvulaceae, Euphorbiaceae, Lauraceae, Magnoliaceae, Papaveraceae, Petiveraceae, Piperaceae, Phytolaccaceae, Poaceae, Solanaceae, and Verbenaceae (<5% each).

Twenty pest insects were evaluated in the reviewed studies. The maize pest Spodoptera frugiperda J.E. Smith (Lepidoptera: Noctuidae) is the most frequently tested target together with Spodoptera littoralis Boisduval (Lepidoptera: Noctuidae) and Spodoptera exigua Hübner (Lepidoptera: Noctuidae), collectively representing 30% of the target pests assayed in the reviewed studies, and these species were followed by Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae, 14%), the sucker Bemisia tabaci Gennadius (Homoptera: Aleyrodidae, 11%), and Trialeurodes vaporariorum West. (Homoptera: Aleyrodidae, 7%). The remaining targets included Anastrepha ludens Loew (Diptera: Tephritidae), Bactericera cockerelli (Hemiptera: Psylloidea), Copitarsia decolora Guenée (Lepidoptera: Noctuidae), Dactylopius opuntiae Cockerell (Hemiptera: Coccoidea), Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), Prostephanus truncatus Horn (Coleoptera: Bostrichidae), Scyphophorus acupunctatus Gyllenhaal (Coleoptera: Curculionidae), Stomoxys calcitrans Linneo (Diptera: Muscidae), Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae), Trichoplusia ni Hübner (Lepidoptera: Noctuidae), and Zabrotes subfasciatus Boheman (Coleoptera: Bruchidae). Other targets assayed included Aedes aegypti Linnaeus, Anopheles albimanus C.R.G. Wiedemann, and Culex quinquefasciatus Say (Diptera: Culicidae), which have been included in this review because they are all very important pest insects of humans and are also virus vectors.

In this review, first, the insecticidal compounds isolated and identified in enriched fractions (as alkaloids and terpenes) and essential oils (EOs) from Mexican plants are described by the targeted pests. The second part includes plant extracts which the active principles of are not yet known.

2.1. Spodoptera sp.

During investigations carried out on the control of Spodoptera sp. (S. frugiperda and S. littoralis), 43 effective natural compounds have been identified including terpenes (1–30), flavonoids (31–35), stilbenes (36–38), a coumarin (39), a ketone (40), and fatty acids (41–44). In addition, enriched fractions with metabolites that were identified as alkaloids (45–50) have been described. All of these compounds were isolated from 21 plant species and exhibited different degrees of effectiveness against the assayed pest insects, with the most active metabolites obtained from plants of the Asteraceae family (Cedrela dugessi, Cedrela salvadorensis, Gutierrezia microcephala, Parthenium argentatum, and Roldana barba-johannis), the Fabaceae family (Lupinus aschenbornii, Lupinus montanus, and Lupinus stipulates), and the Asparagaceae family (Yucca periculosa), which induced the strongest median lethal concentration (LC50 ≤ 65 ppm) against S. frugiperda. Other plant species with minor activities against S. frugiperda included Carica papaya, Crescentia alata, Lippia graveolens, Myrtillocactus geometrizans, Ricinus communis, Ruta graveolens, Vitex Hemsley, and Vitex mollis. In addition, five species from the genus Salvia and a member of the family Asteraceae (Senecio toluccanus) were found to have active compounds against S. littoralis.

2.1.1. Terpenes

The tocotrienols and hydroquinones isolated from the methanol extract (MEx) of the aerial parts of R. barba-johannis (Asteraceae) included sargachromenol (1), methyl and acetyl sargachromenol derivatives (2, 3), sargahydroquinoic acid (4), methyl and acetyl sargahydroquinoic acid derivatives (5, 6), and sargaquinoic acid (7). Metabolites 1, 3, and 6 showed potent insecticidal activity against the fifth-stage larvae of S. frugiperda, with median lethal dose (LD50) values of 2.94, 3.89, and 4.83 ppm, respectively. Metabolite 4 was most effective against first-instar S. frugiperda larvae, with a LC50 of 5.77 ppm. Furthermore, acetylated metabolite 3 was the most potent compound against the emergence of S. frugiperda adults from pupae, while the efficacy was further increased using a mixture of acetylated compounds 1, 3, and 7 (LD50 = 3.26 ppm) [19]. Furthermore, Cespedes [20] identified two cycloarten-type triterpenes, argentatin A (8) and argentatin B (9), from a methanol extract (MEx) of the aerial parts of P. argentatum. Although both metabolites showed good insecticidal and growth inhibition activities, the MEx was consistently more potent than either triterpene alone. Methanol extract, 8, and 9 showed a potent toxicity towards S. frugiperda adults, with LD50 values of 3.1, 12.4, and 19.8 ppm, respectively. In addition, the insecticidal activities of MEx and compound 8 against the fifth-instar larvae of S. frugiperda were tested, with LC50 values of 6.4 and 17.8 ppm and median mortality concentration (MC50) values of 6.9 and 21.3 ppm, respectively. In agreement with these results, the observed growth and relative growth indices seven days after treatment with both metabolites and MEx revealed a delay in the time of S. frugiperda pupation and adult emergence and an increase in deformities. Acetylcholinesterase inhibition (83.5% and 100%) was observed using MEx at 5 and 25 ppm, respectively, but not for the pure compounds (90–100% at 50 ppm).

The G. microcephala clerodane diterpene bacchabolivic acid (10) and its synthetic methyl ester (10a) were shown to cause significant mortality (MC50 = 10.7 and 3.46 ppm, respectively) towards S. frugiperda neonatal larvae, good toxicity against adults (LD50 = 6.59 and 15.05 ppm, respectively), and moderate acetylcholinesterase inhibitory activity [21]. The leaves of two Meliaceae species, C. salvadorensis and C. dugessi, were shown to produce a mixture of photogedunin α and β (11, 12) and gedunin (13). The mixture of compounds 11 and 12, as well as 13 and its acetate derivative (13a), caused good S. frugiperda larval mortality (LC50 = 10, 8, and 39 ppm, respectively) [22]. A labdane-type anticopalic acid (14) from Vitex hemsleyi showed an effective antifeedant dose of 90.6 ppm against sixth-instar S. frugiperda larvae [23]. Sterols isolated from the aerial parts of M. geometrizans (Cactaceae), including macdougallin (15), peniocerol (16), and a mixture of the two metabolites 15:16 (4:6), displayed a high toxicity towards S. frugiperda (LD95 = 285, 125, and 135 ppm, respectively). In addition, at 20 ppm, the mixture of 15 and 16 drastically resulted in the total inhibition of S. frugiperda pupation and the emergence of adults [24].

Terpenes with noticeable activity against S. frugiperda (100 ppm: 65–80% larval mortality) have been identified in enriched fractions from Crescentia alata, including ningpogenin (17), β-sitosterol (18), stigmasterol (19), and 6β,7β,8α,10-tetra-p-hydroxybenzoyl-cis-2-oxabicycle-(4.3.0)nonan-3-one (20) [25,26]. Guevara [27] reported that monoterpenes thymol (21) and carvacrol (22) were the major components in a hexanic extract of L. graveolens leaves. This extract caused deformations in S. frugiperda adults at different concentrations (10–100 ppm).

The pest S. littoralis was also shown to be sensitive to seven antifeedant clerodane-type diterpenoids obtained from several Salvia species (AI50 < 90 ppm). These diterpenoids included kerlinolide (23); 1(10)-dehydrosalviarin (24) from Salvia lineata; from Salvia keerlii, 13,14-dihydro-3,4 epoxy-melissodoric acid methyl ester acetate (25), 2β-acetoxy-7α-hydroxy-neo-clerodan-3,13-dien-18,19:16.15-diolide (26) from Salvia melissodora; salviarin (27) from Salvia rhyacophila; and 6β-hydroxysalviarin (28) and semiatrin (29) from Salvia semiatrata. The most effective of these was 25, with an AI50 value of 1 ppm [28]. The metabolite toluccanolide A (30), isolated from S. toluccanus, and its acetate derivative (30a) showed a significant antifeedant effect against S. littoralis (57% and 69.6%, respectively) after an application of this compound (50 µg/cm2) to leaves (Table 1, Figure 1) [29].

Table 1

Insecticidal terpenes from Mexican flora effective on Spodoptera sp.

Insect	Species/Family	Plant Part	Compound/Extract (Toxicity)	Ref.
S. frugiperda	Roldana barba-johannis * Asteraceae	AP	Sargachromenol (1) (LD50 = 2.94 ppm on fifth instar, 24 h; LC50 = 19.12 ppm on first instar, 7 days)Methyl sargachromenol (2) (LD50 = 15.52 ppm on fifth instar, 24 h; LC50 = 20.76 on first instar, 7 days)Acetyl sargachromenol (3) (LD50 = 3.89 ppm on fifth instar, 24 h; LC50 = 33.31 ppm on first instar, 7 days)Sargahydroquinoic acid (4) (LD50 = 10.17 ppm on fifth instar, 24 h; LC50 = 5.77 on first instar, 7 days)Methyl sargahydroquinoic acid (5) (LD50 = 14.89 ppm on fifth instar, 24 h; LC50 = 62.02 on first instar, 7 days)Acetyl sargahydroquinoic acid (6) (LD50 = 4.83 ppm on fifth instar, 24 h; LC50 = 81.81 on first instar, 7 days)Sargaquinoic acid (7) Mixture 1, 3, and 7 (6:3:1) (LD50 = 9.23 ppm on fifth instar, 24 h; LC50 = 17.76 on first instar, 7 days)Acetylated Mixture (LD50 = 3.26 ppm on fifth instar, 24 h; LC50 = 5.77 on first instar, 7 days)	[19]
	Parthenium argentatum * Asteraceae	AP	Argentatin A (8) (LD50 = 12.4 ppm on fifth instar, 24 h; LC50 = 17.8 ppm, 7 days; MC50 = 21.3 ppm, 7 days)Argentatin B (9) (LD50 = 19.8 ppm, on fifth instar, 24 h; LC50 = 36.1 ppm, 7 days; MC50 = 37 ppm, 7 days)Methanol (LD50 = 3.1 ppm, on fifth instar, 24 h; LC50 = 6.4 ppm, 7 days; MC50 = 6.9 ppm, 7 days)	[20]
	Gutierreza microcephala * Asteraceae	AP	Bacchabolivic acid (10) (MC50 = 10.7 ppm, 7 days; LD50 = 6.59 ppm, 24 h; 50 ppm: 90.2% IAche)Methyl ester of 10 (10a) (MC50 = 3.46 ppm, 7 days; LD50 = 15.05 ppm, 24 h; 50 ppm: 60% IAche)	[21]
	Cedrela dugessi * Meliaceae	Leaves	α and β-Photogedunin (11 and 12) mixture (LC50 = 10 ppm, 7days; 19.2 ppm: 88% larval growth inhibition; 5 ppm: 23 and 85% pupation and emergence reduction)α and β- Photogedunin acetates (11a and 12a) mixture (LC50 = 8 ppm, 7 days)Gedunin (13) (LC50 = 39 ppm, 7days; 5 ppm: 91% larval growth inhibition; 5 ppm: 6.2 and 78.5% pupation and emergence reduction)	[22]
	Cedrela salvadorensis	Leaves	α- and β-Photogedunin (11 and 12), α- and β- photogedunin acetates (11a and 12a) mixture gedunin (13)	[22]
	Vitex hemsleyi * Lamiaceae	Leaves Stem	Anticopalic acid (14) (EC50 = 90.6 ppm, L6 larvae)	[23]
	Myrtillocactus geometrizans * Cactaceae	Whole	Macdougallin (15) (LD95 = 285 ppm; 50 ppm: 97.2% M; 0% pupation; 0% emergence)Peniocerol (16) (LD95 = 125 ppm; 50 ppm: 97.2% M; 0% pupation; 0% emergence)mixture (4:6) 15 + 16 (LD95 = 135 ppm; 20 ppm: 97.2% M; 0% pupation; 0% emergence)	[24]
	Crescentia alata Bignoniaceae	Fruits	Fraction enriched with ningpogenin (17) (100 ppm: 80% larval mortality); fraction enriched with: β-sitosterol (18), stigmasterol (19) and6β,7β,8α,10-tetra-p-hydroxybenzoyl-cis-2-oxabicycle[4.3.0]nonan-3-one (20)(100 ppm: 65% larval mortality)	[25,26]
	Lippia graveolens Verbenaceae	Leaves	Hexane (10–100 ppm: deformed adults), thymol (21, 70.6%), carvacrol (22, 22.8%)	[27]
S. littoralis	Salvia keerlii * Lamiaceae	AP	Kerlinolide (23) (AI50 = 67 ppm)	[28]
	Salvia lineata * Lamiaceae	AP	1(10)-Dehydrosalviarin (24, AI50 = 32 ppm)	[28]
	Salvia melissodora * Lamiaceae	AP	13,14-Dihydro-3,4 epoxy-melissodoric acid methyl ester acetate (25) (AI50 = 1 ppm)2-β-acetoxy-7α-hydroxy-neo-clerodan-3,13-dien-18,19:16.15-diolide (26) (AI50 = 84 ppm)	[28]
	Salvia rhyacophila * Lamiaceae	AP	Salviarin (27) (AI50 = 81 ppm)6β-Hydroxysalviarin (28) (AI50 = 24 ppm)	[28]
	Salvia semiatrata * Lamiaceae	AP	Semiatrin (29) (AI50 = 87 ppm)	[28]
	Senecio toluccanus * Asteraceae	Roots	Toluccanolide A (30) and toluccanolide A acetate (30a) (50 μg/cm2: 57 and 69.6% antifeedant effect, respectively)	[29]

* Endemic; AP: Aerial parts; AI50 = Median antifeedant index; EC50 = Effective antifeedant concentration; GD50 = Median Growth Dose; ID50 = Median Inhibitory Dose; LC50 = Median Lethal Concentration; LD50 = Median Lethal Dose; LV50 = Median Larval Viability; IAche: Inhibition of acetylcholinesterase; MC50 = Median Mortality Concentration.

Figure 1

Terpenes with activity on Spodoptera sp.

2.1.2. Flavonoids

Flavonoids isolated from the aerial parts of G. microcephala exhibited moderate effects against S. frugiperda, with these compounds including 5,7,2′-trihydroxy-3,6,8,4′,5′-pentamethoxyflavone (31), 5,7,4′-trihydroxy-3,6,8-trimethoxyflavone (32), 5,7,2′,4′-tetrahydroxy-3,6,8,5′-tetramethoxyflavone (33), and 5,2′-dihyhydroxy-3,6,7,8,4′,5′-hexamethoxyflavone (34). Flavone 31 displayed the lowest LC50 value (3.9 ppm) against neonatal S. frugiperda larvae [21]. In addition, flavones 31–34 exhibited 93.7–100% acetylcholinesterase inhibitory activity at 50 ppm (Table 2, Figure 2).

Table 2

Insecticidal flavonoids from Mexican flora effective on Spodoptera frugiperda.

Species/Family	Plant Part	Compound (Toxicity)	Ref.
Gutierreza microcephala * Asteraceae	AP	5,7,2′-Trihydroxy-3,6,8,4′,5′-pentamethoxyflavone (31) (MC50 = 3.9 ppm, 7 days; LD50 = 36.65 ppm, 24 h; 50 ppm: 35.9% IAche)5,7,4′-Trihydroxy-3,6,8-trimethoxyflavone (32) (50 ppm: 27.5% IAche)5,7,2′,4′-Tetrahydroxy-3,6,8,5′-tetramethoxyflavone (33) (MC50 = 27.8 ppm, 7 days; 50 ppm: 27.5% IAche)5,2-dihydroxy-3,6,7,8,4′,5′-hexamethoxyflavone (34) (50 ppm: 17.8% IAche)	[21]

* Endmic; IAche: Inhibition of acetylcholinesterase; LD50 = Median Lethal Dose; MC50 = Median Mortality Concentration.

Figure 2

Insecticidal flavonoids (31–35) and stilbenes (36–38) effective on Spodoptera frugiperda.

Rutin (35) is a flavonol glycoside-reported R. graveolens constituent (Figure 2), which was also tested and showed no effect towards S. frugiperda [30].

2.1.3. Stilbenes

Stilbenes identified from the bark of Y. periculosa (Asparagaceae) included resveratrol (36), 4,4′-dihydroxystilbene (37), and 3,3′,5,5′-tetrahydroxy-4-methoxystilbene (38), with 38 being the most potent and exhibiting an LC50 value of 5.4 ppm towards neonatal larvae at seven days and a median growth inhibition (GI50) value of 3.45 ppm at 21 days (Table 3, Figure 2) [31].

Table 3

Stilbenes from Mexican flora active on Spodoptera frugiperda.

Species/Family	Plant Part	Compound (Toxicity)	Ref.
Yucca periculosa * Asparagaceae	Bark	Resveratrol (36) (LD50 = 24.1 ppm, 24 h; GI50 = 5.94 ppm, 21 days; LC50 = 6.4 ppm, 7 days)4,4′-Dihydroxystilbene (37) (LD50 = 38 ppm, 24 h; GI50 = 9.24 ppm, 21 days; LC50 = 27.6 ppm, 7 days)3,3′,5,5′-Tetrahydroxy-4-methoxystilbene (38) (LD50 = 10.1 ppm, 24 h; GI50 = 3.45 ppm, 21 days; LC50 = 5.4 ppm, 7 days)	[31]

* Endemic; GI50 = Median Growth inhibition; LD50 = Median Lethal Dose; LC50 = Median Lethal Concentration.

2.1.4. Coumarin and Ketone

The leaves of R. graveolens were shown to produce psoralen (39) and a median chain ketone 2-undecanone (40), both of which were effective against neonatal S. frugiperda larvae. However, metabolite 39 was more potent than 40, with larval mortalities of 100% and 50% respectively observed at a concentration of 1 mg/mL (Table 4) [30].

Table 4

A coumarin and a ketone active on Spodoptera frugiperda.

Species/Family	Plant Part	Compound (Toxicity)	Ref.
Ruta graveolens Rutaceae	Leaves	Psoralen (39) (1 mg/mL: 100% larval mortality)2-Undecanone (40) (1 mg/mL: 50% larval mortality)	[30]

2.1.5. Fatty Acids

Additional compounds with reported activity against S. frugiperda include palmitic (41), oleic (42), linoleic (43), and linolenic (44) acids (Table 5), which exhibited LV50 values of ≤ 1354 ppm, with the most active compounds being unsaturated fatty acids. These active fatty acids were detected in C. papaya seeds and R. communis leaves grown in Mexico [32,33]. Both of these plant species are widely distributed, and R. communis is recognized for its pesticidal effects and high fatty acid content [34]. Furthermore, the powdered seed of C. papaya has been shown to cause larval mortality and weight reduction in S. frugiperda [35,36].

Table 5

Fatty acids with biological activity on Spodoptera frugiperda.

Species/Family	Plant Part	Compound (Toxicity)	Ref.
Carica papaya Caricaceae	Seeds	Palmitic acid (41) (LV50 = 989 ppm)Oleic acid (42) (LV50 = 1353.4 ppm)Powder in artificial diet (15%: 90% mortality, 72 h, all varieties)	[32]
Ricinus communis Euphorbiaceae	Leaves	Linoleic acid (43) (LV50 = 857 ppm, 1st instar larvae)Linolenic acid (44) (LV50 = 849 ppm, 1st instar larvae)	[33]

LV50 = Median Lethal Volume.

2.1.6. Alkaloidal Fractions

Alkaloid-enriched fractions from leaves of three species of Lupinus (Fabaceae) showed remarkable toxic effects against S. frugiperda (LD50 = 16–70 ppm). These fractions primarily contained lupanine (45), multiflorine (46), sparteine (47), aphylline (48), α-sparteine (49), and epi-aphylline (50) (Table 6, Figure 3), with a commercial standard of 47 used during the evaluations. Interestingly, L. montanus and L. aschenbornii had high amounts of 47 (640 and 780 μg/g, respectively), whereas it was absent from L. stipulatus, which instead contained 48 and 50 as major alkaloids (280 and 307 μg/g, respectively). The alkaloidal fraction of L. stipulatus was the most toxic and fast-acting against S. frugiperda, with an LD50 value of 20 μg/mL at seven days, similar to that observed for 47 (LD50 = 11 μg/mL) [37].

Table 6

Alkaloids effective on Spodoptera frugiperda.

Plant Species/Family	Plant Part	Compound (Toxicity)	Ref.
Lupinus aschenbornii * Fabaceae	Leaves	Alkaloids extract (LD50 = 24 μg/mL, 7 days)Lupanine (45, 86 μg/g), multiflorine (46, 31 μg/g), sparteine (47, 780 μg/g),47 commercial standard (LD50 = 11 μg/mL, 7 days)	[37]
Lupinus montanus * Fabaceae	Leaves	Alkaloids extract (LD50 = 65 μg/mL, 7 days)Aphylline (48, 17.6 μg/g), 45 (9.2 μg/g), α-sparteine (49, 5 μg/g), 47 (640 μg/g)	[37]
Lupinus stipulates * Fabaceae	Seeds	Alkaloids extract (LD50 = 20 μg/mL, 7 days)48 (280 μg/g), epi-aphylline-like (50, 307 μg/g), 45 (11.7 μg/g)	[37]

* Endemic; LD50 = Median Lethal Dose.

Figure 3

Metabolites with activity on Spodoptera frugiperda.

2.1.7. Plant Extracts with Activity against Spodoptera sp.

The crude organic extracts of 10 plant species exhibited effective insecticidal activities against S. frugiperda, with one showing activity against S. exigua, the results of which are shown in Table 7. These plants included Bursera copallifera, Bursera grandiflora, Bursera lancifolia, Ipomoea murucoides, Ipomoea pauciflora, Salvia connivens, Salvia microphylla, Tagetes erecta, Trichilia havanensis, and Vitex mollis.

Table 7

Plant extracts from Mexican flora with activity on Spodoptera sp.

Insect	Plant Species/Family	Plant Part	Extract (Toxicity)	Ref.
S. exigua	Trichilia havanensis * Meliaceae	Seeds	Oil (7000 mg/L: 56% LM, 12 days; 100 mg/L: 71.3% LWR)Solid fraction (7000 mg/L: 56% LM, 12 days; 100 mg/L: 98.5% LWR)	[38]
S. frugiperda	Bursera copallifera * Burseraceae	Leaves	Ethyl acetate (1000 ppm: 73% LWR, 7 days; IC50 = 553 µg/mL IAche)Methanol (1000 ppm: 55% LWR, 7 days; IC50 = 367 µg/mL IAche)	[42]
		Leaves stem	Acetonic leaves extract (500 ppm: 47% LM; 50% LWR, 14 days); hexanic leaves extract (500 ppm: 44% deformed pupae, 14 days);	[41]
	Bursera grandifolia * Burseraceae	Leaves	Methanol leaves extract (500 ppm: 45% LM; 35% deformed pupae, 14 days)	[41]
	Bursera lancifolia * Burseraceae	Seeds	Ethyl acetate (1000 ppm: 39% LWR, 7 days; IC50 = 397 µg/mL IAche)Methanol (1000 ppm: 32% LWR, 7 days; IC50 = 707 µg/mL IAche)	[42]
	Ipomoea murucoides * Convolvulaceae	Roots	Methanol (LC50 = 2.69 mg/mL)	[45]
	Ipomoea pauciflora * Convolvulaceae	Seeds	Hexane (LC50 = 1.68 mg/mL)Chloroform (LC50 = 0.55 mg/mL)	[43]
	Salvia connivens * Lamiaceae	AP	Chloroform (LV50 = 936 ppm, 1st instar larvae)	[44]
	Salvia microphylla Lamiaceae	AP	Chloroform (LV50 = 916 ppm, 1st instar larvae)	[44]
	Tagetes erecta Asteraceae	Leaves	Hexane, acetone, and ethanol (LC50 = 312.2, 264.9, and 152.2 ppm respectively on L1 larvae)	[40]
	Vitex mollis * Lamiaceae	Leaves	Dichloromethane (LC50 = 46.35 ppm)Chloroform-methanol 1:1 (LC50 = 13.63 ppm)methanol (LC50 = 61.05 ppm)	[39]

* Endemic; IC50 = Median Inhibitory Concentration; IAche: Inhibition of acetylcholinesterase; LC50 = Median Lethal Concentration; LV50 = Median Larval Viability; LM: larval mortality; LWR: larval weight reduction.

Against S. exigua, only the activity of an extract from T. havanensis seeds was reported, with an acetonic extract and its supernatant oil causing significant larval mortality and weight reduction. Furthermore, the acetone extract caused a noticeable delay in the development of S. exigua larvae when used at 500 mg/L [38].

The insecticidal activity of V. mollis extracts (dichloromethane, chloroform-methanol, and methanol) towards S. frugiperda was very interesting. A chloroform-methanol (1:1) extract from V. mollis leaves caused noteworthy mortality against S. frugiperda larvae, with an LC50 value of 13.63 ppm observed, greater than that of previously reported terpenes (vide infra). In addition, the percentage of larvae reaching pupation decreased in the presence of all of the extracts [39]. As expected, leaf and flower extracts of T. erecta showed activity against S. frugiperda larvae. At 500 ppm, the acetonic extract from leaves was the most effective, with a 50% reduction in larval weight observed after seven days. However, the hexane, acetone, and ethanol leaf extracts all exhibited lethal activities against S. frugiperda larvae, with observed LC50 values of 312.2, 246.9, and 152.2 ppm, respectively [40].

Other organic plant extracts with activity against S. frugiperda include acetonic extracts of B. copallifera, ethyl acetate extracts of B. lancifolia, and a methanol extract of B. grandifolia, which caused deformations in pupae or adults at different concentrations; acetylcholinesterase is also inhibited by these extracts [41,42]. In addition, I. murucoides, I. pauciflora, S. connivens, and S. microphylla extracts displayed slight effects against first-stage larvae of S. frugiperda at high concentrations (Table 7) [42,43,44,45].

2.2. Aedes aegypti, Anopheles albimanus, and Culex quinquefasciatus

The extracts and metabolites of 11 plant species displayed activity against the Culicides A. aegypti, A. albimanus, and C. quinquefasciatus, vectors of the human diseases, dengue fever, malaria, and lymphatic filariasis, respectively. These plant species included A. indica, Argemone mexicana, Erythrina Americana, Heliopsis longipes, Persea americana, Pseudocalymma alliaceum, Pseudosmodingium perniciosum, Ruta chalepensis, Salmea scandens, Thymus vulgaris, and Zanthoxylum fagara (Table 8, Table 9 and Table 10 and Figure 4).

Table 8

Metabolites from Mexican flora with effect against Culicidae.

Insect	Species/Family	Plant Part	Compound/Extract (Toxicity)	Ref.
Aedes aegypti	Heliopsis longipes * Asteraceae	Roots	Ethanol (LC50 = 4.07 mg/L, LM 48 h)Affinin (51) (LC50 = 7.38 mg/L, LM 48 h)N-Isobutyl-2E-decenamide (52) (LC50 = 36.97 mg/L, LM, 48 h)	[46]
	Salmea scandens * Asteraceae	Stem bark	EOs (LC50 = 0.3 μg/mL, 24 h)N-isobutyl-(2E,4E,8Z,10Z)-dodecatetraenamide (55, 22.5%)N-isobutyl-(2E,4E,8Z,10E)-dodecatetraenamide (56, 17.2%)	[48]
Anopheles albimanus	Heliopsis longipes * Asteraceae	Roots	Ethanol (LC50 = 2.48 mg/L, LM 48 h)51 (LC50 = 4.24 mg/L, LM 48 h)52 (LC50 = 7.47 mg/L, LM 48 h)	[46]
	Salmea scandens * Asteraceae	Stem bark	EOs (LC50 = 2.5 μg/mL, 24 h)	[48]
Culex quinquefasciatus	Erythrina americana Fabaceae	Seeds	Alkaloidal fraction (LC50 = 87.5 mg L−1, LM)β-eritroidina (53, LC50 = 225 mg L−1; LM)Erisovina (54, LC50 = 399 mg L−1, LM)	[47]
	Persea Americana Lauraceae	Leaves	EOs (50 mg/L: 40% mortality); (800 mg/L: 57.5% mortality; RGI = 0.74)estragole (57) (61.86%), sabinene (58, 15.16%), α-pinene (59, 14.25%)	[49]
	Pseudocalymma alliaceum * Bignonaceae	Fresh leaves	EOs: (LC50 = 385.29 ppm, 48 h)hydrolat (LC50 = 9.05%, 48 h)diallyl disulphide (60) (50.05%), diallyl sulphide (61, 11.77%), trisulphide di-2-propenyl (62, 10.37%)	[50]

* Endemic; Eos = Essential Oils; LC50 = Median Lethal Concentration; LM =Larval Mortality.

Table 9

Plant extracts from Mexican flora with activity on Aedes aegypti and Culex quinquefasciatus.

Insect	Species/Family	Plant Part	Extract (Toxicity)	Ref.
Aedes aegypti	Argemone mexicana Papaveraceae	Seeds	Hexane (LC50 = 80 μg /mL, 48 h)acetone (LC50 = 50 μg/mL, 48 h)	[51]
	Pseudosmodingium perniciosum * Anacardiaceae	Stem Bark	Hexane (LC50 = 20 μg/mL, 48 h)	[51]
	Ruta chalepensis Rutaceae	Aerial part	Ether and methanol (LC50 = 1.8 and 6.4 µg/mL, respectively, 24 h)	[52]
	Thymus vulgaris Lamiaceae	Leaves	Ether (LC50 = 4.4 ppm, 24 h, 4th instar larvae)	[52]
	Zanthoxylum fagara Rutaceae	Fruits	Ether (LC50 = 75.1 µg/mL, 24 h)	[52]
Culex quinquefasciatus	Azadirachta indica Meliacea	Seeds	Aqueous (1st instar: LD50 = 460 ppm; 2nd instar LD50 = 440 ppm; 3rd instar LD50 = 410 ppm; 4th instar; LD50 = 550 ppm)	[53]

* Endemic; LC50 = Median Lethal Concentration; LD50 = Median Lethal Dose.

Table 10

Plant extracts from Mexican flora with activity on Anastrepha ludens and Bactericera cockerelli.

Insect	Species/Family	Plant Part	Extract (Toxicity)	Ref.
Anastrepha ludens	Annona diversifolia Annonaceae	Leaves Stems	Ethanol stems (1000 μg/mL: 89.3%, third instar LM, 72 h)Aqueous leaves (100 μg/mL: 70.3% third instar LM, 72 h)Aqueous stems (1000 μg/mL: 74.3 third instar LM, 72 h)	[54]
	Annona lutescens Annonaceae	Leaves Stems	Ethanol leaves (100 μg/mL: 27.0%, third instar LM, 72 h)Ethanol stems (1000 μg/mL: 70.3%, third instar LM, 72 h)Aqueous leaves (100 μg/mL: 81.7% third instar LM, 72h)Aqueous stems (100 μg/mL: 95.9% third instar LM, 72 h)	[54]
	Annona muricata Annonaceae	Leaves Stems	Ethanol leaves (100 μg/mL: 63.3%, third instar LM, 72 h)Ethanol stems (1000 μg/mL: 61.3%, third instar LM, 72 h)Aqueous leaves (100 μg/mL: 78.3% third instar LM, 72 h)Aqueous stems (100 μg/mL: 86.0 third instar LM, 72 h)	[54]
	Magnolia dealbata Magnoliaceae	Dry sarcotesta	Ethanol (0.1 mg/mL: 12.8% survival after 3 days; Abbott index: 86.8%, adults)	[55]
Bactericera cockerelli	Annona muricata Annonaceae	Seeds	Hexanol (LC50 = 193.5 ppm, 72 h)	[55]

LC50 = Median Lethal Concentration LM: Larval Mortality.

Figure 4

Metabolites with effect on Aedes aegypti, Anopheles albimanus, and Culex quinquefasciatus.

2.2.1. Alkaloids

An alkamide named affinin (51), isolated from H. longipes roots, and its reduced product N-isobutyl-2E-decenamide (52) were moderately active against A. aegypti (LC50 = 7.38 and 36.97 mg/L, respectively). Moreover, the Coleoptera A. albimanus was more sensitive to these compounds, with LC50 values of 4.24 and 7.47 mg/L, respectively. However, a crude ethanol extract displayed lower lethal activity against the larval stage of A. albimanus and A. aegypti, with LC50 values of 2.48 and 4.07 mg/L, respectively (Table 8) [46]. The alkaloidal fraction from E. americana seeds induced high C. quinquefasciatus larval mortality, with an LC50 value of 87.5 mg/L. After chromatographic purification, β-eritroidina (53) and erisovina (54) were obtained and tested; however, these pure compounds exhibited lower C. quinquefasciatus larvicidal activities in comparison with the alkaloidal fraction (LC50 = 225 and 399 mg/L, respectively) [47]. In contrast, EOs from S. scandens’ stem bark caused a potent lethal effect on A. albimanus larvae (2.5 µg/mL), with the isomers N-isobutyl-(2E,4E,8Z,10Z)-dodecatetraenamide and N-isobutyl-(2E,4E,8Z,10E)-dodecatetraenamide (55, 56; 39.7%) constituting the majority of the compounds in this EO [48].

2.2.2. EOs

Among the assayed EOs, the EO obtained from leaves of S. scandens was the most active and had the lowest LC50 of 0.3 µg/mL on the larvae of A. aegypti [48]. Culex quinquefasciatus larvae were moderately sensitive to EOs from the leaves of P. americana (800 mg/L: 57.5% mortality) and P. alliaceum (LC50 = 385.29 ppm). The EO from P. americana was observed to contain estragole (57, 61.86%), sabinene (58, 15.16%), and α-pinene (59, 14.26%), while that of P. alliaceum consists primarily of diallyl disulphide (60, 50.05%), diallyl sulphide (61, 11.77%) and trisulphide di-2-propenyl (62, 10.37%) (Table 8, Figure 4) [49,50].

2.2.3. Plant Extracts

The screening of extracts from six plants for activity against the fourth-instar A. aegypti larvae identified those of A. mexicana and P. perniciosum as the most effective (Table 9). Hexane and acetone extracts from A. mexicana seeds and hexane extracts from the bark of P. perniciosum showed the lowest larvicidal activities, with LC50 values of, 80, 50, and 20 µg/mL, respectively [51]. Other organic extracts observed to have larvicidal activity against A. aegypti include those of R. chalepensis, T. vulgaris, and Z. fagara, exhibiting notable LC50 values of 1.8, 4.4 and 75.1 µg/mL, respectively [52]. In contrast, the aqueous extract of A. indica showed slight effects towards four different instars of C. quinquefasciatus (LD50 = 410–550 ppm) [53].

2.3. Anastrepha ludens

Foliarn and stem extracts from three species of the family Annonaceae, Annona diversifolia, A. lutescens, and A. muricata, as well as one species of the family Magnoliaceae, Magnolia dealbata, showed good activity against the Mexican fruit fly A. ludens (Coleoptera). Among the assayed extracts, the aqueous extracts from stems exhibited the best effect at 100 μg/mL, with the greatest effect (95.9%) caused by A. lutescens (Table 10) [54,55].

2.4. Bactericera Cockerelli

The potato psyllid (B. cockerelli) displayed sensitivity to hexanol extracts of A. muricata seeds, with a lethal effect observed using 193.5 ppm after 72 h (Table 10) [56].

2.5. Bemisia tabaci

To date, five studies have reported on the use of natural Mexican plant products in whitefly (B. tabaci) management. The results of these studies identified 11 Mexican plants with extracts that are effective against various B. tabaci life stages (eggs, nymphs, and adults). The plant species included Acalypha gaumeri, Agave tequilana, Annona squamosa, A. indica, Capsicum chinense, Carlowrightia myriantha, C. ambrosioides, Petiveria alliacea, Piper nigrum, Pluchea sericea, and Trichilia arborea.

Plant Extracts

Cruz-Estrada [57] investigated the effects of extracts from six plant species against B. tabaci eggs and reported that aqueous extracts from the leaves of A. gaumeri, A. squamosa, P. alliacea, and T. arborea exhibited activity (LC50 = 0.36–0.42%, w/v), as did the ethanol extracts of P. alliacea (LC50 = 2.09 mg/mL) and T. arborea (LC50 = 2.14 mg/mL). The latter two species showed the highest activity against B. tabaci nymphs (LC50 = 1.27 and 1.61 mg/mL, respectively). In parallel, leaf extracts from A. indica plants grown in Mexico were assayed. The toxic effects of the aqueous extracts of native plants were similar to those of A. indica aqueous extracts (LC50 = 0.30%, w/v) and were greater than those of the A. indica ethanolic extract against eggs (LC50 = 3.60 mg/mL) and nymphs (LC50 = 2.57 mg/mL). A. tequilana juice (undiluted) and its hexanic extract (2%) promoted B. tabaci nymph mortality (100% and 91%, respectively), which is interesting given the significant quantities of juice obtained from the waste of this agave (Table 11) [58].

Table 11

Plant extracts from Mexican flora with activity on Bemisia tabaci.

Species/Family	Plant Part	Extract (Toxicity)	Ref.
Acalypha gaumeri * Euphorbiaceae	Leaves	Aqueous (LC50 = 0.39% w/v on egg, 48 h)Ethanol (LC50 = 3.54 mg/mL on eggs; 3.15 mg/mL on nymphs, 48 h)	[57]
Annona squamosa Annonaceae	Leaves	Aqueous (LC50 = 0.36% w/v on eggs, 48 h)Ethanol (LC50 = 2.71 mg/mL on eggs, 48 h; 2.66 mg/mL on nymphs, 48 h)	[57]
Agave tequilana Asparagaceae	Leaves	Juice (undiluted: 31% mortality on adults)hexane (4%: 100% mortality on adults)	[58]
Azadirachta indica Meliacea	Leaves	Aqueous (LC50 = 0.30% w/v eggs, 48 h)Ethanol (LC50 = 4.14 mg/mL, eggs, 48 h; 10 ppm: 99.3% mortality of nymphs)	[57]
Capsicum chinense Solanaceae	Fruits	Ethanol (LC50 = 29.4% w/v; LT50 = 7.31 h; RI = 0.11)	[59]
Carlowrightia myriantha * Acanthaceae	Leaves	Aqueous (LC50 = 1.1% w/v on eggs)Ethanol (LC50 = 2.69 mg/mL on eggs; 3.10 mg/mL on nymphs)	[57]
Chenopodium ambrosioides Chenopodiaceae	Leaves Stems	Ethanol (LC50: 3.26% w/v, resuspended in water)	[60]
Petiveria alliacea Petiveriaceae	Aerial part	Aqueous (LC50 = 0.42% w/v on eggs)Ethanol (LC50 = 2.09 mg/mL on eggs; 1.27 mg/mL on nymphs)	[57]
Piper nigrum Piperaceae	Fruits	Ethanol (LC50: 1.6% w/v, resuspended in water)	[60]
Pluchea serícea Asteraceae	Leaves Stems	Aqueous leaves (LC50: 1190 ppm; RI = 0.52 on adults, 24 h)Acetone leaves (LC50: 700 ppm; RI = 0.78 on adults, 24 h)Ethanol leaves (LC50: 1250 ppm RI = 0.66 on adults, 24 h)Aqueous stems (LC50: 2620 ppm; RI = 0.54 on adults, 24 h)	[61]
Trichilia arborea Meliaceae	Leaves	Aqueous (LC50 = 0.39% w/v on eggs, 48 h)Ethanol (LC50 = 2.14 mg/mL on eggs, 48 h; 1.61 mg/mL on nymphs)	[57]

* Endemic; LC50: Median Lethal Concentration; RI: Repellency index.

In another study (Table 11), the ethanol extracts of mature C. chinense fruits (creole orange variety) showed slight repellency and mortality effects against B. tabaci adults (LC50 = 29.4% w/v, LT50 = 7.31 h). The concentration of capsaicinoids in the fruit of the habanero pepper was 1193.6 mg/kg. Capsaicinoids have been reported to have toxic and repellent effects against insects [59]. Ethanolic extracts from the leaves of C. ambrosioides and the fruits of P. nigrum showed good lethal activity against B. tabaci, with the lowest LC50 of 1.6% (w/v) observed for the P. nigrum extracts. Furthermore, P. nigrum produces high ethanolic extract yields (3.69%), and this plant is inexpensive and accessible [60]. Finally, P. sericea is an interesting Asteraceae species which the extracts of have been shown to be effective against B. tabaci adults, with acetone, aqueous, and ethanolic extracts of the leaves shown to have moderate repellence activity (RI50 of 0.52–0.78) [61].

2.6. Copitarsia Decolora and Dactylopius Opuntiae

The EOs of Beta vulgaris, C. graveolens, and Chenopodium berlandieri subsp. nuttalliae reduced the fecundity and fertility (75–99%) of C. decolora and increased (19–38%) the lengths of the larval and pupal periods (Table 12) [62].

Table 12

Plant extracts from Mexican flora with activity against Copitarsia decolora and Dactylopius opuntiae.

Insect	Species/Family	Plant Part	Extract (Toxicity)	Ref.
Copitarsia decolora	Beta vulgaris Chenopodiaceae	Stems Leaves	EOs (0.5%: 19% and 27% increased larval and pupal period length; 99% reduced fecundity and fertility)	[62]
	Chenopodium berlandieri subsp. nuttalliae Chenopodiaceae	Whole plant	EOs (0.5%: 22% and 38% increased larval and pupal period length; 94% and 85% reduced fecundity and fertility)	[62]
	Chenopodium graveolens Chenopodiaceae	Whole plant	EOs (0.5%: 19% and 28% reduced larval and pupal period length; 75% and 96% reduced fecundity and fertility)	[62]
Dactylopius opuntiae	Cymbopogon winterianus Poaceae	Leaves	EOs (LC50 = 6.6 mL/100 mL on 1st instar cochineal)	[63]
	Lippia graveolens Verbenaceae	Leaves	EOs (LC50 = 5.2 mL/100 mL on cochineal mobile juveniles)	[63]
	Mentha spicata Lamiaceae	Leaves	EOs (LC50 = 0.8 mL/100 mL solvent on cochineal mobile juveniles). Carvone (63, 61.03%) and limonene (64, 15.18%)	[63]
	Ocimum basilicum Lamiaceae	Leaves	EOs (LC50 = 2.4 mL/100 mL solvent on cochineal mobile juveniles)	[63]

LC50 = Median Lethal Concentration.

Vazquez-García [63] reported that EOs obtained from Cymbopogon winterianus, L. graveolens, Mentha spicata, and Ocimum basilicum were active against the first-instar larvae of the prickly pear cochineal D. opuntiae, with LC50 values ranging from 0.8–6.6 mL/100 mL. The most effective was the EO of M. spicata, the primary constituents of which were carvone (63, 61.03%) and limonene (64, 15.18%) (Table 12, Figure 5).

Figure 5

The majority components in the EOs of Mentha spicata effective on Dactylopius opuntiae.

2.7. Leptinotarsa decemlineata

The metabolite 6-hydroxyeuryopsin (65) isolated from S. toluccanus, and its acetate derivative (65a) exhibited a higher antifeedant effect (85 and 93.3% at 50 μg/cm2, respectively) against the Colorado potato beetle (L. decemlineata) than did S. frugiperda (vide supra) (Table 13, Figure 6) [29].

Table 13

Metabolites from Mexican flora with activity against Leptinotarsa decemlineata.

Insect	Species/Family	Plant Part	Extract/Compound (Toxicity)	Ref.
Leptinotarsa decemlineata	Senecio toluccanus * Asteraceae	Roots	6-Hydroxyeuryopsin (65) and acetyloxyeuropsin (65a) (50 μg/cm2: 85.5% antifeedant effect)	[29]

* Endemic; LC50 = Median Lethal Concentration.

Figure 6

Insecticidal metabolite 6-hydroxyeuryopsin from Senecio toluccans.

2.8. Prostephanus truncates

The larger grain borer (P. truncates) was shown to be susceptible to EO from the leaves of Lippia palmeri, with an LC50 value of 320.5 μL/L observed after 72 h. After the application of the EOs, a strong repellency against the insect at 200 μL/L was observed, and no insect emerged at 500 μL/L in 24 h. These EOs primarily contained 22 (58.9%) and p-cimene (66, 21.8%) as majority compounds (Table 14, Figure 7) [64].

Table 14

Essential oils from Mexican flora with activity on Prostephanus truncates.

Insect	Species/Family	Plant Part	Extract/Compound (Toxicity)	Ref.
Prostephanus truncates	Lippia palmeri Verbenaceae	Leaves	EOs (LC50 = 320.52 μL/L mortality, 24 h); carvacrol (22, 5.2%), 21 (58.9%)p-cimene (66, 21.8%)	[64]

LC50 = Median Lethal Concentration

Figure 7

Majority metabolite (p-Cimene) from extract of Lippia palmeri.

2.9. Sitophilus zeamais

The EOs of 14 plant species with activities against the stored grain pest S. zeamais were compiled. These EOs were primarily derived from members of the Asteraceae family (Aster subulatus, Bahia absinthifolia, Chrysactinia mexicana, Erigeron longipes, Eupatorium glabratum, Heliopsis annua, Heterotheca inuloides, Hippocratea celastroides, Hippocratea excelsa, Senecio flaccidus, Stevia serrata, and Zaluzania peruviana) as well as members of the Rutaceae and Verbenaceae families (Stauranthus perforates and L. palmeri, respectively).

2.9.1. Terpenes

The triterpenoid pristimerin (67) was isolated from the roots of H. excelsa and displayed a high antifeeding activity index (AAI) of 89% and slight mortality (M = 16%) when used in a 1% formulation against S. zeamais (Table 15, Figure 8) [65].

Table 15

Plant extracts and metabolites from Mexican flora with activity against Sitophilus zeamais.

Species/Family	Plant Part	Extract/Compound (Toxicity)	Ref.
Hippocratea excels * Asteraceae	Root cortex	1% Pristimerin (67) (AAI = 89.2% and M = 16%, 5 days)	[65]
Eupatorium glabratum Asteraceae	Leaves	EOs (LC50 = 16 (females) and 20 μL/mL (males) after 1 week); LT50 = 53 (females) and 70 h (males); α-pinene (59, 29.5), α-phellandrene (68, 19.6%)	[66]
Lippia palmeri * Verbenaceae	Leaves	EOs (LC50 = 441.45 μL/L mortality, 48 h)p-cimene (66, 21.8%), 21 (58.9%)	[64]
Aster subulatus Asteraceae	Leaves	1% Leaves powder (M = 80.5%, 15 days)	[67]
Bahia absinthifolia Asteraceae	Leaves	1% powder (AE = 21.6%, 55 days)	[67]
Chrysactinia mexicana Asteraceae	Leaves Flower	1% Leaves powder (M = 80.5%, 15 days; AE = 0.0%, 55 days)1% Flower powder (AE = 45.0%, 55 days)	[67]
Erigeron longipes Asteraceae	Flower	1% powder (M = 88.3%, 15 days)	[67]
Heliopsis annua Asteraceae	Leaves	1% powder (M = 80.6%, 15 days)	[67]
Heterotheca inuloides var. rosei * Asteraceae	Leaves Flower	1% Leaf powder (M = 87.7%, 15 days; AE = 0.0%, 55 days)1% Flower powder (M = 87.7%, 15 days; AE = 45.0%, 55 days)	[67]
Hippocratea celastroides Asteraceae	Roots	1% Dichloromethane (AAI = 70.7%, 5 days)1% Hexane (AAI = 67.8%, 5 days)1% Acetone (soluble part: AAI = 72.3%, precipitate: AAI = 73.9%, 5 days)	[65]
Senecio flaccidus Asteraceae	Flower	1% Powder (M = 80.7%, 55 days)	[67]
Stevia serrata Asteraceae	Leaves Flower	1% Leaf powder (M = 80.2%, 55 days)1% Flower powder (M = 81.8%, 55 days)	[67]
Zaluzania peruviana Asteraceae	Leaves Flower	1% Leafs powder (M = 88.1%, 15 days; AE = 50.0%, 55 days)1% Flower powder (M = 48.3%, 15 days; AE 40%, 55 days)	[67]
Stauranthus perforates Rutaceae	Roots	Powder mixed with maize kernels (1–3%: 91, 95.5. and 100% mortality respectively, 15 days)	[67]

* Endemic; AAI: Antifeedant Activity Index; AE: Adults emergence; M= Mortality; LC50 = Median Lethal Concentration; LT50 = Median Lethal Time.

Figure 8

Metabolites with activity against Sitophilus zeamais.

2.9.2. EOs

A bioactive EO from E. glabratum exhibited high activity against female and male S. zeamais, with LC50 values of 16 and 20 µL/mL, respectively, and median lethal times of 53 and 70 h, respectively. Chromatographic analyses of E. glabratum EO revealed the presence of α-pinene (59) and α-phellandrene (68, 19.6%) as the major compounds (29.5%) [66]. In contrast, the pest insect S. zeamais exhibited a slight sensitivity to EO from L. palmeri leaves, with LC50 value of 441.45 μL/L against adults after 48 h. In addition, this EO induced total repellency against maize weevil adults, with no emergence observed using a concentration of 1000 μL/L after 24 h, with major EO components having been previously described (21 and 66) (Table 15, Figure 8) [64].

2.9.3. Plant Extracts

Juárez-Flores [67] screened flower powder and leaf powders from 81 plant species belonging to the Asteraceae family. Among the 162 plant powders tested (1%, w/w), twelve powders showed remarkable lethal activities (>80%) against S. zeamais, but only two inhibited adult emergence (<22 insects), B. absinthifolia and C. Mexicana (Table 15). The most effective of these powders were those produced from the leaves of C. mexicana, which caused a mortality of 98% and no adult emergence. Similarly, the root powder of S. perforates mixed with maize kernel (3%) displayed total mortality against S. zeamais [68], while an acetone extract produced from the roots of H. celastroides and its precipitate resulted in slight antifeeding activity index values of 72.3 and 73.8 against the stored grain pest S. zeamais, respectively (Table 15) [65].

2.10. Stomoxys calcitrans and Scyphophorus acupunctatus

The flavanone pinocembrine (69) obtained from the aerial parts of Teloxys graveolens showed an LC50 value of 418.69 μg/mL against the third-stage larvae of the stable fly S. calcitrans, an ectoparasite of mammals (Table 16, Figure 9) [69]

Table 16

Plant extracts and a metabolite from Mexican flora with activity on Stomoxys calcitrans and Scyphophorus acupunctatus.

Insect	Species/Family	Plant Part	Extract/Compound (Toxicity)	Ref.
Stomoxys calcitrans	Teloxys graveolens Chenopodiaceae	Aerial part	Pinocembrine (69) (LC50 = 418.69 μg/mL, 3rd stage larvae, 24 h)	[69]
Scyphophorus acupunctatus	Annona cherimola Annonaceae	Seeds	Podwer (15% in artificial diet: 63% LM; larval, pupal, and adult weight reductions of 98.5, 40.6, and 45.0%, respectively, 24 days)	[70]
	Carica papaya Caricaceae	seeds	fresh seed (15% in artificial diet: 90% LM, 24 days)dry seed powder (15% in artificial diet: 100% LM, 24 days)	[70]
	Trichilia havanensis Meliacea	seeds	Seed powder (15% in artificial diet: 100% LM, 24 days)	[70]

LC50: Median Lethal Concentration; LM: Larval mortality.

Figure 9

Metabolite effective on Stomoxys calcitrans.

Valdés-Estrada [70] reported that seed powders (15%) from Trichilia havanensis, C. papaya, and Annona cherimola had good effects (100, 90, and 63%, respectively) on the mortality of the larvae of S. acupunctatus. All powders inhibited the weight of the agave weevil. The most effective was A. cherimola. (Table 16).

2.11. Tenebrio molitor and Trichoplusia ni

Sterols 15 and 16 (Figure 1) from M. geometrizans (Cactaceae) and their combination (6:4) exhibited a high toxicity against the last-instar larvae of T. molitor, the yellow mealworm, causing acute toxicities with 5, 3, and 0% survival at 100 ppm, respectively. Interestingly, 15, 16, and their combination induced shortened T. molitor pupation and emergence, and many of the pupae died (Table 17) [24].

Table 17

Plant extracts and metabolites from Mexican flora with activity on Tenebrio molitor and Trichoplusia ni.

Insect	Species/Family	Plant Part	Extract/Compound (Toxicity)	Ref.
Tenebrio molitor	Myrtillocactus geometrizans * Cactaceae	Whole plant	Macdougallin (15) (100 ppm: 5% survival)Peniocerol (16) (100 ppm: 3% survival)mixture (6:4) 15 + 16 (100 ppm: 0% survival)	[24]
Trichoplusia ni	Azadirachta indica Meliacea	Leaves	Volatile compounds released (1 and 10 g: 24% and 63% neonate mortality; 77% and 79% larval mortality; LD50 = 5.6 g, 7 days)	[71]

* Endemic; LD50: Median Lethal Dose.

Only one report described assays against the cabbage looper T. ni, where volatile organic compounds from A. indica stems promoted significant neonatal and larval mortality (24 and 77%, respectively) at 1 g doses and an LD50 of 5.6 g after 7 days (Table 17) [71].

2.12. Trialeurodes vaporariorum

In reviewing investigations on the effectiveness of Mexican plant products against the greenhouse whitefly, the species Arundo donax, Petiveria alliacea, Phytolacca icosandra, Piper auritum, Raphanus raphanistrum, and Tagetes filifolia were compiled.

2.12.1. EOs

Native populations of T. filifola in Mexico contain high proportions of anethole, a phenylpropene present in the EOs from the plant. Therefore, the EOs from the flowers, leaves, and whole plants of T. filifolia were tested together with a commercial standard of trans-anethole (70) against T. vaporariorum. The lowest LC50 value was observed using 70 (Figure 10), which produced an LC50 value of 1.74 mg/mL and a median oviposition inhibition concentration (IOC50) of 1.55 mg/mL, followed by the floral oil (LC50 = 6.59 mg/mL), the foliar oil (LC50 = 10.29 mg/mL), and the whole plant oil (LC50 = 9.99 mg/mL). Another parameter measured was the median repellent concentration (RC50), with the floral oil being the most effective with an RC50 value of 0.13 mg/mL against T. vaporariorum. The second instar of the nymphal stage of T. vaporariorum was noticeably sensitive to foliar oil (Table 18) [72].

Figure 10

Metabolites active against Sitophilus zeamais.

Table 18

Plant extracts from Mexican flora with activity on Trialeurodes vaporariorum.

Species/Family	Plant Part	Extract (Toxicity)	Ref.
Tagetes filifolia Asteraceae	Flower Leaves Whole plant	Flower (RC50 = 0.13 mg/mL; LC50 = 6.59 mg/mL, 24 h; OIC50: 8.43 mg/mL, adults)Leaves (0.23 mg/mL; LC50 = 10.29 mg/mL, 24 h; OIC50: 3.88 mg/mL, adults)Whole plant (RC50 = 0.24 mg/mL; LC50 = 9.9 mg/mL, 24 h; OIC50: 3.56 mg/mL, adults)trans-anethole (70) commercial standard (RC50 = 0.45 mg/mL; LC50 = 1.74 mg/mL, 24 h; OIC50: 1.55 mg/mL, adults)	[72]
Piper auritum Piperaceae	Leaves stems	Ethanol (LC50 = 116 mg/mL on adult, 24 h)Acetone (IOC50 = 89.1 mg/mL on adult, 24 h)	[73]
Raphanus raphanistrum Brassicaceae	Leaves	Water (IOC50 = 77.3 mg/mL, on adult, 24 h)Ethanol (LC50 = 185.2 mg/mL, on adult, 24 h)	[73]
Petiveria alliacea Petiveriaceae	Aerial part	Laboratory assays:Aqueous (LC50 = 4.6%),methanol (LC50 = 1.1%),dichloromethane (LC50 = 0.3%),In greenhouse (tomato)aqueous (LC50 = 16.6%),methanol (LC50 = 13.3%),dichloromethane (LC50 = 3.5%)	[74]
Arundo donax Poaceae	Roots	Aqueous (non-active)Methanol (LC50 = 0.57% and 34.79% w/v, in vitro and greenhouse RC50 =, respectively)	[75]
Phytolacca icosandra Phytolaccaceae	Leaves stems	Aqueous (non-active)Methanol (LC50 = 0.34% and 36.47% w/v, in vitro and greenhouse, respectively)Qualitative analysis: Terpenoids and saponins	[75]

IOC50: Median Inhibition of Oviposition Concentration; LC50 = Median Lethal Concentration; RC50 = Median Repellent Concentration.

2.12.2. Plant Extracts

Mendoza-García [73] reported that an ethanolic extract of P. auritum was the most toxic extract (LC50 = 116 mg/mL) tested against T. vaporariorum and that an aqueous extract of R. raphanistrum effectively inhibited oviposition (IOC50 = 77.3 mg/mL) against the greenhouse whitefly.

Evaluations of extracts applied to tomato crops under greenhouse conditions were reported to control T. vaporariorum. In one study, aqueous, methanol, and dichloromethane extracts from P. alliacea leaves showed remarkable LC50 values of 16.6, 13.3, and 3.5%, respectively [74]. In contrast, methanolic extracts from A. donax and P. icosandra exhibited slightly higher target LC50 values of 34.79 and 36.47%, respectively, under greenhouse conditions (Table 18) [75].

2.13. Zabrotes subfasciatus

The species L. palmeri and Senecio salignus exhibited effective activities against Z. subfasciatus, the main pest of common beans (Phaseolus vulgaris). A 0.07% solution of a root powder of the Asteraceae species S. salignus exerted lethal toxicity by contact against bean weevil adults after five days. When the concentration was increased, fewer days were required to control the pest, with a 0.07% solution producing LC50 values of 0.03% and 0.08% after 3 days and median lethal times of 1.21 and 3.20 days observed for male and females, respectively. Therefore, males were more sensitive than females. In addition, the authors determined the optimal size of the root powder that should be used (<0.25 mm particles) [76].

EOs

EOs obtained from leaves of L. palmeri collected in the localities of Puerto de Oregano (PO) and Alamo (Al) exhibited lethal and ovicidal activities against Z. subfasciatus at 1.35 µL/g, with two months of persistence. EOs from leaves collected in PO was slightly more lethal than EOs obtained from leaves collected in Al. A comparison of the components of the two EOs revealed a number of differences, with carvacrol (22, 37.35%), thymol (21, 24.56%), and p-cimene (64, 15.62%) being abundant in EO from PO, whereas 64 (33.7%) and 22 (18.32%) were abundant in EOs from Al (Table 19) [77].

Table 19

Plant extracts from Mexican flora with insecticidal activity against Zabrotes subfasciatus.

Species/Family	Plant Part	Extract (Toxicity)	Ref.
Senecio salignus Asteraceae	Roots	Powder (male: LC50 = 0.03%, 3–6 days; LT50 = 1.31 days)(female: 0.08% 3–6 days; LT50 = 3.2 days)	[76]
Lippia palmeri * Verbenaceae	Leaves	EOs Puerto del oregano (LC50 = 1.35 μL/g mortality, 48), 22 (37.35%), 21 (24.56%), 64 (15.62%)Alamos (LC50 = 1.35 μL/g mortality, 48), 64 (33.70%), 22 (18.32%)	[77]

* Endemic; LC50: Median Lethal Concentration; LT50: Median Lethal Time.

3. Nematicidal Compounds and Plant Extracts

To date, very few bioprospecting studies have been performed to identify plants with nematicide effects. In this review, we identified reports describing 37 plant species with toxic activities towards plant and animal nematode parasites. These plant species belong to 21 botanical families, with those of the family Fabaceae (41%) being predominant. A total of 18 secondary metabolites were identified as active principles or presenting an active fraction against at least one of the parasitic nematodes tested in the reviewed studies, including terpenes (71–82), flavonoids (44, 69, 83, and 86), a pehnylpropaoid (84), and a coumarin (85). These metabolites were obtained from C. anuum, Gliricidia sepium, Leucaena leucocephala, Microsechium helleri, Sicyos bulbosus, and T. graveolens.

3.1. Plant Extracts Effective against Parasitic Plant Nematodes

Although data on the subject is scarce, we focused on compiling reports on plants that have toxic effects on phytonematodes Meloidogyne incognita, Meloidogyne javanica, and Nacobbus aberrans. A total of twelve metabolites from M. helleri, S. bulbosus, and C. annuum have been purified and identified as active principles against plant parasite nematodes.

3.1.1. Meloidogyne javanica

Seven saponins isolated from S. bulbosus, namely, tacacoside B3 (71) and C (72),16-OH tacacoside B3 (73), durantanin III (74), heteropappus saponin 7 rhamnoside (75), and heteropappus saponin 5 and 7 (76–77), were the active compounds responsible for the nematicidal effect against M. javanica J2 (73.8–100% mortality at 0.5 µg/µL). Highly similar compounds, such as amole F-G (78, 79) and 16-OH amole F-G (80, 81), were isolated from M. helleri and caused lower (<8%) J2 immobility at the 0.5 µg/µL dose [78]. In addition, the hexane extract from the leaves of L. graveolens caused significant mortality against M. javanica J2 with an LC50 of 0.672 mg/mL (Table 20, Figure 11). [27].

Table 20

Phytonematicidal metabolites and plant extracts from Mexican flora.

Nematode	Species/Family	Plant Part	Compound/Extract (Toxicity)	Ref.
Meloidogyne javanica	Lippia graveolens Verbenaceae	Leaves	Hexane (LC50 = 0.672 mg/mL)21 (70.6%), 22 (22.8%)	[27]
	Sicyos bulbosus * Cucurbitaceae	Roots	Tacacoside B3 (71) (0.5 µg/µL: 93% J2 I)tacacoside C (72) (0.5 µg/µL: 97% J2 I)16-OH-tacacoside B3 (73) (0.5 µg/µL: 100% J2 I), durantanin III (74) (0.5 µg/µL: 74% J2 I)heteropappussaponin 7 rhamnoside (75) (0.5 µg/µL: 80% J2 I), heteropappussaponin 5 (76) (0.5 µg/µL: 91% J2 I)heteropappussaponin 7 (77) (0.5 µg/µL: 93% J2 I)	[78]
	Microsechium helleri * Cucurbitaceae	Roots	Amole F (78) (0.5 µg/µL: 4.78% J2 I)amole G (79) (0.5 µg/µL: 7.83% J2 I)16-OH-amole F (80) (0.5 µg/µL: 6.52% J2 I)16-OH-amole G (81) 0.5 µg/µL: 6.34% J2 I)	[78]
Nacobbus aberrans	Capsicum annuum Solanaceae	Roots	Capsidiol (82) (1 μg/mL: >80% J2 I, 72 h)	[79]
Meloidogyne incognita	Calea urticifolia Asteraceae	Roots	Ethanol (250 ppm: 80% larval mortality, 72 h)In greenhouse:Water (50% w/v: 72% decrease eggs formation; 50% galling reduction)	[80]
	Eugenia winzerlingii * Myrtaceae	Leaves	Ethanol (ED50 = 133.4 ppm)	[81]
	Tephrosia cinerea Fabaceae	Stem	Ethanol (250 ppm: 85% larval mortality, 72 h)	[81]

* Endemic; ED50: Median Effective Dose; I: Immobility; LC50: Median Lethal Concentration.

Figure 11

Metabolites effective against Meloidogyne javanica and Nacobbus aberrans.

3.1.2. Nacobbus aberrans

The capsidiol (82) produced by C. annuum (Solanaceae) was reported to affect N. aberrans (Table 19). Pure capsidiol caused an 80% immobility in the J2 of N. aberrans after exposure for 72 h at a concentration of 1 μg/mL and caused a nematostatic effect (Table 20, Figure 11) [79].

3.1.3. Meloidogyne incognita

Plant extracts from Calea urticifolia, E. winzerlingii, and Tephrosia cinerea were shown to have lethal activities against M. incognita (Table 20). An aqueous extract from the roots of C. urticifolia was tested on second-stage M. incognita juveniles under greenhouse conditions. The results showed that 50% (w/v) of the C. urticifolia root extract effectively reduced gall formation (50%) and the number of eggs (72% reduction) on tomato seedlings that had been inoculated with 1000 eggs and 130 M. incognita J2 [80]. Ethanol extracts from the roots of C. urticifolia, the stems of T. cinerea, and the leaves of E. winzerlingii produced immobility in M. incognita J2 (>80%) when applied at 250 ppm. Finally, the ethanol extract from E. winzerlingii leaves was very active against M. incognita and had the lowest LC50 (133.4 ppm) of the tested extracts [81].

3.2. Plant Extracts with Activity against Parasitic Animal Nematodes

To date, 27 plant species have been identified with an effect against animal nematodes, 12 of which belong to the family Fabaceae (43%). The relevant studies primarily focused on the control of Haemonchus contortus (93%): one study investigated Haemonchus placei, and three investigated Trichostrongylus colubriformis, zooparasites of sheep. In addition, three studies focused on Cooperia puntacta and Cyatostomin sp., zooparasites of grazing cattle and horses, respectively, and one focused on Ascaridia galli, a bird parasite. Herein, the active plant extracts are included, as well as some fractions or subfractions, with the predominant compounds described by the authors. Only five natural compounds were reported to have an anthelmintic activity against animal nematodes, two of which were purified and identified from plant species and the remaining two as enriched fractions, with compound rutin (35) assayed as a commercial standard.

3.2.1. Ascaridia galli

Only one study investigated the effect of metabolites from T. graveolens (Amaranthaceae) against A. galli. Flavonoid 69 (Figure 9) was the active ingredient isolated from the aerial parts of T. graveolens, and it had an LC50 of 623.5 μg/mL against A. galli (Table 21) [69].

Table 21

Nematicidal metabolites and plant extracts from Mexican plants with activity on Ascaridia galli, Cooperia puntacta, and Cyathostomin sp.

Nematode	Species/Family	Plant Part	Compound/Extract (Toxicity)	Ref.
Ascaridia galli	Teloxys graveolens Chenopodiaceae	Aerial part	Pinocembrine (69) (LC50 = 623.49 μg/mL)	[69]
Cooperia punctata	Leucaena leucocephala Fabaceae	Fresh Leaves	Water (LC50 = 7.93 mg/mL EHI)Fraction LlC1F3 (LC50 = 0.06 mg/mL EHI)Quercetin (83, 82.21%), caffeic acid (84, 13.42%)	[82,83]
	Gliricidia sepium Fabaceae	Fresh Leaves	Acetone (LC50 = 1.03 mg/mL EHI)2H-Chromen-2-one (85) (EC50 = 0.024 mg/mL EHI)	[84]
			Oxytroside (86) (2400 µg/mL inhibited exsheathment)	[85]
Cyathostomin sp.	Diospyros anisandra Ebenaceae	Leaves Bark	Methanol bark (LC50 = 10.28 µg/mL EHI in rainy season)Methanol leaves (LC50 = 18.48 µg/mL EHI in rainy season)	[86]
	Petiveria alliacea Petraceae	Stem	Methanol (LC50 = 28.27 µg/mL EHI in rainy season)	[86]

EC50: Median Effective Concentration; LC50: Median Lethal Concentration. EHI: Egg Hatching inhibition.

3.2.2. Cooperia puntacta

Plant species with ovicidal activity against C. puntacta included G. sepium and L. leucocephala. These plants were extracted with water, acetone–water 30:70, and acetone solvents, and all of these fractions were tested. For each plant, at least one of the extracts showed ovicidal activity. The most effective were the acetone extract from G. sepium and the aqueous extract from L. leucocephala, which showed significant LC50 values of 1.03 and 7.93 mg/mL on egg hatching inhibition (EHI), respectively. The addition of a tannin inhibitor (polyethylene glycol) in all of the extracts showed that, with the exception of the G. sepium acetone extract, all exhibited enhanced ovicidal effects. Next, an aqueous extract of L. leucocephala was fractionated using chromatographic methods. Among the fractions obtained, the highest ovicidal effect was observed in LlC1F3, with an LC50 value of 0.06 mg/mL detected on Cooperia spp. The analytical data indicated that the majority of components in LlC1F3 were quercetin (83, 82.21%) and caffeic acid (84, 13.42%) [82,83].

In contrast, the metabolite 2H-chromen-2-one (85) was purified from the acetone extract of G. sepium by bio-guided fractionation. Metabolite 85 had the highest ovicidal effect (EC50 of 0.024 mg/mL), EHI, and embryonic development against C. puntacta [84]. A second metabolite isolated from the leaves of G. sepium was identified as oxytroside (86) which inhibited the C. punctata exsheathment process at 2400 µg/mL (Table 21, Figure 12) [85].

Figure 12

Metabolites from Gliricida sepium and Leucaena leucocephala with activity on Cooperia sp.

3.2.3. Cyatostomin sp.

An investigation on the control of the zooparasitic nematode Cyatostomin sp. using plant extracts was recently reported [86]. The authors indicated that methanol extracts from the leaves and bark of Diospyros anisandra (Ebenaceae) and the leaves and stems of P. alliacea, which were collected in the rainy seasons, showed promising activities in controlling the eggs and the development of L1 Cyastotomin sp. larvae. The highest ovicidal activity was produced by the bark extract of D. anisandra, followed by the leaf extract, both of which were collected in the rainy season. These extracts presented LC50 values of 10.28 and 18.48 µg/mL on the EHI, respectively, while extracts from P. alliacea exhibited lower lethal activities (LC50 ≥ of 28.27 µg/mL). However, P. alliacea stems, which were also collected in the rainy season, induced the failed eclosion of larvae (90.7% at 75 µg/mL). The continued study of both plant species was highly recommended (Table 21) [86].

3.2.4. Haemonchus sp.

Haemonchus placei

A hydroalcoholic extract with significant activity against H. placei, was obtained from Caesalpinia coriaria. In this case, the extracts from fruits presented a greater activity than the leaves, with LC50 values of 3.91 and 11.68 mg/mL, respectively [87].

Haemonchus contortus

In ruminants, H. contortus is one of the most important gastrointestinal parasitic nematodes in sheep and goats, as well as H. placei, a hematophagous parasite in bovines. Several plant extracts exhibited promising activities in controlling the larval stage of H. contortus in vitro (Table 22. Among these extracts, the dichloromethane extract from Phytolaccca icosandra leaves (Phytolaccaceae) was one of the most active, with an LD50 of 0.90 mg/mL on larval migration inhibition and an LD50 of 0.28 mg/mL on egg hatch inhibition (EHI) in H. contortus. Additionally, ethanolic extracts from the same plant caused >92% of EHI at a 0.9 mg/mL in vitro level [88]. In addition, the methanolic extract from Gliricidia sepium (Fabaceae) displayed a good EHI effect, with an ED50 value of 394.96 µg/mL [89]. The hydroalcoholic extract from the leaves of Acacia cochliacantha (Fabaceae) showed total mortality against eggs of H. contortus. However, this extract was used at a high concentration (100 mg/mL), and its organic fraction obtained with ethyl acetate displayed one of the lowest EHI at an LC50 of 0.33 mg/mL. This EHI effect increased ten-fold when it was subfractionated with dichloromethane to produce soluble and precipitate subfractions, with the low LC50 values of 0.06 and 0.04 mg/mL observed, respectively. The ethyl acetate fraction was enriched with caffeoyl and coumaroyl derivatives [90]. The hydroalcoholic extract from C. coriaria showed a slightly higher effect against H. contortus larvae than on H. placei. In this case, the extracts from fruits presented LC50 values of 1.63 and 3.98 mg/mL, respectively [87]. In addition, the ethanol extract from the seeds of C. papaya (Caricaceae) induced an EHI of 92% at 2.5 mg/mL [91].

Table 22

Plant extracts and metabolites from Mexican flora with in vitro activity against Haemonchus contortus.

Species/Family	Plant Part	Extract (Toxicity)	Ref.
Caesalpinia coriaria Fabaceae	Fruits Leaves	Hydroalcoholic (fruits: LC50 = 1.63 mg/mL; leaves: LC50 = 3.98 mg/mL on EHI, 48 h)	[87]
Phytolacca icosandra Phytolaccaceae	Leaves	Dichloromethane (LD50 = 0.90 mg/mL LMI; LD50 = 0.28 mg/mL EHI)Ethanol (2 mg/mL: 55.4% LMI; 1.8 mg/mL: 95% EHI)	[88]
Gliricidia sepium Fabaceae	Leaves	Methanol (ED50 = 394.96 µg/mL EHI)	[89]
Acacia cochliacantha Fabaceae	Fresh Leaves	Hydroalcoholic (100 mg/mL: 100% EHI)Ethyl acetate (LC50 = 0.33 mg/mL EHI)Dichloromethane soluble fraction (LC50 = 0.06 mg/mL EHI)Dichloromethane precipitate (LC50 = 0.04 mg/mL EHI)	[90]
Carica papayaCaricaceae	Seeds	Ethanol (2.5 mg/mL: 92% EHI)Hydroalcoholic (2.5 mg/mL: 50% EHI)	[91]
Acacia pennatula Fabaceae	Leaves	Tannins (1200 µg/mL: 51% LMI)	[92]
Arachis pintoiFabaceae	Leaves	Condensed tannins (4.5–45 µg/mL: 76.6–100% LM, 96 h)	[92]
Guazuma ulmifolia Malvaceae	Leaves	Condensed tannins (4.5–45 µg/mL: 86.0–99.4% LM, 96 h)	[92]
Manihot esculenta Euphorbiaceae	Leaves	Condensed tannins (4.5–45 µg/mL: 69.9–100%, LM, 96 h)	[92]
Leucaena leucocephala Fabaceae	Leaves	Condensed tannins (4.5–45 µg/mL: 71.0–98.4% LM, 96 h)	[92]
	Leaves	Tannin (1200 µg/mL: 53.6% LMI)	[93]
Lysiloma latisiliquum Fabaceae	Leaves Leaves	Tannin (1200 µg/mL: 49.1% LMI)	[93]
Piscidia piscipula Fabaceae	Leaves	Tannin (1200 µg/mL: 63.8% LMI)	[93]
Laguncularia racemosa Combretaceae	Leaves	30% Acetone–water (3600 µg/mL: 50.29 larvae failing eclosion)	[94]
Senegalia gaumeri * Fabaceae	Leaves	Acetona–water 70:30 (EC50= 401.8 EHI; 83.1 LMI)	[95]
Bursera copallifera * Burseraceae	Stem	Acetone (20 mg/mL: 66% LM, 72 h)	[96]
Prosopis laevigata Fabaceae	Aerial part	Hexane (20 mg/mL: 86% LM, 72 h postexposure)	[96]
Cydista aequinoctialis Bignonaceae	Leaves	Aqueous (20 mg/mL: 39.57% LM, 72 h)	[97]
Heliotropium indicum * Boraginaceae	Leaves	Aqueous (20 mg/mL: 34.59% LM, 48 h)	[97]
Momordica charantia Cucurbitaceae	Leaves Fruits	Aqueous (20 mg/mL: 53.83% LM, 72 h)Aqueous (20 mg/mL: 68.13% LM, 72 h)	[97]
Larrea tridentata Zygophyllaceae	Leaves	Hydro-methanol 30% (EC50 = 36 mg/mL on exsheathed larvae, 24 h)	[98]
Allium sativum Amaryllidaceae	Bulbs	Hexane (LC50 = 3.8 mg/mL LM, 72 h)	[99]
Tagetes erectaAsteraceae	Flowers	Acetone (40 mg/mL: 36.6% LM, 72 h)	[99]
A. sativum-T. erecta	Combined	Combined bulbs and flower (LC50 = 1.3 mg/mL LM, 72 h)	[99]
Castela tortuosa * Simaroubaceae	Aerial part	Hexane (LC50 = 17.3 mg/mL EGI, 72 h)	[100]
Chenopodium ambrosioides Chenopodiaceae	Aerial part	Hexane (LC50 = 1.5 mg/mL EGI, 72 h)	[100]
C. ambrosioides-C. tortuosa	Combined	Hexane (LC50 = 6.5 mg/mL EGI, 72 h)	[100]

* Endemic; EHI: Egg hatch inhibition; LM: Larval mortality; LMI: larval migration inhibition; LC50: Median Lethal Concentration; LD50: Median Lethal Dose.

The extracts of partially purified tannins obtained from the leaves of Arachis pintoi, L. leucocephala, Guazuma ulmifolia, and Manihot esculenta reduced the migration of the third-stage larvae of H. contortus by 69.9–87.4% at 4.5 µg/mL and 74.2–100% at 45 µg/mL after 96 h of exposure. However, an ovicidal effect from these plants was not observed [92]. Alonso-Diaz [93] confirmed the role of tannins in the larvicidal effect of L. leucocephala and other tropical Fabaceae, Acacia pennatula and Lysiloma latisiliquum, with larval migration inhibitions (LMI) of 51–53.6% at 1200 µg/mL through the use of polyvinyl polypyrrolidine, an inhibitor of tannins. In contrast, Piscidia piscipula was not affected. Vargas-Magaña [94] demonstrated that tannins in a 30% acetone–water extract (3600 µg/mL PBS) from the leaves of Laguncularia racemose blocked the eclosion of eggs of H. contortus (50.29%). Besides, Senegalia gaumeri induced an EC50 of 401.8 and 83.1 µg/mL of EHI and larval mortality on H. contortus, respectively [95].

In in vitro studies, other investigations reported a lesser effect (20–40 mg/mL) on H. contortus larval mortality, including the hexane extract from the aerial parts of Prosopis laevigata, an acetone extract from the stem of B. copallifera [96], a hydro-methanolic extract from Larrea tridentata and aqueous extracts from Cydista aequinoctialis, Heliotropium indicum, and Momordica charantia (Table 22) [97,98].

There are seven reports on in vivo experiments that describe the effects of plant extracts. One of these studies included a mixture of extracts from the bulbs of A. sativum and the flowers of T. erecta. First, the extracts alone or in combination were tested in vitro. After 72 h, the lowest larval mortality of H. contortus (L3) occurred at an LC50 of 1.3 mg/mL, which was induced by the mixed extract (Table 22). Subsequently, it was administered in one dose of 100 µg/mL (40 mg/mL) to gerbils infected with H. contortus (L3). After 13 days, the nematode in the gastric lumen of both treatment and control animals were counted. The highest larvae population reduction (LPR) was 87.5%, which was induced by the T. erecta and A. sativum mixed extracts. Each extract of these plants alone showed a lower effect in comparison with their combination in both assays, suggesting a synergistic action [99]. Similarly, Zamilpa [100] reported that a combined extract from the aerial parts of Castela tortuosa and C. ambrosioides induced a 57.36% population reduction on L3 H. contortus in infected gerbils (Table 23). In contrast, in vitro, the lowest lethal activity was produced by a hexane extract of C. ambrosioides (LC50 = 1.5 mg/mL) at 72 h (Table 22). Other hexane extracts administered (100 µg/mL at 40 mg/mL) to gerbils was from Prosopis laevigata, which reduced parasite population (42.5%) [101].

Table 23

The in vivo evaluations of plant extracts against Haemonchus contortus.

Plant Species	Host	Sample (Toxicity)	Ref.
Allium sativum Amaryllidaceae	Gerbils	Oral administration extract (40 mg/mL) (100 µL: 68.7% LPR)	[99]
Tagetes erecta Asteraceae	Gerbils	Oral administration extract (40 mg/mL) (100 µL: 53.9% LPR)	[99]
Allium sativum-Tagetes erecta 1:1 combined	Gerbils	Oral administration combined extract (40 mg/mL) (100 µL: 87.5% LPR)	[97]
Castela tortuosa *	Gerbils	Hexane extract intraperitoneally administred (40 mg/kg BW: 27.15% LPR)	[100]
Chenopodium ambrosioides	Gerbils	Hexane extract (100 µL) intraperitoneally administred (40 mg/kg: 45.86% LPR)	[100]
Castela tortuosa Chenopodium ambrosioidescombined	Gerbils	Hexane extract (100 µL) intraperitoneally administred (40 mg/kg BW: 57.36% LPR)	[100]
Prosopis laevigata	Gerbils	Hexane extract (40 mg/mL) intraperitoneally administred (100 µL: 42.5% reduced the parasite population)	[101]
Lysiloma acapulcensis *	Lambs	Ethyl acetate fraction (25 mg/kg BW: 94.8% EHI; 62.9% EPGR)Dried leaves (5g/kg BW: 50.1% EPGR)	[102]
	Sheep	Rutin (36) (10 mg/kg BW: 66.2% EPGR)	[102]
Phytolacca icosandra	Sheep	Ethanol (250 mg/kg, 2 days: 72% reduction on eggs/g of faeces)	[103]
Oxalis tetraphylla Oxalidaceae	Lambs	(20 mg/kg: 45.6% reduction in the eggs/g of feces)	[104]
Acacia cochliacantha	Goats	Fresh foliage (1.48 log10 excreted eggs per gram; control 2.18 log10; 0.6 kg/ animal weight gained)	[105]
Pithecellobium dulce	Goats	Fresh foliage (1.18 log10 excreted eggs per gram; control 2.18 log10; 2.4 kg/ animal weight gained)	[105]

* Endemic; BW: Body weight; EHI: Egg hatch inhibition; EPGR: Egg per gram reduction; LPR: Larval population reduction.

An organic ethyl acetate fraction obtained from aqueous extracts of Lysiloma acapulcensis leaves showed a high EHI on L3 (94.85%) at 6.25 g/mL and a 100% larval mortality at 50 mg/mL after 72 h at the in vitro level. Subsequently, an organic fraction of dry and ground leaves of L. acapulcensis and the flavonol rutin (35) used to treat infected sheep were tested in vivo. The reduction in the excretion of eggs per gram (EPGR) of faeces was recorded, with 35 and the ethyl acetate fraction exhibiting a 66.2 and 62.9% EPGR at a concentration of 10 and 25 mg/kg body weight (BW), respectively. The application of the ethyl acetate fraction was more effective than dried leaves (5 g/kg BW), presenting a 62.9% EPGR. The chromatographic separation of the ethyl acetate fraction revealed the presence of the flavonol myricitrin (87) as a major component, though this enriched fraction was not tested (Figure 13). In this experiment, the larvae of Cooperia curticei, H. contortus, and Teladorsagia circumcincta and the eggs of Trichuris sp. from faeces were identified by morphological and morphometric analyses [102]. Another in vivo test was reported with the ethanolic extract from P. icosandra leaves which was encapsuled and orally administered to infected goats. Results showed a reduction of 72% in H. contortus eggs/g of faeces at two doses of 250 mg/kg BW, on day 11 post-treatment (Table 23). Fatty acids and a ketone were detected in the ethanol extract of P. icosandra as major components [103].

Figure 13

Majority component (Myricitrin) of active extract from Lysiloma acapulcensis eaves.

In further studies, a hydroalcoholic extract from Oxalis tetraphylla (Oxalidaceae) leaves was orally applied daily (20 mg/kg BW) for eight days to lambs infected with H. contortus. The results showed a 45.6% reduction in the number of eggs/gram of faeces. Flavonol compounds in O. tetraphylla were also detected [104].

Finally, an in vivo test in goats, Creole male kids, experimentally infected with L3 H. contortus was reported. In this investigation, kids were fed fresh leaves (10% of the total diet) of A. cochliacantha, G. ulmifolia, and Pithecellobium dulce (Fabaceae) for sixty days. A lower EPG was observed in kids fed with A. cochliacantha and P. dulce, with 1.28 Log10 and 1.48 Log10, respectively. Moreover, the total body weight in kids noticeably increased with P. dulce foliage in the diet, with 0.2% (control) to 2.4% kg/animal (treatment) weight gained, which was attributed to the decrease in parasite load [105] (Table 23).

3.2.5. Trichostongyus colubriformis

With regards to the nematode T. colubriformis, the extracts from three species of the family Fabaceae (1200 ppm), Acacia pennatula, L. leucocephala, and Lysiloma latisiliquum, reduced the migration of T. colubriformis third-stage larvae by 71%, 72%, and 56%, respectively (Table 24) [106].

Table 24

Extracts from Mexican plants active on Trichostrongylus colubriformis.

Species/Family	Plant Part	Extract (Toxicity)	Ref.
Acacia pennatula Fabaceae	Leaves	Tannin (1200 µg/mL: 71% Lm)	[106]
Leucaena leucocephala Fabaceae	Leaves	Tannin (1200 µg/mL: 72% Lm)	[106]
Lysiloma latisiliquum Fabaceae	Leaves	Tannin (1200 µg/mL: 56% Lm)	[106]

Lm: larval migration of third-stage larvae.

4. Conclusions

This review demonstrates the relevant pesticidal activity of several native plant species of Mexico, the majority of which were reported at the in vitro level, while some were reported in in vivo assays. Unfortunately, at present, research on bioprospecting plant species from Mexican flora with the aim of developing natural pesticides against insects and nematode pests is still in its early stages. To date, only 114 species of Mexican plants with biological activity against insects or nematode pests have been reported, most of which belong to the Asteraceae (20%), Fabaceae (15%), and Lamiaceae (11%) families (Figure 14). The investigations on the activities of these plants have primarily focused on evaluating the biological activity of raw vegetable extracts or their enriched fractions, and less than 35% have led to the purification, identification, and evaluation of the active compounds. Among the most common metabolites with activity detected against some of the tested targets are terpenes (58%), followed by phenols and flavonoids. A mixture of extracts or their pure compounds provides a strategy in the search for natural and safer pesticides. Despite these limitations, species with a high potential for effectiveness were identified for further study in the development of biotechnological products.

Figure 14

The percentage of (a) plant families explored and (b) types of metabolites isolated from native plants of México that are active on some parasitic pest.

Evaluations of promising plant extracts in the field are needed to identify appropriate formulations. Therefore, the use of an adequate and low-cost extract should be considered during in vitro evaluations. Although botanical pesticides are less persistent in the environment, toxicological studies on beneficial organisms and mammals should still be performed.

The high diversity of plant species in Mexico coupled with the increasing demand and urgency for new natural pesticides makes it extremely important to continue bioprospecting studies in this country. Additional studies will help generate new and alternative natural products that can improve the biological effectiveness, lower residuals, and increase the innocuousness of agricultural products as well as decrease their presence in foods. These studies will contribute to the recognition and dissemination of the importance of propagating plant species for their conservation and sustainable use.