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    Topic review

    Effects of Quercetin on Herbivores

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    Submitted by: Eric W. Riddick

    Definition

    Quercetin is one of the most abundant flavonoids in terrestrial plants and pollen. In living plants, quercetin can function as a secondary metabolite to discourage insect herbivory. Literature on insect-quercetin interactions was searched and data synthesized to test the hypothesis that quercetin can become an effective biocide to reduce herbivory. The USDA, National Agricultural Library, DigiTop Navigator platform was used to search the literature for harmful versus nonharmful effects of quercetin on insect behavior, physiology, and life history parameters. Quercetin effects were evaluated on herbivores in five insect orders. Quercetin was significantly more harmful to Hemiptera, Diptera, and Lepidoptera but significantly more nonharmful to Coleoptera. Harmful and nonharmful effects to Orthoptera were indistinguishable. Quercetin had significantly more harmful (than nonharmful) effects on herbivores when data from the five insect orders were combined. Quercetin concentration (mg/mL) did not significantly affect these results. This study suggests that quercetin could prevent herbivory but field experiments are necessary to substantiate these results.

    1. Hemiptera (True Bugs)

    Four herbivorous hemipterans (three aphid species and one mirid species) were subjects in bioassays with quercetin based on the review of the literature (Table 1). Quercetin had harmful (negative) effects on survival rate of the aphid species Macrosiphum rosae (L.) and Acyrthosiphon pisum Harris, both nymphs and adults. Quercetin also had harmful (negative) effects on development, preoviposition time, and fecundity of Apisum and fecundity of the aphid Sitobion miscanthi (Takahashi) via innate resistance in wheat ears in a field bioassay. In contrast, quercetin had nonharmful (positive) effects on the mirid Tupiocoris notatus (Distant); nymphs were attracted to quercetin treated leaves in the laboratory.
    Table 1. Exemplary research that tested the effects of quercetin on behavior and life history parameters of agriculturally important insect herbivores.
    In a summary of this section, quercetin caused 0.857 and 0.143 proportional harmful and nonharmful effects on hemipteran species; the two effects were significantly different (z = 2.672, p = 0.008; n = 7). A concentration of 1 mg/mL or less was sufficient to cause harmful effects on MrosaeApisum, and Smiscanthi, whereas an extremely low quercetin concentration (0.9 × 10−4 mg) caused nonharmful (positive) effects on Tnotatus (Table 1). Quercetin concentrations were variable amongst these studies. Concentration data were not subjected to statistical analysis for this order, only for combined data for all five orders.
    Table 1. Exemplary research that tested the effects of quercetin on behavior and life history parameters of agriculturally important insect herbivores.
    Category Bioassay Method 1 Effects on Behavior and Life History 2 Effective Concn. Reference
    Herbivore:
    Hemiptera; true bugs
           
    Macrosiphum rosae, nymphs and adults
    (Aphididae)
    Treated red rose (Rosa) foliage Survival (−−) 1 mg/mL [1]
    Acyrthosiphon pisum, nymphs and adults
    (Aphididae)
    In artificial diet Development (−−),
    Pre-oviposition time (−−),
    Fecundity (−−),
    Survival (−−)
    1–10 mg/mL,
    0.1–10 mg/mL,
    1–10 mg/mL,
    0.01–10 mg/mL
    [2]
    Sitobion miscanthi, adults
    (Aphididae)
    Innate resistance in wheat ears in field Fecundity (−−) 0.199 mg/mL [3]
    Tupiocoris notatus, nymphs
    (Miridae)
    Treated tobacco (Nicotiana) leaves Attractancy (++) 0.09 μg [4]
    Herbivore:
    Coleoptera; beetles
           
    Callosobruchus chinensis, eggs and adults
    (Bruchidae)
    On filter paper and in plastic jar Survival (−−),
    Oviposition (−−)
    5.0 mg/mL,
    5.0 mg/mL
    [5]
    C. chinensis, adults On glass beads Oviposition (oo) 0.001–1.0 mg/mL [6]
    Tribolium castaneum, adults
    (Tenebrionidae)
    On wheat wafer discs Feeding (−−) 2.0 mg/mL [7]
    Melolontha melolontha, larvae
    (Scarabaeidae)
    In potted soil, in field Survival (oo) 20.0 mg/mL [8]
    Popillia japonica, adults
    (Scarabaeidae)
    In artificial diet Feeding (++) 30.2 mg/mL [9]
    P. japonica, adults In artificial diet Feeding (++) 0.302–3.02 mg/mL [10]
    Carpophilus hemipterus, larvae and adults
    (Nitidulidae)
    In artificial diet Feeding (++) 0.025 mg/mL [11]
    Leptinotarsa decemlineata, larvae
    (Chrysomelidae)
    In artificial diet plus insecticide Survival (−−) 0.1 mg/mL [12]
    Phaedon brassicae, adults
    (Chrysomelidae)
    Treated filter paper Feeding (−−) 3.02 mg/mL [13]
    Oulema oryzae, adults
    (Chrysomelidae)
    Treated filter paper Feeding (−−) 3.02 mg/mL [13]
    Plagiodera versicolora, adults
    (Chrysomelidae)
    Treated filter paper Feeding (++) 3.02 mg/mL [13]
    Altica oleracea, adults
    (Chrysomelidae)
    Treated filter paper Feeding (+ +) 3.02 mg/mL [13]
    Altica nipponica, adults Treated filter paper Feeding (++) 3.02 mg/mL [13]
    Anthonomus grandis, larvae and adults
    (Curculionidae)
    In artificial diet Feeding (oo),
    Oviposition (oo),
    Body weight (++)
    1–10 mg/mL,
    1–10 mg/mL,
    6 mg/mL
    [14]
    A. grandis, adults Treated filter paper Feeding (++) 0.5 mg/mL [15]
    Epilachna paenulata, larvae
    (Coccinellidae)
    Treated squash (Curcubita) leaves Feeding (++), Survival (−−) 0.01 μg/cm2,
    10–100 μg/cm2
    [16]
    Epaenulata, larvae Treated squash (Cucurbita) leaves Feeding (oo),
    Body Weight (oo), Survival (oo)
    0.1–50.0 μg/cm2, 0.1–50.0 μg/cm2, 0.1–50.0 μg/cm2 [16]
    Herbivore:
    Lepidoptera; moths/butterflies
           
    Helicoverpa armigera, larvae
    (Noctuidae)
    In artificial diet; leaf-dip toxicity test Development (−−),
    Pesticide sensitivity (oo)
    0.1% (w/w),
    0.1% (w/w)
    [17]
    Spodoptera litura, larvae
    (Noctuidae)
    Toxicity test Development (−−),
    Survival (−−)
    0.005 mg/mL,
    0.005 mg/mL
    [18]
    Helicoverpa armigera, larvae
    (Noctuidae)
    In artificial diet Development (−−),
    Survival (−−),
    Pesticide sensitivity (oo)
    16 mg/g,
    16 mg/g,
    16 mg/g
    [19]
    Helicoverpa armigera, larvae
    (Noctuidae)
    Ingested with liquid solution Development (−−),
    Survival (−−)
    3 mg/g,
    3 mg/g
    [20]
    Spodoptera frugiperda, larvae
    (Noctuidae)
    Treated foliage (Lettuce) Feeding (++),
    Feeding (−−)
    0.01 μg/cm2,
    100 μg/cm2
    [21]
    Chilesia rudis, larvae
    (Arctiidae)
    Treated foliage (cultivated Murtilla) Feeding (++) 0.005 mg/mL [22]
    Lymantria dispar, larvae
    (Lymantriidae)(from Quercus forest)
    In artificial diet Survival (−−),
    Body weight (−−)
    2% (w/w),
    2% (w/w)
    [23]
    Bombyx mori, larvae
    (Bombycidae)
    In artificial diet Body weight/Weight gain (−−) 0.1% (w/w) [24]
    Ostrinia nubilalis, larvae
    (Pyralidae)
    In artificial diet Development (−−)
    Survival (−−)
    1 mg/g [25]
    Heliothis virescens, larvae
    (Noctuidae)
    In artificial diet Development (−−) 0.25% (w/w) [26]
    Heliothis virescens, larvae
    Helicoverpa zea, larvae
    (Noctuidae)
    In artificial diet Body Weight (−−)
    Feeding (oo)
    0.10% (w/w) [27]
    Pectinophora gossypiella, larvae
    Heliothis virescens, larvae
    Helicoverpa zea, larvae
    (Noctuidae)
    In artificial diet Body Weight (−−)
    Development (−−)
    0.10% (w/w), Pgossypiella; 0.10% (w/w), Hvirescens;
    0.20% (w/w), Hzea
    [28]
    Heliothis virescens, larvae
    Helicoverpa zea, larvae
    (Noctuidae)
    In artificial diet Development (−−)
    Survival (−−)
    0.20% (w/w), Hvirescens; 0.80% (w/w), Hzea [29]
    Herbivore:
    Diptera; true flies
           
    Bactrocera cucurbitae, adults
    (Tephritidae)
    On substrate (pumpkin) Oviposition (−−) 0.125 mg/mL [30]
    Bcucurbitae, eggs, larvae, and pupae Dipped in test solution Development (−−),
    Development (−−),
    Development (−−)
    3.125 mg/mL,
    0.125 mg/mL,
    0.005 mg/mL
    [31]
    Rhagoletis pomonella, larvae
    (Tephritidae)
    In artificial diet Development (−−) 1.0 mg/mL [32]
    Drosophila melanogaster, larvae
    (Drosophilidae)
    In artificial diet Development (++) 1.75% (w/w) [33]
    Dmelanogaster, adults In artificial diet Fecundity (++) 5% (w/w) [34]
    Lycoriella pleuroti, larvae
    (Sciaridae)
    In artificial culture media Survival (−−) 0.1–0.3% (w/w) [35]
    Herbivore:
    Orthoptera; grasshoppers
           
    Calliptamus abbreviatus, nymphs
    (Acrididae)
    Sprayed on alfalfa foliage, field cages Development (−−)
    Survival (−−)
    0.10 mg/mL [36]
    Oedaleus asiaticus, nymphs
    (Acrididae)
    Sprayed on natural host plant foliage, field cages Development (−−)
    Survival (−−)
    0.10–10 mg/mL [37]
    Melanoplus sanguinipes, nymphs
    (Acrididae)
    In artificial diet Body weight (oo)
    Survival (oo)
    0.125–4.0% (w/w) [38]
    1 Quercetin had harmful effects (negative (−−)) or non-harmful effects (positive (++) or neutral (oo)) on insects in comparison to control. 2 Effective concentration (concn) was the minimum concentration that caused a significant effect on insect behavior, physiology, or a life history parameter.

    2. Coleoptera (Beetles)

    Fourteen herbivorous coleopteran species were exposed to quercetin in bioassays (Table 1). The species included one bruchid Callosobruchus chinensis L., one tenebrionid Tribolium castaneum Herbst, two scarabaeids Melolontha melolontha (L.) and Popillia japonica Newman, one nitidulid Carpophilus hemipterus (L.), six chrysomelids Leptinotarsa decemlineata Say, Phaedon brassicae Baly, Oulema oryzae Kuwayama, Plagiodera versicolora Laicharting, Altica oleracea (L.), Altica nipponica (Ohno), one curculionid Anthonomus grandis Boheman, and one herbivorous coccinellid Epilachna paenulata (Germar). Quercetin had harmful (negative) effects and nonharmful (neutral and positive) effects on these species. For example, quercetin decreased the survival of Cchinensis eggs, Ldecemlineata larvae, and Epaenulata larvae, and reduced feeding by Tcastaneum adults, Pbrassicae adults, and Ooryzae adults. In contrast, quercetin did not affect the survival of Mmelolontha and Epaenulata larvae or feeding behavior by Agrandis and Epaenulata larvae. In other coleopteran species, quercetin increased feeding behavior (Table 1).
    In summary, quercetin caused 0.304 and 0.696 proportional harmful and nonharmful effects, respectively, on herbivorous coleopterans (z = 2.652, p = 0.008, n = 23); nonharmful effects were predominant. There was variability in quercetin concentration and positive feeding responses between and within coleopteran species. For example, a concentration of 0.30 mg/mL stimulated feeding by Pjaponica adults in one study; but a higher concentration of 30.22 mg/mL stimulated feeding of the same species in another study (Table 1). Quercetin had harmful effects on oviposition by Cchinensis in one study but not in another; quercetin concentration was at least five times greater in the bioassay indicating reduced oviposition than in the one indicating neutral effects. At 1–10 mg/mL, quercetin had nonharmful (neutral) effects on oviposition and feeding behavior by Agrandis in one study, but nonharmful (positive) effects on feeding behavior at a lower concentration, 0.5 mg/mL, in another study.

    3. Lepidoptera (Moths/Butterflies)

    Ten lepidopteran species, representing five families, were challenged with quercetin in bioassays (Table 1). The noctuids included Helicoverpa armigera (Hübner), Helicoverpa zea (Boddie), Heliothis virescens (F.), Spodoptera litura (F.), Spodoptera frugiperda (J. E. Smith), and Pectinophora gossypiella (Saunders). One arctiid Chilesia rudis (Butler), one lymantriid Lymantria dispar (L.), one bombycid Bombyx mori (L.), and one pyralid Ostrinia nubilalis (Hübner) were also challenged with quercetin.
    Quercetin had harmful effects on development or body weight, i.e., growth, of noctuid larvae in most studies (Table 1). Effects on feeding behavior were variable, with nonharmful (positive) effects on Sfrugiperda at low concentration (0.01 μg/cm2) on treated foliage as well as nonharmful (neutral) effects on Hvirescens and Hzea at low concentration (0.10%, w/w) in an artificial diet. Quercetin also had nonharmful (positive) effects on feeding behavior of the arctiid Crudis at 0.005 mg/mL on treated foliage. Quercetin had harmful effects on development, body weight, or survival of LdisparBmori, and Onubilalis at a concentration ranging from 0.1–2% (w/w) in an artificial diet (Table 1).
    In summary, quercetin caused 0.792 and 0.208 proportional harmful and nonharmful effects on lepidopterans, respectively. A statistical analysis indicated a significant difference between the two effects (z = 4.046, p < 0.001, n = 24); harmful effects were predominant.

    4. Diptera (True Flies)

    Dipteran species subjected to quercetin in bioassays included two tephritids Rhagoletis pomonella (Walsh) and Bactrocera cucurbitae (Coquillett), one drosophilid Drosophila melanogaster Meigen and one sciarid Lycoriella pleuroti Yang & Zhang. Records indicated harmful (negative) effects of quercetin on BcucurbitaeRpomonella, and Lpleuroti after direct physical bodily contact with the compound in test arenas, in an artificial diet or artificial culture media at variable quercetin concentrations. For example, quercetin at 0.05–3.1 mg/mL, in bioassays involving Bcucurbitae, reduced egg hatch rate, pupation, adult emergence, oviposition, and survival rate (Table 1). In two studies, quercetin had nonharmful (positive) effects on development time and fecundity of Dmelanogaster larvae and adult females, respectively. Quercetin concentration ranged from 1.7% to 5.0% across these two studies. In summary of this section, quercetin caused 0.75 and 0.25 proportional harmful and nonharmful effects on dipterans, respectively. The statistical analysis indicated a significant difference between the two effects (z = 2.00, p = 0.046, n = 8); harmful effects were more prevalent.

    5. Orthoptera (Grasshoppers)

    Three acridid species were tested against quercetin in field cage and laboratory bioassays. These species included Calliptamus abbreviatus Ikonn, Oedaleus asiaticus Bey-Bienko, and Melanoplus sanguinipes (F.) (Table 1). Quercetin had harmful (negative) effects on development and survival of Cabbreviatus nymphs at a concentration of 0.10 mg/mL. Quercetin concentrations ranging from 0.10–10 mg/mL significantly reduced growth/development and survival of Oasiaticus nymphs. In contrast, body weight and survival rate of Msanguinipes nymphs were unaffected by quercetin at a concentration of ranging from 0.125–4.0% (w/w). In summary, quercetin caused 0.67 and 0.33 proportional harmful and nonharmful effects on orthopterans, respectively. A statistical analysis did not indicate a significant difference between the two effects (z = 1.155, p = 0.248, n = 6).

    6. Summary of Herbivores

    The sections above indicated that quercetin caused more harmful effects to Hemiptera, Lepidoptera, and Diptera but more nonharmful effects to Coleoptera. In concluding the herbivore section, quercetin caused 0.618 and 0.382 proportional harmful and nonharmful effects on herbivores, respectively, across the five insect orders combined. The two effects were significantly different (z = 2.744, p = 0.006, n = 68); harmful effects were predominant. Quercetin concentration (mg/mL) did not significantly influence the observed harmful and nonharmful effects on herbivores, based on pooling of data, when available, across the five insect orders (U = 105.50; p = 0.583; n = 20 for harmful effects; n = 12 for nonharmful effects). Median values with 25% and 75% confidence intervals were 0.56 mg/mL (0.10, 2.76) for harmful effects and 1.00 mg/mL (0.09, 3.02) for nonharmful effects. Specific harmful effects of quercetin on herbivores, of five orders combined, are illustrated in Figure 1. Quercetin frequently affected survival rate and development/growth.
    Figure 1. Proportion of specific harmful effects of quercetin on herbivores in five insect orders combined.

    The entry is from 10.3390/agriculture11060476

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