Pyraclostrobin Impairs Energetic Mitochondrial Metabolism and Productive Performance of Silkworm (Lepidoptera: Bombycidae) Caterpillars

Nicodemo, Daniel; Mingatto, Fábio Ermínio; Carvalho, Amanda de; Bizerra, Paulo Francisco Veiga; Tavares, Marco Aurélio; Balieira, Kamila Vilas Boas; Bellini, William César

doi:10.1093/jee/toy060

Cited by 20 publications

(13 citation statements)

References 25 publications

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“…We found that pyraclostrobin acts as a respiratory chain inhibitor, affecting mitochondrial bioenergetics in the honey bee thorax. This is consistent with what was previously found in another domesticated insect, the silkworm ( Bombyx mori ; Nicodemo et al 2018). Mitochondrial oxidative phosphorylation is the primary process by which aerobic cells produce ATP by esterification of ADP with inorganic phosphate.…”

Section: Discussionsupporting

confidence: 93%

Mitochondrial Respiratory Inhibition Promoted by Pyraclostrobin in Fungi is Also Observed in Honey Bees

Nicodemo

Mingatto

Jong

et al. 2020

Enviro Toxic and Chemistry

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There is no use restriction associated with bees for many fungicides used in agriculture; however, this does not always mean that these pesticides are harmless for these nontarget organisms. We investigated whether the fungicide pyraclostrobin, which acts on fungal mitochondria, also negatively affects honey bee mitochondrial bioenergetics. Honey bees were collected from 5 hives and anesthetized at 4°C. The thoraces were separated, and mitochondria were isolated by grinding, filtering, and differential centrifugation. An aliquot of 0.5 mg of mitochondrial proteins was added to 0.5 mL of a standard reaction medium with 4 mM succinate (complex II substrate) plus 50 nM rotenone (complex I inhibitor), and mitochondrial respiration was measured at 30°C using a Clark-type oxygen electrode. Mitochondrial membrane potential was determined spectrofluorimetrically using safranin O as a probe, and adenosine triphosphate (ATP) synthesis was determined by chemiluminescence. Pyraclostrobin at 0 to 50 μM was tested on the mitochondrial preparations, with 3 repetitions. Pyraclostrobin inhibited mitochondrial respiration in a dose-dependent manner at concentrations of 10 μM and above, demonstrating typical inhibition of oxidative phosphorylation. Pyraclostrobin also promoted a decline in the mitochondrial membrane potential at doses of 5 μM and above and in ATP synthesis at 15 μM and above. We conclude that pyraclostrobin interferes with honey bee mitochondrial function, which is especially critical for the energy-demanding flight activity of foraging bees. Environ Toxicol Chem 2020;39:1267-1272. © 2020 SETAC

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Section: Discussionsupporting

confidence: 93%

Mitochondrial Respiratory Inhibition Promoted by Pyraclostrobin in Fungi is Also Observed in Honey Bees

Nicodemo

Mingatto

Jong

et al. 2020

Enviro Toxic and Chemistry

Self Cite

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“…This research gap is noteworthy since some experiments show negative effects of herbicides on Lepidoptera performance, including reduced survival or wing size [18][19][20] , adult emergence 21 and sex-pheromone production 22 . Similar studies, mainly on commercial (Bombyx mori L.) and pest (Spodoptera litura F.) lepidopteran species, have found that fungicides can also reduce larval survival, pupal weight or adult longevity 23,24 . Moreover, fungicides synergize the action of insecticides by inhibiting cytochrome P450 enzymes in honey bees [25][26][27][28] .…”

Section: Larval Pesticide Exposure Impacts Monarch Butterfly Performamentioning

confidence: 74%

Larval pesticide exposure impacts monarch butterfly performance

Olaya-Arenas

Hauri

Scharf

et al. 2020

Sci Rep

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cabbage butterfly, Pieris brassicae, larvae was unaffected by wide variation (up to 200 ppb) of the neonicotinoid imidacloprid in their diet, but even the lowest dose (1 ppb) reduced adult wing size 34. The monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae), is an iconic species whose population is declining in North America. Numerous causal factors have been implicated in their decline 35-37 , with disappearance of its larval host-plant, milkweed (Asclepias sp.), due to the introduction of the herbicide glyphosate being the leading hypothesis 38-43. Some have noted, however, that the decline temporally coincides with the introduction and growing popularity of neonicotinoids and thus speculate that insecticides or other agrochemicals could act as a contributing factor. To date, only a few studies have experimentally assessed the impact of agricultural pesticides on monarch larvae, providing some pieces of the puzzle. Yet, these studies suffer from methodological limitations that prevent us from extrapolating to the broader question of monarch decline. All used ornamental milkweeds that are planted in home gardens such as tropical milkweed A. curassavica 44,45 or swamp milkweed A. incarnata 46,47 , rather than the common milkweed A. syriaca, which is the most abundant and widely used larval host-plant for eastern migratory monarchs 48,49. This discrepancy is potentially important since milkweed species differ dramatically in defensive traits affecting host-plant suitability 50 (e.g., latex, trichomes); for instance, tropical and swamp milkweeds are notable for having extremely high and low levels of cardenolides, respectively 51. Similarly, experiments mostly employ brief 'pulsed' exposure periods with larvae consuming a known insecticide dose over a 24-48 h period 45,46. This approach is useful in defining acute toxicity and calculating LD 50 values but does not accurately portray natural exposure where larvae consume trace amounts over their entire developmental period. Additionally, all prior studies investigated insecticides; none have tested other pesticide types, e.g., fungicides, herbicides. Here, we evaluated the effects of six pesticides-the insecticide clothianidin; the herbicides atrazine and S-metolachlor; the fungicides azoxystrobin, pyraclostrobin and trifloxystrobin-and their combination on monarch development. These were among the most commonly detected chemicals on A. syriaca leaves in a 2-year field survey of milkweeds bordering cropland 52. Because we know their specific concentrations, we tested each at mean and maximum levels; thus, all data represent field-realistic pesticide types and doses. Importantly, we exposed monarchs to these treatments on A. syriaca leaves over their complete larval period, measuring both immediate (i.e., larval mortality) and delayed responses (i.e., changes in adult size and longevity). These data are ultimately used in risk assessment to estimate the likelihood of lethal or nonlethal effects and their potential to harm monarchs in the wild. Methods Pla...

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“…4D,E), perhaps because larval mitochondria are heavily involved in protein synthesis (Nicodemo et al. 2018) or because HIF activation affects DNA methylation across the genome (Choudhry and Harris 2018). Reduced growth rate should have a negative effect on larval fitness by prolonging exposure to factors such as adverse weather, parasitoids, predators, host plant depletion, and seasonal drying of the habitat (Lampert and Trubetskova 1996; Van Nouhuys and Hanski 1999; Whitney‐Johnson et al.…”

Section: Discussionmentioning

confidence: 99%

Alleles in metabolic and oxygen‐sensing genes are associated with antagonistic pleiotropic effects on life history traits and population fitness in an ecological model insect*

et al. 2020

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Genes with opposing effects on fitness at different life stages are the mechanistic basis for evolutionary theories of aging and life history. Examples come from studies of mutations in model organisms, but there is little knowledge of genetic bases of life history tradeoffs in natural populations. Here, we test the hypothesis that alleles affecting oxygen sensing in Glanville fritillary butterflies have opposing effects on larval versus adult fitness‐related traits. Intermediate‐frequency alleles in Succinate dehydrogenase d, and to a lesser extent Hypoxia inducible factor 1α, are associated in larvae with variation in metabolic rate and activation of the hypoxia inducible factor (HIF) pathway, which affects tracheal development and delivery of oxygen to adult flight muscles. A dominant Sdhd allele is likely to cause antagonistic pleiotropy for fitness through its opposing effects on larval metabolic and growth rate versus adult flight and dispersal, and may have additional effects arising from sensitivity to low‐iron host plants. Prior results in Glanville fritillaries indicate that fitness of alleles in Sdhd and another antagonistically pleiotropic metabolic gene, Phosphoglucose isomerase, depend strongly on the size and distribution of host plant patches. Hence, these intermediate‐frequency alleles are involved in ecoevolutionary dynamics involving life history tradeoffs.

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Pyraclostrobin Impairs Energetic Mitochondrial Metabolism and Productive Performance of Silkworm (Lepidoptera: Bombycidae) Caterpillars

Cited by 20 publications

References 25 publications

Mitochondrial Respiratory Inhibition Promoted by Pyraclostrobin in Fungi is Also Observed in Honey Bees

Mitochondrial Respiratory Inhibition Promoted by Pyraclostrobin in Fungi is Also Observed in Honey Bees

Larval pesticide exposure impacts monarch butterfly performance

Alleles in metabolic and oxygen‐sensing genes are associated with antagonistic pleiotropic effects on life history traits and population fitness in an ecological model insect*

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