Uptake and bioaccumulation of Cry toxins by an aphidophagous predator

Paula, Danielli Parrilha de; Andow, David A.

doi:10.1016/j.envpol.2015.11.036

Cited by 16 publications

(20 citation statements)

References 37 publications

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“…These results are inconsistent with some studies that reported that natural enemy species can uptake and even bio-accumulate Cry toxins delivered by their prey (Couty et al, 2001;Bernal et al, 2002;Zhang et al, 2006a;Gao et al, 2010;Paula & Andow, 2016), as Cry1Ab concentrations in corresponding aphids were still detectable at low levels. The Cry1Ab concentrations in P. japonica agreed with the results of Cry1Ab concentrations in aphids and feeding amounts for the 5422Bt1 and 5422CBCL treatments.…”

Section: Discussioncontrasting

confidence: 98%

“…A detectable amount of Cry1Ab was reported in brown planthopper nymphs and adults feeding on transgenic Bt rice (Bai et al, 2006;Gao et al, 2010;Tian et al, 2010). Bernal et al (2002) and Paula & Andow (2016) also noted that Bt proteins have been detected in the honeydew of aphids reared on transgenic rice. Ren et al (2016) showed that no Cry1Ab was found in aphid adults feeding on Bt or non-Bt rice lines.…”

Section: Discussionmentioning

confidence: 93%

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Presence of Cry1Ab in the Bt maize – aphid (Rhopalosiphum maidis) – ladybeetle (Propylea japonica) system has no adverse effects on insect biological parameters

Shu

Wang

2019

Entomologia Exp Applicata

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Transgenic Bacillus thuringiensis Berliner (Bt) crops receive particular attention because they carry genes encoding insecticidal proteins that might negatively affect non-target arthropods. Here, laboratory experiments were conducted to evaluate the impact of Cry1Ab-expressing transgenic maize [5422Bt1 (event Bt11) and 5422CBCL (MON810)] on the biological parameters of two non-target arthropods, the aphid Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae) and its predator the ladybeetle Propylea japonica (Thunberg) (Coleoptera: Coccinellidae). In a long-term assay (three generations), no significant differences were found between R. maidis fed Bt maize and those fed a near-isogenic line (5422) when individual parameters were compared, including nymph development time, adult longevity, aphid spawning period, and fecundity. No negative effects were detected throughout the life cycle of P. japonica in aphids' feeding amount, development (nymphs, pupae, adults, and progeny eggs), fecundity, or egg hatching when they preyed on Bt maize-fed aphids compared with non-Bt maize treatments. A tritrophic assay revealed that Cry1Ab was highly diluted through the food chain (Bt maize leaves, R. maidis, and P. japonica), as detected by an enzymelinked immunosorbent assay (ELISA). In conclusion, although Cry1Ab concentrations in maize leaves increased as the plants developed, Cry1Ab levels were significantly reduced in the aphid R. maidis, and no traces of Cry1Ab were detected in P. japonica preying on Bt maize-fed aphids. The two hybrids of Bt maize expressing Cry1Ab had no negative effects on the measured biological parameters of the aphid R. maidis or its predator, the ladybeetle P. japonica.

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Section: Discussioncontrasting

confidence: 98%

Section: Discussionmentioning

confidence: 93%

Presence of Cry1Ab in the Bt maize – aphid (Rhopalosiphum maidis) – ladybeetle (Propylea japonica) system has no adverse effects on insect biological parameters

Shu

Wang

2019

Entomologia Exp Applicata

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“…About 74 and 70 % of H. axyridis pupae had Cry1Ac and Cry1F respectively, while only 9 and 14 % of C. sanguinea did. The detection of the toxins in the predator pupae is a proof of uptake (Paula and Andow 2015), as prior to pupation, insects like coccinellids empty their guts, and during pupation they shed both the external cuticle and the cuticular lining of the gut (Chapman 1998). Thus, most H. axyridis were exposed internally to Cry toxins, while most C. sanguinea were not.…”

Section: Differential Uptake Of the Cry Toxinsmentioning

confidence: 99%

“…In the last 15 years, laboratory studies have demonstrated that some natural enemy species can uptake and even bioaccumulate Cry toxins delivered from their prey (Couty et al 2001;Zhang et al 2006;Gao et al 2010;Paula and Andow 2015). Uptake is the absorption of a chemical from the food (USEPA 2013), i.e.…”

Section: Introductionmentioning

confidence: 99%

Limitations in dose–response and surrogate species methodologies for risk assessment of Cry toxins on arthropod natural enemies

Paula¹,

Andow

Bellinati

et al. 2016

Ecotoxicology

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Dose-response assays and surrogate species are standard methods for risk analysis for environmental chemicals. These assume that individuals within a species have unimodal responses and that a surrogate species can predict responses of other related taxa. We exposed immature individuals of closely related aphidophagous coccinellid predators, Cycloneda sanguinea and Harmonia axyridis, to Cry1Ac and Cry1F toxins through uniform and constant artificial tritrophic exposure through Myzus persicae aphids. Both toxins were detected in coccinellid pupae, with individual and interspecific variation. Uptake was significantly higher in H. axyridis than in C. sanguinea, both in the proportion of individuals and the concentrations per individual. We also observed bimodal uptake of the Cry toxins by H. axyridis, which indicated that some individuals had low bioaccumulation and some had high bioaccumulation. This suggests that standard dose-response assays need to be interpreted with caution and future assays should examine the modality of the responses. In addition, the similarity in the biological effects of the Cry toxins in the two predators was due to different biological exposure mechanisms. The majority of H. axyridis were exposed both internally and in the gut, while C. sanguinea was exposed primarily in the gut. Thus, despite their close phylogenetic relatedness, these species would not be good surrogates for each other and the surrogate species methodology should be tested more rigorously.

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“…Exposure to natural enemies can be greater if the herbivore consuming a GM crop plant is only partially susceptible to the toxin and therefore consumes a greater quantity of plant tissue. Many herbivores do contain transgenic toxins (e.g., Harwood et al, 2005; Meissle et al, 2005; Obrist et al, 2005, 2006b; Peterson et al, 2016), but accumulation in higher trophic levels is uncommon (Dutton et al, 2002; Obrist et al, 2006a; Paula and Andow, 2016). While tritrophic transfer of Bt proteins has been documented, it is at low levels (e.g., Harwood et al, 2005, 2007; Meissle et al, 2005; Zwahlen and Andow, 2005; Obrist et al, 2006a; Wei et al, 2008; Chen et al, 2009; Meissle and Romeis, 2009; Peterson et al, 2009, 2016; Tian et al, 2010; Han et al, 2015).…”

Section: Genetically Modified Crops and Interactions With Biological mentioning

confidence: 99%

Integration of Plant Defense Traits with Biological Control of Arthropod Pests: Challenges and Opportunities

et al. 2016

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Uptake and bioaccumulation of Cry toxins by an aphidophagous predator

Cited by 16 publications

References 37 publications

Presence of Cry1Ab in the Bt maize – aphid (Rhopalosiphum maidis) – ladybeetle (Propylea japonica) system has no adverse effects on insect biological parameters

Presence of Cry1Ab in the Bt maize – aphid (Rhopalosiphum maidis) – ladybeetle (Propylea japonica) system has no adverse effects on insect biological parameters

Limitations in dose–response and surrogate species methodologies for risk assessment of Cry toxins on arthropod natural enemies

Integration of Plant Defense Traits with Biological Control of Arthropod Pests: Challenges and Opportunities

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