Assessment of prey-mediated effects of the coleopteran-specific toxin Cry3Bb1 on the generalist predator Atheta coriaria (Coleoptera: Staphylinidae)
Abstract
A laboratory study was carried out to assess the potential prey-mediated effects of Cry3Bb1-expressing Bt maize on the fitness and predatory ability of Atheta coriaria Kraatz (Coleoptera: Staphylinidae), using Tetranychus urticae Koch (Acari: Tetranychidae) as prey. The concentration of Cry3Bb1 toxin through the trophic chain significantly decreased from Bt maize (21.7 μg g−1 FW) to mites (5.6 μg g−1 FW) and then to A. coriaria adults (1.4 μg g−1 FW), but not from mites to A. coriaria L 1–L 3 larvae (4.1–4.6 μg g−1 FW). Interestingly, the toxin levels detected in A. coriaria larvae represent more than 20% of the concentration found in Bt maize, and the toxin was detected up to 48 h after exposure. To our knowledge, this is the highest level of exposure ever reported in a predatory beetle to the Cry3Bb1 protein. When A. coriaria larvae were reared on Bt-fed mites, Bt-free mites or rearing food, no significant differences among treatments were observed in development, morphological measurements of sclerotized structures and body weight. Moreover, no negative effects on reproductive parameters were reported in adults feeding on Bt-fed prey after 30 days of treatment, and survival was not affected after 60 days of exposure. Similarly, predatory ability and prey consumption of A. coriaria larvae and adults were not affected by exposure to the toxin. All together, these results indicate a lack of adverse effects on A. coriaria, a species commonly used as a biological control agent. The use of A. coriaria as a surrogate species for risk assessment of GM crops that express insecticidal proteins is discussed.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Studies with Dalotia coriaria indicated no effects on different life table parameters when beetles were fed spider mites reared on Cry1Ab- or Cry3Bb-producing maize or when purified Cry3Aa and Cry1Ab was provided in artificial diet.
“Studies with Dalotia coriaria (Col.: Staphylinidae) indicated no effects on different life table parameters when beetles were fed spider mites reared on Cry1Ab-[53] or Cry3Bb-producing maize [54] or when purified Cry3Aa and Cry1Ab was provided in artificial diet [55].”
From Does the growing of Bt maize change abundance or ecological function of non-target animals compared to the growing of non-GM maize? A systematic review (2022) · cites this paper as [54]
Except for Staphylinidae, no controlled exposure studies examining direct toxic effects of Bt proteins are available for taxa where our meta-analyses showed lower populations in Bt maize.
“With the exception of Staphylinidae [53–55], no controlled exposure studies to examine direct toxic effects of Bt proteins are available for the taxa where our meta-analyses showed lower populations in Bt maize.”
From Does the growing of Bt maize change abundance or ecological function of non-target animals compared to the growing of non-GM maize? A systematic review (2022) · cites this paper as [54]
Cites
Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control
Bravo, A., Gill, S. S., & Soberón, M. (2006) · Toxicon · doi:10.1016/j.toxicon.2006.11.022 · Cited by 1,415 · see citing works
On the Use of Surrogate Species in Conservation Biology
Caro, T. M., & O'Doherty, G. M. (1999) · Conservation Biology · doi:10.1046/j.1523-1739.1999.98338.x · Cited by 943 · see citing works
The Number of Molts of Lepidopterous Larvae
Dyar, H. G. (1890) · Psyche A Journal of Entomology · doi:10.1155/1890/23871 · Cited by 655 · see citing works
The Role of Nourishment in Oogenesis
Wheeler, D. E. (1996) · Annual Review of Entomology · doi:10.1146/annurev.en.41.010196.002203 · Cited by 522 · see citing works
Multiple Transatlantic Introductions of the Western Corn Rootworm
Miller, N. J., Estoup, A., Toepfer, S., Bourguet, D., Lapchin, L., Derridj, S., Kim, K. S., Reynaud, P., Furlan, L., & Guillemaud, T. (2005) · Science · doi:10.1126/science.1115871 · Cited by 332 · see citing works
Staphylinid beetles as bioindicators
Boháč, J. (1999) · Agriculture Ecosystems & Environment · doi:10.1016/s0167-8809(99)00043-2 · Cited by 265 · see citing works
Vaughn, T. T., Cavato, T., Brar, G. S., Coombe, T., DeGooyer, T. A., Ford, S., Groth, M. E., Howe, A. R., Johnson, S. N., Kolacz, K. H., et al. (2005) · Crop Science · doi:10.2135/cropsci2004.0304 · Cited by 242 · see citing works
Daly, H. V. (1985) · Annual Review of Entomology · doi:10.1146/annurev.en.30.010185.002215 · Cited by 195 · see citing works
Western corn rootworm ( <i>Diabrotica virgifera virgifera</i> LeConte) population dynamics
Meinke, L. J., Sappington, T. W., Onstad, D. W., Guillemaud, T., Miller, N. J., Komáromi, J., Levay, N., Furlan, L., Kiss, J., & Toth, F. (2009) · Agricultural and Forest Entomology · doi:10.1111/j.1461-9563.2008.00419.x · Cited by 186 · see citing works
The impact of transgenic plants on natural enemies: a critical review of laboratory studies
Löveï, G. L., & Arpaia, S. (2005) · Entomologia Experimentalis et Applicata · doi:10.1111/j.0013-8703.2005.00235.x · Cited by 170 · see citing works
Impact of farm-scale Bt maize on abundance of predatory arthropods in Spain
de la Poza, M., Pons, X., Farinós, G. P., López, C., Ortego, F., Eizaguirre, M., Castañera, P., & Albajes, R. (2005) · Crop Protection · doi:10.1016/j.cropro.2004.12.003 · Cited by 111 · see citing works
Self-citationLundgren, J. G., & Wiedenmann, R. N. (2002) · Environmental Entomology · doi:10.1603/0046-225x-31.6.1213 · Cited by 110 · see citing works
Álvarez‐Alfageme, F., Bigler, F., & Romeis, J. (2010) · Transgenic Research · doi:10.1007/s11248-010-9430-5 · Cited by 104 · see citing works
Duan, J. J., Head, G., McKee, M. J., Nickson, T. E., Martin, J. W., & Sayegh, F. S. (2002) · Entomologia Experimentalis et Applicata · doi:10.1046/j.1570-7458.2002.01013.x · Cited by 93 · see citing works
Li, Y., & Romeis, J. (2009) · Biological Control · doi:10.1016/j.biocontrol.2009.12.003 · Cited by 91 · see citing works
Icoz, I., & Stotzky, G. (2007) · Transgenic Research · doi:10.1007/s11248-007-9133-8 · Cited by 91 · see citing works
Meissle, M., & Romeis, J. (2009) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2009.00431.x · Cited by 90 · see citing works
Miethling-Graff, R., Dockhorn, S., & Tebbe, C. C. (2009) · European Journal of Soil Biology · doi:10.1016/j.ejsobi.2009.10.003 · Cited by 80 · see citing works
Ecological risk assessment for Bt crops
Andow, D. A., Löveï, G. L., & Arpaia, S. (2006) · Nature Biotechnology · doi:10.1038/nbt0706-749 · Cited by 70 · see citing works
Farinós, G. P., de la Poza, M., Hernández‐Crespo, P., Ortego, F., & Castañera, P. (2008) · Biological Control · doi:10.1016/j.biocontrol.2007.11.007 · Cited by 67 · see citing works
Self-citationDelbac, L., Lecharpentier, P., & Thiéry, D. (2010) · Crop Protection · doi:10.1016/j.cropro.2010.01.009 · Cited by 66 · see citing works
Álvarez‐Alfageme, F., Ferry, N., Castañera, P., Ortego, F., & Gatehouse, A. M. R. (2008) · Transgenic Research · doi:10.1007/s11248-008-9177-4 · Cited by 65 · see citing works
Self-citationBitrophic and tritrophic effects of Bt Cry3A transgenic potato on beneficial, non-target, beetles
Ferry, N., Mulligan, E. A., Majerus, M. E. N., & Gatehouse, A. M. R. (2007) · Transgenic Research · doi:10.1007/s11248-007-9088-9 · Cited by 59 · see citing works
Records of adventive aleocharine beetles (Coleoptera: Staphylinidae: Aleocharinae) found in Canada
Klimaszewski, J., Assing, V., Majka, C. G., Pelletier, G., Webster, R. P., & Langor, D. W. (2007) · The Canadian Entomologist · doi:10.4039/n05-105 · Cited by 51 · see citing works
García, M., Ortego, F., Castañera, P., & Farinós, G. P. (2010) · Biological Control · doi:10.1016/j.biocontrol.2010.08.002 · Cited by 48 · see citing works
Self-citationBalog, A., Kiss, J. G., Szekeres, D., Szénási, Á., & Markó, V. (2010) · Crop Protection · doi:10.1016/j.cropro.2009.12.020 · Cited by 43 · see citing works
Ahmad, A., Wilde, G. E., Whitworth, R. J., & Zolnerowich, G. (2006) · Journal of Economic Entomology · doi:10.1093/jee/99.4.1085 · Cited by 42 · see citing works
Todd, J. H., Ramankutty, P., Barraclough, E. I., & Malone, L. A. (2008) · Environmental Biosafety Research · doi:10.1051/ebr:2008003 · Cited by 39 · see citing works
Duan, J. J., Paradise, M. S., Lundgren, J. G., Bookout, J. T., Jiang, C., & Wiedenmann, R. N. (2006) · Environmental Entomology · doi:10.1603/0046-225x-35.1.135 · Cited by 39 · see citing works
Porcar, M., García-Robles, I., Domínguez-Escribà, L., & Latorre, A. (2010) · Bulletin of Entomological Research · doi:10.1017/s0007485309990290 · Cited by 37 · see citing works
Jandricic, S., Scott‐Dupree, C. D., Broadbent, A. B., et al. (2006) · The Canadian Entomologist · doi:10.4039/n05-106 · Cited by 36 · see citing works
Brunke, A. J., Bahlai, C. A., Sears, M. K., et al. (2009) · Environmental Entomology · doi:10.1603/022.038.0418 · Cited by 32 · see citing works
Miller, K. V., & Williams, R. N. (1983) · Annals of the Entomological Society of America · doi:10.1093/aesa/76.2.158 · Cited by 28 · see citing works
Rauschen, S., Schaarschmidt, F., & Gathmann, A. (2009) · Transgenic Research · doi:10.1007/s11248-009-9351-3 · Cited by 28 · see citing works
Bhatti, M. A., Duan, J., Head, G. P., Jiang, C., McKee, M. J., Nickson, T. E., Pilcher, C. L., & Pilcher, C. D. (2005) · Environmental Entomology · doi:10.1093/ee/34.5.1336 · Cited by 28 · see citing works
Chege, P. G., Clark, T. L., & Hibbard, B. E. (2005) · Environmental Entomology · doi:10.1603/0046-225x-34.6.1441 · Cited by 28 · see citing works
Bhatti, M. A., Duan, J. J., Head, G., Jiang, C., McKee, M. J., Nickson, T. E., Pilcher, C., & Pilcher, C. D. (2005) · Environmental Entomology · doi:10.1093/ee/34.5.1325 · Cited by 23 · see citing works
Arpaia, S., Marzo, L. D., Leo, G. M. D., et al. (2000) · Entomologia Experimentalis et Applicata · doi:10.1046/j.1570-7458.2000.00638.x · Cited by 21 · see citing works
A Colour Handbook of Biological Control in Plant Protection
Goodwin, S. (2005) · Australian Journal of Entomology · doi:10.1111/j.1440-6055.2005.00445.x · Cited by 9 · see citing works
A Color Handbook of Biological Control in Plant Protection
MORSE, J. G., Helyer, N. L., Brown, K. A., & Cattlin, N. D. (2006) · Environmental Entomology · doi:10.1603/0046-225x(2006)35[1718:achobc]2.0.co;2 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Meissle, M., Naranjo, S. E., & Romeis, J. (2022) · Environmental Evidence · doi:10.1186/s13750-022-00272-0 · Cited by 41 · see citing works
“: Staphylinidae) indicated no effects on different life table parameters when beetles were fed spider mites reared on Cry1Ab-[53] or Cry3Bb-producing maize [54] or when purified Cry3Aa and Cry1Ab was provided in artificial diet [55].”
BackgroundGuo, Y.-Y., Tian, J.-C., Shi, W.-P., Dong, X.-H., Romeis, J., Naranjo, S. E., Hellmich, R. L., & Shelton, A. M. (2016) · Transgenic Research · doi:10.1007/s11248-015-9917-1 · Cited by 14 · see citing works
- Authors
- García, M., Ortego, F., Castañera, P., & Farinós, G. P.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- Corresponding author
- Farinós, G.P.
- Venue
- Bulletin of Entomological Research
- Publisher
- Cambridge University Press (CUP)
- Published
- 2011-11-24
- Volume
- 102
- Issue
- 3
- Pages
- 293-302
- ISSN
- 0007-4853 (ISSN-L)
- 1475-2670
- OpenAlex
- W2034876369
- Cited by
- 22
- References
- 40
- Citations by year
- 2023: 1 · 2022: 7 · 2020: 1 · 2017: 2 · 2016: 4 · 2015: 2 · 2014: 2 · 2012: 3
- FWCI
- 0.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Bulletin of Entomological Research (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Funders
- Ministerio para la Transición Ecológica y el Reto Demográfico
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetically Modified Organisms Research
- Keywords
- Bt maize, Staphylinidae, Tetranychus urticae, trophic transfer, biological control agents, insecticidal proteins, larval development, reproductive parameters
- MeSH terms
- Animals, Coleoptera, Zea mays, Endotoxins, Female, Larva, Male, Predatory Behavior, Reproduction, Food Chain, Plants, Genetically Modified, Tetranychidae
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review