High susceptibility of Bt maize to aphids enhances the performance of parasitoids of lepidopteran pests

Abstract

Concerns about possible undesired environmental effects of transgenic crops have prompted numerous evaluations of such crops. So-called Bt crops receive particular attention because they carry bacteria-derived genes coding for insecticidal proteins that might negatively affect non-target arthropods. Here we show a remarkable positive effect of Bt maize on the performance of the corn leaf aphid Rhopalosiphum maidis, which in turn enhanced the performance of parasitic wasps that feed on aphid honeydew. Within five out of six pairs that were evaluated, transgenic maize lines were significantly more susceptible to aphids than their near-isogenic equivalents, with the remaining pair being equally susceptible. The aphids feed from the phloem sieve element content and analyses of this sap in selected maize lines revealed marginally, but significantly higher amino acid levels in Bt maize, which might partially explain the observed increased aphid performance. Larger colony densities of aphids on Bt plants resulted in an increased production of honeydew that can be used as food by beneficial insects. Indeed, Cotesia marginiventris, a parasitoid of lepidopteran pests, lived longer and parasitized more pest caterpillars in the presence of aphid-infested Bt maize than in the presence of aphid-infested isogenic maize. Hence, depending on aphid pest thresholds, the observed increased susceptibility of Bt maize to aphids may be either a welcome or an undesirable side effect.

Figure 1. Aphid performance.

Average number of R. maidis adults and nymphs on six pairs of transgenic and near isogenic varieties and on two conventional varieties (+SE). All comparisons are performed within each transgenic and near isogenic pair. Symbols indicate significant differences within each transgenic and isogenic pair (** p<0.01, *** p<0.001).

Figure 2. Phloem amino acid content.

Amino acid concentrations (mM) in phloem samples from three transgenic varieties belonging to three transformation events and their correspondent near isogenic lines. Different letters indicate significant differences between amino acid concentration within one transgenic/isogenic pair (p<0.05). Amino acid abbreviations: arg, arginine; tyr, tyrosine; lys, lysine; orn, ornithine; phe, phenylalanine; leu/ile, leucine/isoleucine; his/val, histidine/valine; gln, glutamine; pro, proline; thr, threonine; ala, alanine; ser, serine; asn, asparagine; gly, glycine; glu, glutamate; asp, aspartate. Asterisks indicate the essential amino acids.

Figure 3. Correlating transformation with amino acid content.

Distribution of amino acid concentrations (plotted as vectors) in samples of transgenic/isogenic pairs of maize plants belonging to three transformation events (vector Mon 810 denotes the pair MEB307Bt/Monumental; vector Bt11 denotes the pair N4640Bt/N4640; vector Event 176 denotes the pair Valmont/Prelude, vector trans indicates transgenic varieties belonging to all three transformation events) in the ordination biplot of an redundancy analysis (RDA). Axis 1 (Eigen Value = 0.054) and axis 2 (Eigen Value = 0.018) are presented. The ellipses group the different transgenic/isogenic pairs. For amino acid abbreviations see figure 2. Asterisks indicate the essential amino acids.

Figure 4. Amino acid content and aphid performance.

Distribution of amino acid concentrations (plotted as vectors) in samples of transgenic/isogenic pairs of maize plants in the ordination biplot of a principal component analysis (PCA). Axis 1 (Eigen Value = 0.56) and axis 2 (Eigen Value = 0.19) are presented. The two clusters formed by either the transgenic or the isogenic varieties are indicated. The vector aphid performance indicates the colony performance of aphids (for details see figure 3). For amino acid abbreviations see figure 2. Asterisks indicate the essential amino acids.

Figure 5. Parasitoid longevity.

Survival curves showing the survival probability of C. marginiventris when feeding on honeydew produced by R. maidis on maize of transgenic/isogenic pairs belonging to three different events. Different letters indicate significant differences between curves (p<0.01).

Figure 6. Parasitism.

Total number of offspring (number of cocoons) produced by C. marginiventris when feeding on honeydew produced by R. maidis on different maize varieties. Different letters indicate significant differences between treatments within one transgenic/isogenic pair (p<0.05).

Figure 7. Sugar composition of the honeydew produced by the corn leaf aphid R. maidis feeding on different maize genotypes.