Effect of stacked insecticidal Cry proteins from maize pollen on nurse bees (Apis mellifera carnica) and their gut bacteria

PLoS One. 2013;8(3):e59589. doi: 10.1371/journal.pone.0059589. Epub 2013 Mar 22.

Abstract

Honey bee pollination is a key ecosystem service to nature and agriculture. However, biosafety research on genetically modified crops rarely considers effects on nurse bees from intact colonies, even though they receive and primarily process the largest amount of pollen. The objective of this study was to analyze the response of nurse bees and their gut bacteria to pollen from Bt maize expressing three different insecticidal Cry proteins (Cry1A.105, Cry2Ab2, and Cry3Bb1). Naturally Cry proteins are produced by bacteria (Bacillus thuringiensis). Colonies of Apis mellifera carnica were kept during anthesis in flight cages on field plots with the Bt maize, two different conventionally bred maize varieties, and without cages, 1-km outside of the experimental maize field to allow ad libitum foraging to mixed pollen sources. During their 10-days life span, the consumption of Bt maize pollen had no effect on their survival rate, body weight and rates of pollen digestion compared to the conventional maize varieties. As indicated by ELISA-quantification of Cry1A.105 and Cry3Bb1, more than 98% of the recombinant proteins were degraded. Bacterial population sizes in the gut were not affected by the genetic modification. Bt-maize, conventional varieties and mixed pollen sources selected for significantly different bacterial communities which were, however, composed of the same dominant members, including Proteobacteria in the midgut and Lactobacillus sp. and Bifidobacterium sp. in the hindgut. Surprisingly, Cry proteins from natural sources, most likely B. thuringiensis, were detected in bees with no exposure to Bt maize. The natural occurrence of Cry proteins and the lack of detectable effects on nurse bees and their gut bacteria give no indication for harmful effects of this Bt maize on nurse honey bees.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Bacterial Proteins / pharmacology*
  • Bees / drug effects*
  • Bees / microbiology*
  • Endotoxins / genetics
  • Endotoxins / metabolism*
  • Endotoxins / pharmacology*
  • Gastrointestinal Tract / drug effects*
  • Gastrointestinal Tract / microbiology*
  • Hemolysin Proteins / genetics
  • Hemolysin Proteins / metabolism*
  • Hemolysin Proteins / pharmacology*
  • Plants, Genetically Modified / genetics
  • Plants, Genetically Modified / metabolism*
  • Pollen / chemistry
  • Pollen / metabolism*
  • Zea mays / genetics
  • Zea mays / metabolism*

Substances

  • Bacterial Proteins
  • Endotoxins
  • Hemolysin Proteins
  • insecticidal crystal protein, Bacillus Thuringiensis

Grant support

The work was financially supported by the German Federal Ministry for Education and Research (BMBF) (Project numbers 0315215C and 31P5398) and by AMIGA (European Union, 7th Framework Programme, Grant agreement no. 289706). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.