Apr 16, 2004

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Effect of Bt toxin on non-target organisms

Lacewings not in danger after all

At the Swiss Federal Research Station for Agroecology and Agriculture (FAL) researchers have been able to demonstrate using a new test method that lacewing larvae are not harmed by Bt toxin. A few years previously, a similar study from the same research institute had found indications of direct harm to the insects.

A big concern with the cultivation of insect-resistant Bt maize plants are possible negative effects on so-called non-target organisms. These include beneficial organisms like ladybirds, Bembidion (ground beetles), the marmalade hoverfly and lacewing, which help keep pest numbers down by acting as predators in the field.

These creatures can come into contact with the Bt toxin either directly, e.g. through the Bt maize pollen, or indirectly through prey that feeds on Bt maize

Lacewing larvae are important beneficial organisms. They are also called “aphid lions” because they eat several hundred aphids in the course of their development. But they also eat other types of prey. They use their mouth parts to penetrate the skin of prey and the shell of butterfly eggs and suck out the insides. The larvae pass through three larval stages, i.e. moult twice before pupating.

The adult insects have lacy wings and glittering golden eyes. They feed mainly on honeydew, nectar and pollen. Their pale green colour changes to yellow-brown in the autumn. The females lay up to 700 eggs in their lifetime on the undersides of leaves.

Image from a video documentation of lacewings produced at the Institute of Phytopathology at Kiel University.

First study (Angelika Hilbeck et al, 1998/99):

Feeding experiments with lacewing larvae over all three larval stages

There were three trial series:

direct feeding with Bt toxin mixed with an artificial nutritive medium specially developed for lacewing larvae. The average total mortality rate was 57% compared with 30% among the control insects not fed on Bt toxin.

Feeding with caterpillars that had eaten Bt maize. Average mortality: 59% compared with 37% among controls without Bt.

Feeding with caterpillars that had eaten Bt toxin in artificial food. Average mortality rate for different Bt concentrations between 55 and 78% compared with 26% for the Bt-free controls.

Second study (Jörg Romeis et al, 2003):

The following are some of the trial series conducted:

lacewing larvae in the first larval stage (L1) were fed a sugar solution with and without Bt toxin.

No direct effect of the Bt toxin was detected, not even with 10000 times the level of Bt concentration that the lacewing larvae ingest when eating caterpillars fed on Bt maize.

The lacewing larvae in the first stage (L1) were fed a sugar solution with and without Bt toxin for 6 days. They were then offered insect eggs as a high-grade food.

Development in the following larval stages was not impaired by Bt toxin doses in the first larval stage.

Lacewing larvae in the first larval stage (L1) were fed high-grade food (insect eggs) or a lower-grade food (caterpillars). In the following larval stages (L2 and L3) they were offered only a sugar solution with and without Bt toxin.

The Bt toxin was not found to have any effect on older larval stages, even when the larvae had been subjected to additional stress by feeding with a lower-grade food during the L1 stage.

Significant effects

Whereas investigations with most beneficial organisms have found no evidence of damage caused by the Bt toxin, a FAL study carried out about seven years ago found a higher mortality rate among lacewing larvae after they were fed directly with Bt toxin mixed into an artificial nutritive medium. The mortality rate was almost twice as high as among insects that were not fed the Bt toxin food.

These results pointed to a direct toxic effect. This was very surprising, since until then it had been assumed that Bt toxin was only effective on butterflies like the European corn borer, a key maize pest.

Another trial series, in which the lacewing larvae were fed caterpillars that had eaten Bt maize, showed a similar level of mortality. This was a worrying finding, since the Bt toxin level in Bt maize is much lower than in the trial with the artificial nutritive medium. It was suspected that the effect of the toxin was amplified on its way through the food chain.

New experiment with Bt sugar solution

In order to check the possible toxic effect of Bt toxin on lacewing larvae, FAL Reckenholz developed a new test for feeding the lacewing larvae directly with Bt toxin

Instead of using an artificial food, they used a simple sugar solution and dissolved the Bt toxin in it. Food uptake was monitored by weighing the insects on micro scales and the amount of toxin ingested was measured using a biochemical method. Even with a level of Bt toxin 10,000 times higher than that which the lacewing larvae would ingest when eating caterpillars fed on Bt maize, no harmful effects were found.

Another trial series showed that the development times of the larvae in the second and third larval stages are not affected by a Bt toxin dose during the first larval stage.

A third trial showed that the following two larval stages are not negatively affected by feeding with the Bt sugar solution, even if the insects had received a lower-grade food in the first larval stage. Negative effects from the Bt toxin would have been most likely to occur among such stressed insects.

Reduced nutritional quality instead of toxic effect?

According to the authors of the latest study, the negative effects observed previously are probably due to reduced nutritional quality rather than a direct toxic effect of the Bt toxin.

Their tentative explanations for the very divergent results:

  • In the first study, the researchers did not monitor whether the lacewing larvae actually ate the food offered and if so how much of it. Any irregularities in the trial would not have been apparent.
  • Artificial food and sugar solution could have different effects on the composition and activity of digestive enzymes, with corresponding knock-on effects on the breakdown process and detoxification of the toxin. But now other studies too are showing that Bt toxin cannot in principal have a toxic effect on lacewing larvae and therefore does not need to be ‘detoxified’ by the insect. In fact, for Bt toxin to have a toxic effect, it must be able to bind to receptors in the insects’ midgut. A Dutch research group has demonstrated that lacewings do not have these binding sites.
  • In the first study, a complex artificial food was used, the ingredients of which were not fully disclosed by the manufacturer. It is possible that interactions took place between some of the food ingredients and the toxin. Physical or chemical changes to the artificial food caused in this way might have impaired the nutritional quality, which was not ideal in the first place. This assumption is backed up by the fact that in earlier experiments no negative effect was found in the first larval stage. The negative effects appeared only after a fairly long stress phase under suboptimal nutritional conditions.

A preference for aphids

Even the high mortality rate observed among insects that ate caterpillars fed on Bt plant material would therefore appear to be an indirect effect. The caterpillars fed on Bt maize present a lower nutritional quality for the lacewing larvae and lead to increased stress.

The suspicion that Bt toxin could be converted into a more active form in the caterpillars is not very likely. The authors of the new study extracted the Bt toxin from the caterpillars fed on Bt maize and fed it to European corn borer caterpillars. No evidence was found of increased toxic activity of the Bt toxin.

In any case, under natural field conditions, lacewing larvae prefer aphids to caterpillars. Aphids are not affected by the Bt toxin since they suck sap from the maize plant’s phloem and this does not contain Bt toxin. In addition, another study has shown that most of the caterpillars in the Bt maize field can successfully escape their predator.

The results of the latest laboratory experiments are confirmed by five field studies which again found no negative effects of Bt maize on lacewings. The FAL researchers therefore no longer see any indication that Bt maize could represent a serious risk to lacewings.