Want to solve the locust plague by "eating"? Unfortunately, they have already predicted it.

Produced by: Science Popularization China

Author: Xiao Xiaobo (PhD in Biology)

Producer: China Science Expo

Everyone may have some understanding of locust plagues. A large number of migratory locusts gather to form a huge population, which is conducive to their foraging, finding habitats and choosing mates. Locust plagues are extremely harmful. After a large-scale locust plague is formed, no grass will grow wherever it passes.

However, such a large-scale gathering is bound to attract the attention of natural enemies, increasing the risk of being preyed upon. So why don't the large numbers of locusts become a "buffet" for various predators and be eliminated? What strategies do locusts use to avoid being preyed upon by natural enemies?

Plague of locusts

(Photo source: veer photo gallery)

The research team led by Academician Kang Le from the Institute of Zoology, Chinese Academy of Sciences, conducted in-depth research on this and solved the mystery of locust colony defense.

The Locust Team held a meeting and changed their vests after the meeting

After gathering, locusts change from solitary to gregarious, and their bodies also begin to change along with their long-evolved defense strategies. From the appearance point of view, the most obvious change is the change in body color. Before gathering, locusts use green body color as a natural protective color, hiding in the surrounding plants and living a "low-key" life to avoid being exposed and preyed upon by natural enemies.

As swarming occurs, a large number of individuals gather together, making it difficult for them to hide as before, and the body color of the locusts gradually changes to black-brown. Such a conspicuous body color is called warning color.

(For details about the body color change of migratory locusts, please see the article "Locusts: What, you don't recognize me after changing my vest?"

http://www.kepu.net.cn/kpqykj/all/2022/202211/t20221130_503347.html）

Solitary and gregarious locusts

(Image source: References)

Locust: I smell bad, everyone, stay away from me!

In addition to the difference in body color, the research team also found differences in the smell of locusts. Compared with solitary locusts, gregarious locusts specifically release a volatile compound called benzyl nitrile. Benzyl nitrile has an irritating smell and may cause adverse reactions such as dizziness and vomiting after inhaling excessive amounts. This volatile compound is very sensitive to changes in population density. The greater the population density, the more benzyl nitrile is produced. Benzyl nitrile is an intermediate product in the metabolic pathway of phenylalanine in organisms and will eventually synthesize the highly toxic compound hydrocyanic acid.

Based on this, the research team proposed a scientific hypothesis: the benzyl cyanide volatilized by gregarious locusts may be an olfactory warning compound, which can be further synthesized into the poison hydrocyanic acid to defend against predators.

In order to verify this scientific hypothesis, the research team first explored how migratory locusts synthesize phenylacetonitrile. It was found that only gregarious migratory locusts can produce phenylacetaldehyde oxime, the precursor compound of phenylacetonitrile, and it only exists in the epidermis. Solitary migratory locusts cannot produce it, and the biosynthesis of phenylacetonitrile often involves genes of the cytochrome P450 family. Through screening of P450 genes with differences in gregarious and solitary migratory locusts and functional verification, it was proved that the gene named CYP305M2 is the key enzyme for the synthesis of phenylacetonitrile.

The expression of this gene is upregulated as the population density increases. The lack of expression of this gene in solitary locusts prevents the synthesis of phenylacetonitrile and its precursor compound phenylacetaldehyde oxime in solitary locusts. At the same time, pharmacokinetic studies using isotope-labeled phenylalanine and phenylacetaldehyde oxime confirmed that CYP305M2 is the rate-limiting enzyme that catalyzes the first step of the phenylalanine metabolic pathway. It is the difference in the expression of this gene between solitary locusts that only gregarious locusts can produce phenylacetonitrile.

Therefore, if predators want to attack locusts living in groups, they must first overcome the unpleasant smell.

Great tit: I hate the smell of it

To further prove that benzyl cyanide plays a role in olfactory alertness in group defense, the research team used the natural enemy predator of locusts, the great tit, to conduct an interaction study between the two. It was found that when given a choice, the great tit preferred and liked to eat solitary locusts rather than gregarious locusts. By artificially applying benzyl cyanide to solitary locusts, it was found that the great tits refused to attack and eat the solitary locusts treated with benzyl cyanide.

On the contrary, knocking down CYP305M2 expression through RNA interference technology can make gregarious locusts specifically unable to produce phenylacetonitrile without affecting other chemical and body color characteristics, which makes the gregarious locusts attacked more frequently and preferentially eaten by great tits. Therefore, the results show that phenylacetonitrile produced by gregarious locusts reduces bird predation and serves as an olfactory warning signal in group defense.

Synthesis of phenylacetonitrile and hydrocyanic acid from phenylalanine and the response of bird predators to solitary migratory locusts

(Image source: References)

Locust: Don’t mess with me, or I will poison you!

As mentioned earlier, benzyl cyanide is the chemical precursor of hydrocyanic acid, a common toxin in the animal kingdom. In order to determine whether the deterrent effect of phenethyl in gregarious locusts can be attributed to the conversion of benzyl cyanide into the highly toxic hydrocyanic acid, the research team conducted a hydrocyanic acid test on locusts and found that the concentration of hydrocyanic acid released in solitary locusts and undisturbed gregarious locusts was relatively low.

However, the hydrocyanic acid released by gregarious locusts under attack by great tits was 11 times higher than that released by undisturbed gregarious locusts. At the same time, when gregarious locusts were artificially supplemented with benzyl cyanide, the disturbed solitary locusts also released hydrocyanic acid. In short, when gregarious locusts are attacked by birds or disturbed, benzyl cyanide can be converted into highly toxic hydrocyanic acid, indicating that locusts can use benzyl cyanide to warn predators not to act rashly.

This study fully illustrates the collective defense mechanism of locusts. The color of a large number of locusts changes to a black-brown warning color, and the gregarious locusts release unpleasant-smelling benzyl cyanide, which is a precursor of poison and can serve as an olfactory warning signal. When attacked, locusts convert benzyl cyanide into the poison hydrocyanic acid, which effectively resists predators.

Locusts use this swarm defense mechanism against predators, which explains why there aren't large numbers of predators to wipe them out during plagues.

It seems that the wish to rely on eating to deal with the locust plague is indeed difficult to achieve!

Editor: Sun Chenyu

References:

【1】J. Wei et al., Phenylacetonitrile in locusts facilitates an antipredator defense by acting as an olfactory aposematic signal and cyanide precursor. Sci. Adv. 5, eaav5495(2019).