Scientists identify pheromone that triggers locust swarming and a way to block it

Human societies have struggled to fend off locust infestations for millennia. The insects’ destructive effects persist to this day, especially when they collect in large swarms and eat through thousands of hectares of crops in a matter of days. Such swarms have occurred once every few years of late. Most recently, in 2019-2020, a record number of locusts emerged in East Africa and eventually passed through Pakistan and India, making it the region’s worst infestation in 25 years.

In the last century or so, experts and farmers have tried to control locusts using synthetic pesticides, but unfortunately they also damage the land, food security, and the environment. Thus finding suitable, eco-friendly alternatives to pesticides has been an active area of research.

In a new proof of concept, researchers from the Institute of Zoology at the Chinese Academy of Sciences in Beijing, have shown that it’s possible to manipulate pheromones released by locusts to prevent them from swarming or engaging in group behaviour that leads to the feeding frenzy.

The team was able to identify the pheromone responsible for triggering swarming and also tested a candidate molecule to block its function.

The study, published in Nature on June 25, also recommended more research to identify other molecules that can safely keep locusts from swarming, including at large scales. Overall, the study offers potentially one of the earliest pollution-free solutions for locust control.

Jiving to jump

Several animal, bird, and insect species — including locusts — exhibit a social behaviour called gregariousness: it helps them form societies in which large numbers of individuals work together, instead of competing, in order to survive. In the first phase of their lives, individual locusts are solitary creatures; then they transition to their gregarious phase and begin to collect and operate in physical groups, including feeding together.

Scientists have sought to identify the hormones that trigger this behaviour for many decades now. In fact the same team behind the new study had identified a pheromone of interest, called 4-vinylanisole (4VA), in 2020.

After a locust eats food, it often emits large quantities of 4VA from its hind legs. This hormone is an aggregation pheromone: it promptly begins to attract other members of the species when it’s released into the air. Other locusts nearby subsequently collect together and rub their hind legs against each other. This in turn triggers the release of serotonin, a neurotransmitter, which leads to swarming.

In the new study, the researchers figured that preventing locusts from releasing 4VA could potentially prevent swarming, so they set to work on understanding its production.

Locusts release 4VA only after they eat, which means certain molecules in the plants that locusts feed on could be triggering its production. The researchers figured right: the culprit was a compound called phenylalanine.

When locusts digested phenylalanine, two enzymes — mainly 4VPMT1 and 4VPMT2 less so — were found to be responsible for converting the non-aggregating pheromone 4VP in solitary locusts into the aggregating pheromone 4VA.

To confirm the link, the researchers turned to genetic engineering. When they deactivated the gene that encoded for 4VPMT1, the insects stopped transitioning from their solitary to gregarious phases and didn’t exhibit any swarming tendencies.

Molecular deactivation

The researchers also studied how the 4VP molecule bound to the 4VPMT1 enzyme and the amino acids on its structure. Then they identified chemically similar molecules that could bind to the enzyme. When they did, they’d block the receptor for the 4VP molecule, thus stopping enzyme activity and preventing it from converting to 4VA.

Among the many molecules the researchers studied, they found 4-nitrophenol (4NP) fit the two 4VPMTs’ binding sites the best as well as prevented the biosynthesis of 4VA.

Xiaojiao Guo, the first author of the paper and insect behaviour researcher at the State Key Laboratory of Integrated Management of Pests and Rodents with a focus on locusts, said locusts’ bodies could synthesise the 4VA in only two steps, so the team needed a way to precisely regulate the expression of the 4VPMT enzymes and quickly halt the release of 4VA.

“The two 4VPMTs are key enzymes in the biosynthesis of 4VA and are important targets for inhibiting locust aggregation,” Guo said. “It’s worth noting that the binding affinity of 4NP to the 4VPMTs is higher than that of 4VP, thus it can competitively occupy the enzyme’s active site.”

“From the perspective of protein structural characteristics, the specific interaction between 4NP and 4VPMTs ensures the selectivity of the inhibitor and minimizes the off-target effects when interfering with other metabolic pathways. Therefore, the small molecule regulation of 4VA biosynthesis is an efficient strategy for sustainable locust plague management,” she added.

There is one catch, however: nitrophenols can be dangerous in an open environment.

Industries widely use compounds like 4-nitrophenols to make dyes, darken leather, and manufacture drugs — and in fungicides and insecticides. The compounds are toxic and are often detected in polluted water and in hazardous waste. They also persist in the environment for a while — roughly two weeks in soil and over two months in sea water — and have shown to irritate the eyes, skin, and airways in humans.

“As an alternative to small-molecule inhibitors, RNAi insecticides targeting 4VPMTs could also be developed to control locust swarming behaviours,” the team wrote in the published paper. RNAi is a process in which RNA molecules are used to prevent genes from being expressed inside cells, preventing the corresponding proteins (including enzymes) from being produced.

Non-toxic insecticides

In a swarm, the millions of locusts eat their own body weight in food and can fly more than 150 km in a day.

Human attempts to tame these swarms go back thousands of years, and have taken forms like creating noise and smoke and even shooting arrows. In the 19th century chemical insecticides came to the fore. Even today, spraying locust swarms in the air with insecticides is still the most commonly used method, and its efficacy is unclear.

The 2019-2020 swarm originated in East Africa after heavy rains and floods created the right conditions for dormant locust eggs to come to life, rendering an 8000-fold increase in the insects’ numbers. The havoc they subsequently wrought reminded the world to develop an effective control strategy.

In one response, for example, scientists from 34 organisations worldwide penned an article in Journal of Orthoptera Research detailing major topics of interest vis-à-vis swarming behaviour and organisational weaknesses in the field that allowed the problem to persist. As alternatives to 4NP, this paper identified seven candidate compounds for further study.

Likewise, the Guo et al. study also proposed a five-step locust control strategy: using synthetic or other 4VA substitutes to attract locusts to a trapping area, where they can be killed by fungal pathogens or pesticides at a small scale; spraying 4VA to prevent aggregation; monitoring population dynamics by tracking 4VA signatures; releasing genetically modified locusts into the field to establish non-gregarious populations; and using the combined strategy of small-molecule regulators in conjunction with biopesticides.

Sandhya Ramesh is a freelance science journalist.