Brain chemical Serotonin behind locusts’ swarming instinct

January 31, 2009

The usually inhibited desert locust Schistocerca gregaria, which wiles away the months as a solitary, insignificant grasshopper can shift into horrifying swarms due to a chemical commonly found in people’s brain, a research showed.

The solitary and gregarious phases of locusts are so different that they were considered distinct species until 1921. Scientists have known for several years that touching a solitary desert locust on the hind legs, or allowing it to see or smell other locusts, is enough to transform it into the gregarious phase. This week, Science magazine published strong scientific evidence that the behavioural and physical makeover is effected by serotonin, a carrier of nerve signals in virtually all animals.

Researchers from the University of Sydney, University of Oxford, and University of Cambridge have pinpointed a single neurochemical - serotonin - as the cause of an instinctive behavioural change from the locusts' solitarious phase to become gregarious and form disastrous swarms of millions.

Serotonin (5-hydroxytryptamine, or 5-HT) is a monoamine neurotransmitter synthesized in serotonergic neurons in the central nervous system (CNS) and enterochromaffin cells in the gastrointestinal tract of animals including humans. Serotonin is also found in many mushrooms and plants, including fruits and vegetables.

In the central nervous system, serotonin plays an important role as a neurotransmitter in the modulation of anger, aggression, body temperature, mood, sleep, human sexuality, appetite, metabolism, as well as stimulating vomiting. Keeping serotonin levels high is the aim of many anti-depressant drugs. "Serotonin profoundly influences how we humans behave and interact," said co-author Dr Swidbert Ott, from Cambridge University. "So to find that the same chemical is what causes a normally shy, antisocial insect to gang up in huge groups is amazing," he explained.

Prior to swarming, the locusts undergo a series of physical changes - their body colour darkens and their muscles grow stronger. The 'Phase change' is at the heart of the locust pest problem, for locusts are one of the world's most destructive insect pests, affecting the livelihoods of 1 in 10 people on the planet. "To effectively control locust swarms, we must first understand exactly how it is that a single shy locust becomes a highly social animal that swarms," said University of Sydney Professor Steve Simpson who led the research for almost 20 years.

The 'phase change' was caused by stimulation of sensory hairs on the hind leg of locusts. Professor Simpson's team began to investigate the neurological and neurochemical basis of this effect. Dr Michael L. Anstey, of the University of Oxford, supervised by Professor Simpson, and Dr Stephen M. Rogers, part of Professor Malcolm Burrows' team at Cambridge, led the research investigating this novel field. "Here we have a solitary and lonely creature, the desert locust. But just give them a little serotonin, and they go and join a gang," said Malcolm Burrows.

Of 13 neurochemicals in locusts that were gregarious (swarming form) and solitarious (non-swarming), the only neurochemical that showed a relationship with social behaviour was serotonin. "It was clear that as locusts switched from solitarious to gregarious, the amount of serotonin in their central nervous systems also increased," explained Professor Simpson. "The next step was to determine if this relationship actually meant that serotonin was the cause of gregarious, and thus swarming, behaviour in locusts," he added.

To do this, the researchers either added serotonin or prevented the production of serotonin in locusts. The results show unequivocally that serotonin is responsible for the behavioural transformation of locusts from solitarious to gregarious. Serotonin was also found to be involved in social behaviour of species across the animal kingdom, including crustaceans, rats, and humans.

The team has found that swarm-mode locusts had approximately three times more serotonin in their thoracic ganglia, part of the central nervous system, than their calm, solitary peers. "The question of how locusts transform their behaviour in this way has puzzled scientists for almost 90 years," said co-author Dr Michael L. Anstey, from Oxford University. "We knew the [physical] stimuli that cause locusts' amazing Jekyll and Hyde-style transformation. But nobody had been able to identify the changes in the nervous system that turn antisocial locusts into monstrous swarms. Now we finally have the evidence to provide an answer," he added.

"The fact that serotonin causes the transition from a shy, antisocial animal into a party animal means that pharmacologically, gregarious locusts are on Ecstasy or Prozac," said Professor Simpson, who also explained that "(whilst a very good idea, in reality) it would be difficult to create a locust control agent that interferes with serotonin."

Professor Simpson's team has significantly discovered that "locusts offer an exemplar of the how to span molecules to ecosystems - one of the greatest challenges in modern science." He also offered an explanation on the problem of using a locust control agent: "Because social behaviour in so many animals depends on serotonin, if we used unspecific serotonin antagonists in the environment, we run the risk of affecting other processes in locusts, as well as severely impacting animals other than locusts. We would need to be sure that locusts have a unique serotonin receptor that causes phase change, which we haven't identified yet. Any locust control agent would have to be specific for this serotonin receptor in locusts."

This study, which was sponsored by the Biotechnology and Biological Sciences Research Council of England, England's Royal Society, the Australian Research Council Federation, and the Natural Sciences and Engineering Research Council of Canada. The scientists that the conclusions of the study will provide a hint as to how to solve the problem of locust infestations, which affect China, Africa, and Australia. Dr. Rogers said the landmark discovery has opened a new area of study into ways of blocking specific serotonin receptors, “something that would allow us to break apart these swarms before they develop.”

Charles Valentine Riley, Norman Criddle, and Sir Boris Petrovich Uvarov were also involved in the understanding and destructive control of the locust. Research at Oxford University has earlier identified that swarming behaviour is a response to overcrowding. Increased tactile stimulation of the hind legs causes an increase in levels of serotonin.

This causes the locust to change color, eat much more, and breed much more easily. Green locusts turn bright yellow and gain large muscles. The transformation of the locust to the swarming variety is induced by several contacts per minute over a four-hour period. It is estimated that the largest swarms have covered hundreds of square miles and consisted of many billions of locusts.

"Locust" is the swarming phase of short-horned grasshoppers of the family Acrididae. The origin and apparent extinction of certain species of locust&mdash;some of which reached 6 inches (15 cm) in length&mdash;are unclear. These are species that can breed rapidly under suitable conditions and subsequently become gregarious and migratory. They form bands as nymphs and swarms as adults — both of which can travel great distances, rapidly stripping fields and greatly damaging crops. Though there are about 8,000 currently known species of grasshoppers, only 12 form locust swarms.

In the history of the insect Desert locust (Schistocerca gregaria) is probably the most important because of its wide distribution (North Africa, Middle East, and Indian subcontinent) and its ability to migrate widely. Adult Desert Locusts grow to between 2-2.5 inches in length, can weigh 0.05-0.07 oz, and are excellent fliers. In religious mythology, the eighth Plague of Egypt in the Bible and Torah, a swarm of locusts ate all the crops of Egypt. "The gregarious phase is a strategy born of desperation and driven by hunger, and swarming is a response to find pastures new," Steve Rogers from Cambridge University emphasises.

The extinction of the Rocky Mountain locust (Melanoplus spretus) in the late 19th century has been a source of puzzlement. Recent research suggests that the breeding grounds of this insect in the valleys of the Rocky Mountains came under sustained agricultural development during the large influx of gold miners, destroying the underground eggs of the locust. That species of locust had some of the largest recorded swarms.

In the 1915 locust plague, which lasted from March to October 1915, locusts stripped areas in and around Palestine of almost all vegetation. This invasion of awesome proportions seriously compromised the already-depleted food supply of the region and sharpened the misery of all Jerusalemites. The plague resulted in several increases to the price of food. On April 25, 1915, the New York Times described the price increases: "Flour costs $15 a sack. Potatoes are six times the ordinary price. Sugar and petroleum are unprocurable and money has ceased to circulate."

In the 2004 locust outbreak, the largest infestation of Desert Locust happened in Western and Northern Africa, affected a number of countries in the fertile northern regions of Africa. These infestations covered hundreds of square miles and involve billions of vegetation-munching insects, which repeatedly devastated agriculture, and cost huge amounts of money to control.

In November, a locusts swarm 3.7 miles (6km) long devastated parts of Australia. Along the process of their active phases, these insects can eat their own bodyweight daily, and can fly swiftly, in swarms of billions covering 60 miles in five to eight hours in search of food. Researchers are now considering the development of sprays that convert swarming locusts back into solitary insects.

“We hope that this greater understanding of the mechanisms causing such a big change in behaviour will help in the control of this pest, and more broadly help in understanding the widespread changes in behavioural traits of animals.” Malcolm Burrows said. However, according to Paul Anthony Stevenson of Germany's University of Leipzig, the discovery will not likely to a short-term pest control solution.

"To be effective, antiserotonin-like chemicals would need to be applied when the animals are solitary locusts and scarce targets in vast expanses of desert -- about three locusts per 100 square meters (1,076 sq ft)," Stevenson explained. "Current serotonergic drugs are not designed for passing through the insect cuticle and sheath encasing the nervous system, nor are they insect-selective, hence their use is ecologically unjustifiable," he added.