Locusts (Insects)

Locusts are medium- to large-sized grasshopper-like insects that form swarms of hundreds of millions of individuals with the potential to migrate long distances in the tropics and subtropics. Locusts differ from grasshoppers in their responses to crowding. Locusts behave as solitary insects immediately after hatching or when maintained in isolation, but if they are forcibly crowded for as little as 6 h they subsequently tend to group together, or exhibit gregarious behavior. In contrast, if grasshoppers are kept in a crowd they usually remain as solitary insects and show no tendency to come together. A few grasshopper species, however, do have some tendency to gregarize when forcibly grouped, although this does not occur naturally. Thus, there is no absolute distinction between a “grasshopper” and a “locust.”
Locusts do not comprise a single taxonomic group. Rather, they occur in three subfamilies of Acrididae, the Cyrtacanthacridinae, Oedipodinae, and Gomphocerinae. Even within a genus, some species exhibit the swarming habits of locusts, while others lack the habit and never swarm. This is most obvious in the genus Schistocerca, where a majority of the American species are non-swarming, and Dociostaurus, with many nonswarming species in Asia. Locusta migratoria, which extends from Australia and eastern Asia to Europe and West Africa, has a number of subspecies, which differ in their propensity to swarm. The species usually regarded as locusts and their distributions are given in Table I .
In addition to the behavioral change, locusts exhibit a marked color change when crowded. In isolation they are often green or exhibit a more or less uniform color matching that of the background; crowded locusts, however, exhibit a striking black and yellow or orange coloration in the nymphal stages. These changes, however, are not peculiar to locusts; similar changes are shown by some grasshoppers. The proportions of different parts of the body also differ between locusts reared in isolation and those reared in crowds. The most striking difference occurs in the migratory locust, where insects reared in isolation have a strongly crested pronotum (upper surface of the first thoracic segment), but in crowded insects the upper surface of the pronotum is saddle shaped.

PHASE THEORY OF LOCUSTS

Locusts do not swarm continuously; periods of swarming may last for several years but are separated by times when no swarms are reported (i.e., recession periods). The mystery of their apparent disappearance during recession periods was solved for L. migratoria by B. P. Uvarov in a paper published in 1921. He proposed the phase theory of locusts, suggesting that during recession periods the insects exist in a form that differs phenotypically and behavio-rally from swarming locusts. He referred to these two forms as the “solitary” (later called “solitarious”) and “gregarious” phases. Locusta in the solitarious phase had, until that time, been placed in a different genus, Pachytylus. Subsequent work showed that similar phases occur in the other locust species. Solitarious locusts are typically cryptically colored, relatively inactive as nymphs (but not necessarily as adults; see later), and live in isolation. Gregarious locusts are conspicuous, with contrasting colors; they form bands (as larvae) or swarms (as adults), and are usually highly mobile. The change from one form to another does not occur in a regular manner, but is dependent on environmental conditions. For example, a period of grouping may increase the tendency of nymphs to group (i.e., to become gregarious), but if they then become isolated again they will tend to lose these characteristics. Consequently, there is no regularity in the timing of outbreaks when swarms occur.

PHASE CHANGE IN THE FIELD

During recessions between outbreaks, solitarious locusts may be very widely distributed, but sometimes these insects are very uncommon. The transformation from solitarious to gregarious involves several discrete phenomena that were first recognized by J. S. Kennedy. Outbreaks are initiated by conditions that favor successful breeding,

leading to an increase in the population size. Then the population becomes concentrated in particular areas as other parts become uninhabitable. This leads to aggregation in which the previously isolated individuals are forced into intimate contact with one another. Finally, in the process of gregarization, the behavior and physiology of the insects is changed, and they now tend to aggregate spontaneously. Concentration, aggregation, and gregarization are generally dependent on a drying out of the habitat following good breeding conditions.
Population increases may occur in any part of the distribution area of the insects, but swarming of most species seems to originate only in what are called outbreak areas. The peculiarity of these areas is that only here do the conditions for population increase, concentration, and aggregation coexist. The migratory locust has only a single outbreak area in Africa, even though the species is widespread and often common in many parts of the continent. This outbreak area is the delta of the middle River Niger in Mali. The area is unique because, in addition to local rain, it receives considerable moisture from precipitation on the mountains of Senegal, the source of the Niger. From the mountains, the river runs inland to a low-lying area in Mali, where it branches to form a delta before flowing southwest through Nigeria to the Atlantic Ocean. The combined effects of rain and river flooding in the delta region produce an extended growing period for vegetation and so enable the locusts to have as many as four generations within a year, whereas elsewhere in Africa the species usually has only two. As a result, huge population increases can occur. However, as the floodplains dry out, suitable areas of vegetation become increasingly restricted, and the insects are first concentrated and then aggregated into smaller areas, where gregarization occurs. Biogeographical analysis of the occurrence of swarms during the last great outbreak of the migratory locust, which lasted from 1930 until 1940, shows clearly that the plague originated from the single outbreak area and spread progressively over Africa south of the Sahara.
The red locust, in southern Africa, unlike the migratory locust, has only a single annual generation. It has several outbreak areas in Tanzania and Zambia that, like the middle Niger, are floodplains. The red locust outbreak areas, however, have either no or very limited outflow of water. As a result, the water that accumulates and sometimes forms a lake has become salty over time. Nymphal development coincides with the rainy season, when extensive flooding produces lush, tall grasslands in which the locusts feed. As the vegetation dies, its distribution becomes more limited, perhaps as a consequence of increasingly saline conditions in the slightly lower parts of the floodplain and as the area of vegetation becomes more restricted, the locusts become concentrated, with the potential to give rise to swarms.
The desert locust differs from these species in that swarms arise in different places depending on the success of breeding and vegetation changes; there is no evidence of any single outbreak area from which the plagues of the 20th century originated.

MIGRATION

Locust swarms fly during the day and, if they are flying close to the ground, often tend to stream in one direction. This is still true at any one position within a high-flying swarm; in the swarm as a whole, however, the orientation of these streams is random. This would rapidly cause the swarm to disperse except that upon reaching the edge of the swarm, individuals turn back into it. It is not known what stimuli produce this behavior, but vision, sound, or even smell may be involved. Because the locusts within the swarm are, effectively,randomly oriented, the swarm itself has no directional movement and is carried downwind. The rate of displacement of swarms flying close to the ground is less than the airspeed because the insects tend to land at intervals, taking off again as the rest of the swarm passes. In high-flying swarms, however, this is not possible. The locusts may be carried on thermals as high as 3000 m above the ground, and then the swarms are displaced downwind at about the speed of the wind. If the winds are light and variable, swarm displacement is negligible. With sustained winds, however, displacements over hundreds or even thousands of kilometers can occur. This behavior is one of the factors enabling the desert locust to survive in some of the most arid regions on earth, the Sahara and Arabian deserts. Downwind displacement takes the insects to areas of wind convergence, where rain is most likely to occur, if it occurs at all, so that the chances of the insects breeding and producing viable offspring are greatly increased. Because wind patterns are not completely reliable, however, this strategy is not always effective. As a result, swarms of desert locusts in West Africa are sometimes carried out into the Atlantic or north to western Europe. The most spectacular recorded flight occurred in October 1988, when huge swarms were carried right across the Atlantic, with large numbers reaching the Caribbean and the northern coasts of South America, a distance of about 6000 km from the insects ‘ source in West Africa.
The bulk of the work leading to our current understanding of swarm behavior was carried out by R. C. Rainey and Z. Waloff, working on the desert locust in the 1950s and 1960s. The assumption is that swarms of other locusts behave in the same way, although the other species do not generally form such massive swarms and are much less well studied.
It is also known that adults of the solitarious phases of at least some locust species migrate, but they do so at night. Evidence for night migration by solitarious individuals exists for Anacridium spp., L. migratoria migratorioides (the African subspecies), Locustana pardalina, and S. gregaria. Nomadacris septemfasciata, on the other hand, appears to be sedentary in the solitarious phase. In this respect, locusts are similar to tropical grasshoppers, many of which are sedentary, whereas a few are known to make extensive night migrations. These solitary migrants, unlike day-flying swarms, deliberately climb to relatively high altitudes (200—500 m above the ground) and then may maintain flight for some hours, although probably a majority of flights are relatively short. In the case of L. m. migratorioides, regular flights occur within the floodplains of the outbreak area and from them to the surrounding semi-arid country, where breeding may occur. Return migrations to the floodplains also occur, and this strategy moves populations with the Inter-Tropical convergence, along which rain is likely. These flights are sometimes downwind, but there is also some evidence from radar observations that the insects can maintain a particular heading despite shifts in wind direction. These seasonal movements make an important contribution to the survival of the insects. Night flights by the Australian plague locust, Chortoicetes terminifera, are also well documented, but these generally are of shorter range.

CONTROL OF PHASE

The physiology of phase change is not yet fully understood. It has been known for some time that grouping can be induced in isolated nymphs by touching individuals with fine wires dangling from a rotating circle, indicating that it is primarily physical contact with other locusts that initiates gregarization. More recent work has shown that touching the hind femora is more effective than touching other parts of the body. Presumably, the effects are registered by mechanoreceptors on the femora, leading to a change in the nervous system that alters the insect’s behavior toward gregariousness. It is very likely, though not yet proved, that this sequence involves neuro-modulators. A peptide hormone that enters the hemolymph via the corpora cardiaca induces the dark coloration of gregarious nymphs.
Pheromones play a part in the maintenance of gregarization. A number of experiments indicate that gregarious locusts of both sexes produce a gregarization pheromone. In adult desert locusts, benzal-dehyde, veratrole, guaiacol, phenol, and phenylacetonitrile are its major components. This pheromone enhances the tendency to group as well as having some effect on color change. Solitarious locusts do not produce the full suite of compounds in comparable concentrations. It has been shown that the chemicals are produced from plant material ingested by the locusts and that bacteria are responsible for their production. Locusts reared on axenic (microbe-free) diets do not produce the pheromone. Mature males in the gregarious phase of both the desert and migratory locusts produce from epidermal glands a pheromone that accelerates maturation of insects of either sex. The major component of this pheromone in the desert locust is phenylacetonitrile. Its effect under natural conditions is, presumably, to tend to synchronize oviposition by the individuals in a swarm, which increases the likelihood that the first-stage nymphs, when they hatch, will be present in large numbers and so will be likely to interact with each other and gregarize. A chemical produced in the accessory glands of gregarious females of the desert locust promotes gregarious behavior and coloration in the nymphs hatching from the eggs; solitarious females do not produce the chemical. The chemical is contained in the frothy material that forms a plug above the egg mass and that is interpolated in spaces between the eggs. There is thus a marked intergenerational effect of phase with gregarious females producing offspring that already have some characteristics of gregarious individuals.

EVOLUTION OF SWARMING BEHAVIOR

It was once thought that the contrasting coloration of gregarious nymphs was likely to have a function in promoting gregarious behavior, but experimental evidence does not support this. Recent studies with the desert locust show that when the locusts feed on plants containing deterrent chemicals, such as the alkaloid hyoscyamine, predaceous lizards rapidly learn to avoid individuals with gregarious coloration but do not avoid solitariously colored nymphs even when they have eaten the same food. Other plants in the desert areas that are the habitat of S. gregaria also contain potentially noxious compounds, and it may be that the gregarious coloration results from selection for warning coloration. This, in turn, may have led to gregarious behavior, since aposematic insects commonly group together. Whether similar arguments can be applied to other locust species is not known.
The tendency to migrate is clearly an adaptation to living in arid habitats, enabling the insects to colonize new areas before the initial food supply is totally depleted. This is most clearly seen in the desert locust. Because some grasshoppers in these same habitats exhibit annual migrations, and some solitary locusts are also known to migrate, it must be supposed that swarm migrations arose from these individual movements. This, however, involved a switch from nighttime migration within the insects’ boundary layer, where flight can be directed by the insect, to daytime flight that is often outside the boundary layer and displacement is largely determined by the wind.