The physiology of locust phase polymorphism: an update

The considerable progress made between 1990 and 1997 in locust phase-related research and in understanding the physiology of locust phase polymorphism is reviewed. The traits of locust phases are discussed and it is concluded that there are distinct strain-dependent differences in phase characteristics and their amplitudes even in the same species. Despite some advances, no major break-through was achieved in the putative endocrine control of locust phase polymorphism. Phase-dependent differences in adipokinesis, flight fuels and migration of adult locusts, as well as novel methods in studying aggregation behaviour and activity of hoppers and adults, opened new lines in research of the physiology of locust phase polymorphism. Marked advances were made in phase-related locust pheromone research, revealing, in Schistocerca gregaria, differences between the pheromonal system of the hoppers and that of the adults. These systems turned out to be more complex than previously assumed. Phenylacetonitrile, produced by sexually mature adult males, serving both as an attractant and a mutration-accelerating factor, was identified as the major compound of the adult pheromonal system in S. gregaria. A new aspect of transmission of phase characteristics from parent to progeny through the foam (froth) of the egg pod was revealed. Effects of some plant substances on locust phases were reported. However, no research has yet been published on the aspects of molecular biology of locust phase polymorphism.     

Structure and physiology of the locust femoral chordotonal organ

The connective chordotonal organs (COs) in the femora of the prothoracic and mesothoracic legs of the locust Schistocerca gregaria are divided into two parts, the proximal and the distal scoloparia. The proximal scoloparium contains about 150 small neurons and is anchored to the femoral cuticle. The distal scoloparium contains about 50 larger neurons and is connected at its proximal end to both the cuticle and the flexor tibiae muscle.Records were made from the distal scoloparium, classifying units by spike size. The tibial position/total activity response curve is ∪-shaped but when a small number of units is selected the responses occur only when the tibia is on one side of its centre position. The tonic responses display considerable hysteresis and a degree of adaptation which varies with the tibial angle. Units with phasic and phasic-tonic responses are common and their responsiveness depends on the range of angles the tibia is moved through. The same units respond strongly to flexor tibiae contraction with the tibia either fixed or free, and so may serve as receptors for tension in that muscle.The CO mediates phasic resistance reflexes in all three extensor tibiae motoneurons and tonic reflexes in the extensor ‘slow’ neuron. It is suggested that the very detailed information furnished by the CO is used in a complex way in the control of the femoral muscles.     

The generation of DPOAEs in the locust ear is contingent upon the sensory neurons

Tympanal organs of insects emit distortion-product otoacoustic emissions (DPOAEs) that are indicative of nonlinear ear mechanics. Our study sought (1) to define constraints of DPOAE generation in the ear of Locusta migratoria, and (2) to identify the sensory structures involved. We selectively destroyed the connection between the (peripheral) sensory ganglion and the tympanal attachment points of the “d-cell” dendrites; d-cells are most sensitive to sound frequencies above 12 kHz. This led to a decrease of DPOAEs that were evoked by f ₂ frequencies above 15 kHz (decrease of 15–40 dB; mean 28 dB; n = 12 organs). DPOAEs elicited by lower frequencies remained unchanged. Such frequency-specific changes following the exclusion of one scolopidial sub-population suggest that these auditory scolopidia are in fact the source of DPOAEs in insects. Electrical stimulation of the auditory nerve (with short current pulses of 4–10 μA or DC-currents of 0.5 μA) reversibly reduced DPOAEs by as much as 30 dB. We assume that retrograde electrical stimulation primarily affected the neuronal part of the scolopidia. Severing the auditory nerve from the central nervous system (CNS) did not alter the DPOAE amplitudes nor the effects of electrical stimulation.     

The association of serotonin with the alimentary canal of the African migratory locust, Locusta migratoria: distribution, physiology and pharmacological profile

The association of serotonin with the alimentary canal of Locusta migratoria was investigated using immunohistochemistry and high performance liquid chromatography (HPLC) coupled to electrochemical detection. Serotonin-like immunoreactive processes were differentially distributed between and within three regions of the alimentary canal; the foregut, midgut and hindgut. The midgut possessed the most serotonin-like immunoreactive processes, while the hindgut contained only a few immunoreactive processes. Using HPLC coupled to electrochemical detection the serotonin content was highest in the midgut followed by the foregut and hindgut. The physiological response of the midgut to serotonin as well as to the combination of serotonin and proctolin was also examined. It was found that the application of serotonin to the midgut leads to a dose-dependent reduction in tonus of the circular muscles. Serotonin was also able to inhibit a proctolin-induced contraction of the midgut in a dose-dependent manner. The physiological and pharmacological properties of serotonin agonists and antagonists on the midgut were also investigated. The results indicate that alpha-methyl 5-HT was the most effective agonist leading to a 108% relaxation at 10(-9) M compared to that caused by the same serotonin concentration. Among several serotonin receptor antagonists tested, mianserin was the most potent. The application of mianserin at 10(-5) M in combination with 5x10(-6) M serotonin resulted in a 66% reduction of the serotonin-induced relaxation of midgut muscle. The serotonin antagonist cyproheptadine was less effective leading to a 39% reduction of the 5x10(-6) M serotonin-induced relaxation. Ketanserin was a weak antagonist.     

The locust foraging gene

Our knowledge of how genes act on the nervous system in response to the environment to generate behavioral plasticity is limited. A number of recent advancements in this area concern food‐related behaviors and a specific gene family called foraging (for), which encodes a cGMP‐dependent protein kinase (PKG). The desert locust (Schistocerca gregaria) is notorious for its destructive feeding and long‐term migratory behavior. Locust phase polyphenism is an extreme example of environmentally induced behavioral plasticity. In response to changes in population density, locusts dramatically alter their behavior, from solitary and relatively sedentary behavior to active aggregation and swarming. Very little is known about the molecular and genetic basis of this striking behavioral phenomenon. Here we initiated studies into the locust for gene by identifying, cloning, and studying expression of the gene in the locust brain. We determined the phylogenetic relationships between the locust PKG and other known PKG proteins in insects. FOR expression was found to be confined to neurons of the anterior midline of the brain, the pars intercerebralis. Our results suggest that differences in PKG enzyme activity are correlated to well‐established phase‐related behavioral differences. These results lay the groundwork for functional studies of the locust for gene and its possible relations to locust phase polyphenism. © 2010 Wiley Periodicals, Inc.     

The stabilization of locust cuticle

Cuticle from the metathoracic femur of adult locusts (Locusta migratoria) is characterized with respect to changes in water content and in protein extractability during maturation. The swelling behaviour and extractability of fully-sclerotized cuticle are compared to those of chemically-modified, unsclerotized cuticle.It is concluded that although dehydration may contribute to the stabilization of cuticle, it cannot account for the observed differences. The properties of mature cuticle can best be explained by the assumption that covalent cross-links are present between protein molecules.     

The control of meal termination in the locust

The relationship between the amount eaten during a meal, meal duration and ingestion rate was investigated in the locust, Locusta migratoria (L.). The results suggested a relatively simple model for the control of meal termination whereby a variety of exogenous and endogenous factors, including chemosensory stimuli provided by the food, the presence of other locusts nearby, age and deprivation-related factors, are integrated within the central nervous system and together contribute to the level of excitation present at the start of a meal. The amount of excitation determines both the mean rate of ingestion during the meal and the amount of inhibition needed to end the meal. Since much of the inhibitory feedback comes from gut stretch, meal size and mean ingestion rate are positively correlated, in fact increasing proportionally, and, hence, meal duration remains constant. At high levels of excitation, however, ingestion becomes rate limited and meal duration subsequently increases proportionally with meal size. Changes in the rate of ingestion throughout a meal were also investigated. The rate declined exponentially but, unlike in the rat, the initial ingestion rate remained constant with changes in excitation and the decay function varied such that small meals began at the same ingestion rate as large meals but the rate of decline was subsequently faster.     

The hormonal content of the locust corpus cardiacum

Summary The amounts of adipokinetic and diuretic hormone in the separate storage and glandular lobes of the locust corpora cardiaca during the imaginal moult and up to the onset of sexual maturation have been measured. The levels of the hormones are high prior to the imaginal moult, fall at emergence and increase during the somatic growth period. The effects of surgical interference with the neuroendocrine system upon the hormonal content of the corpora cardiaca have been investigated. Cautery of the brain neurosecretory cells or allatectomy in mature locusts has no effect on the content of adipokinetic hormone. Diuretic hormone is absent from the storage lobes of locusts deprived of their cerebral neurosecretory cells but normal levels are present in the corpora cardiaca of allatectomised animals. Severance of the nervus corporis cardiacum I and II reduces the level of diuretic hormone in the storage lobes of the corpora cardiaca but is without effect on the levels of adipokinetic hormone in the glandular lobes. This work is supported by grants from the Science Research Council and the Royal Society.