Effect of Paranosema locustae (Microsporidia) on the behavioural phases of Locusta migratoria (Orthoptera: Acrididae) in the laboratory

The ability of parasites to modify the behaviour of their hosts is a wide spread phenomenon, but the effects of microsporidian parasites on locust behaviour remain unexplored. Here the frequencies of directional changes (ND) and jumping (NJ) per minute of gregarious locusts infected with 2000 spores of the microsporidian parasite Paranosema locustae were significantly different from those of untreated locusts 10 and 16 days after infection, being similar to values for solitary nymphs. In contrast, the behaviour of locusts inoculated with the lower doses of 200 spores/locust was sometimes like that of solitary nymphs. At other times, behaviour was intermediate between solitary and gregarious, i.e. transitional. The rearing density did not affect the turning and jumping behaviour of infected locusts, and their behaviours were similar to those of solitary locusts at 10–16 days after infection. Our study demonstrates that infection with P. locustae may lead gregarious locusts to change some of their behaviour to that typical of solitary locusts.     

Modelling locust foraging: How and why food affects group formation

Locusts are short horned grasshoppers that exhibit two behaviour types depending on their local population density. These are: solitarious, where they will actively avoid other locusts, and gregarious where they will seek them out. It is in this gregarious state that locusts can form massive and destructive flying swarms or plagues. However, these swarms are usually preceded by the aggregation of juvenile wingless locust nymphs. In this paper we attempt to understand how the distribution of food resources affect the group formation process. We do this by introducing a multi-population partial differential equation model that includes non-local locust interactions, local locust and food interactions, and gregarisation. Our results suggest that, food acts to increase the maximum density of locust groups, lowers the percentage of the population that needs to be gregarious for group formation, and decreases both the required density of locusts and time for group formation around an optimal food width. Finally, by looking at foraging efficiency within the numerical experiments we find that there exists a foraging advantage to being gregarious.     

Composition and emission dynamics of migratory locust volatiles in response to changes in developmental stages and population density

Chemical communication plays an important role in density‐dependent phase change in locusts. However, the volatile components and emission patterns of the migratory locust, Locusta migratoria, are largely unknown. In this study, we identified the chemical compositions and emission dynamics of locust volatiles from the body and feces and associated them with developmental stages, sexes and phase changes. The migratory locust shares a number of volatile components with the desert locust (Schistocerca gregaria), but the emission dynamics of the two locust species are significantly different. The body odors of the gregarious nymphs in the migratory locust consisted of phenylacetonitrile (PAN), benzaldehyde, guaiacol, phenol, aliphatic acids and 2,3‐butanediol, and PAN was the dominant volatile. Volatiles from the fecal pellets of the nymphs primarily consist of guaiacol and phenol. Principal component analysis (PCA) showed significant differences in the volatile profiles between gregarious and solitary locusts. PAN and 4‐vinylanisole concentrations were significantly higher in gregarious individuals than in solitary locusts. Gregarious mature males released significantly higher amounts of PAN and 4‐vinylanisole during adulthood than mature females and immature adults of both sexes. Furthermore, PAN and 4‐vinylanisole were completely lost in gregarious nymphs during the solitarization process, but were obtained by solitary nymphs during gregarization. The amounts of benzaldehyde, guaiacol and phenol only unidirectionally decreased from solitary to crowded treatment. Aliphatic aldehydes (C7 to C10), which were previously reported as locust volatiles, are now identified as environmental contaminants. Therefore, our results illustrate the precise odor profiles of migratory locusts during developmental stages, sexes and phase change. However, the function and role of PAN and other aromatic compounds during phase transition need further investigation.     

Social aggregation of adult Schistocerca gregaria and Locusta migratoria migratorioides in relation to the final moult and ageing

Laboratory experiments, were carried out on nymphs and adults of the desert locust, Schistocerca gregaria, and the African migratory locust, Locusta migratoria migratorioides, in view of the field observation that locusts become temporarily less gregarious after the final moult. The experiments showed no reduction in grouping after the final moult but did show a reduction in grouping in mature Schistocerca. There was little change in the numbers of locusts found in small groups but a dramatic reduction in the number found in large groups.     

A miniaturized assay to quantify effects of chemicals or physical stimuli upon locust activity

Solitary and gregarious locusts differ in many traits, such as body color, morphometrics and behavior. With respect to behavior, solitary animals shun each other, while gregarious animals seek each other＇s company, hence their crowding behavior. General activity, depending on the temperature, occurs throughout the day but is much lower in solitary locusts. Solitary locusts occasionally fly by night while gregarious locusts fly regularly during daytime （swarming）. In search of new assays to identify substances that control or modify aspects of （phase） behavior, we designed a simple activity assay, meant to complement existing behavioral measurement tools. The general activity is reflected in the number of wall hits, that is, the number of contacts between the locust and the vertical walls of a small arena. Using this single parameter we were able to quantify differences in total activity of both nymphs and adults of isolation-reared （solitary）, regrouped- and crowdreared （gregarious） locusts under different conditions. Furthermore, we demonstrate that there are inter- and intra-phase dependent differences in activities of 5th instar nymphs afar injections of the three different adipokinetic hormones.     

Effects of juvenile hormone treatment on phase changes and pheromone production in the desert locust,Schistocerca gregaria (Forskal) (Orthoptera: Acrididae)

The roles of juvenile hormone III (JH III) on phase changes and pheromone production were examined in laboratory-reared gregarious desert locust, Schistocerca gregaria (Forskal). The hormone was applied to 5th instar nymphs and newly emerged adult locusts. Generally, the 5th instar nymphs exhibited a higher sensitivity to hormone treatments than the adults. Hormone applications inhibited pheromone production (as measured by the amounts of phenylacetonitrile released). In addition, JH III had a significant effect on the external colouration and absorbance ratios of the haemolymph pigments. It is concluded that the effects of exogenous JH III on gregarious locusts represent a shift towards the solitarious phase.     

Central nervous processing of behaviourally relevant odours in solitary and gregarious fifth instar locusts, Schistocerca gregaria

Physiological and morphological characteristics of antennal lobe neurons of solitary and gregarious fifth-instar nymphs of the desert locust, Schistocerca gregaria, were studied using intracellular recording and staining techniques. Physiological characteristics of antennal lobe neurons of both locust phases responding to stage-dependent aggregation pheromones, egg-laying attractants, a putative sex pheromone and plant-associated volatiles are described. Antennal lobe neurons showed excitatory, inhibitory, combined excitatory and inhibitory and delayed responses. In addition, one neuron␣showing an initial inhibition followed by an excitation and inhibition response was found. Pheromone-specific-, plant-specific- and pheromone-plant-generalist neurons were found in both locust phases. Antennal lobe neurons displayed stage- and phase-dependent differences in the processing of aggregation pheromone component input. Nymphal antennal lobe neurons showed stage-dependent response characteristics highly correlated with the preferential behavioural attraction to the nymphal aggregation pheromone. Phase-dependent differences were found in the response spectra and the sensitivity of the same neuron types. Neurons of solitary locusts responded significantly more frequently to some of the tested components than neurons of gregarious locusts. Furthermore, antennal lobe neurons of solitary locusts showed a higher sensitivity to most of the tested compounds. Accepted: 4 July 1998     

Disruption of aggregation behaviour of oriental migratory locusts (Locusta migratoria manilensis) infected with Nosema locustae

Abstract:  The effect of Nosema locustae infection on the aggregation behaviour of the oriental migratory locust, Locusta migratoria manilensis , was studied using a two-choice arena olfactometer and electroantennography (EAG). Infected locusts had low antennal sensitivity and aggregation responses to faecal extracts and to locust body volatiles. Infected fifth instar nymphs had significantly lower aggregation index than the uninfected nymphs, although with fourth instars the effect on aggregation behaviour only occurred in infected females. With regard to antennal receptor sensitivity, infected adult locusts had significantly lower EAG amplitudes in response to extracts from faeces of the adult males. The effect was most pronounced in female locusts. In contrast, there was no significant difference in the EAG responses between the fifth instar male and female nymphs. Further analysis revealed that EAG responses of fifth instar nymphs and adults infected with N. locustae to the faecal extract and volatiles from fifth instar solitary-reared nymphs were not significantly affected. In contrast, infected nymphs and adults had remarkably low EAG amplitudes for the remaining stimuli.     

Social determinants of aggregation behaviour in adults of the desert locust

The social aggregation behaviour of adults of the desert locust Schistocerca gregaria, was found to be determined by rearing density, in the same way but not to the same extent as that of nymphs. Adult locusts reared crowded since hatching showed more social grouping than adults reared in isolation. For adults, the least amount of grouping was shown by isolates, F₁ of solitaria caught in the field. Both nymphs and adults were found to be attracted to the edge of the testing arena in inverse proportion to their attraction to each other. This edge effect could be used as one behavioural measure of phase polymorphism complimentary to the measure of social aggregation. Unlike nymphs, adults did not rapidly learn to group when forced into contact with one another. Grouping of isolated adults was not found to change with age.     

Phase-related morphological changes induced by [His7]-corazonin in two species of locusts, Schistocerca gregaria and Locusta migratoria (Orthoptera: Acrididae)

The effects of a neurohormone, [His(7)]-corazonin, on phase-related morphological traits (F/C and E/F ratios; F = length of the hind femur, C = maximum width of the head; E = length of fore wing) were re-examined in the desert locust, Schistocerca gregaria Forsk?l. The F/C ratio was significantly different between adults with five and six nymphal instars, respectively, indicating that they need to be analysed separately. Injections of the synthesized peptide (1 nmol) into individually-reared (solitary) nymphs at the second and third instars caused a shift in classical morphometric ratio towards the value typical for crowded (gregarious) individuals in both sexes. The E/F ratio, which is smaller in solitary locusts than in gregarious ones, was also influenced significantly by injections of [His(7)]-corazonin into individually-reared locusts. The effect of [His(7)]-corazonin on E/F ratios was shown more clearly when the nymphs were injected at a higher dose (2 nmol) at the beginning of the third instar. Single injections of the peptide into individually-reared nymphs at different instars revealed that the earlier the injection the larger the 'gregarizing' effects of the peptide on F/C and E/F ratios. The same tendency was also detected in Locusta migratoria Linnaeus. These results supported the hypothesis that [His(7)]-corazonin plays an important role in the control of phase polymorphism in locusts.     

Stimuli inducing gregarious colouration and behaviour in nymphs of Schistocerca gregaria

Solitarious nymphs of Schistocerca gregaria were reared under various conditions in both Jerusalem and Oxford to tease apart cues involved in behavioural and colour phase change. Treatments included rearing nymphs from the IInd or IIIrd until the final nymphal stadium in physical contact with similarly aged conspecific groups or with another locust species, Locusta migratoria migratorioides, as well as confining single nymphs in mesh cages, which were kept within crowds of S. gregaria or L. migratoria migratorioides, providing visual and olfactory but no physical contact with other locusts. In the Oxford experiments, an extra treatment was included which provided olfactory cues without visual or contact stimulation. Our results confirm that transformation from the solitarious to the gregarious phase of locusts is complex, and that different phase characteristics not only follow different time courses, but are also controlled by different suites of cues. As predicted from earlier studies, behavioural phase change was evoked by non-species-specific cues. Rearing in contact with either species was fully effective in inducing gregarious behaviour, as was the combination of the sight and smell of other locusts, but odour alone was ineffective. Colour phase change was shown to comprise two distinct elements that could be dissociated: black patterning and yellow background. The former of these could be induced as effectively by rearing S. gregaria nymphs in a crowd of L. migratoria migratorioides as by rearing with conspecifics. Sight and smell of other locusts also triggered black patterning and, unlike behavioural change, some black patterning was induced by odour cues alone. Hence, physical contact was not needed to induce gregarious black patterning. Yellow colouration, however, was only fully induced when locusts were reared in contact with conspecifics, implying the presence of a species-specific contact chemical cue.     

Do desert locust hoppers develop gregarious characteristics by watching a video?

Various sensory stimuli have been suggested to induce gregarious body coloration in locusts, but most previous studies ignored the importance of substrate color. This study tested the effects of visual, olfactory and tactile stimuli from other locusts on the induction of gregarious body coloration in single (isolated-reared) Schistocerca gregaria nymphs housed in yellow-green cups. Odor from gregarious (crowd-reared) locusts, which is believed to induce black patterns in single locusts, had little effect when applied to visually isolated nymphs at the 2nd stadium onward, and all test nymphs remained green without black patterns at the last stadium, as in controls reared without odor and visual stimuli. Visual stimuli alone induced black patterns when a single solitarious nymph was allowed to see other locusts in another cup. The degree of black patterns increased as the number of locusts shown increased, and some test nymphs developed body coloration typically observed in gregarious forms. A classical morphometric ratio (hind femur length/head width) shifted toward the value typical of gregarious forms when the single nymphs were allowed to see 5 or 10 locusts. Single nymphs also developed black patterns when presented green conspecific nymphs and adults of two hemipteran species kept in another cup. No synergetic effects of visual and odor stimuli were detected. Movies of locusts, crickets and tadpoles were found effective in inducing black patterns in single locusts. Ontogenetic variation in the sensitivity to crowding and experimental methodology might be responsible for some discrepancies in the conclusions among different researchers.     

Is there an intraspecific role for density-dependent colour change in the desert locust?

Attempts to uncover the adaptive significance of density-dependent colour polyphenism in the desert locust, Schistocerca gregaria (Orthoptera: Acrididae), have been unsuccessful. Desert locust juveniles can change colour as part of a phenotypically plastic response to changes in local population density known as phase polyphenism. They are typically cryptic in colour at low rearing density (solitarious phase), but become conspicuous at high density (gregarious phase). Recent evidence indicates that this colour change functions interspecifically as an aposematic signal. Other recent evidence, however, suggests that previous attempts to demonstrate an intraspecific function of gregarious coloration in mediating group interactions among locusts may have been confounded by the effects of multiple sensory cues. We reinvestigated the intraspecific function of density-dependent colour polyphenism and specifically controlled for potentially confounding olfactory and tactile cues. We found no effect of gregarious phase (yellow and black) coloration as either a gregarizing stimulus to behaviourally solitarious locusts or as a visual aggregation stimulus behaviourally to gregarious locusts. We did, however, find that nonmoving solitarious phase (green) coloration significantly increased the activity levels of behaviourally gregarious locusts. We cannot explain this result and its biological relevance remains unknown. In the absence of support for the intraspecific visual cue hypothesis, we favour an aposematic perspective on the function of density-dependent colour polyphenism in the desert locust. The aposematic perspective parsimoniously accounts for density-dependent changes in both colour and behaviour. Copyright 2000 The Association for the Study of Animal Behaviour.     

Phase-dependent locomotor activity in first-stadium nymphs of the desert locust, Schistocerca gregaria: effects of parental and progeny rearing density

This study examined the effects of parental and progeny rearing density on locomotor activity of 1st-stadium nymphs of the desert locust, Schistocerca gregaria, using an actograph. Progeny obtained from solitarious (isolated-reared) or gregarious (crowd-reared) locusts were reared in isolation or in a group of 30 nymphs. Crowding after hatching had a slight influence on mean activity shortly after the start of measurements, but no clear effect was detected until day 2, when maximum activity during the 6-24 h of observation was significantly higher than that of the nymphs kept in isolation. On the other hand, the effects of parental rearing density on locomotor activity manifested at all ages examined (0-2 days old). Progeny of gregarious locusts showed consistently higher activity than those of solitarious locusts. In newly hatched nymphs, the effect of parental rearing density was explained by variation in body size at hatching, one of the phase-dependent characteristics. Hatchling body color was also correlated with locomotor activity and body weight. Similar levels of locomotor activity were exhibited when green, solitarious and black, gregarious nymphs were similar in body weight. These results suggested that parental rearing density indirectly influences locomotor activity in the progeny shortly after hatching by affecting their body size as eggs or hatchlings.     

Innate phase behavior in the desert locust,Schistocerca gregaria

Abstract Detailed aspects of the transition from the solitarious to the gregarious phase in the framework of locust ecology are undoubtedly most important for understanding locust phase polyphenism. Nevertheless, due to obvious difficulties in studying the solitarious phase in nature, such information is limited and mostly available from research carried out under laboratory conditions. In the current study, we examined the dispersal patterns of newly hatched locust nymphs in a laboratory setup that simulated seminatural conditions. This was carried out with no previous manipulation of the nymphs other than controlling their parental density. We comparatively tested the spatial distribution of newly hatched nymphs on perches located at different ranges within an emergence arena, and the expected Poisson (random) distribution. Hatchlings were found to disperse among the perches in a pattern significantly different from that expected by random. Irrespective of their parents’ phase, the observed distributions of all nymphs were clearly clumped, similar or close to those expected for gregarious locusts. It seems that rather than emerging with a parentally derived and predetermined phase, hatchlings have an independent default or innate behavioral state, which reflects at least tolerance if not attraction to conspecifics. The typical phase behavior may later become dominant under the appropriate environmental conditions. These results imply novel perspectives on locust phase transformation, which contribute to our understanding of the formation of locust crowds under field conditions. These should be considered in any rationale for developing a preventative management strategy of locust populations.     

Differences in numbers of sensilla on the antennae of solitarious and gregarious Locusta migratoria L. (Orthoptera: Acrididae)

It has been assumed that differences in the behaviour of solitarious and gregarious locusts arise from differences in the central nervous processing of information, and that no essential differences occur in the sensory systems. This investigation reveals that solitarious adults and fifth instar nymphs of Locusta migratoria (Orthoptera: Acrididae) have more olfactory sensilla on the antennae than comparable gregarious phase insects. Behavioural differences could thus arise as a result of different peripheral inputs. It is suggested that social facilitation, resulting from the gregarious habit, permits a decrease in individual sensitivity with an associated reduction in the numbers of olfactory sensilla. The numbers of contact chemoreceptors are proportional to the lengths of the antennal annuli and do not differ greatly between the phases.     

Small-scale vegetation patterns in the parental environment influence the phase state of hatchlings of the desert locust

Desert locusts (Schistocerca gregaria Forskål (Orthoptera: Acrididae)) change phase in response to population density. Solitarious insects avoid one another; when crowded, they shift to the gregarious phase and aggregate. Laboratory experiments and individual‐based modelling have shown that small‐scale resource distribution can affect locust phase state via an influence on crowding. Laboratory work has also shown that parental phase state is transmitted to offspring via maternal inheritance. These effects had not been investigated in the field previously. We maintained small populations of adult desert locusts in semi‐field enclosures with different distribution patterns of a single plant species (Hyoscyamus muticus L. (Solanaceae)). The offspring of locusts exposed to more clumped patterns of vegetation exhibited more gregarious behaviour when tested in a behavioural phase assay than did progeny from parents left in enclosures with more scattered vegetation. These effects on nymphal behaviour appeared to be mediated by influences of resource distribution on adult phase state. Phase state in small semi‐field populations was influenced by small‐scale vegetation distribution. Phase differences engendered by environmental structure were maintained in time and transmitted to progeny.     

Fever and phenotype: transgenerational effect of disease on desert locust phase state

Natural enemy attack can cause transgenerational shifts in phenotype such that offspring are less vulnerable to future attack. Desert locusts (Schistocerca gregaria) show density‐dependent variation in their resistance to pathogens, such that they are less vulnerable to pathogens when in the high‐density gregarious phase state (when they would probably be more exposed to pathogens) than when in the solitarious phase state. We therefore hypothesized that infected gregarious parents would maintain this phenotype in their offspring. We infected gregarious desert locust nymphs with the fungal pathogen Metarhizium anisopliae var. acridum, and allowed them to survive to reproduction by means of behavioural fever. The phase state of the locust offspring was assessed by their colouration and behavioural assays. Contrary to our hypothesis, we found an increase in solitarization in the infected population (14.6% solitarious offspring from infected parents, vs. <2% from uninfected counterparts at equivalent density). In a second experiment, we simulated behavioural fever temperatures and obtained a similar result (13.6% solitarious offspring vs. 4.4% from controls), implying that the phenomenon is probably a side‐effect of the hosts’ fever response. Identification of this novel environmental factor affecting locust phase state could have important implications for the biological control of these major pests.