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.     

The influence of environmental microstructure on the behavioural phase state and distribution of the desert locust Schistocerca gregaria

Abstract. In previous studies we used logistic regression analysis to quantify the change in behavioural phase state of Schistocerca gregaria (Forskål) nymphs subjected to variations in population density. Such work involved restricting insects in small containers either alone or in a crowd. In the present paper we have shown that the fine-scale distribution of food plants, perches and favourable microclimatic sites influences the spatial distribution of locusts, both in the laboratory and under semi-field conditions. When multiple resource sites were provided, solitarious locusts tended to disperse and behavioural gregarization was inhibited. However, provision of only a single site promoted congregation, overcoming the tendency of solitarious insects to avoid each other, and led to behavioural gregarization. The time-course and extent of this response was fully consistent with our earlier experiments using enforced crowding. We suggest that such quantitative, experimental studies of the effects of environmental microstructure on behaviour may yield fundamental insights into the dynamics of plague formation in the desert locust.     

Effects of parental and progeny rearing densities on locomotor activity of 1st-stadium nymphs in the migratory locust, Locusta migratoria: An analysis by long-term monitoring using an actograph

The effects of parental and progeny rearing densities on locomotor activity in 1st-stadium nymphs of the migratory locust, Locusta migratoria, were observed over a 24- or 36-h period using an actograph. Newly hatched nymphs showed a small activity peak shortly after hatching and the peak level was significantly higher in offspring (gregarious nymphs) of crowd-reared adults than in those (solitarious nymphs) of isolated-reared adults. However, no significant difference was found between the two groups in maximum activity levels exhibited after the initial peak. Post-hatching crowding enhanced locomotor activity during 2-5 h of measurements in 2-day-old nymphs. In this case, the parental density resulted in no significant influence on locomotor activity. However, the maximum activity level shown later in the observation period was higher in gregarious nymphs than in solitarious nymphs. Interestingly, this parental effect was more pronounced in nymphs reared in group than in those reared in isolation. The parental density appeared to affect the degree of response to crowding in the progeny. No evidence was found for the phase accumulation in terms of locomotor activity. The variation observed in locomotor activity among geographical populations did not correspond to their phylogenetic relationships.     

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.     

Body‐color and behavioral responses by the mid‐instar nymphs of the desert locust,Schistocerca gregaria (Orthoptera: Acrididae) to crowding and visual stimuli

The effects of crowding and isolation on body color and behavior were observed for the mid‐instar nymphs of the desert locust, Schistocerca gregaria. Some of the solitarious (isolation‐reared) nymphs that were crowded for 1 or 4 h during the third instar developed black patterns at the fourth instar, but most individuals remained unaffected. Black patterns appeared in all individuals that were crowded for 1 day or longer, but even after 4 days of crowding the black patterning for some individuals was not as intense as that for the gregarious (crowd‐reared) controls. Isolation of gregarious nymphs caused the black patterns to recede or disappear at the last (fifth) nymphal instar, but it was necessary to isolate the nymphs from the beginning of the first instar to obtain body coloration looking like solitarious nymphs in most individuals. Solitarious nymphs that were allowed to see gregarious nymphs developed different intensities of black patterns depending on the body size and number of nymphs shown. The behavioral phase shift from one phase to another was observed when the nymphs were crowded or isolated for 2 days or longer, as previously reported for the last nymphal instars of the same strain. Behavioral gregarization was induced for isolated nymphs that were allowed to see a group of nymphs through a transparent double wall. These results suggested that body‐color phase shift occurred more rapidly for mid‐instar nymphs than for late instar nymphs but the rate of behavioral phase shift was similar for the two instars.     

Density-dependent accumulation of phase characteristics in a natural population of the desert locust Schistocerca gregaria

Abstract. Phase characteristics of locusts from parents that experienced different population densities were investigated under field conditions in Morocco. The density experienced by adults induced a marked phase change in colour, behaviour and morphometry of their offspring. A high-density subpopulation gave rise to a preponderance of black hatchlings that exhibited a high level of aggregation as later stage nymphs and showed gregarious morphometric features as adults, whereas a low-density subpopulation produced a majority of green hatchlings with a lesser tendency to group as final-instar nymphs and more solitarious morphometry as adults. The constrained isolation of insects from the low-density subpopulation, or crowding of insects from the high-density subpopulation, resulted in a behavioural and morphometric change towards even more solitarious characteristics in the former and more pronounced gregarious characteristics in the latter, relative to field-caught insects of the same age. These results from the field are consistent with those in the laboratory and provide more evidence for the dual roles of an individual locust's experience of crowding as well as that of its parents in density-dependent phase change.     

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.     

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.     

飞蝗变型及体色多型的内分泌控制机理

飞蝗具变型现象,散居型和群居型在形态特征、生理机能、行为及体色等方面存在明显差异。保幼激素已被证实能诱导飞蝗散居型绿色的出现。近年,从飞蝗心侧体成功地分离了一种神经肽——黑化诱导激素([His^7]-corazonin),并用白化型进行检测,证实了其对体色黑化作用的活性。不同时间对飞蝗若虫注射不同剂量的[His^7]-corazonin,能诱导出现除绿色以外的散居型体色,如浅褐色、褐色、赤褐色、黑色等;也能诱导出现群居型的体色,即黑色配以橘黄色的底色。而且,对散居型若虫注射[His^7]-corazonin能诱导其形态向群居型转换。这些研究证实[His^7]-corazonin对飞蝗的变型有着重要的控制作用,但又不是唯一的。     

Phase-independent responses to phase-specific aggregation pheromone in adult desert locusts, Schistocerca gregaria (Orthoptera: Acrididae)

Abstract. Volatiles from solitary-reared (solitarious) and crowd-reared (gregarious) adult male desert locusts, Schistocerca gregaria (Forskal) (Orthoptera: Acrididae), were quantitatively and qualitatively different.In particular, solitarious males did not emit phenylacetonitrile, a key component of the aggregation pheromone produced by gregarious adult males.In laboratory bioassays, solitarious and gregarious adults of both sexes responded similarly to the natural aggregation pheromone blend, the major pheromone component phenylacetonitrile, and a synthetic pheromone blend comprising benzaldehyde, guaiacol, phenylacetonitrile and phenol.EAG measurements showed significant differences in the responsiveness of adults of the two phases to the four synthetic components at high doses; however, the general response patterns were similar.These results suggest that the gregarious adult male aggregation pheromone may play a role in the arrestment and subsequent recruitment of solitarious individuals into gregarious or gregarizing groups during the early stages of a locust outbreak.     

Effects of isolation and crowding on the haemolymph pigment composition of the desert locust, Schistocerca gregaria (Orth., Acrididae)

Abstract:  An experimental study on the effect of isolation and crowding of the desert locust, Schistocerca gregaria (Forskål) on haemolymph pigment composition (as measured by absorbance ratios at 460 and 680 nm) was carried out at the International Centre of Insect Physiology and Ecology, Nairobi. The results showed that haemolymph absorbance ratios of gregarious and solitarious locusts were different (P < 0.05) and that there was no phase-specific sex differentiation with regard to this measure (P < 0.05). The haemolymph pigment composition changes during isolation and grouping showed contrasting trends. It changed rapidly in nymphs, but slowly and erratically in adults both resulting from isolation and grouping at hopper stage. Significant shifts in locust phase status were recorded in both situations in nymphs in F₀ generation, and in the adults by the end of the F₂ and F₃ generations of solitary and gregarious conditions, respectively. Shifting of fledglings did not induce significant changes in their mean absorbance ratios in both situations, i.e. isolation and crowding within F₀ generation. The ratio of length of posterior femur (F) to greatest width of the head capsule (C) changed either at a similar rate or more often slower than the haemolymph pigment ratio and both required more than a generation to transform fully. The study has shown that haemolymph pigment composition could be a suitable measure for monitoring phase changes at nymphal stages of the desert locust.     

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.     

Knockdown of the corazonin gene reveals its critical role in the control of gregarious characteristics in the desert locust

The two plague locusts, Schistocerca gregaria and Locusta migratoria, exhibit density-dependent phase polyphenism. Nymphs occurring at low population densities (solitarious forms) are uniformly colored and match their body color to the background color of their habitat, whereas those occurring at high population densities (gregarious) develop black patterns. An injection of the neuropeptide, corazonin (Crz) has been shown to induce black patterns in locusts and affect the classical morphometric ratio, F/C (F, hind femur length; C, maximum head width). We herein identified and cloned the CRZ genes from S. gregaria (SgCRZ) and L. migratoria. A comparative analysis of prepro-Crz sequences among insects showed that the functional peptide was well conserved; its conservation was limited to the peptide region. Silencing of the identified SgCRZ gene in gregarious S. gregaria nymphs markedly lightened their body color and shifted the adult F/C ratio toward the value typical of solitarious forms. In addition, knockdown of the gene in solitarious nymphs strongly inhibited darkening even after a transfer to crowded conditions; however, these individuals developed black patterns after being injected with the Crz as a rescue treatment. SgCRZ was constitutively expressed in the brains of S. gregaria during nymphal development in both phases. This gene was highly expressed not only in the brain in both phases, but also in the corpora allata in the gregarious phase. This conspicuous phase-dependent difference in SgCRZ gene expression may indicate a functional role in the control of phase polyphenism in this locust.     

Food mixing strategies in the desert locust: effects of phase, distance between foods, and food nutrient content

Food mixing strategies were compared in the cryptically coloured, relatively sedentary `solitarious' and the highly mobile, conspicuously coloured `gregarious' phases of the desert locust, Schistocerca gregaria. Based on phase related differences in behaviour and nutritional regulatory responses, we predicted that solitarious nymphs, compared to gregarious nymphs, would move less between nutritionally complementary foods, particularly as the distance between the foods increased. We manipulated the nutritional composition [protein (p) and digestible carbohydrate (c) content] of two foods in an experimental arena and varied the distance between the foods using a factorial experimental design. Results indicated that in general, solitarious nymphs showed greater fidelity to individual food dishes than did gregarious insects (i.e., they concentrated their feeding mainly on one dish). However, results also demonstrated that for both phases fidelity to a particular food dish increased as the distance between the dishes increased, and that the number of switches between dishes decreased with increasing distance. In the smallest arenas, though, gregarious nymphs switched more frequently between the two food dishes than solitarious nymphs, even when the two dishes contained the same, near-optimal food (p18:c24). When challenged by having the two dishes either placed furthest apart (2 m) or more divergent in nutritional composition (p29:c13 vs. p7:c35), insects of both phases regulated protein intake more strongly than carbohydrate intake, by eating more from the dish containing higher-protein food.     

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.     

Role of Olfactory and Visual Cues in the Attraction/Repulsion Responses to Conspecifics by Gregarious and Solitarious Desert Locusts

Desert locusts [Schistocerca gregaria Forskål (Orthoptera, Acrididae)] change phase in response to population density: solitarious insects avoid one another, but when crowded they change to the gregarious phase and aggregate. The attraction/repulsion responses of gregarious and solitarious locusts maintain phase differences in locust populations. Despite considerable research, the cues for aggregation are poorly understood; moreover, the repulsion response of solitarious locusts has not previously been investigated. This study analyzes the role of visual and olfactory stimuli in triggering these different responses to conspecifics. Isolation-reared insects were repelled by both olfactory and visual stimuli from other locusts. Crowd-reared insects were attracted by the combination of olfactory and visual cues. In addition, olfactory stimuli affected other behaviors in both phases, and behavioral differences between isolation- and crowd-reared locusts were clear even in the absence of conspecifics. The sensory and neurological mechanisms underlying these responses are not well understood and will form the basis for neurobiological investigations of locust phase.     

Adaptive difference in daily timing of hatch in two locust species,Schistocerca gregaria and Locusta migratoria: The effects of thermocycles and phase polyphenism

This study examined the effects of temperature and phase polyphenism on egg hatching time in the desert locust, Schistocerca gregaria, and the migratory locust, Locusta migratoria. The two species exhibited differences and similarities in hatching behavior when exposed to different temperature conditions. In 12-h thermocycles of various temperatures, the S. gregaria eggs hatched during the cryoperiod (low temperature period), whereas L. migratoria eggs hatched during the thermoperiod (high temperature period). The eggs of both species hatched during the species-specific period of the thermoperiod in response to a temperature difference as small as 1 °C. Furthermore, the locusts adjusted hatching time to a new thermal environment that occurred shortly before the expected hatching time. In both species, the hatching of the eggs was synchronized to a specific time of the day, and two hatching peaks separated by approximately 1 day were observed at a constant temperature after the eggs were transferred from thermocycles 3 days before hatching. Eggs laid by gregarious females hatched earlier than those laid by solitarious females in S. gregaria but this difference was not observed in L. migratoria.