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.     

Pheromones in relation to aggregation and reproduction in desert locusts

Abstract. Desert locusts, Schistocerca gregaria (Forskål) (Orthoptera: Acrididae), exhibit a population density-dependent phase polymorphism which includes the gradual change of many morphological, physiological and behavioural characteristics. Many volatiles associated with desert locusts have been identified recently and it is assumed that they are involved in pheromonal control of behaviour and development of locusts. Ovipositing females deposit with their egg pods several volatiles that appear to be attractive to other females resulting – possibly in combination with environmental factors – in an aggregated oviposition. Mature males release several volatiles, among them phenylacetonitrile, which are reported to accelerate sexual maturation in young males. Also, aggregation pheromone systems for hoppers and adults have been described. However, recent studies and publications shed a new light on the postulated effects of some of these volatiles. Gregarious behaviour can undoubtedly be induced by mechanical stimuli. Furthermore, the main component of the adult aggregation pheromone system, phenylacetonitrile, is found to be a repellent obviously not involved in aggregation. Comprehensive studies have demonstrated that phenylacetonitrile is used by mature gregarious males as a courtship inhibition pheromone to enhance mate guarding. Recent progress, contradictory results and perspectives in desert locust pheromone research related to reproduction are summarized and discussed in this paper.     

Mass spectral determination of phenylacetonitrile (PAN) levels in body tissues of adult desert locust, Schistocerca gregaria

Wings and legs of the gregarious desert locust, Schistocerca gregaria have been shown to be release sites of phenylacetonitrile (PAN), the major adult male-produced pheromone. However, there is limited information on the distribution of PAN within the locust. Here we show, using gas chromatography-mass spectrometry (GC-MS), that PAN occurs in nearly all body parts of both adult males and females of the locust in varying amounts. PAN was 20-fold more concentrated in males than in females. In females, PAN was concentrated more in the tarsal segments. The greatest amounts of PAN were in 2- and 3-week old female and male body parts, respectively. No trace of PAN was found in similar ages and sexes of the solitarious phase desert locust. Our results show that PAN is distributed in the body matrix of both sexes of gregarious phase locusts and suggest that no specific tissue is responsible for biosynthesis of the pheromone.     

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.     

Courtship inhibition pheromone in desert locusts,Schistocerca gregaria

Male desert locusts in the gregarious phase release phenylacetonitrile (PAN) on becoming sexually mature. It has been assumed that this chemical is responsible for aggregation of adult desert locusts. However, PAN has repellent characteristics and is involved in sexual behavior. Mature males release PAN as a volatile to serve as a kind of olfactory concealment during mating and to prevent competing males from homosexual encounters. We conclude that PAN is a courtship-inhibiting pheromone exclusively used under crowded conditions in dense populations when high sperm competition occurs among desert locust males. By chemically enhancing their mate guarding, gregarious males improve the protection of their mate from rivals and ensure their reproductive success.     

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     

Concentration-dependent parsimonious releaser roles of gregarious male pheromone of the desert locust, Schistocerca gregaria

The responses of (i) groups of crowd-reared mature males of desert locust, Schistocerca gregaria to a choice of two columns of air, one permeated with different concentrations of phenylacetonitrile (PAN), the major component of gregarious-phase male-produced pheromone, and the other untreated, and (ii) individual crowd-reared mature males of the insect to varying concentration gradients of PAN, were studied in two different types of arena. In the choice assay, locusts preferred to be within PAN-permeated air column at low relative doses of the pheromone, but away from PAN at high relative doses. In the second assay, individual locusts were arrested close to PAN source at low PAN concentration gradients, but away from the source at high concentration gradients. The results are consistent with two reported releaser functions of the adult male-released pheromone that are dependent on different sensory thresholds: arrestment and cohesion at lower relative concentrations and male-male homosexual avoidance at higher relative concentrations.     

Effect of phase status on responses to AKHI in the desert locust,Schistocerca gregaria gregaria

Hyperlipaemic response to adipokinetic hormone (AKH I) was demonstrated in both solitary and gregarious phases of the desert locust, Schistocerca gregaria gregaria. Time-course studies showed that the gregarious locusts had a faster response to the hormone than their solitary counterparts. At peak response time (90 min), the gregarious locusts were more sensitive to AKH I doses below 2 pmol while the solitary locusts had a higher response above this dose. Upon injection of the hormone, lipoprotein conversion occurred, resulting in the formation of the low density lipoprotein (LDLp). The LDLp formed in the gregarious locusts was much larger than that of the solitary locusts. The fat body lipid reserve (expressed as % fat body dry weight) was significantly (P < 0.01) higher in the gregarious (79.02 ± 2.77%) than in the solitary locusts (65.23 ± 2.55%). Triacylglycerol was the major lipid class representing 83.9 and 73.9% of the total lipids in gregarious and solitary locusts, respectively. The higher fat body lipid reserves and efficient LDLp formation in response to AKH in gregarious locusts compared to solitary locusts suggests a physiological adaptation for prolonged flights. © 1996 Wiley-Liss, Inc.     

Morphological and behavioural characteristics of a gynandromorph of the desert locust, Schistocerca gregaria

Abstract.  Morphological and behavioural characteristics are investigated for a gynandromorph of the desert locust, Schistocerca gregaria , appearing under isolated rearing conditions in the laboratory. It has both male and female external reproductive organs bilaterally. The body size and dimensions are similar to a normal male. Morphometric traits (fore wing length/maximum head width ratio and fore wing length/hind femur length ratio) of the gynandromorph are typical for the values of solitarious locusts. When the gynandromorph is placed into an arena holding ten sexually mature gregarious females, it shows a distinct male behaviour: it jumps on a female and tries to mate with her. When kept together with males, males recognize this gynandromorph as a female because some of them try to mount, although no successful copulation is observed. The results suggest that the gynandromorph might have had a female-specific pheromone. Dissection reveals that the gynandromorph has no testis but abnormal ovaries containing vitellogenic oocytes. These observations indicate that the gynandromorph obtained has a mixture of male and female morphological characteristics and behaves like a male but is recognized as a female by conspecific males.     

Phase-specific responses to different qualities of food in the desert locust, Schistocerca gregaria: developmental, morphological and reproductive characteristics

Solitarious female adults are known to produce smaller hatchlings than those produced by gregarious adults of the desert locust, Schistocerca gregaria. This study investigated developmental, morphological and reproductive responses to different qualities of food in hatchlings of different phases. Mortality was higher, the duration of nymphal development longer and adult body weight lighter with a low-quality food than a high-quality food. Gregarious hatchlings showed better survivorship, grew faster and became larger adults than did solitarious ones. The incidence of locusts exhibiting extra molting, which was typically observed in the solitarious phase, was dramatically increased when a low-quality food was given to the solitarious hatchlings. Low-quality food caused locusts to shift morphometric ratios toward the values typical of gregarious forms; smaller F/C (hind femur length/maximum head width) and larger E/F (elytra length/hind femur length). Solitarious hatchlings grown at either high- or low-quality foods and then given high-quality food after adult emergence revealed that food qualities during the nymphal stage influence their progeny quality and quantity via adult body size that influenced reproductive performance. Female adults showed an overshooting response to a shift from low- to high-quality food by increasing egg production that was specific to body size. This study may suggest that gregarious hatchlings are better adapted to adverse food conditions than solitarious counterparts and extra molting is induced even among gregarious hatchlings under poor food conditions.     

Novel cross-stage solitarising effect of gregarious-phase adult desert locust (Schistocerca gregaria (Forskål)) pheromone on hoppers

Previous studies had demonstrated stage differentiation in the cohesion (aggregation) pheromone systems of the desert locust, Schistocerca gregaria. In laboratory arena, the nymphal and adult stages responded aggregatively to their own pheromone, but dispersed evenly within the arena in the presence of the other. In the present study, we explored the effects of longer-term contact of field gregarious hopper bands and laboratory crowd-reared nymphs with the major constituent of the adult pheromone. During the first few days, hoppers in treated bands became relatively hyperactive. Over the next few days, their movements became random and they stopped marching as coherent groups, they started to roost for longer periods on vegetations, and they fragmented into smaller and smaller groupings and individuals. When attacked by birds, they demonstrated subdued levels of collective defensive behaviour compared to normal hoppers, and there were clear signs of increased predation and cannibalism at the roosting sites. In cage experiments, crowd-reared nymphs treated with the pheromone component became hyperactive, showed abnormal diel patterns and reduced feeding on plants but increased cannibalism. Our observations show that the major adult pheromone constituent has a solitarising effect on gregarious hoppers. The mechanism underlying this effect and the potential of the agent in desert locust control are discussed.     

Fecal volatile components elicit aggregation in the oriental migratory locust,Locusta migratoria manilensis (Orthoptera: Acrididae)

Abstract The aggregation components from fecal volatiles of the oriental migratory locust, Locusta migratoria manilensis were identified with gas chromatographic/electroantennographic detector (GC‐EAD), GC‐MS (mass spectrometry) analyses and behavioral bioassays. Both last instar nymphs and adults of the oriental migratory locust have similar aggregation pheromones in their volatiles. A total of 11 electrophysiologically active compounds, namely, hexanal, cyclohexanol, heptanal, phenol, 2,5‐dimethyl‐pyrazine, benzyl alcohol, benzaldehyde, guaiacol, nonanal, 2,6,6‐trimethyl‐2‐cyclohexene‐1,4‐dione and decyl aldehyde were identified in the fecal volatiles of 2‐day‐old immature adult male locusts. Only hexanal, nonanal, benzaldehyde, cyclohexanol and 2,5‐dimethyl‐pyrazine elicited significant aggregation responses in immature 2‐day‐old adult males. However, adult males had significantly lower behavioral responses to synthetics of five single compounds than the blend of cyclohexanol, 2,5‐dimethyl‐pyrazine, benzaldehyde, nonanal, hexanal in ratios of 100: 100: 2: 60: 30 in the range of 30–60 μg/mL. We propose that it is the blend of these five compounds that plays a key role in eliciting and sustaining aggregation in gregarious oriental migratory locusts. These results also showed that the aggregation pheromones of the oriental migratory locust are significantly different from those found in the desert locust.     

警惕沙漠蝗的猖獗发生

沙漠蝗在史前期就是北非、西亚和印度等热带荒漠地区的河谷与绿洲上的农业大害虫。我国云南和西藏自治区的聂拉木均有沙漠蝗的分布记载 ,虽尚未发生灾害 ,但是沙漠蝗猖獗发生的最大扩散区已达我国云南接壤的缅甸和西藏接壤的尼泊尔、印度。故我国的西藏自治区和云南省的有关边防及农业植物保护机构应予以高度重视并加强监测和预警 ,谨防沙漠蝗的发生危害     

Adult female desert locusts require contact chemicals and light for progeny gregarization

Crowding causes many organisms to express phenotypic plasticity in various traits. Phase polyphenism in desert locusts represents one extreme example in which a solitary form (solitarious phase) turns into a gregarious form (gregarious phase) in response to crowding. Conspicuous differences in body size and colour occur even in hatchlings. The phase‐specific differences in hatchling characteristics are caused by the tactile stimuli perceived by the antennae of their mother. However, the nature of the tactile stimuli and the mechanism by which the perceived stimuli are processed as a gregarizing signal remain unknown. To explore this problem, the antennae of solitarious adult females of the desert locust Schistocerca gregaria are touched with the bodies of conspecific locusts at different physiological stages and those of other species. The results suggest that a cuticular chemical factor at a specific developmental stage of conspecific locusts causes the solitarious females to produce large eggs that give rise to black hatchlings characteristic of gregarious forms (progeny gregarization), and that this or a similar compound occurs in other acridids, crickets and cockroaches but not in beetles. The involvement of a chemical substance is also supported by hexane extracts of cuticular surfaces of locusts that induce the same effects. Interestingly, crowding induces such gregarizing effects only when the female receives the appropriate stimulus in the presence of light. Solitarious female S. gregaria with their head capsule coated with phosphorescent paint exhibit progeny gregarization in response to crowding and light pulses in darkness, whereas those treated in the same way without light pulses fail to do so.     

Integration of behaviourally relevant odours at the central nervous level in solitary and gregarious third instar locusts,Schistocerca gregaria

Integration of behaviourally relevant odours at the central nervous level of 3rd instar nymphal desert locusts, Schistocerca gregaria, showed phase- and (developmental) stage-dependent characteristics which correlated with differences in the number of olfactory sensilla. Antennal lobe (AL) neurons of gregarious locusts generally responded more frequently and showed a higher sensitivity to the tested stimuli. However, AL neurons of solitary locusts responded significantly more frequently to phenylacetonitril, the major component of the adult aggregation pheromone. Pheromone-specific, plant-specific and pheromone-plant generalist neurons were found in both phases. The response spectra of pheromone-specific neurons correlated with the potential behavioural significance of attractant chemical cues in the environment. Neurons of both phases responded specifically to stage-specific aggregation-pheromone components and to other chemical cues that may be involved in the location of suitable roosting and foraging sites.     

Maternal effects on progeny body size and color in the desert locust, Schistocerca gregaria: examination of a current view

Hatchling body color and size of the desert locust, Schistocerca gregaria, are determined by the population density of the mothers during their reproductive period. Smaller green hatchlings are produced by adults at low population density (solitarious conditions) and larger dark hatchlings at high population density (gregarious conditions). One claim states that a pheromonal factor secreted by gregarious mothers into foam plugs of egg pods induces darkening in hatchlings. Previous research suggests that the foam factor can be removed by separating eggs individually within 1h of deposition, causing presumptive gregarious eggs to hatch without darkening. The present study re-examined this claim and possible factors that have been proposed which could account for the difference between our results and those reported earlier. Early separation was performed on eggs with a low mortality rate. The results showed that the egg separation did not increase the incidence of green hatchlings. Once chorionated in the ovary, eggs remained unchanged in size until the second day after oviposition in either isolated or crowded locusts. This and other results suggest that the phase-dependent differences in body size and color of hatchlings are established in the ovary and that modifications by the accessory gland factor either in the oviduct or after deposition are unlikely.     

Identification of pheromone-like compounds in male reproductive organs of the oriental locust Locusta migratoria

Despite the great economical interest of locusts in agriculture, knowledge on their chemoreception systems is still poor. Phenylacetonitrile is recognised as a pheromone of the desert locust Schistocerca gregaria, triggering gregarization, promoting aggregation and inhibiting courtship. However, in the other major locust species, Locusta migratoria, pheromones have not been reported. We have identified the two isomers of naphthylpropionitrile from the male reproductive organs of L. migratoria. Chemical synthesis has confirmed the identity of the two compounds. Both isomers show significant affinity to CSP91, a protein reported in the testis, but not to three other proteins of the same family (CSP180, CSP540 and CSP884) expressed in female accessory glands. The striking similarity of these compounds with phenylacetonitrile and the unusual nature of such chemicals strongly suggest that naphthylpropionitrile could be pheromones for L. migratoria, while their site of expression and binding activity indicate a role in communication between sexes.     

Time-course haemolymph juvenile hormone titres in solitarious and gregarious adults of Schistocerca gregaria, and their relation to pheromone emission, CA volumetric changes and oocyte growth

The haemolymph JH III titres in solitarious and gregarious adult desert locusts, Schistocerca gregaria, were examined in relation to corpus allatum (CA) volumes, aggregation-maturation pheromone production in males and oocyte growth in females. The JH titres of gregarious females were generally higher than those of solitarious females at all ages studied. The titre patterns, however, were similar: relatively high on day 10, dropping to low levels between days 20 and 25, before rising again by day 25. In the solitarious males, the JH titre was very low on day 10 after fledging, but increased gradually and reached a maximal amount on day 30. The JH titre in gregarious males was low on day 10, elevated on day 15 coinciding with the start of the production of the pheromone, and dropped to a relatively low level on day 20 around the time of maximal pheromone production, then rising again by day 25. These results suggest that biosynthesis of the pheromone is associated with a high JH titre peak in the haemolymph. Although a clear relationship was found during the first gonadotropic cycle between JH titres, on one hand, and CA volume and oocyte growth, on the other, in both phases, no such correlation could be discerned in the second cycle.