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.     

Functional Characterization of the Short Neuropeptide F Receptor in the Desert Locust,Schistocerca gregaria

Whereas short neuropeptide F (sNPF) has already been reported to stimulate feeding behaviour in a variety of insect species, the opposite effect was observed in the desert locust. In the present study, we cloned a G protein-coupled receptor (GPCR) cDNA from the desert locust, Schistocerca gregaria. Cell-based functional analysis of this receptor indicated that it is activated by both known isoforms of Schgr-sNPF in a concentration dependent manner, with EC₅₀ values in the nanomolar range. This Schgr-sNPF receptor constitutes the first functionally characterized peptide GPCR in locusts. The in vivo effects of the sNPF signalling pathway on the regulation of feeding in locusts were further studied by knocking down the newly identified Schgr-sNPF receptor by means of RNA interference, as well as by means of peptide injection studies. While injection of sNPF caused an inhibitory effect on food uptake in the desert locust, knocking down the corresponding peptide receptor resulted in an increase of total food uptake when compared to control animals. This is the first comprehensive study in which a clearly negative correlation is described between the sNPF signalling pathway and feeding, prompting a reconsideration of the diverse roles of sNPFs in the physiology of insects.     

Density-dependent aposematism in the desert locust

The ecological processes underlying locust swarm formation are poorly understood. Locust species exhibit phenotypic plasticity in numerous morphological, physiological and behavioural traits as their population density increases. These density-dependent changes are commonly assumed to be adaptations for migration under heterogeneous environmental conditions. Here we demonstrate that density-dependent nymphal colour change in the desert locust Schistocerca gregaria (Orthoptera: Acrididae) results in warning coloration (aposematism) when the population density increases and locusts consume native, toxic host plants. Fringe-toed lizards (Acanthodactylus dumerili (Lacertidae)) developed aversions to high-density-reared (gregarious-phase) locusts fed Hyoscyamus muticus (Solanaceae). Lizards associated both olfactory and visual cues with locust unpalatability, but only gregarious-phase coloration was an effective visual warning signal. The lizards did not associate low rearing density coloration (solitarious phase) with locust toxicity. Predator learning of density-dependent warning coloration results in a marked decrease in predation on locusts and may directly contribute to outbreaks of this notorious pest.     

Relationships between food quality and fitness in the desert locust, Schistocerca gregaria, and its distribution over habitats on the Red Sea coastal plain of Sudan

The effect of millet, Pennisetum typhoideum Rich. (Poaceae), leaf nitrogen content on fitness parameters of the desert locust, Schistocerca gregaria Forsk. (Orthoptera: Acrididae), was studied under laboratory conditions. Locusts reared on high‐nitrogen leaves were larger, developed faster, had higher survival, reproduced more and earlier, and showed greater synchronization than those fed on low‐nitrogen leaves. Active and passive cannibalism contributed to mortality when locusts were reared on low‐nitrogen leaves, but not when reared on high‐nitrogen leaves. Elevated leaf nitrogen content of host plants increased net reproduction and intrinsic rate of increase, and lowered generation time. The findings show that nitrogen content of host plants affects the potential for population increase in the desert locust. Leaf samples of common plant species were collected in the Heliotropium arbainense (Fresen.) (Boraginaceae) and Panicum turgidum (Forssk.) (Poaceae) plant communities on the Red Sea coastal plain of Sudan during the winters of 1999 and 2000. The levels of leaf nitrogen in host plants were comparable to those in the laboratory studies and consistently higher in plant samples from the Heliotropium community than in samples from the Panicum community. Both in 1999 and 2000, locust densities were much higher in the Heliotropium than in the Panicum plant community. It should be assessed whether the desert locust would be attracted to sites where host plants have high leaf nitrogen content, as this would not only increase their fitness, but also the likelihood of gregarization and outbreaks.     

博落回生物碱对蝗虫成虫毒力试验简报

目的:测定博落回生物碱对蝗虫成虫的毒力作用,为利用药用植物提取物杀灭蝗虫的无公害防治提供参考。方法:用文献法提取博落回果实中的生物碱,制备博落回生物碱溶液;采用喷雾法将博落回生物碱溶液喷施于蝗虫成虫;进行了博落回生物碱溶液对蝗虫成虫的田间小面积试验;用计算机软件SPSS11.5进行统计学分析。结果:在96小时内,博落回生物碱对蝗虫成虫的LD50为29.568mg/L,95%可信限为2.5563～69.473mg/L。田间小面积施药3天后,每平方米内虫口减退达90%左右,持效时间7天。结论:博落回溶液对蝗虫成虫具有一定的杀灭作用。     

Invasion of the pathogenic fungus Metarhizium anisopliae through the guts of germfree desert locusts,Schistocerca gregaria

Less than 1% of an ingested inoculum of the pathogenic fungus Metarhizium anisopliae was retained for long enough (ca. 24 h) in the gut of the desert locust, Schistocerca gregaria, for germination and penetration to have occurred. The residual inoculum did not initiate an infection in guts of fed conventional or axenic locusts. However, symptoms of mycosis (hyphal bodies in the haemolymph, fungal penetration of the hindgut intima and epithelium, tetanic paralysis) were consistently observed in axenic but not conventional locusts which were starved post-inoculation.It is concluded that the antifungal toxin produced by the gut bacteria defends the desert locust against gut invasion by Metarhizium anisopliae during periods of starvation when the physical defences, prominent in fed insects, are less apparent.     

The role of food distribution and nutritional quality in behavioural phase change in the desert locust

The behaviour of herbivorous insects is influenced by their nutritional state. Nutrition-induced behavioural changes are often interpreted as adaptive mechanisms for controlling nutrient intake; however, their influence on other life history traits has received far less attention. We investigated the effect of food quality and distribution on the behaviour and phase state of desert locusts, Schistocerca gregaria Forsk?l (Orthoptera, Acrididae), which change from the 'solitarious' to the 'gregarious' phase in response to population density. Phase change involves many morphological, physiological and behavioural changes. Solitarious insects are cryptic whereas gregarious locusts aggregate. Individual phase change is stimulated by mechanical contact with other locusts. A clumped resource distribution promotes change to the gregarious phase by increasing crowding and contact between individuals. In this study, we found that the effect of food distribution on locust phase depended on the nutritional quality of the food. We used three synthetic food treatments: near optimal, dilute and a choice of two unbalanced but complementary foods. Clumped resource distribution led to increased gregarization in the dilute and the complementary diet treatments. This effect was particularly pronounced on the complementary foods, owing to the interaction of crowding and locomotion. Gregarization was most pronounced in the dilute diet treatment, owing to increased activity. These diet-induced effects are explained in terms of behavioural changes in locomotion, quiescence and feeding that are consistent with what is known from earlier work on locust feeding behaviour and behavioural phase change. Copyright 2000 The Association for the Study of Animal Behaviour.     

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     

Diversity of locust gut bacteria protects against pathogen invasion

Diversity–invasibility relationships were explored in the novel context of the colonization resistance provided by gut bacteria of the desert locust Schistocerca gregaria against pathogenic bacteria. Germ‐free insects were associated with various combinations of one to three species of locust gut bacteria and then fed an inoculum of the pathogenic bacterium Serratia marcescens. There was a significant negative relationship between the resulting density of Serratia marcescens and the number of symbiotic gut bacterial species present. Likewise there was a significant inverse relationship between community diversity and the proportion of locusts that harboured Serratia. Host mortality was not negatively correlated with resistance to gut‐invasion by Serratia marcescens, although there were significantly more deaths among pathogen fed germ‐free insects than tri‐associated gnotobiotes. The outcome is consistent with the predictions of community ecology theory that species‐rich communities are more resistant to invasion than species‐poor communities.     

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.     

Feeding causes the appearance of a factor in the haemolymph that stimulates protein synthesis

Soon after a locust (Locusta migratoria) begins to feed, an increase in protein synthesis can be detected in the animal. Isolation of fat body shows that this tissue synthesizes protein at a faster rate in recently fed animals than it does in fasting insects. Fasting locusts injected with haemolymph from fed insects increased protein synthesis when compared with locusts injected with haemolymph from fasting locusts. The factor causing this increase was present in the haemolymph within 5 min of feeding. Feeding or direct contact with the food was not essential to increase protein synthesis. Exposure of fasting locusts to feeding insects was sufficient to elevate the rates of protein synthesis in the fasting animals.The increase inprotein synthesis was not a result of general excitation or an increase in the concentration of tryptophan or isoleucine in the haemolymph. Ecdysteroid titres were uniformly low during the first ten days of adult life. Gel filtration of the fed haemolymph revealed a low molecular weight fraction (about 600 daltons) which stimulated protein synthesis upon injection into fasting locusts.     

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.     

Effects of a Mycoinsecticide on Feeding and Fecundity of the Brown Locust Locustana pardalina

The entomopathogenic fungus Metarhizium anisopliae var. acridum is being developed for use as a mycoinsecticide against locusts and grasshoppers in Africa. In addition to causing significant mortality, studies have shown the pathogen to cause reductions in feeding of a number of target species during the disease incubation period. The present study extends this work by demonstrating significant reductions in feeding following infection in another important pest species, the brown locust Locustana pardalina (Walker). Insects collected from the field following a spray application and subsequently maintained in a field laboratory showed a significant reduction in per capita feeding, as indicated by faecal production, as early as 2 days after treatment; this was before any pathogen-induced mortality. This per capita reduction in feeding by infected individuals contributed to a total reduction in feeding of 65% relative to controls. In addition to this laboratory based assessment, experiments were conducted to examine the effects of infection on mortality, feeding and fecundity in the field. Mortality rates of infected individuals in the field were significantly slower than those in the laboratory (average survival time of approximately 39 days compared with 6 days), although total mortality and percentage mycosis were equivalent. Treated individuals showed a significant reduction in body fat accumulation at sexual maturity compared with controls. This may reduce dispersal ability and total reproductive fitness. However, treated individuals exhibited a reduced pre-oviposition period resulting in them laying more eggs than untreated individuals within the first weeks following fledging. Thus, no significant reductions in fecundity were recorded by the end of the assessment period when mortality of treated individuals exceeded 90%. Given that many untreated locusts were still alive and had the potential to continue oviposition for several more weeks, however, it is likely that differences in fecundity would have become apparent if the assessment had continued. These results provide important insights for evaluating overall impacts of spray applications of the mycoinsecticide.     

Effect of Paranosema (Nosema) locustae (Microsporidia) on morphological phase transformation of Locusta migratoria manilensis (Orthoptera: Acrididae)

Field and laboratory studies demonstrated that Paranosema (Nosema) locustae had significant effects on the morphological phase transformation of Locusta migratoria manilensis (Meyen 1835). In the field, spraying P. locustae on gregarious locusts caused a substantial population reduction by 16 days after treatment, with most of the surviving locusts being phase solitaria. However, the effects of P. locustae on locust phase transformation began before direct mortality had caused a substantial reduction in locust density: locust numbers were still high at day 10, but locusts had already transformed to phase transiens. Laboratory assays showed that while a low dose of P. locustae had no effect on phase transformation, at a higher dose of 1×10⁵ spores/mL, locusts had F/C ratios that were significantly (P<0.05) more solitaria than untreated locusts, with locusts having ratios that were either phase solitaria or on the solitaria side of phase transiens. In a second laboratory experiment that analysed the effects of locust density on phase transformation by P. locustae, there was no obvious effect of density on female locusts 10 days later as all were solitaria at all locust densities. At day 16, female locusts were transiens at higher densities, but were solitaria at 4/cage. With males there were lesser effects. These results provide new evidence for P. locustae having sub-lethal effects on locust phase transformation at a wide range of locust densities.     

Syntaxin 1A modulates the sexual maturity rate and progeny egg size related to phase changes in locusts

The migratory locust (Locusta migratoria) exhibits clear phenotypic plasticity depending on its population density. Previous studies have explored the molecular mechanisms of body colour, behavior, immunity, and metabolism between high population density gregarious (G) and low population density solitarious (S) locusts. However, the molecular mechanisms underlying differences in reproductive traits remain unknown. G locusts reach sexual maturation much faster and lay larger eggs compared with S locusts. The traits of G locusts decreased significantly with isolation, whereas those of S locusts increased with crowding. Analysis of gene expression in female adults indicated that syntaxin 1A (Syx1A) was expressed significantly higher in G locusts than in S locusts. After silencing Syx1A expression in G locusts by RNA interference (RNAi), their sexual maturity rate and progeny egg size changed towards those of S locusts. Similarly, increment in the traits of S locusts with crowding was blocked by Syx1A interference. Changes in the traits were also confirmed by decrease in the level of vitellogenin, which is regulated by Syx1A. In conclusion, plasticity of the sexual maturity rate and progeny egg size of G and S locusts, which is beneficial for locusts to adapt to environmental changes, is regulated by Syx1A.     

Haemolymph levels of Schistocerca gregaria ion transport peptide and ion transport-like peptide

Abstract.  Titres of ion transport peptide (ITP) and ion transport-like peptide (ITP-L) in the haemolymph of the desert locust Schistocerca gregaria Forskål are investigated using a combination of enzyme-linked immunosorbent assay and reversed-phase high-performance liquid chromatography (HPLC). The estimated circulating levels of these two peptides are used to investigate their putative physiological roles. Haemolymph levels of ITP-L are significantly higher in fed and exercise-stressed locusts than in starved insects, suggesting a role for ITP-L in postfeeding osmoregulation and metabolism associated with stress. The higher titres of ITP-L in the final nymphal stadium could be related to increased levels of ecdysteroids over this same period. In addition detection of ITP-L in the brain and corpus cardiacum of the locust demonstrates for the first time that the ITP-L is expressed in these tissues. Immunoreactivity to antibodies raised against ITP is significantly higher in fed locusts compared with starved insects. However, >95% of this immunoreactivity elutes later than synthetic ITP when separated by HPLC. The results suggest that this more hydrophobic immunoreactivity is neither native ITP nor a metabolic breakdown product of ITP. Haemolymph levels of immunoreactivity to ITP during the last nymphal stadium are similar to ITP-L but, unlike ITP-L, there is no measured increase in immunoreactivity to ITP due to exercise stress.     

A behavioural analysis of phase change in the desert locust

A programme of research into phase change in the desert locust, Schistocerca gregaria, is described. The ability to change phase between solitarious and gregarious forms in response to population density is a key feature of locusts and is central to their occasional yet catastrophic impact on humans. Phase polymorphism is an extreme form of phenotypic plasticity. The most labile phase characteristic is behaviour. It is argued that a fully integrated study of behavioural phase change provides a powerful tool for understanding both the mechanisms of phase change and locust population dynamics, both of which offer possibilities for improved management and control of desert locust plagues. An assay for measuring behavioural phase-state in individual locusts was derived, based on logistic regression analysis. Experiments are described that used the assay to quantify the time-course of behavioural change, both within the life of individual locusts and across generations. The locust-related stimuli that provoke behavioural gregarization were investigated. Complex interactions were found between tactile, visual and olfactory stimuli, with the former exerting the strongest effect. Behavioural analysis also directed a study of the mechanisms whereby adult females exert an epigenetic influence over the phase-state of their developing offspring. Female locusts use their experience of the extent and recency of being crowded to predict the probability that their offspring will emerge into a high-density population, and alter the development of their embryos accordingly through a gregarizing agent added to the foam that surrounds the eggs at laying. There is also a less pronounced paternal influence on hatchling phase-state. An understanding of the time-course of behavioural phase change led to a study of the effect of the fine-scale distribution of resources in the environment on interactions between individual locusts, and hence on phase change. This, in turn, stimulated an exploration of the implications of individual behavioural phase change for population dynamics. Cellular automata models were derived that explore the relationships between population density, density of food resources and the distribution of resources in the environment. The results of the simulation showed how the extent of gregarization within a population increases with rising population size relative to food abundance and increasing concentration of food resources. Of particular interest was the emergence of critical zones across particular combinations of resource abundance, resource distribution and population size, where a solitarious population would rapidly gregarize. The model provided the basis for further laboratory and field experiments, which are described.     

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.     

Socially Influenced Behaviour and Learning in Locusts

As a part of our research on the evolution of social learning in insects, we examined socially influenced behaviour and social learning in desert locust (Schistocerca gregaria) nymphs and adults. In the nymphs, the only positive effect we documented was an increased tendency to feed while in the company of another locust than alone. The adults, on the other hand, showed significant preference for joining others (local enhancement) in both the contexts of feeding and egg laying. Neither nymphs nor adults, however, showed social learning. Our preliminary analyses pointed to locusts as a likely insect that might possess social learning. Our research, when taken together with research on phase‐shifts and swarm/marching behaviour of gregarious locusts, suggests that the behavioural dynamics of gregarious locusts may make local enhancement but not social learning beneficial. The possible difference we documented between the nymphs and adults could enable us to further explore the proximate and ultimate mechanisms that underlie socially influenced behaviour.