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.     

Neural correlates to flight-related density-dependent phase characteristics in locusts

Locust phase polymorphism is an extreme example of behavioral plasticity; in response to changes in population density, locusts dramatically alter their behavior. These changes in behavior facilitate the appearance of various morphological and physiological phase characteristics. One of the principal behavioral changes is the more intense flight behavior and improved flight performance of gregarious locusts compared to solitary ones. Surprisingly, the neurophysiological basis of the behavioral phase characteristics has received little attention. Here we present density-dependent differences in flight-related sensory and central neural elements in the desert locust. Using techniques already established for gregarious locusts, we compared the response of locusts of both phases to controlled wind stimuli. Gregarious locusts demonstrated a lower threshold for wind-induced flight initiation. Wind-induced spiking activity in the locust tritocerebral commissure giants (TCG, a pair of identified interneurons that relay input from head hair receptors to thoracic motor centers) was found to be weaker in solitary locusts compared to gregarious ones. The solitary locusts' TCG also demonstrated much stronger spike frequency adaptation in response to wind stimuli. Although the number of forehead wind sensitive hairs was found to be larger in solitary locusts, the stimuli conveyed to their flight motor centers were weaker. The tritocerebral commissure dwarf (TCD) is an inhibitory flight-related interneuron in the locust that responds to light stimuli. An increase in TCD spontaneous activity in dark conditions was significantly stronger in gregarious locusts than in solitary ones. Thus, phase-dependent differences in the activity of flight-related interneurons reflect behavioral phase characteristics.     

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.     

Neural correlates to flight‐related density‐dependent phase characteristics in locusts

Locust phase polymorphism is an extreme example of behavioral plasticity; in response to changes in population density, locusts dramatically alter their behavior. These changes in behavior facilitate the appearance of various morphological and physiological phase characteristics. One of the principal behavioral changes is the more intense flight behavior and improved flight performance of gregarious locusts compared to solitary ones. Surprisingly, the neurophysiological basis of the behavioral phase characteristics has received little attention. Here we present density‐dependent differences in flight‐related sensory and central neural elements in the desert locust. Using techniques already established for gregarious locusts, we compared the response of locusts of both phases to controlled wind stimuli. Gregarious locusts demonstrated a lower threshold for wind‐induced flight initiation. Wind‐induced spiking activity in the locust tritocerebral commissure giants (TCG, a pair of identified interneurons that relay input from head hair receptors to thoracic motor centers) was found to be weaker in solitary locusts compared to gregarious ones. The solitary locusts' TCG also demonstrated much stronger spike frequency adaptation in response to wind stimuli. Although the number of forehead wind sensitive hairs was found to be larger in solitary locusts, the stimuli conveyed to their flight motor centers were weaker. The tritocerebral commissure dwarf (TCD) is an inhibitory flight‐related interneuron in the locust that responds to light stimuli. An increase in TCD spontaneous activity in dark conditions was significantly stronger in gregarious locusts than in solitary ones. Thus, phase‐dependent differences in the activity of flight‐related interneurons reflect behavioral phase characteristics. © 2003 Wiley Periodicals, Inc. J Neurobiol 57: 152–162, 2003     

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.     

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.     

Neurophysiological studies of flight-related density-dependent phase characteristics in locusts

Locusts show an extreme example of density-dependent phase polymorphism, demonstrating within the species differences in morphology as well as biology, dependent on the population density. Behavior is the primary density-dependent change which facilitates the appearance of various morphological and physiological phase characteristics. We have studied density dependent differences in flight related sensory and central neural elements in the desert locust Schistocerca gregaria. Wind generated high frequency spiking activity in the tritocerebral commissure giant (TCG, an identified interneuron that relay inputs from head hair receptors to thoracic motor centers) that was much less intense in solitary locusts, compared to gregarious ones. In addition the solitary locusts' TCG demonstrated much stronger adaptation of its response. In cases when flight was initiated high frequency TCG activity was independent of the locust phase. The tritocerebral commissure dwarf (TCD) is a GABAergic flight related interneuron that is sensitive to ambient illumination intensity. An increase in the TCD spontaneous activity under dark vs. light conditions was significantly higher in gregarious locusts then in solitary ones, implying a flight-related inhibitory mechanism that is far more active in gregarious locusts under dark conditions. Thus, density-dependent phase differences in interneuron activity pattern and properties well reflect and may be at least partially responsible to behavioral flight-related characteristics.     

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.     

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.     

Listening to the environment: hearing differences from an epigenetic effect in solitarious and gregarious locusts

Locusts display a striking form of phenotypic plasticity, developing into either a lone-living solitarious phase or a swarming gregarious phase depending on population density. The two phases differ extensively in appearance, behaviour and physiology. We found that solitarious and gregarious locusts have clear differences in their hearing, both in their tympanal and neuronal responses. We identified significant differences in the shape of the tympana that may be responsible for the variations in hearing between locust phases. We measured the nanometre mechanical responses of the ear''s tympanal membrane to sound, finding that solitarious animals exhibit greater displacement. Finally, neural experiments signified that solitarious locusts have a relatively stronger response to high frequencies. The enhanced response to high-frequency sounds in the nocturnally flying solitarious locusts suggests greater investment in detecting the ultrasonic echolocation calls of bats, to which they are more vulnerable than diurnally active gregarious locusts. This study highlights the importance of epigenetic effects set forth during development and begins to identify how animals are equipped to match their immediate environmental needs.     

CSP and takeout genes modulate the switch between attraction and repulsion during behavioral phase change in the migratory locust

Behavioral plasticity is the most striking trait in locust phase transition. However, the genetic basis for behavioral plasticity in locusts is largely unknown. To unravel the molecular mechanisms underlying the behavioral phase change in the migratory locust Locusta migratoria, the gene expression patterns over the time courses of solitarization and gregarization were compared by oligonucleotide microarray analysis. Data analysis revealed that several gene categories relevant to peripheral olfactory perception are strongly regulated in a total of 1,444 differentially expressed genes during both time courses. Among these candidate genes, several CSP (chemosensory protein) genes and one takeout gene, LmigTO1, showed higher expression in gregarious and solitarious locusts, respectively, and displayed opposite expression trends during solitarization and gregarization. qRT-PCR experiments revealed that most CSP members and LmigTO1 exhibited antenna-rich expressions. RNA interference combined with olfactory behavioral experiments confirmed that the CSP gene family and one takeout gene, LmigTO1, are involved in the shift from repulsion to attraction between individuals during gregarization and in the reverse transition during solitarization. These findings suggest that the response to locust-emitted olfactory cues regulated by CSP and takeout genes is involved in the behavioral phase change in the migratory locust and provide a previously undescribed molecular mechanism linked to the formation of locust aggregations.     

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.     

Effect of vegetation on density thresholds of adult desert locust gregarization from survey data in Mauritania

In the desert locust, Schistocerca gregaria (Forskål) (Orthoptera: Acrididae), the threshold density inducing the gregarization phenomenon has never been determined under natural conditions. The influence of environmental factors on this phenomenon has been studied mostly in controlled environments. Based on data collected during several years by the survey teams of the National Center for Locust Control in Mauritania, we analyzed the influence of locust density, vegetation cover, and vegetation status on the probability of observing gregarious locusts. We assumed that a probability to observe gregarious locusts of 0.5 corresponded to the density threshold of gregarization. The results showed in detail the change in the threshold of gregarization according to the cover and status of the vegetation. Low cover and dry vegetation led to a low density threshold of gregarization probably due to high probability of individuals to touch each other. Dense and green vegetation favored a high threshold of gregarization probably due to a dispersion of the individuals and a low probability of individual encounters. These findings should help the management of locusts and decision making during control operations.     

Solitary and gregarious locusts differ in circadian rhythmicity of a visual output neuron

Locusts demonstrate remarkable phenotypic plasticity driven by changes in population density. This density dependent phase polyphenism is associated with many physiological, behavioral, and morphological changes, including observations that cryptic solitarious (solitary-reared) individuals start to fly at dusk, whereas gregarious (crowd-reared) individuals are day-active. We have recorded for 24-36 h, from an identified visual output neuron, the descending contralateral movement detector (DCMD) of Schistocerca gregaria in solitarious and gregarious animals. DCMD signals impending collision and participates in flight avoidance maneuvers. The strength of DCMD's response to looming stimuli, characterized by the number of evoked spikes and peak firing rate, varies approximately sinusoidally with a period close to 24 h under constant light in solitarious locusts. In gregarious individuals the 24-h pattern is more complex, being modified by secondary ultradian rhythms. DCMD's strongest responses occur around expected dusk in solitarious locusts but up to 6 h earlier in gregarious locusts, matching the times of day at which locusts of each type are most active. We thus demonstrate a neuronal correlate of a temporal shift in behavior that is observed in gregarious locusts. Our ability to alter the nature of a circadian rhythm by manipulating the rearing density of locusts under identical light-dark cycles may provide important tools to investigate further the mechanisms underlying diurnal rhythmicity.     

飞蝗抱对行为的进化意义及两型间相异的交配策略

飞蝗Locusta migratoriaL.不仅交配时间长,而且进行频繁的、长时间的交配前抱对。一般认为,交配前抱对行为是雄虫为了等待时机获取适时的交配。最近的研究表明,飞蝗的交配时间与P2值(最后交配雄虫子代的比例)、交配前抱对时间与交配时间存在显著的正相关关系,即飞蝗长时间的交配前抱对行为能延长其后续的交配时间,从而提高P2值。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。最近的研究结果显示,散居型较群居型具更高的P2值,较短的交配前抱对和较长的交配时间。冲绳和筑波种群散居型成虫的交配前抱对时间与交配时间存在显著的正相关关系,而群居型无此相关性。这些结果证实飞蝗散居型和群居型之间存在着繁殖策略的差异。     

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.     

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.