Behavioural Gregarization Research Articles

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

AbstractThe 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.

Rapid behavioural gregarization in the desert locust, Schistocerca gregaria entails synchronous changes in both activity and attraction to conspecifics

Desert Locusts can change reversibly between solitarious and gregarious phases, which differ considerably in behaviour, morphology and physiology. The two phases show many behavioural differences including both overall levels of activity and the degree to which they are attracted or repulsed by conspecifics. Solitarious locusts perform infrequent bouts of locomotion characterised by a slow walking pace, groom infrequently and actively avoid other locusts. Gregarious locusts are highly active with a rapid walking pace, groom frequently and are attracted to conspecifics forming cohesive migratory bands as nymphs and/or flying swarms as adults. The sole factor driving the onset of gregarization is the presence of conspecifics. In several previous studies concerned with the mechanism underlying this transformation we have used an aggregate measure of behavioural phase state, Pgreg, derived from logistic regression analysis, which combines and weights several behavioural variables to characterise solitarious and gregarious behaviour. Using this approach we have analysed the time course of behavioural change, the stimuli that induce gregarization and the key role of serotonin in mediating the transformation. Following a recent critique that suggested that using Pgreg may confound changes in general activity with genuine gregarization we have performed a meta-analysis examining the time course of change in the individual behaviours that we use to generate Pgreg. We show that the forced crowding of solitarious locusts, tactile stimulation of the hind femora, and the short-term application of serotonin each induce concerted changes in not only locomotion-related variables but also grooming frequency and attraction to other locusts towards those characteristic of long-term gregarious locusts. This extensive meta-analysis supports and extends our previous conclusions that solitarious locusts undergo a rapid behavioural gregarization upon receiving appropriate stimulation for a few hours that is mediated by serotonin, at the end of which their behaviour is largely indistinguishable from locusts that have been in the gregarious phase their entire lives.

Behavioral phase shift in nymphs of the desert locust, Schistocerca gregaria: Special attention to attraction/avoidance behaviors and the role of serotonin

Schistocerca gregaria exhibits a phase-specific behavior in response to crowding. Nymphs occurring at low population densities (solitarious phase) tend to avoid one another, whereas those occurring at high population densities (gregarious phase) are attracted to one another. This study examined how this attraction/avoidance behavior changed after isolation or crowding. The behavior of the test nymphs was assessed by determining their positioning with respect to a stimulus cup, which contained 12 gregarious nymphs, placed at one end of an elliptical arena and an empty cup placed at the opposite end. Gregarious (crowd-reared) nymphs were most frequently observed close to the stimulus cup, whereas solitarious (isolated-reared) nymphs tended to avoid it. This tendency was easily changed by exposing the nymphs to isolation or crowding. However, contrary to a previously reported conclusion that behavioral gregarization occurs in 4–8h of crowding, the nymphs required at least 3days to achieve a significant change in the attraction/avoidance behavior in either direction, from solitarious to gregarious or the converse. The discrepancies between the present study and previous studies appear to result from the different behaviors observed. The present study focused on the attraction/avoidance behavior that is most likely the most important element in the gregarization and solitarization processes, whereas other studies used a mixture of various activity-related behaviors. No evidence was obtained for a trans-generational accumulation in the attraction/avoidance behaviors. Serotonin, a biogenic amine that is suggested by others to be involved in behavioral phase changes in S. gregaria, had no influence on this behavior or body color when injected into the solitarious nymphs.

Hormonal Control of the Phase Polyphenism of the Desert Locust: A Review of Current Understanding

Locusts show density-dependent continuous phase polyphenism; they appear in two forms or phases, gregari- ous and solitary, and there is a continuous range of intermediates between the extreme phases. The endocrine control of phase polyphenism has been the most intensively studied in desert locusts, Schistocerca gregaria, Indeed, results of inves- tigations over the past 15 years, provide some of the most detailed information on the endocrine mechanisms that poten- tially regulate desert locust phase polyphenism. In addition, recent studies on the juvenile hormone titres, ecdysteroid ti- tres, the discovery of (His 7 )-corazonin as dark-colour-inducing neuropeptide (DCIN) and the involvement of serotonin pulse in the metathoracic ganglion that triggers behavioural gregarization in the desert locust have yielded not only a good progress in our understanding the endocrine control of phase polyphenism but also unexpected results which indicate that the endocrine control of desert locust phase polyphenism is more complex than envisioned by the classical model. This review gives an overview of the progress made to date in elucidating the hormonal control of the desert locust phase polyphenism. Moreover, this review will summarize these findings and present some questions that still need to be an- swered.

Phase-dependent associative learning in desert locusts

Phase-dependent associative learning in desert locusts

Phase change in the desert locust: A novel computerised behavioural assay to study the effects of anaesthesia on gregarisation

Phase change in the desert locust: A novel computerised behavioural assay to study the effects of anaesthesia on gregarisation

Behavioural phase change in the Australian plague locust, Chortoicetes terminifera, is triggered by tactile stimulation of the antennae

Density-dependent phase polyphenism is a defining characteristic of the paraphyletic group of acridid grasshoppers known as locusts. The cues and mechanisms associated with crowding that induce behavioural gregarization are best understood in the desert locust, Schistocerca gregaria, and involve a combination of sensory inputs from the head (visual and olfactory) and mechanostimulation of the hind legs, acting via a transient increase in serotonin in the thoracic ganglia. Since behavioural gregarization has apparently arisen independently multiple times within the Acrididae, the important question arises as to whether the same mechanisms have been recruited each time. Here we explored the roles of visual, olfactory and tactile stimulation in the induction of behavioural gregarization in the Australian plague locust, Chortoicetes terminifera. We show that the primary gregarizing input is tactile stimulation of the antennae, with no evidence for an effect of visual and olfactory stimulation or tactile stimulation of the hind legs. Our results show that convergent behavioural responses to crowding have evolved employing different sites of sensory input in the Australian plague locust and the desert locust.

To Swarm or Not to Swarm?

In desert locusts, the radical transformation from a harmless “solitarious” form to the swarm-forming “gregarious” phase is one of the most extraordinary and iconic examples of density-dependent phenotypic plasticity in nature, as well as one of the most economically devastating. Now Anstey et al. (see the Perspective by Stevenson) reveal a neurochemical mechanism linking the changed behavior of individuals to profound changes in population structure, which, in this instance, lead to swarming and mass migration. The key to the phenotypic change is the ubiquitous neurotransmitter serotonin, which is synthesized in response to multiple sensory cues that gauge locust population density, switching locusts from mutual aversion to mutual attraction—the first and essential stage in establishing swarms. M. L. Anstey, S. M. Rogers, S. R. Ott, M. Burrows, S. J. Simpson, Serotonin mediates behavioral gregarization underlying swarm formation in desert locusts. Science 323 , 627–630 (2009). [Abstract][Full Text] P. A. Stevenson, The key to Pandora9s box. Science 323 , 594–595 (2009). [Summary][Full Text]

Serotonin Mediates Behavioral Gregarization Underlying Swarm Formation in Desert Locusts

Desert locusts, Schistocerca gregaria, show extreme phenotypic plasticity, transforming between a little-seen solitarious phase and the notorious swarming gregarious phase depending on population density. An essential tipping point in the process of swarm formation is the initial switch from strong mutual aversion in solitarious locusts to coherent group formation and greater activity in gregarious locusts. We show here that serotonin, an evolutionarily conserved mediator of neuronal plasticity, is responsible for this behavioral transformation, being both necessary if behavioral gregarization is to occur and sufficient to induce it. Our data demonstrate a neurochemical mechanism linking interactions between individuals to large-scale changes in population structure and the onset of mass migration.

Mechanosensory-induced behavioural gregarization in the desert locustSchistocerca gregaria

Desert locusts show an extreme form of phenotypic plasticity, changing between a cryptic solitarious phase and a swarming gregarious phase that differ in many aspects of behaviour, physiology and appearance. Solitarious locusts show rapid behavioural phase change in response to tactile stimulation directed to the hind femora. Repeatedly touching as little as one quarter of the anterior (outer) surface area of a hind femur produced full behavioural gregarization within 4 h. Solitarious locusts have approximately 30% more mechanosensory trichoid sensilla on the hind femora than do gregarious locusts but have similar or fewer numbers of sensilla elsewhere on the legs. Tactile stimulation of a hind femur in solitarious locusts that had been restrained so that they could not move their legs failed to induce any behavioural gregarization. Patterned electrical stimulation of metathoracic nerve 5, which innervates the hind leg, however, produced full gregarization in restrained locusts. Our data show for the first time that the gregarizing signal combines both exteroceptive and proprioceptive components, which travel in both nerves 5B1 and 5B2, and provides us with a powerful experimental method with which to elicit and study neuronal plasticity in this system. Acetic acid odour, a strong chemosensory stimulus that activates the same local processing pathways as exteroceptive stimuli, failed to elicit behavioural gregarization, suggesting an early segregation in the central nervous system of the mechanosensory signals that leads to gregarization.

Effects of [His 7]-corazonin on the phase state of isolated-reared (solitarious) desert locusts, Schistocerca gregaria

[His 7]-corazonin is a neuropeptide produced in the pars lateralis of the brain. It is stored in the corpora cardiaca and probably released from there. The only well-documented effect in locusts is increased melanization of the cuticle. We investigated whether this hormone might also be causally related to changes in behavior and morphometrics that, like melanization, occur during crowding-induced gregarization. Solitary fourth-instar nymphs of Schistocerca gregaria (Forsk.) were injected thrice with 1 nmol [His 7]-corazonin. After molting to the 5th stadium their behavioral phase state was measured in an arena assay and analyzed using multiple logistic regression analysis. The hormone was found not to induce behavioral phase changes. Upon reaching adulthood, morphometrics shifts occurred towards values typical for crowd-reared and regregarized animals. Our results thus indicate that [His 7]-corazonin is not involved in behavioral gregarization but may participate in morphometrical phase change.

The influence of mechanical, visual and contact chemical stimulation on the behavioural phase state of solitarious desert locusts ( Schistocerca gregaria)

We investigated the influence of mechanical, visual and contact chemical stimulation on behavioural gregarization of fifth-instar solitarious nymphs of the desert locust. The stimuli were applied in two 2×2 factorial experimental designs, the first with contact chemical and mechanical stimuli, and the second with contact chemical and visual stimulation. Stimulus treatments were applied for a 4–5 h period, after which the behavioural phase state of individual locusts was measured using an assay based on multiple logistic regression analysis of behavioural variables. Mechanical stimulation was provided by showering test insects with millet seeds, thereby excluding the possibility of contact chemical self-stimulation by repeated contact with the same objects. Visual stimulation consisted of the sight of crowd-reared locusts, while contact chemical stimulation was a dichloromethane extract of cuticular hydrocarbons from gregarious nymphs applied to the perch of the test insect. Mechanical stimulation was powerfully gregarizing, whether alone or in combination with contact chemical stimuli. Application of cuticular extract to the perch had no measurable effect on behavioural phase state, either alone or when presented with mechanical or visual stimuli. Visual stimulation alone partly gregarized test locusts. These results appear to conflict with other reports of the gregarizing effect of cuticular hydrocarbons and possible reasons for this discrepancy are discussed.

A behavioural analysis of phase change in the desert locust

ABSTRACTA 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.

Effects of sensory stimuli on the behavioural phase state of the desert locust, Schistocerca gregaria

The nature of stimuli, emanating from other locusts, which are effective in inducing gregarization in the desert locust was investigated. Isolated-reared fifth-instar nymphs were subjected to tactile, visual and olfactory stimuli, presented singly and in combination, and the effect on the behavioural phase state was quantified using logistic regression analysis. Tactile stimulation provided by rolling paper spheres proved to be highly gregarizing, whether presented alone or in combination with the other stimuli. Olfactory and visual stimuli together caused partial behavioural gregarization. Visual stimulation alone was weakly gregarizing after prolonged exposure, while olfactory stimuli alone were ineffective. Nymphs and pre-reproductive and reproductive adults of both sexes were also treated with synthetic adult male `aggregation' pheromone blend (Torto et al., 1994, Journal of Chemical Ecology 20, 1749). No effect of this blend was found on the behavioural phase state, even when visual stimuli were present. Non-locust related stimuli, including wheat odour and flashing lights, were also tested on nymphs. Neither induced any change in the behavioural phase state, indicating that increased sensory flow is not a sufficient explanation for locust-induced behavioural phase change.

A Gregarizing Factor Present in the Egg Pod Foam of the Desert Locust Schistocerca gregaria

The behavioural phase state and coloration of hatchling Schistocerca gregaria were examined in a series of experiments to determine the means by which phase characteristics are passed between generations. Both crowding of solitary-reared females at the time of oviposition and high egg pod densities promoted behavioural gregarization, although the former appeared to be a rather more potent factor. In contrast, egg pod density alone appeared to promote the development of hatchlings with dark patterns characteristic of the gregarious phase. The phase characteristics of hatchlings were unaffected when sand previously used for oviposition was used to collect further egg pods. Early separation of presumptive gregarious eggs from egg pods laid by crowd reared females led to solitarization of the hatchlings, indicating that a factor, either in or around the eggs, removed by early separation promoted gregarization. Both the eggs and foam plugs of egg pods from crowd reared, gregarious females appeared to be a source of this gregarizing factor. In contrast, there was no evidence for a solitarization factor in egg pods from solitary-reared S. gregaria. Saline extracts of egg pod foam plugs produced an active factor which promoted gregarization both in eggs from solitary-reared females and in eggs from gregarious females which were separated and washed to remove the factor. Solitary eggs were influenced by the gregarizing factor in foam plug extracts for up to 1 day after oviposition. Saline extracts of foam plug retained their activity for up to 1 day. Initial studies on the properties of this factor were made. We conclude that the foam plugs of egg pods from crowd-reared, gregarious locusts contain a small (<3 kDa), hydrophilic gregarizing factor which is produced at the time of oviposition and which predisposes hatchlings to attain characteristics of the gregarious phase.

A gregarizing factor present in the egg pod foam of the desert locust Schistocerca gregaria.

The behavioural phase state and coloration of hatchling Schistocerca gregaria were examined in a series of experiments to determine the means by which phase characteristics are passed between generations. Both crowding of solitary-reared females at the time of oviposition and high egg pod densities promoted behavioural gregarization, although the former appeared to be a rather more potent factor. In contrast, egg pod density alone appeared to promote the development of hatchlings with dark patterns characteristic of the gregarious phase. The phase characteristics of hatchlings were unaffected when sand previously used for oviposition was used to collect further egg pods. Early separation of presumptive gregarious eggs from egg pods laid by crowd-reared females led to solitarization of the hatchlings, indicating that a factor, either in or around the eggs, removed by early separation promoted gregarization. Both the eggs and foam plugs of egg pods from crowd-reared, gregarious females appeared to be a source of this gregarizing factor. In contrast, there was no evidence for a solitarization factor in egg pods from solitary-reared S. gregaria. Saline extracts of egg pod foam plugs produced an active factor which promoted gregarization both in eggs from solitary-reared females and in eggs from gregarious females which were separated and washed to removed the factor. Solitary eggs were influenced by the gregarizing factor in foam plug extracts for up to 1 day after oviposition. Saline extracts of foam plug retained their activity for up to 1 day. Initial studies on the properties of this factor were made. We conclude that the foam plugs of egg pods from crowd-reared, gregarious locusts contain a small (<3 kDa), hydrophilic gregarizing factor which is produced at the time of oviposition and which predisposes hatchlings to attain characteristics of the gregarious phase.

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.

The time‐course of behavioural phase change in nymphs of the desert locust, Schistocerca gregaria

Abstract. The time‐course of behavioural phase change was investigated in nymphs of Schistocerca gregaria, using logistic regression analysis of behaviour recorded in a standard assay. Gregarization occurred very rapidly. Solitary‐reared nymphs became markedly gregarious in behaviour within 1‐4h of being placed in a crowd. These insects re‐solitarized equally quickly if removed from the crowd. Crowd‐reared locusts also solitarized within l‐4h, but this effect was not complete. Results indicate that, while behavioural gregarization is maximal within a few hours of crowding, solitarization is a two‐stage process, changing rapidly at first, then more slowly as a function of the period of previous crowding.