Individual Locusts Research Articles

Unveiling the role of climate in spatially synchronized locust outbreak risks.

Desert locusts threaten crop production and food security. Spatially synchronized locust outbreaks further exacerbate these crises. Continental-scale understanding of such compound locust risks and underlying climatic drivers is crucial to designing coordinated and predictive control strategies but remains elusive. Here, we develop a data-driven framework to assess the compound risk of locust outbreaks in the Middle East and North Africa (MENA) and elucidate the role of climate in locust dynamics. We find that more than one-fifth of high-risk country pairs faced spatially synchronized locust risks from 1985 to 2020, dominated by concurrent winds or inundations. Individual locusts are more prone to infest arid areas punched by extreme rainfall. The spatial prevalence of locusts is strongly modulated by climate variability such as El Niño-Southern Oscillation. A warming climate will lead to widespread increases in locust outbreaks with emerging hotspots in west central Asia, posing additional challenges to the global coordination of locust control.

An effective hydrodynamic description of marching locusts

A fundamental question in complex systems is how to relate interactions between individual components (‘microscopic description’) to the global properties of the system (‘macroscopic description’). Furthermore, it is unclear whether such a macroscopic description exists and if such a description can capture large-scale properties. Here, we address the validity of a macroscopic description of a complex biological system using the collective motion of desert locusts as a canonical example. One of the world’s most devastating insect plagues begins when flightless juvenile locusts form ‘marching bands’. These bands display remarkable coordinated motion, moving through semiarid habitats in search of food. We investigated how well macroscopic physical models can describe the flow of locusts within a band. For this, we filmed locusts within marching bands during an outbreak in Kenya and automatically tracked all individuals passing through the camera frame. We first analyzed the spatial topology of nearest neighbors and found individuals to be isotropically distributed. Despite this apparent randomness, a local order was observed in regions of high density in the radial distribution function, akin to an ordered fluid. Furthermore, reconstructing individual locust trajectories revealed a highly aligned movement, consistent with the one-dimensional version of the Toner-Tu equations, a generalization of the Navier–Stokes equations for fluids, used to describe the equivalent macroscopic fluid properties of active particles. Using this effective Toner–Tu equation, which relates the gradient of the pressure to the acceleration, we show that the effective ‘pressure’ of locusts increases as a linear function of density in segments with the highest polarization (for which the one-dimensional approximation is most appropriate). Our study thus demonstrates an effective hydrodynamic description of flow dynamics in plague locust swarms.

Anisotropic interaction and motion states of locusts in a hopper band.

Swarming locusts present a quintessential example of animal collective motion. Juvenile locusts march and hop across the ground in coordinated groups called hopper bands. Composed of up to millions of insects, hopper bands exhibit aligned motion and various collective structures. These groups are well-documented in the field, but the individual insects themselves are typically studied in much smaller groups in laboratory experiments. We present, to our knowledge, the first trajectory data that detail the movement of individual locusts within a hopper band in a natural setting. Using automated video tracking, we derive our data from footage of four distinct hopper bands of the Australian plague locust, Chortoicetes terminifera. We reconstruct nearly 200 000 individual trajectories composed of over 3.3 million locust positions. We classify these data into three motion states: stationary, walking and hopping. Distributions of relative neighbour positions reveal anisotropies that depend on motion state. Stationary locusts have high-density areas distributed around them apparently at random. Walking locusts have a low-density area in front of them. Hopping locusts have low-density areas in front and behind them. Our results suggest novel insect interactions, namely that locusts change their motion to avoid colliding with neighbours in front of them.

A journey towards an integrated understanding of behavioural phase change in locusts

Behavioural phase change initiates and functionally couples the suite of traits that comprise density-dependent polyphenism in locusts. Here I provide a semi-expurgated account of my 25-year research journey studying behavioural phase transition in the desert locust. The journey spans continents, involves a cast of extraordinary colleagues, and travels across levels of biological organisation from deep within the nervous system of individual locusts to mass migration and the evolution and population dynamics of swarming.

Radar monitoring unveils migration dynamics of the yellow-spined bamboo locust (Orthoptera: Arcypteridae)

Accurate monitoring of locust migration is the basis for early warning and emergency control programs. This article integrates laboratory recordings with the use of Ku-band vertical insect radar to assess migration of the yellow-spined bamboo locust Ceracris kiangsu (Orthoptera: Arcypteridae) in the China-Laos border area. Under laboratory conditions, field-caught individuals engaged in flight at temperatures above 20℃ and exhibited a wingbeat frequency of 18.5–31.1 Hz. Between July 6 and August 23, 2020, a total of 39C. kiangsu migration events were recorded by radar. Locust individuals only engaged in diurnal migration, with peak activity after 15:00. Flight was recorded at an average height, flight speed and density of 410 m above ground level, 35.8 km/h, and 1305.9 individuals/km3, respectively. High-density C. kiangsu swarms exhibited high flight speeds. Departing from Laos, locusts migrated north by west 27.4–35.0° into Jiangcheng county (Yunnan, China). Migration flight was affected by ambient temperature, while its speed was determined by that of prevailing wind currents. Individual locusts autonomously adjusted their heading direction in order to unify the travel direction of the migrant swarm. Ku-band high-resolution fully polarimetric insect radar can thus accurately assess the migration patterns of C. kiangsu locusts and thereby constitutes an important forecasting tool.

Extremely Low-Frequency Electromagnetic Fields Entrain Locust Wingbeats.

Extremely low-frequency electromagnetic fields (ELF EMFs) have been shown to impact the behavior and physiology of insects. Recent studies have highlighted the need for more research to determine more specifically how they affect flying insects. Here, we ask how locust flight is affected by acute exposure to 50 Hz EMFs. We analyzed the flights of individual locusts tethered between a pair of copper wire coils generating EMFs of various frequency using high-speed video recording. The mean wingbeat frequency of tethered locusts was 18.92 ± 0.27 Hz. We found that acute exposure to 50 Hz EMFs significantly increased absolute change in wingbeat frequency in a field strength-dependent manner, with greater field strengths causing greater changes in wingbeat frequency. The effect of EMFs on wingbeat frequency depended on the initial wingbeat frequency of a locust, with locusts flying at a frequency lower than 20 Hz increasingtheir wingbeat frequency, while locusts flying with a wingbeat frequency higher than 20 Hz decreasing their wingbeat frequency. During the application of 50 Hz EMF, the wingbeat frequency was entrained to a 2:5 ratio (two wingbeat cycles to five EMF cycles) of the applied EMF. We then applied a range of ELF EMFs that were close to normal wingbeat frequency and found that locusts entrained to the exact frequency of the applied EMF. These results show that exposure to ELF EMFs lead to small but significant changes in wingbeat frequency in locusts. We discuss the biological implications of the coordination of insect flight in response to electromagnetic stimuli. © 2021 Bioelectromagnetics Society.

Hyperkalaemia, not apoptosis, accurately predicts insect chilling injury.

There is a growing appreciation that insect distribution and abundance are associated with the limits of thermal tolerance, but the physiology underlying thermal tolerance remains poorly understood. Many insects, like the migratory locust (Locusta migratoria), suffer a loss of ion and water balance leading to hyperkalaemia (high extracellular [K+]) in the cold that indirectly causes cell death. Cells can die in several ways under stress, and how they die is of critical importance to identifying and understanding the nature of thermal adaptation. Whether apoptotic or necrotic cell death pathways are responsible for low-temperature injury is unclear. Here, we use a caspase-3 specific assay to indirectly quantify apoptotic cell death in three locust tissues (muscle, nerves and midgut) following prolonged chilling and recovery from an injury-inducing cold exposure. Furthermore, we obtain matching measurements of injury, extracellular [K+] and muscle caspase-3 activity in individual locusts to gain further insight into the mechanistic nature of chilling injury. We found a significant increase in muscle caspase-3 activity, but no such increase was observed in either nervous or gut tissue from the same animals, suggesting that chill injury primarily relates to muscle cell death. Levels of chilling injury measured at the whole animal level, however, were strongly correlated with the degree of haemolymph hyperkalaemia, and not apoptosis. These results support the notion that cold-induced ion balance disruption triggers cell death but also that apoptosis is not the main form of cell damage driving low-temperature injury.

Molecular characterization of cultivable bacteria associated with adult Schistocerca gregaria, using 16S rRNA

S. gregaria is able to swarm and disseminate bacterial load over vast areas. Adult locusts were collected from Kingdom of Saudi Arabia (KSA), individual locust was divided into head, thorax and abdomen. External and internal cultivable bacteria were cultured, cell and colony characteristics were investigated. Pure colonies were sequenced using 16S rRNA. Sequences and phylogeny were analyzed. Using morphological and molecular results, 9 bacterial genera belonging to 5 families, 3 orders, 2 classes, and 2 phyla were recorded. Ribosomal Database Project (RDP) Classifier succeeded to confirm 8 out of 9 genera. The ninth isolate was designated as unclassified. To specify a genus to its closest species, 16S rRNA genes of the type species have been downloaded. Phylogenetic tree was generated using all available sequences. Similarity measures and phylogenetic trees were used to place each genus to its closest species. Six genera created similarities less than 98% to related species. Generally, analyses of 16S rRNA gene succeeded to identify 3 isolates to species level, 5 isolates to genus level and designated one isolate “unclassified”. Investigations are recommended to place all genera to their operational taxonomic units (OTU). Significance of our findings relies on the impact of locust-microbiota on heath of people who consumed insects as food. Bacterial species which were internally, isolated from abdomen were described beneficial commensals. Bacterial species which were internally, isolated from thorax and head were described non-pathogenic beneficial endosymbionts, except Bacillus sp. Salmonella sp. was isolated as external species and was described external contaminant of the locust.

Respiratory patterns in field collected brown locust, Locustana pardalina, in the gregarious phase

In this paper we report on the metabolic rates and respiratory patterns measured from gregarious brown locusts, Locustana pardalina, collected from the Nama Karoo region in South Africa. All five instar hopper stages and adults were collected over a three year period when significant numbers of locust swarms were seen. Flow-through respirometry was used to measure the CO2 emission from individual locusts from all the developmental stages and adults within a week of collection. Carbon dioxide emission scaled hypometrically with mass, 0.863 ± 0.026. Except in the 1st and 5th instar stage there was no difference in the mass specific rate of CO2 emission (V̇<ce:small-caps>CO2</ce:small-caps>). These had significantly higher metabolic rates compared to the other stages which reflects their biology, with the 1st instar undergoing rapid growth and the 5th instar also undergoing rapid growth and development in preparation for becoming an adult. The 1st instars used a form of continuous gas exchange while all the other stages showed discontinuous gas exchange cycles. A clear burst phase and interburst periods could be seen. The 2nd and 3rd instars use mainly diffusion to expel CO2 and so exhibited an open form of the burst phase. There was an increase in CO2 volleys seen in the burst phase from the 4th instar stage onwards thus indicating an increased use of convection. There was no change in the duration or frequency of the discontinuous gas exchange cycles through the locust development or with body mass.

Individual pause-and-go motion is instrumental to the formation and maintenance of swarms of marching locust nymphs.

The principal interactions leading to the emergence of order in swarms of marching locust nymphs was studied both experimentally, using small groups of marching locusts in the lab, and using computer simulations. We utilized a custom tracking algorithm to reveal fundamental animal-animal interactions leading to collective motion. Uncovering this behavior introduced a new agent-based modeling approach in which pause-and-go motion is pivotal. The behavioral and modeling findings are largely based on motion-related visual sensory inputs obtained by the individual locust. Results suggest a generic principle, in which intermittent animal motion can be considered as a sequence of individual decisions as animals repeatedly reassess their situation and decide whether or not to swarm. This interpretation implies, among other things, some generic characteristics regarding the build-up and emergence of collective order in swarms: in particular, that order and disorder are generic meta-stable states of the system, suggesting that the emergence of order is kinetic and does not necessarily require external environmental changes. This work calls for further experimental as well as theoretical investigation of the neural mechanisms underlying locust coordinative behavior.

Memoirs of a locust: Density-dependent behavioral change as a model for learning and memory

A locust outbreak is a stupendous natural phenomenon that remains in the memory of whoever has been lucky (or unlucky) enough to witness it. Recent years have provided novel and important insights into the neurobiology of locust swarming. However, the central nervous system processes that accompany and perhaps even lie at the basis of locust phase transformation are still far from being fully understood. Our current work deals with the memory of a locust outbreak from a new perspective: that of the individual locust. We take locust density-dependent phase transformation – a unique example of extreme behavioral plasticity, and place it within the context of the accepted scheme of learning and memory. We confirm that a short time period of exposure to a small crowd of locusts is sufficient to induce a significant behavioral change in a previously solitary locust. Our results suggest that part of the behavioral change is due to long-term habituation of evasive and escape responses. We further demonstrate that the memory of a crowding event lasts for at least 24 h, and that this memory is sensitive to a protein synthesis blocker. These findings add much to our understanding of locust density-dependent phase polyphenism. Furthermore, they offer a novel and tractable model for the study of learning and memory-related processes in a very distinctive behavioral context.

Inherent noise can facilitate coherence in collective swarm motion.

Among the most striking aspects of the movement of many animal groups are their sudden coherent changes in direction. Recent observations of locusts and starlings have shown that this directional switching is an intrinsic property of their motion. Similar direction switches are seen in self-propelled particle and other models of group motion. Comprehending the factors that determine such switches is key to understanding the movement of these groups. Here, we adopt a coarse-grained approach to the study of directional switching in a self-propelled particle model assuming an underlying one-dimensional Fokker-Planck equation for the mean velocity of the particles. We continue with this assumption in analyzing experimental data on locusts and use a similar systematic Fokker-Planck equation coefficient estimation approach to extract the relevant information for the assumed Fokker-Planck equation underlying that experimental data. In the experiment itself the motion of groups of 5 to 100 locust nymphs was investigated in a homogeneous laboratory environment, helping us to establish the intrinsic dynamics of locust marching bands. We determine the mean time between direction switches as a function of group density for the experimental data and the self-propelled particle model. This systematic approach allows us to identify key differences between the experimental data and the model, revealing that individual locusts appear to increase the randomness of their movements in response to a loss of alignment by the group. We give a quantitative description of how locusts use noise to maintain swarm alignment. We discuss further how properties of individual animal behavior, inferred by using the Fokker-Planck equation coefficient estimation approach, can be implemented in the self-propelled particle model to replicate qualitatively the group level dynamics seen in the experimental data.

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.

Resource distribution mediates synchronization of physiological rhythms in locust groups

Synchronized behaviour is common in animal groups. In ant colonies, synchronization occurs because active ants stimulate their neighbours to activity. We use oscillator theory to explain how stimulation from active neighbours synchronizes activity in groups of solitarious locusts via entrainment of internal physiological rhythms. We also show that the spatial distribution of food resources controls coupling between individual locusts and the emergence of synchronized activity. In locusts (Schistocerca gregaria), individual schedules of activity and quiescence arise from an irregular physiological oscillation in feeding excitation (i.e. hunger). We show that contact with an active neighbour increases the probability that a locust becomes active. This entrained activity decreases the time until the locust feeds, shifting the phase of its hunger oscillation. The locusts' internal physiological rhythms are thus brought into alignment and their activity becomes synchronized. When food resources are clumped, contact with active locusts increases, and this increase in the strength of coupling between individuals leads to greater synchronization of behaviour. Activity synchronization might have functional significance in inhibiting swarming when resources are dispersed and accelerating it in more favourable clumped environments.

Nonlinear time-periodic models of the longitudinal flight dynamics of desert locusts Schistocerca gregaria.

Previous studies of insect flight control have been statistical in approach, simply correlating wing kinematics with body kinematics or force production. Kinematics and forces are linked by Newtonian mechanics, so adopting a dynamics-based approach is necessary if we are to place the study of insect flight on its proper physical footing. Here we develop semi-empirical models of the longitudinal flight dynamics of desert locusts Schistocerca gregaria. We use instantaneous force-moment measurements from individual locusts to parametrize the nonlinear rigid body equations of motion. Since the instantaneous forces are approximately periodic, we represent them using Fourier series, which are embedded in the equations of motion to give a nonlinear time-periodic (NLTP) model. This is a proper mathematical generalization of an earlier linear-time invariant (LTI) model of locust flight dynamics, developed using previously published time-averaged versions of the instantaneous force recordings. We perform various numerical simulations, within the fitted range of the model, and across the range of body angles used by free-flying locusts, to explore the likely behaviour of the locusts upon release from the tether. Solutions of the NLTP models are compared with solutions of the nonlinear time-invariant (NLTI) models to which they reduce when the periodic terms are dropped. Both sets of models are unstable and therefore fail to explain locust flight stability fully. Nevertheless, whereas the measured forces include statistically significant harmonic content up to about the eighth harmonic, the simulated flight trajectories display no harmonic content above the fundamental forcing frequency. Hence, manoeuvre control in locusts will not directly reflect subtle changes in the higher harmonics of the wing beat, but must operate on a coarser time-scale. A state-space analysis of the NLTP models reveals orbital trajectories that are impossible to capture in the LTI and NLTI models, and inspires the hypothesis that asymptotic orbital stability is the proper definition of stability in flapping flight. Manoeuvre control on the scale of more than one wing beat would then consist in exciting transients from one asymptotically stable orbit to another. We summarize these hypotheses by proposing a limit-cycle analogy for flapping flight control and suggest experiments for verification of the limit-cycle control analogy hypothesis.

Linking Locust Gregarization to Local Resource Distribution Patterns Across a Large Spatial Scale

Abstract Spatial resource distribution patterns play an important role in mediating density-dependent phase change (gregarization) in locusts. The degree of contagion or aggregation of resources in a habitat can increase the probability of locust gregarization by increasing the frequency of contact among individual locusts. The spatial distribution patterns of two resources upon which gregarization can occur, the tussock grasses Aristida pungens and Panicum turgidum (Poaceae), were examined in two adjacent regions of the desert locust (Schistocerca gregaria Forskal) plague recession area in Mauritania that differ in their frequencies of locust gregarization. The hypothesis that the distribution of grass tufts should be more aggregated and thus more likely to promote locust phase change in the high frequency gregarization area was tested. Tufts were more abundant, and both species were larger in the high frequency gregarization area. The spatial distribution patterns of tufts in both areas were largely agg...

Fractal index captures the role of vegetation clumping in locust swarming

Summary This paper evaluates box‐counting dimension as a quantitative clumping index for discontinuous plant cover, and applies it to studies of both small‐ and large‐scale ecological processes in desert locust (Schistocerca gregaria) swarming. The quadrat under study is tiled with squares of increasing size, and the relationship between the number of occupied squares and square size gives the box‐counting dimension. This index is high for random distributions and decreases when the vegetation is clumped; it is also positively linked to the abundance of vegetation. At the scale of individual locusts, this index captures the space‐filling properties of vegetation that promote change to the gregarious phase and the onset of swarming. At the very large scale, box‐counting dimension measured from satellite imagery reflects topography, which influences the concentration and migration of locust swarms. Fractal geometry considers scale of measurement in quantifying pattern and provides a framework to interpret ecological phenomena across spatial scales. Demonstration of a statistically significant relationship between the box‐counting exponent and locust behaviour shows how this approach can be applied to ecological studies.

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

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

Coordinated righting behaviour in locusts.

A locust placed upside down on a flat surface uses a predictable sequence of leg movements to right itself. To analyse this behaviour, we made use of a naturally occurring state of quiescence (thanatosis) to position locusts in a standardised upside-down position from which they spontaneously right themselves. Locusts grasped around the pronotum enter a state of thanatosis during which the limbs can be manipulated into particular postures, where they remain, and the animal can be placed upside down on the ground. When released, thanatosis lasts 4-456 s (mean 73 s) before the animal suddenly becomes active again and rights itself within a further 600 ms. Thanatosis is characterised by very low levels of leg motor activity. During righting, one hind leg provides most of the downward force against the ground that rolls the body around a longitudinal axis towards the other side. The driving force is produced by femoral levation (relative to the body) at the trochanter and by tibial extension. As the animal rolls over, the hind leg on the other side is also levated at the trochanter, so that it does not obstruct the movement. The forelegs and middle legs are not required for successful righting but they can help initially to tip the locust to one side, and at the end of the movement they help stop the roll as the animal turns upright. Individual locusts have a preferred righting direction but can, nevertheless, roll to either side. Locusts falling upside down through the air use both passive and active mechanisms to right themselves before they land. Without active movements, falling locusts tend to rotate into an upright position, but most locusts extend their hind leg tibiae and/or spread their wings, which increases the success of mid-air righting from 28 to 49 % when falling from 30 cm. The rapid and reliable righting behaviour of locusts reduces the time spent in a vulnerable upside-down position. Their narrow body geometry, large hind legs, which can generate substantial dorsally directed force, and the particular patterns of coordinated movements of the legs on both sides of the body are the key features that permit locusts to right themselves effectively. The reliability of autonomous multi-legged robots may be enhanced by incorporating these features into their design.

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.