Risk of migration: not all gregarious locust nymphs reach appropriate refuges.

Sedentary animals choose appropriate refuges against predators, while migratory ones may not necessarily do so. In ectotherms, refuge selection is critical during low temperatures, because they cannot actively evade predators. To understand how migratory ectotherms alter their defensive behaviors depending on refuge quality in cold temperatures, we evaluated migratory gregarious desert locust nymphs (Schistocerca gregaria) in the Sahara Desert, where daily thermal constraints occur. We recorded how roosting plant type (bush/shrub) and its height influenced two alternative defense behaviors (dropping/stationary) during cold mornings, in response to an approaching simulated ground predator. Most locusts in bushes dropped within the bush and hid irrespective of their height, whereas those roosting > 2 m height in shrubs remained stationary. These defenses are effective and match with refuge plant types because dynamic locomotion is not required. When nymphs roosted on shrubs < 1.5-m height, which was an unsafe position, nearly half showed both defensive behaviors, indicating that escaping decisions become ambiguous when the refuges are inappropriate. These results suggest that locusts display flexible defensive behaviors when finding appropriate refuges and selecting refuge before daily thermal limitations occur could be critical for migratory ectotherms, which is a risk associated with migration.

Thermoregulatory behavior of lekking male desert locusts, Schistocerca gregaria, in the Sahara Desert.

Most terrestrial animals are constrained by extreme heat conditions such as midday desert environments, while a few terrestrial ectothermic insects are active in such ecological niches. Sexually mature males of the desert locust (Schistocerca gregaria) in the Sahara Desert remain on the open ground, despite the ground temperatures exceeding their lethal limit, to form leks and to mate incoming gravid females during the daytime. Lekking male locusts apparently suffer from extreme heat stress and greatly fluctuating thermal conditions. The present study examined the thermoregulatory strategies of the lekking male S. gregaria. Our field observations showed that lekking males changed their body orientation toward the sun depending on the temperature and time of day. In the relatively cool morning, males basked by orienting perpendicular to the sun's rays, maximizing the area of body surface exposed to the sun's rays. In contrast, around midday, when the ground surface temperature exceeded lethal high temperatures, some males tended to shelter inside the plants or remain in the shade. However, the remainder stayed on the ground, stilted (i.e., extending their legs to raise their bodies off the hot ground) and oriented parallel to the sun's rays, which minimized radiative heating. Measurements of body temperature throughout the hot middle period of the day confirmed that the stilting posture prevented overheating. Their critical lethal body temperature was as high as 54.7 °C. In this lekking system, gravid females enter male leks by flying. These incoming females usually landed on open ground, whereupon nearby males immediately approached, mounted, and mated the female, implying that males with greater heat-tolerance can increase mating chance. These results suggest that behavioral thermoregulation and physiologically high heat tolerance of male desert locusts allows them to endure extreme thermal conditions for lekking.

Egg size-dependent embryonic development in the desert locust, Schistocerca gregaria.

Phenotypic plasticity in body size is a product of modification of the developmental pathway. Although hatchlings of the desert locust, Schistocerca gregaria, show egg size-dependent plasticity in body size, it remains unclear how embryogenesis during egg development regulates final embryonic body size. To determine the developmental pathway causing body size variation at hatching, we examined egg and embryonic development at the early, middle, and late egg developmental stages in S. gregaria by comparing small and large eggs. Crowd-reared females produced larger eggs than isolated-reared females. The daily egg developmental rate was similar between small and large eggs: eggs dramatically absorbed external water after days 3 to 7 and nearly doubled the initial egg weight at the late stage of day 12. Morphological measurements of eggs and embryos at different days after oviposition revealed that large eggs were longer than small eggs throughout developmental stages. However, embryo length was similar between small and large eggs at the early stage (anatrepsis). Embryos begin to absorb yolk into their bodies after blastokinesis. The size of large-egg embryos increased significantly from the middle stage (katatrepsis) due to absorption of more yolk than small eggs. Egg length and embryo length were conspicuously larger in large eggs than in small eggs on day 12 of late katatrepsis. These results suggest that egg size did not influence the egg developmental rate and initial embryo size. Large eggs had more yolk and space, resulting in larger final embryos than small eggs. The amount of yolk and size of eggshells during katatrepsis could play a key role in determining hatchling body size in S. gregaria.

Allocation of more reproductive resource to egg size rather than clutch size of gregarious desert locust (Schistocerca gregaria) through increasing oogenesis period and oosorption rate.

The desert locust, Schistocerca gregaria, shows a density-dependent reproductive trade-off by laying fewer but larger eggs in crowded conditions (gregarious phase) than in isolated conditions (solitarious phase). However, the physiological mechanisms controlling reproductive resource allocation remain unclear. We examined how egg production processes, including ovulation timing (i.e., oogenesis period), oocyte and ovarian growth rates, and oosorption rate (resorbing developing terminal oocytes), regulate reproductive outputs (egg biomass per clutch, egg size, and clutch size) during a reproductive cycle in S. gregaria by rearing them either under isolated or crowded conditions. We observed a common density-dependent negative correlation between egg size and clutch size, with no significant difference in egg biomass between the two rearing conditions. Dissection of female locusts after different days of oviposition revealed that the daily oocyte growth rate was almost similar between the two rearing conditions, but crowd-reared females ovulated later than isolated-reared ones, resulting in further oocyte growth in the former. Terminal oocytes were renewed by previous penultimate oocytes at the onset of a new reproductive cycle, and oosorption mainly occurred at an early stage in both rearing conditions; however, crowd-reared locusts displayed higher levels of oosorption compared to their isolated-reared counterparts. Crowding induced a high oosorption rate, resulting in a reduced clutch size and a prolonged oogenesis period, which in turn allowed oocytes to intake more yolk, which was probably recycled via oosorption. These results suggest that the length of the oogenesis period and oosorption rate are manipulated by maternal density, and these physiological modifications interactively regulate reproductive trade-off in S. gregaria.

Band movement and thermoregulation in Schistocerca cancellata.

At high density, juvenile locusts create marching hopper bands. Understanding the roles of temperature and vegetation on the movement of these bands shall allow to better forecast and control them. Following a hopper band in North Argentina in November 2019, we explored the thermoregulation behaviours of the South American locust, Schistocerca cancellata. Gut-content samples informed about the feeding status at different time of the day. Hoppers' body temperature was above cold air temperature in the mornings during basking and group-basking activities and before the onset of marching behaviour. Marching by walking or hopping was dominant at body temperatures close to 40 °C. Jumping, stilting, shading and perching on plants were seen as thermoregulatory behaviours to avoid ground temperatures above 50 °C. Feeding was observed throughout the day with continuous high gut contents despite an intermittent pattern of feeding-resting-marching. Speed and daily travelled distance of the front of the hopper band was depending on the type of encountered vegetation. Daily behavioural patterns, thermoregulatory behaviours, walking speed and daily travelled distances of S. cancellata were similar to the ones observed for the Desert locust, S. gregaria, in Africa. High air temperatures recorded during the observation times could explain the continuous feeding patterns. These species may have evolved behaviours of alternating consuming a bit and marching as a migration strategy to avoid staying where no food is available after the havoc left behind large hopper bands. Recommendations made for the control of Desert locust hopper bands can be extended to South American locust ones.

Density-dependent mating behaviors reduce male mating harassment in locusts.

Male mating harassment may occur when females and males do not have the same mating objectives. Communal animals need to manage the costs of male mating harassment. Here, we demonstrate how desert locusts in dense populations reduce such conflicts through behaviors. In transient populations (of solitarious morphology but gregarious behavior), we found that nongravid females occupied separate sites far from males and were not mating, whereas males aggregated on open ground (leks), waiting for gravid females to enter the lekking sites. Once a male mounted a gravid female, no other males attacked the pair; mating pairs were thereby protected during the vulnerable time of oviposition. In comparison, solitarious locusts displayed a balanced sex ratio in low-density populations, and females mated irrespective of their ovarian state. Our results indicate that the mating behaviors of desert locusts are density dependent and that sex-biased behavioral group separation may minimize the costs of male mating harassment and competition.

A general model of the thermal constraints on the world's most destructive locust, Schistocerca gregaria.

All terrestrial ectotherms are constrained to some degree by their thermal environment and the extent to which they can behaviorally buffer variable thermal conditions. New biophysical modeling methods (NicheMapR) allow the calculation of the body temperature of thermoregulating animals anywhere in the world from first principles, but require detailed observational data for parameterization and testing. Here we describe the thermoregulatory biology of marching bands of the desert locust, Schistocerca gregaria, in the Sahara Desert of Mauritania where extreme heat and strong diurnal fluctuations are a major constraint on activity and physiological processes. Using a thermal infrared camera in the field, we showed that gregarious nymphs altered the microhabitats they used, as well as postural thermoregulatory behaviors, to maintain relatively high body temperature (nearly 40°C). Field and laboratory experiments demonstrated that the preferred body temperature accelerated digestive rates. Migratory bands frequently left foraging sites with full guts before consuming all vegetation and moved to another habitat before emptying their foregut. Thus, the repertoire for behavioral thermoregulation in the desert locust strongly facilitates foraging and digestion rates, which may accelerate developmental rates and increase survival. We used our data to successfully parameterize a general biophysical model of thermoregulatory behavior that could capture hourly body temperature and activity at our remote site using globally available environmental forcing data. This modeling approach provides a stronger basis for forecasting thermal constraints on locust outbreaks under current and future climates.

The desert locust, Schistocerca gregaria, plastically manipulates egg size by regulating both egg numbers and production rate according to population density.

Egg-size adjustment is one of the important plastic life-history traits for animals living in heterogeneous environments. The adaptive investment hypothesis predicts that mothers should increase progeny size according to certain cues predicting adverse future conditions of their offspring. However, reproductive resources are limited, and females have to simultaneously reduce egg number to allocate more resources to increase size. It remains unclear how single individuals alter egg size and number according to temporally heterogeneous environments. In the present study, we examined how desert locusts, Schistocerca gregaria, plastically alter egg size and number according to population density. We also investigated the trans-generational maternal effects on progeny characteristics as well as their own maternal physiological response (oviposition interval). Females kept in crowded conditions laid significantly larger and heavier eggs by reducing clutch size (number of eggs per egg pod) compared to isolated females, suggesting the existence of a reproductive trade-off between the two traits. The crowding-forced isolated females induced concerted changes not only in egg size but also in egg number tending towards those characteristics of gregarious control, implying that single individuals showed trade-off when egg size was increased. Double-blind testing confirmed the rapid crowding effects on egg size. Females also responded to crowding by extending the oviposition interval. As the oviposition interval extended, egg size increased, but clutch size decreased. Eggs from crowding-forced isolated females began to produce gregarious-phase type hatchlings (large and black) instead of solitarious-phase type ones (small and green). These results suggested that S. gregaria plastically manipulate egg size by regulating egg numbers and egg production rate, and indicated the presence of trans-generational maternal effects on progeny phase.

Aggregation Site Choice by Gregarious Nymphs of the Desert Locust, Schistocerca gregaria, in the Sahara Desert of Mauritania.

Animals often aggregate at certain sites during vulnerable periods such as night-roosting as an anti-predatory strategy. Some migratory gregarious animals must regularly find new night-roosting sites, but how they synchronously choose such sites is poorly understood. We examined how gregarious nymphs of the desert locust, Schistocerca gregaria Forskål (Orthoptera: Acrididae), aggregate at certain plants for night-roosting in the Sahara Desert. Migratory bands of last instar nymphs climbed trees around dusk and roosted there overnight. A spatial autocorrelation analysis of plants indicated that the larger locust groups formed at the larger plants within the local plant community. Other large groups were not formed near the large tree, but smaller groups were patchily distributed. Plant height was the primary cue used by migratory bands to choose night-roosting plants. A nearest-neighbor distance analysis showed that single conspicuous large trees with scattered smaller plants were distributed locally. This plant community structure and negative geotactic ascending behavior of gregarious nymphs may force them to concentrate at the landmark plant from all directions and afar. This plant-size-dependent roosting site choice may contribute for developing artificial trapping systems for locusts and inciting to a new environment-friendly night control approach.

Daily microhabitat shifting of solitarious-phase Desert locust adults: implications for meaningful population monitoring.

The Desert locust Schistocerca gregaria is a major world pest that causes substantial agricultural and economic damage. Effective pest control relies on effective monitoring, which requires knowledge of locust microhabitat selection. Yet little is known about microhabitat selection of solitarious adult locusts in the field. We conducted field surveys to investigate fine-scale diel temporal and spatial distributions of solitarious adults in the Sahara Desert in Mauritania, a major breeding and recession area. We found that solitarious adults moved among different, specific microhabitats throughout the 24-h period in a cyclical manner. At night, they roosted in trees, moved to the ground to feed shortly after dawn, sheltered in low vegetation during the hot midday, and returned to the ground in the late afternoon. Hence, they switched microhabitats and plant species throughout each day. These cyclical daily movements among diverse microhabitats and specific plant species were correlated with time of day, light intensity, temperature, humidity, and specific plant species, and may relate to anti-predator defence, thermoregulation, and feeding. The present study suggests that locust monitoring should be adjusted, based on time of day, locust age, phase state and relative abundance of specific plant species. For example, we recommend surveying ground after morning and trees at night, for solitarious adults, when at low density.