Stav Talal

To migrate successfully, animals must meet elevated energy demands, often from lipid stores built through direct consumption or lipogenesis from carbohydrates. Locusts are among the most well-known insect migrants, as swarms travel long distances over multiple days, devastating agriculture. Despite their major impact on humans and decades of study, little is known about the nutritional and energetic needs of locust migration. We tested whether migratory locusts, Locusta migratoria, can maintain energy stores when flying multiple days with access to a near-optimal artificial diet. We measured flight durations, fuel stores and self-selected macronutrient intake before, during and after 3 days of up to 5 h of tethered flight, and compared these with a non-flying control group. During flight days, locusts increased carbohydrate consumption by ∼30% with little change in protein intake. Yet, despite 19 h day−1 of access to high quality food, they lost ∼30% of stored body lipid across the three flight days. We developed two models to explore lipid losses during flight. The first model indicates that intake and assimilation capacity constrain daily refueling rates and estimates locusts cannot sustain more than approximately 1 h of daily flight, despite unlimited high energy food, without energy deficits and lipid loss. The second model leverages data of swarms tracked by aircraft for 10–30 days to explore the importance of initial lipid stores and refueling days. Together, the empirical data and models provide evidence that long-distance locust migrations require pre-migratory fattening and/or extended stopovers where locusts can feed for several days. These findings highlight the importance of energetics for predicting migration dynamics.

Aerobic capacity in arachnids is closely linked with considerable structural variation in their respiratory systems. However, although all scorpions are non-tracheated and possess four pairs of book lungs, they vary greatly in their locomotor activity patterns. Many non-burrowing species express short bursts of activity whereas other species dig deep burrows within hours, suggesting more aerobically fueled exercise. We hypothesized that locomotion in surface dwellers is more dependent on anaerobic ATP synthesis, and that this would be reflected in their exercise performance and functional adaptation to potential disturbance of resting-state homeostasis. We used an experimental design consisting of two surface-dwelling Buthidae species (Hottentotta judaicus and Leiurus hebraeus), a burrowing buthid (Buthus israelis) and two burrowing Scorpionidae (Scorpio fuscus and Scorpio palmatus). Maximum running speeds were higher for buthids, which were also more prone to fatigue than scorpionids. Higher respiratory exchange ratios recorded for buthids during activity and subsequent recovery indicated a higher reliance on anaerobically fueled locomotion compared with scorpionids. Our data show that quicker removal of excess CO2 resulting from anaerobic exercise and hemolymph buffering in buthids is associated with significantly higher carbonic anhydrase activity in their hemolymph, compared with that of scorpionids. Efficient CO2 emission may also contribute to the lower respiratory water losses of buthids, and thus assist in facing both biotic and abiotic challenges of surface existence, from which the scorpionid burrows provide refuge.

Organisms require dietary macronutrients in specific ratios to maximize performance, and variation in macronutrient requirements plays a central role in niche determination. Although it is well recognized that development and body size can have strong and predictable effects on many aspects of organismal function, we lack a predictive understanding of ontogenetic or scaling effects on macronutrient intake. We determined protein and carbohydrate intake throughout development on lab populations of locusts and compared to late instars of field populations. Self-selected protein:carbohydrate targets declined dramatically through ontogeny, due primarily to declines in mass-specific protein consumption rates which were highly correlated with declines in specific growth rates. Lab results for protein consumption rates partly matched results from field-collected locusts. However, field locusts consumed nearly double the carbohydrate, likely due to higher activity and metabolic rates. Combining our results with the available data for animals, both across species and during ontogeny, protein consumption scaled predictably and hypometrically, demonstrating a new scaling rule key for understanding nutritional ecology.

Many theoretical treatments of foraging use energy as currency, with carbohydrates and lipids considered interchangeable as energy sources. However, herbivores must often synthesize lipids from carbohydrates since they are in short supply in plants, theoretically increasing the cost of growth. We tested whether a generalist insect herbivore ( Locusta migratoria ) can improve its growth efficiency by consuming lipids, and whether these locusts have a preferred caloric intake ratio of carbohydrate to lipid (C : L). Locusts fed pairs of isocaloric, isoprotein diets differing in C and L consistently selected a 2C : 1L target. Locusts reared on isocaloric, isoprotein 3C : 0L diets attained similar final body masses and lipid contents to locusts fed the 2C : 1L diet, but they ate more and had a ~12% higher metabolic rate, indicating an energetic cost for lipogenesis. These results demonstrate that some animals can selectively regulate carbohydrate-to-lipid intake and that consumption of dietary lipids can improve growth efficiency.

Many theoretical treatments of foraging use energy as currency, with carbohydrates and lipids considered interchangeable as energy sources. However, herbivores must often synthesize lipids from carbohydrates since they are in short supply in plants, theoretically increasing the cost of growth. We tested whether a generalist insect herbivore ( Locusta migratoria ) can improve their growth efficiency by consuming lipids, and whether these locusts have a preferred intake target ratio of carbohydrate (C) to lipid (L). Locusts fed pairs of isocaloric, isoprotein diets differing in C and L consistently selected a 2C:1L target. Locusts reared on isocaloric, isoprotein 3C:0L diets attained similar final body masses and lipid contents as locusts fed the 2C:1L diet but ate more and had a ~12% higher metabolic rate—indicating an energetic cost for lipogenesis. These results demonstrate that some animals can selectively regulate carbohydrate to lipid intake and that consumption of dietary lipid can improve growth efficiency.

Organisms require dietary macronutrients in specific ratios to maximize performance, and variation in macronutrient requirements plays a central role in niche determination. Although it is well-recognized that development and body size can have strong and predictable effects on many aspects of organismal function, we lack a predictive understanding of ontogenetic or scaling effects on macronutrient intake. We determined protein and carbohydrate intake throughout development on lab populations of locusts and tested whether lab responses can predict results for field populations. Self-selected protein:carbohydrate targets declined dramatically through ontogeny, due primarily to declines in mass-specific protein consumption rates which were highly correlated with declines in specific growth rates. Importantly, lab results for protein consumption rates predicted results for field-collected locusts. However, field locusts consumed nearly double the carbohydrate, likely due to higher activity and metabolic rates. Combining our results with the available data for animals, both across species and during ontogeny, protein consumption scaled predictably and hypometrically, demonstrating a new scaling rule key for understanding nutritional ecology.

Air sacs are a well-known aspect of insect tracheal systems, but have received little research attention. In this Commentary, we suggest that the study of the distribution and function of air sacs in tracheate arthropods can provide insights of broad significance. We provide preliminary phylogenetic evidence that the developmental pathways for creation of air sacs are broadly conserved throughout the arthropods, and that possession of air sacs is strongly associated with a few traits, including the capacity for powerful flight, large body or appendage size and buoyancy control. We also discuss how tracheal compression can serve as an additional mechanism for achieving advection in tracheal systems. Together, these patterns suggest that the possession of air sacs has both benefits and costs that remain poorly understood. New technologies for visualization and functional analysis of tracheal systems provide exciting approaches for investigations that will be of broad significance for understanding invertebrate evolution.

Migration allows animals to track favorable environments and avoid harmful conditions. However, migration is energetically costly, so migrating animals must prepare themselves by increasing their energy stores. Despite the importance of locust migratory swarms, we still understand little about the physiology of locust migration. During long-distance flight, locusts rely on lipid oxidation, despite the fact that lipids are relatively rare in their leaf-based diets. Therefore, locusts and other insect herbivores synthesize and store lipid from ingested carbohydrates, which are also important for initial flight. These data suggest that diets high in carbohydrate should increase lipid stores and the capacity for migratory flight in locusts. As predicted, locust lipid stores and flight performance increased with an increase in the relative carbohydrate content in their food. However, locust flight termination was not associated with complete lipid depletion. We propose potential testable mechanisms that might explain how macronutrient consumption can affect flight endurance.

Locusts have been reported to elevate metabolic rate in response to high carbohydrate diets; this conclusion was based on metabolic rates calculated from CO2 production, a common practice for insects. However, respiratory exchange ratio (RER, CO2 production divided by O2 consumption) can rise above 1 as a result of de novo lipid synthesis, providing an alternative possible explanation of the prior findings. We studied the relationship between macronutrient ingestion, RER and lipid synthesis using South American locusts (Schistocerca cancellata) reared on artificial diets varying in protein:carbohydrate (p:c) ratio. RER increased and rose above 1 as dietary p:c ratio decreased. Lipid accumulation rates were strongly positively correlated with dietary carbohydrate content and ingestion. RERs above 1 were only observed for animals without food in the respirometry chamber, suggesting that hormonal changes after a meal may drive lipid synthesis. Schistocerca cancellata does not elevate metabolic rate on low p:c diets; in fact, the opposite trend was observed.