Energetic constraints on multi-day flights in migratory locusts

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.