Nutrient composition varies greatly across landscapes, influencing the spatiotemporal variation and dynamics of populations, yet few studies have investigated this pattern across multiple scales. We tested how nutrient limitation affects herbivore populations, from individual behavior to landscape-level population dynamics, using the Australian plague locust, Chortoicetes terminifera (Walker), with field populations and long-term survey data from across their range. At the individual level, juvenile locusts selected for a carbohydrate-biased intake target of 1 protein (p) to 2 carbohydrate (c), and exhibited the highest growth and shortest development time when fed artificial diets with that same 1p:2c ratio during the final juvenile instar. At the field level, locusts kept in cages with protein-biased plants redressed their nutritional imbalance by selecting carbohydrate-biased diets (up to a 1p:20c ratio) for over a week after being removed from the protein-biased environment, returning to the 1p:2c intake target once the deficiency was met. At the landscape level, locust outbreaks were negatively correlated with soil nitrogen and showed a non-linear relationship with soil phosphorus, peaking at approximately 4% soil phosphorus. We disentangled the interaction between mean annual precipitation and soil nitrogen using comprehensive locust surveys and remotely sensed soil and weather data spanning decades. This study is the first to integrate lab, field, and remote sensing approaches, demonstrating the importance of nutrient balancing and acquisition across scales for herbivores. Specifically for locusts, we show that low-nitrogen environments promote outbreaks, likely by reducing plant protein-to-carbohydrate ratios. Incorporating soil quality data into locust plague forecasting models could help improve prediction accuracy.

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.

Nitrogen limitation theory predicts that terrestrial plants should benefit from nitrogen inputs and that herbivores should benefit from subsequent higher plant protein contents. While this pattern has generally been supported, some herbivorous insects have shown preference and higher performance on low protein (p), high carbohydrate (c) diets as juveniles. However, little is known about the effects on reproduction in adults. Using nitrogen fertilizer, we demonstrate that high plant p:c has negative effects on Senegalese locust (Orthoptera: Oedaeleus senegalensis) reproduction and survival in an agroecological setting. For this, we measured p:c in millet plants (Pennisetum glaucum) that received two level of fertilizer (high and moderate) and a control. We found that fertilization increased p:c ratio in a concentration dependent fashion. When we caged locusts on those plants, we found that eggs laid by locusts that ate plants from the high fertilization treatment were smaller. We counted the number of locusts alive over the course of two weeks and showed that fewer females survived on fertilized plants than on control plants. Furthermore, with a laboratory choice experiment we showed that female locusts prefer unfertilized plants to plants with a high p:c. We hypothesize that this pattern will apply broadly to species that have extensive carbohydrate needs, such as long-distance migrators.