Locusts are major intermittent threats to food security and the ecological factors determining where and when these occur remain poorly understood. For many herbivores, obtaining adequate protein from plants is a key challenge. We tested how the dietary protein : non-structural carbohydrate ratio (p : c) affects the developmental and physiological performance of 4th-5th instar nymphs of the South American locust, Schistocerca cancellata, which has recently resurged in Argentina, Bolivia and Paraguay. Field marching locusts preferred to feed on high carbohydrate foods. Field-collected juveniles transferred to the laboratory selected artificial diets or local plants with low p : c. On single artificial diets, survival rate increased as foods became more carbohydrate-biased. On single local plants, growth only occurred on the plant with the lowest p : c. Most local plants had p : c ratios substantially higher than optimal, demonstrating that field marching locusts must search for adequate carbohydrate or their survival and growth will be carbohydrate-limited. Total body lipids increased as dietary p : c decreased on both artificial and plant diets, and the low lipid contents of field-collected nymphs suggest that obtaining adequate carbohydrate may pose a strong limitation on migration for S. cancellata . Anthropogenic influences such as conversions of forests to pastures, may increase carbohydrate availability and promote outbreaks and migration of some locusts.

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 ratios (RER, CO2 production divided by O2 consumption) can rise above 1 due to de novo lipid synthesis, providing an alternate 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 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. S. cancellata does not elevate metabolic rate on low p:c diets; in fact, the opposite trend was observed.

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.

Matching nutritional requirements throughout development is critical for maximizing adult performance and fitness. Mammalian maternal milk is the ultimate example of a diet well‐matched to meet all requirements of developing infants. Its macronutrient content, specifically, protein:non‐protein (p:np) ratio, changes to match shifting requirements during infant development. Indeed, the developmental requirements of humans, rodents and livestock are well‐described, during juvenile development. However, despite their importance as research models and in ecosystems, the dynamics of nutritional requirements in developing invertebrates is still poorly understood. Here we studied the nutritional requirements and performance from hatching to adulthood of a generalist herbivore, the South American locust, Schistocerca cancellata. In order to do so, we measured protein and carbohydrate consumption from two artificial diets differing strongly in protein:carbohydrate content for the six juvenile instars and adults of the S. cancellata. In addition, we measured growth and survival of locusts reared on single artificial diets varying in protein:carbohydrate ratio for their entire developmental period. When given a choice, demand for protein decreased throughout development, demonstrated by a change in self‐selected intake targets from protein‐biased in early life, to highly carbohydrate‐biased in young adults. Probably because early instars must prioritize growth, while the last instar and adults must prioritize preparation for dispersal and reproduction. On no‐choice diets, lifetime animal performance, including developmental rate and mass gain, was highest on protein‐biased foods, especially during early development. Regardless of late‐juvenile diet, if individuals were not able to obtain sufficient protein in the early juvenile period, they were unable to catch up in size or developmental speed.

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