Field application of the geometric framework reveals a multistep strategy of nutrient regulation in a leaf-miner

Animals have evolved a vast array of behavioral and physiological strategies that allow them to achieve a nutritionally balanced diet. Plants as food for herbivores are often considered suboptimal, but phytophagous insects can employ pre- and post-ingestive mechanisms and/or symbiotic associations to help overcome food nutritional imbalances. This is particularly crucial for permanent multivoltine leaf-miner insects such as the caterpillar Phyllonorycter blancardella which completes development within a restricted area of a single leaf and use deciduous leaves to fuel growth and reproduction even under senescing autumnal conditions. Using the geometric framework for nutrition under natural field conditions, we show that this insect has multiple strategies to deal with inadequate food supply from the plant. First, larvae manipulate the protein-sugar content of both normal, photosynthetically active, and senescing, photosynthetically inactive, leaf tissues. Control of nutritional homeostasis of mined tissues is however higher for late instars, which differ from younger larval instars in their feeding mode (fluid-vs. tissue-feeder). Second, slight differences in the protein-sugar environment remain between mined tissues on green and yellow leaves despite this manipulation of the leaf physiology. This insect uses post-ingestive mechanisms to achieve similar body protein, sugar and lipid composition. This study demonstrates, for the first time under natural conditions, the ability of an insect herbivore to practice a combination of pre- and post-ingestive compensatory mechanisms to attain similar growth and metabolic outcomes in fundamentally different nutritional environments. Additionally, a comparison of larval nutritional requirements of 117 species from various insect groups further reinforces the hypothesis of a close association between P. blancardella and endosymbiotic bacteria for nutritional purposes.