Nutritional ecology of insect-plant interactions: persistent handicaps and the need for innovative approaches

Quantifying the flow of matter and energy in food webs is indispensable when assessing the effects of increases in atmospheric carbon dioxide, ozone level and temperature as a result of global climate change. In insect nutritional ecology, quantification of digestive and metabolic efficiency is performed using gravimetric methods in all published cases. A few cases combined these methods with calorimetric and respirometric techniques. Since 1986, methodological pitfalls and sources of error inherent to applying gravimetry as the only method to construct nutrient budgets have been addressed in a number of papers without noticeable impact on subsequent research. Especially for insects feeding on living plant tissues, the gravimetric method has inherent handicaps as it can only be used with excised plant tissues and does not allow for the dynamics of plant metabolism. We discuss the major constraints of the gravimetric method as it pertains to the physiological processes of both the insect and plant. We apply a relationship between relative metabolic rate and relative growth rate of the insect for an analysis of the gravimetric literature. The analysis reveals that gravimetry has given rise to physiologically unlikely results for poikilothermic insects. This points to serious constraints on progress in this field. We identify plant respiration as the major source of error in gravimetric studies. We establish that no single study has, thus far, determined the metabolic efficiency of a herbivore feeding on a photosynthetically active plant with its phyllosphere microclimate. We argue that a quantitative understanding of the ecophysiology and nutritional ecology of insect-plant interactions must rely on the adoption of a combination of existing and complementary methods such as the double labelled water method and infrared gas analysis