No abstract

Increasing evidence has shown that the energy use of ant colonies increases sublinearly with colony size so that large colonies consume less per capita energy than small colonies. It has been postulated that social environment (e.g., in the presence of queen and brood) is critical for the sublinear group energetics, and a few studies of ant workers isolated from queens and brood observed linear relationships between group energetics and size. In this paper, we hypothesize that the sublinear energetics arise from the heterogeneity of activity in ant groups, that is, large groups have relatively more inactive members than small groups. We further hypothesize that the energy use of ant worker groups that are allowed to move freely increases more slowly than the group size even if they are isolated from queen and brood. Previous studies only provided indirect evidence for these hypotheses due to technical difficulties. In this study, we applied the automated behavioral monitoring and respirometry simultaneously on isolated worker groups for long time periods, and analyzed the image with the state-of-the-art algorithms. Our results show that when activity was not confined, large groups had lower per capita energy use, a lower percentage of active members, and lower average walking speed than small groups; while locomotion was confined, however, the per capita energy use was a constant regardless of the group size. The quantitative analysis shows a direct link between variation in group energy use and the activity level of ant workers when isolated from queen and brood.

The energy requirement for biosynthesis plays an important role in an organism’s life history, as it determines growth rate, and tradeoffs with the investment in somatic maintenance. This energetic trait is different between painted lady (Vanessa cardui) and Turkestan cockroach (Blatta lateralis) due to the different life histories. Butterfly caterpillars (holometabolous) grow 30-fold faster, and the energy cost of biosynthesis is 20 times cheaper, compared to cockroach nymphs (hemimetabolous). We hypothesize that physiologically the difference in the energy cost is partially attributed to the differences in protein retention and turnover rate: Species with higher energy cost may have a lower tolerance to errors in newly synthesized protein. Newly synthesized proteins with errors are quickly unfolded and refolded, and/or degraded and resynthesized via the proteasomal system. Thus, much protein output may be given over to replacement of the degraded new proteins, so the overall energy cost on biosynthesis is high. Consequently, the species with a higher energy cost for biosyntheses has better proteostasis and cellular resistance to stress. Our study found that, compared to painted lady caterpillars, the midgut tissue of cockroach nymphs has better cellular viability under oxidative stresses, higher activities of proteasome 20S, and a higher RNA/growth ratio, supporting our hypothesis. This comparative study offers a departure point for better understanding life history tradeoffs between somatic maintenance and biosynthesis.