Leaf ageing promotes the shift in defence tactics in Mallotus japonicus from direct to indirect defence

1. Most plant species rely upon multiple lines of defence that develop or change functions with leaf age. To date, the effects of leaf age on multiple defence traits have been insufficiently elucidated. For Mallotus japonicus (Euphorbiaceae), we report a shift from direct to indirect defence against herbivory. That shift occurs gradually during leaf ageing. 2. First, the densities of trichomes and pellucid dots, the numbers of extrafloral nectaries (EFNs) and pearl bodies, and the number of ants on leaves of M. japonicus were examined in the field at weekly intervals. Secondly, herbivore species and the degree of herbivory were examined. Thirdly, the effects of ants on herbivore exclusion were investigated experimentally in the field. Finally, to confirm the effectiveness of trichomes and pellucid dots for defence against two herbivore species [the adult flea beetle, Aphthona strigosa (Coleoptera: Chrysomelidae), and the inchworm, Ascotis selenaria (Lepidoptera: Geometridae)], both young and middle-aged leaves were tested using laboratory bioassay. 3. On newly emerged leaves, densities of trichomes and pellucid dots were extremely high, but they decreased rapidly with leaf age. The respective quantities of EFNs that were actually secreting nectar, the pearl bodies, and the ants on middle-aged leaves were greater than those on leaves of other ages. On M. japonicus, we found 11 herbivorous insects, among which Ap. strigosa and As. selenaria were the principal herbivores. 4. The damaged leaf areas of ant-excluded plants were much larger than those of control plants. Most herbivory was attributable to As. selenaria. Laboratory bioassay revealed that against Ap. strigosa and small As. selenaria larvae, trichomes and pellucid dots in young leaves functioned well, although those in middle-aged leaves did not. 5. Synthesis. Young M. japonicus leaves are defended against herbivores through the use of direct defence traits such as trichomes and pellucid dots. However, the plant uses indirect defence traits for middle-aged leaves. This shift from direct defence to indirect defence with leaf ageing supports the 'optimal defence theory': plants have evolved multiple defence traits to maximize their fitness.