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

Abstract

Summary1. 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.

Different combinations of multiple defence traits in an extrafloral nectary‐bearing plant growing under various habitat conditions

“…A plausible answer for the use of direct defence traits is that physical and chemical resistance traits function complementarily: chemical resistance is effective for various herbivores, except for some specialist herbivores that have adapted to toxic chemicals synthesized by their host plants (Howe & Westley 1988;van der Meijden 1996;Gatehouse 2002); physical resistance defends the leaves from both generalist and specialist herbivores (Agrawal 2004;Handley, Ekbom & Agren 2005). For the use of biotic defence, Yamawo et al (2012b) pointed out that the effectiveness of biotic resistance by ants was unstable because ant abundance in the habitat affected the defence efficiency. Therefore, plants that use biotic resistance undergo strong herbivory in some habitats.…”

“…Trichomes, which are produced on leaf surfaces, serve as a physical resistance trait (Yamawo et al 2012a,b). Pellucid dots, which also are present on leaf surfaces, typically contain toxic metabolic substances or essential oils (Wittstock & Gershenzon 2002;Schilmiller, Last & Pichersky 2008;Sirikantaramas, Yamazaki & Saito 2008) and function as a chemical resistance trait (Yamawo et al 2012b). Furthermore, the plant bears extrafloral nectaries (EFNs) on its leaf edges and food bodies (pearl bodies) on its leaf and stem surfaces as biotic resistance traits (Yamawo et al 2012a,b).…”

“…The fifth leaves of both treated and control plants, which grew at three different conditions, were collected on 2 October 2012 because the biotic defence traits functioned effectively on the fifth leaves (Yamawo et al 2012b). The collected leaves were scanned using an image scanner (PM-850; Seiko Epson Corp., Suwa, Japan).…”

“…Earlier studies of simulated herbivory elicited damage levels as low as 1-2% (Heil et al 2001) and as high as 75% (Wooley et al 2007). Young M. japonicus plants were usually damaged to the 10-80% level by the inchworm Ascotis selenaria (Lepidoptera: Geometridae) in the field (Yamawo et al 2012b). Therefore, we selected a damage level of 50% following procedures described by Rogers, Siemann & Lankau (2003) and by Pulice & Packer (2008).…”

Temporal variation in extrafloral nectar secretion in different ontogenic stages of the fruits ofAlibertia verrucosaS. Moore (Rubiaceae) in a Neotropical savanna

“…Moreover, in some cases, the presence of ants may even be undesirable, as they may frighten some possible disperses (Madden & Young 1992;Stapley 1998;Thomas 1988). A recent study performed by Yamawo et al (2012b) showed that the plants can gradually shift from direct to indirect defense against herbivory during leaf aging. Here, we show that the likely change in defense tactics during the ontogenic stages of the fruits of A. verrucosa supports the 'optimal defense theory' (McKey 1974(McKey , 1979Rhoades 1979), in which, plant tissues most closely linked to fitness, such as fruits, should be most defended at high and different levels.…”