Water-repellent plant surface structure induced by gall-forming insects for waste management

Abstract

Many animals and plants have evolved elaborate water-repellent microstructures on their surface, which often play important roles in their ecological adaptation. Here, we report a unique type of water-repellent structure on a plant surface, which develops as an insect-induced plant morphology in a social context. Some social aphids form galls on their host plant, in which they produce large amounts of hydrophobic wax. Excreted honeydew is coated by the powdery wax to form ‘honeydew balls’, which are actively disposed by soldier nymphs through an opening on their gall. These activities are enabled by a highly water-repellent inner gall surface, and we discovered that this surface is covered with dense trichomes that are not found on normal plant surfaces. The trichomes are coated by fine particles of the insect-produced wax, thereby realizing a high water repellency with a cooperative interaction between aphids and plants. The plant leaves on which the gall is formed often exhibit patchy areas with dense trichomes, representing an ectopic expression of the insect-induced plant morphology. In the pouch-shaped closed galls of a related social aphid species, by contrast, the inner surface was not covered with trichomes. Our findings provide a convincing example of how the extended phenotype of an animal, expressed in a plant, plays a pivotal role in maintaining sociality.

Plant Manipulation by Gall-Forming Social Aphids for Waste Management

“…The open galls possess opening(s) on the underside of the gall, so that aphids are able to dispose colony wastes through the openings. Previous studies reported that soldier nymphs in the open galls perform cleaning behavior by pushing or rolling honeydew balls, cast-off skins, and cadavers out of the openings (Aoki, 1980; Aoki and Kurosu, 1989; Benton and Foster, 1992; Uematsu et al, 2018). Inhibition of the waste disposal by turning the gall orientation upside down (the openings to be upward) resulted in high mortality of the aphids inside, indicating that gall cleaning is indispensable for survival of the gall inhabitants (Benton and Foster, 1992).…”

“…Inhibition of the waste disposal by turning the gall orientation upside down (the openings to be upward) resulted in high mortality of the aphids inside, indicating that gall cleaning is indispensable for survival of the gall inhabitants (Benton and Foster, 1992). Besides, aphids produce large amounts of powdery wax, which coats the excreted honeydew to form unsticky “marbles” or “honeydew balls” (Pike et al, 2002; Kutsukake et al, 2012; Uematsu et al, 2018). The wax-coated honeydew balls are repelled by the gall inner wall so that the aphids can easily push them without being wet or contaminated.…”

“…In the subfamily Eriosomatinae, the water-absorbing closed galls have evolved at least once in the tribe Eriosomatini. Paracolopha morrisoni forms water-absorbing closed galls on Zelkova serrata leaves, whereas many other species, including Colophina clematis , form water-repelling open galls on the same Zelkova leaves (Uematsu et al, 2018). Taken together, water-absorbing property in the closed galls has evolved at least three times in the evolutionary history of the gall-forming aphids (Figure 2A).…”

“…The occurrences of the water-absorbing closed galls are indicated in bold branches. The water-absorbing closed galls reported in Kutsukake et al (2012) and Uematsu et al (2018) are indicated in black, whereas others (potential water-absorbing galls) are indicated in gray. The evolution of dense trichomes on gall inner surface is indicated by black stars.…”

“…A subgall of C. japonica with a slit opening and a subgall of C. nekoashi with no opening are also shown. Figures were modified from Kutsukake et al (2012) and Uematsu et al (2018). In, inner side of the gall; Out, outer side of the gall.…”