Avoidance of parasitoid attack is associated with the spatial use within a leaf by a lepidopteran leafminer

Abstract

In prey-predator systems, top-down effects can be a powerful determinant for spatial distributions of prey through their search for enemy-free space. Leafminers live and eat within leaves, making feeding tracks called mines, and mine conspicuousness exposes them to a high risk of parasitism. Those lepidopteran leafminers that use lower leaf surfaces as mining sites show wide evolutionary radiation. We hypothesized that leafminers making mines on the lower surface are less often detected by parasitoids and thus have a selective advantage in avoiding parasitism compared to those on the upper surface. To investigate the adaptiveness of lower-surface mining, we examined the relationship between parasitism and within-leaf mine distribution for 3 years using a field population of the leafminer Phyllocnistis spec. (Lepidoptera: Gracillariidae, Phyllocnistinae), which prefers the lower surface of leaves of the Japanese privet, Ligustrum japonicum Thunb. (Oleaceae). Parasitoid attack was more frequent in the upper-surface mines than in the lower-surface mines and on leaves with uppersurface mines than on leaves with only lower-surface mines. When both surfaces were mined, leafminers on the lower surface could avoid parasitism. Upper-surface mines were attacked by more parasitoid species as compared to lower-surface mines. Although the results demonstrated that mining on the lower surface was advantageous in avoiding parasitism, the vulnerability of lower-surface mines to parasitism varied depending on their abundance. When many lower-surface mines were present, lower-surface mines suffered a higher parasitism rate than upper-surface mines, probably because parasitoids formed search images for and concentrated on lower-surface mines. This study suggests that the preferential use of the lower leaf surface by leafminers is in part attributed to interactions with parasitoids.

Changing Leaf Geometry Provides a Refuge from a Parasitoid for a Leaf Miner

“…The present parasitism rates of A. philippinensis in the wild are also very likely to be affected by other parasitoids that share A. transecta as a host insect. Leaf miners in the linear and flat mines are generally attacked more heavily by idiobionts (parasitoids that kill or inhibit the growth of hosts immediately after oviposition (Askew and Shaw, 1986)) than by koinobionts (Godfray, 1994;Kato, 1994;Sato,1995;Ayabe and Ueno, 2012;Ayabe and Hijii, 2016). Indeed, we observed many early instars of A. transecta, which make linear mines, attacked by idiobionts in the wild, and it appears that it is difficult for the koinobiont parasitoid A. philippinensis to complete its growth in early host instars if they are superparasitized by idiobiont parasitoids.…”