Scab formation and wound healing of plant tissue by soldier aphid

Abstract

In the social aphid Nipponaphis monzeni, a unique gall-repairing behaviour has been known: when a hole is made on the gall, many soldier nymphs discharge body fluid on the breach, which promptly solidifies and plugs the hole. Here, we experimentally investigated the subsequent fate of repaired galls and their inhabitants. Irrespective of natural repair by soldier nymphs or artificial repair with adhesive, repaired galls survived significantly better than non-repaired galls. Within a month after repair, the plant tissue around the hole proliferated and sealed up the hole. Many soldier nymphs were localized at the hole area and extermination of inhabiting aphids by insecticides aborted the gall regeneration, indicating that the gall regeneration requires inhabiting aphids, wherein soldier nymphs are likely to play a major role. This study provides an unprecedented case of scab formation and wound healing, which occurs at an animal-plant interface: scab derived from insect body fluid promptly plugs damaged plant tissue and subsequently the insects actively stimulate regeneration of the plant tissue, whereby the compromised plant tissue recovers. We suggest that the novel system may have evolved in the aphid lineage through enhancement and recruitment of the pre-existing capabilities of haemolymph coagulation and gall formation.

A review on self-destructive defense behaviors in social insects

“…The mechanistic basis of caste divergence in termites has been increasingly understood (Moura et al, 2011), but little is known about the development of the self-destructive autothysis apparatus. Several social aphid species produce nymphs that are differentiated from normal nymphs and are unable to further develop and function as a sterile soldier caste (Kutsukake et al, 2009), similar to ant and termite soldiers. However, in Nipponaphis monzeni, first-instar nymphs seem to invariably develop large globular cells and serve as the only gall defenders, performing self-sacrifice when repairing galls.…”

“…In P. spyrothecae, it takes ten or more days for a colony to seal up the gall, mainly relying on directing an overgrowth of undamaged gall tissue into the wound. While more costly, the self-destructive defensive behavior taken by N. monzeni is sustainable due to its larger colony size, usually containing thousands of individuals (Kutsukake et al, 2009), but no comprehensive cost-benefit analyses have been done in any case of autotomy, autothysis, or nest sealing behavior.…”

“…Soldiers in the gall aphid Nipponaphis monzeni sacrifice their lives to repair the gall even in the absence of predators. When these aphids discover an opening in the gall they secrete a fluid from their cornicles that functions as a plaster and seals the hole and forms a scab, which increases the recovery time of the plant tissue (Kutsukake et al, 2009). This behavior may result in selfsacrifice of the aphid nymphs.…”

Extremely Long-Closed Galls of a Social Aphid

“…During the final expanding phase of the gall (in April/May), nymphs of N. monzeni repair their still-soft gall in a self-sacrificing manner when a hole is bored through the wall [23,24]. This tactics can work well only if there are many "repairers," or firstinstar nymphs, in the gall.…”

“…The old empty gall is called "Saru Bué (monkey whistle)" [21] and children blow into it through the exit hole to whistle [21,22]. This species is also peculiar in that its first-instar nymphs repair their gall in a self-sacrificing manner, by discharging a large amount of body fluid [23,24]. It has been unknown, however, when and how galls of N. monzeni are initiated and developed to mature.…”