Pine defenses against the pitch canker disease are modulated by a native insect newly associated with the invasive fungus

Abstract

Tomicus piniperda (Coleptera, Curculionidae) is a native insect in Europe and now potential enabler of the invasive fungal pathogen of pines, Fusarium circinatum. The co-occurence of T. piniperda and F. circunatum could increase disease incidence via (1) insect wounding when they bore galleries into shoots of healthy trees, and (2) by acting as vectors that introduce fungal propagules directly. The extent of damage by F. circinatum is likely to be influenced by tree defenses, which can depend upon pine species, environmental conditions, and responses to other biotic and abiotic challenges. Indirect interactions among plant enemies can arise when the attack by one enemy alters the shared host plant in a way that affects a second enemy. We tested for indirect interactions between T. piniperda and F. circinatum mediated by plant defenses. Our study employed 100 potted, identically treated, seedlings of Pinus pinaster and P. radiata. Plants were randomly allocated to one of five different treatments: inoculation with T. piniperda alone, inoculation with F. circinatum alone, inoculation with T. piniperda and F. circinatum together, a mock treatment with sterilized water, and true controls. We assessed plant mortality, and measured plant height and diameter, crown size, resin flow after T. piniperda attack, the size of lesions from fungal infection, and phloem chemistry (terpenes and nitrogen). There were conspicuous differences between pine species in their defensive responses to inoculations: P. pinaster showed increases in numerous terpenes following attack by T. piniperda but was unresponsive to F. circinatum, while P. radiata increased terpene concentrations with exposure to either F. circinatum or T. piniperda. In P. radiata, fungal growth within the plant (as reflected by lesion size) was reduced by coincident insect attack. This suggests that plant defensive responses against the insect also functioned as deterrents to a fungal enemy. Thus the combination of T. piniperda and F. circinatum should not be as dangerous to pine stands as if the insect disabled defences against the fungus. Nonetheless, the insect can only increase fungal introductions by increasing wounds and moving propagules. There is a need for field studies of damage from F. circinatum in different pine species with low vs. high abundance of T. piniperda. Better understanding of pine defenses against F. circinatum, and genetic variation in defense responses, would contribute to the development of safe, effective, and sustainable tactics for managing damage from F. circinatum to pine forests in Spain and elsewhere.