Stimulation of tree defenses by Ophiostomatoid fungi can explain attack success of bark beetles on conifers

Our aim is to present why the hypothesis, that Ophiostomatoid fungi play an important role in the establishment of most bark beetle species on living conifers, is valuable. After summarizing knowledge about the relationships of bark beetles with conifers and fungi, we conclude that controversy results from misinterpretations when using fungal pathogenicity to demonstrate the role of Ophiostomatoid fungi in beetle establishment on host trees. We demonstrate that fungal pathogenicity is not the right parameter to appreciate the role of fungus in beetle establishment on host trees. We argue that artificial low density inoculations that allow the appreciation of fungus ability to stimulate tree defenses and thus to help beetles in overcoming tree resistance must be used in complement to mass inoculations. In both cases, results must be expressed in terms of tree defense stimulation rather than in terms of tree killing. (i) Fungal species stimulating tree defenses are generally not those that grow the best in the sapwood. (ii) We argue that beetle development in the phloem, fungal invasion of the sapwood and phloem, and tree death, occur after tree defenses are exhausted, and that any fungus present in the beetle gallery could thus potentially invade the sapwood after defense exhaustion. We conclude that stimulation of the tree defense reactions in both the phloem and the superficial sapwood is a real benefit brought by fungi to the beetles during the first phase of establishment (overcoming tree resistance). Considering the origin of the bark beetle fungus associations attacking living trees and their general functioning based on stimulation of tree defenses, we develop three hypotheses: (i) any beetle species would be helped in its establishment in a given tree species by developing an association, even loosely, with a fungus species belonging to the Ophiostomatoid flora of that tree species; (ii) the necessity of a considerably low level of tree resistance for fungus extension into the tree is the selection pressure that has led fungi to develop their intrinsic ability to stimulate tree defenses, through their ability to grow into the phloem. This association can be completed by antagonistic fungal species controlling extension of the previous fungal species in the tree tissues; (iii) Beetle species using the strategy of overcoming tree resistance are associated with a fungal complex, of which species could assume three roles regarding relationships between beetles and trees: 1- to stimulate tree defenses in the phloem and superficial sapwood, 2- to grow into the sapwood after tree resistance is overcome, and 3- to control phloem extension of the first other two categories. Bringing nutrients to the beetle progeny can be a fourth role. We propose that bark beetle - Ophiostomatoid associations can be categorized, based on associations' frequency and complexity while taking into account beetle aggressiveness. We show that a close correspondence exists between beetles' aggressiveness and the ability of their main associated fungal species to stimulate the defenses of their host tree. We conclude with suggesting that most sapwood invading fungi might be cheaters which have taken advantage of the efficiency of the relationship between beetles and fungi that stimulate tree defenses.