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

La stimulation des défenses de l’arbre par les champignons Ophiostomatoïdes peut expliquer le succès des attaques de Scolytes sur conifères

Annals of Forest Science volume 66, page 801 (2009)Cite this article

Abstract

  • • 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.

  1. (i)

    Fungal species stimulating tree defenses are generally not those that grow the best in the sapwood.

  2. (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:

  1. (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;

  2. (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;

  3. (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.

Résumé

  • • Notre objectif est de présenter les raisons de la validité de l’hypothèse selon laquelle les champignons jouent un rôle important dans l’installation de la plupart des espèces de Scolytes sur conifères vivants.

  • • Après avoir résumé les connaissances sur les relations des Scolytes avec les conifères et les champignons, nous concluons que la controverse résulte d’interprétations erronées lorsque l’on utilise le pouvoir pathogène des champignons pour démontrer le rôle des Ophiostomatoïdes dans l’installation des insectes sur les arbres hôtes.

  • • Nous démontrons que le pouvoir pathogène n’est pas le paramètre correct pour apprécier le rôle du champignon dans l’installation des Scolytes sur les arbres hôtes. Nous soutenons que des inoculations artificielles à faible densité, qui permettent d’apprécier la capacité du champignon à stimuler les défenses de l’arbre et à ainsi aider le Scolyte à surmonter la résistance de celui-ci, doivent être utilisées en complément des inoculations massives. Dans les deux cas, les résultats doivent être exprimés en termes de stimulation des défenses de l’arbre plutôt qu’en termes de mortalité de l’arbre.

  1. (i)

    les espèces de champignons qui stimulent les défenses de l’arbre ne sont généralement pas celles qui présentent la meilleure croissance dans l’aubier.

  2. (ii)

    nous soutenons que le développement de l’insecte dans le phloème, l’invasion de l’aubier et du phloème par le champignon, et la mort de l’arbre, interviennent après épuisement des défenses de l’arbre, et que tout champignon présent dans les galeries de l’insecte pourrait donc potentiellement envahir l’aubier après épuisement de ces défenses.

  • • Nous concluons que la stimulation des réactions de défense de l’arbre à la fois dans le phloème et l’aubier superficiel représente un bénéfice réel apporté par les champignons aux Scolytes pendant la première phase de leur installation (surmonter la résistance de l’arbre).

  • • En ce qui concerne l’origine des associations Scolytes — champignons attaquant les arbres vivants et considérant leur fonctionnement général basé sur une stimulation des défenses de l’arbre, nous développons trois hypothèses :

  1. (i)

    toute espèce de Scolyte serait aidée dans son installation sur une espèce d’arbre donnée en développant une association, même lâche, avec une espèce de champignon appartenant à la flore Ophiostomatoïde de cette espèce d’arbre ;

  2. (ii)

    la nécessité d’un très faible niveau de résistance de l’arbre pour autoriser l’extension fongique dans le végétal est la pression de sélection qui a conduit les champignons à développer leur capacité intrinsèque de stimulation des défenses de l’arbre, à travers leur capacité à croître dans le phloème. Cette association peut être complétée par des espèces fongiques antagonistes contrôlant l’extension des espèces précédentes dans les tissus de l’arbre ;

  3. (iii)

    les espèces de Scolytes utilisant la stratégie de surmonter la résistance de l’arbre sont associées à un complexe fongique dont les espèces assurent trois fonctions eu égard aux relations entre les Scolytes et les arbres : 1— stimuler les défenses de l’arbre dans le phloème et l’aubier superficiel, 2— croître dans l’aubier après que la résistance de l’arbre ait été vaincue, and 3— contrôler l’extension des deux catégories précédentes dans le phloème. L’apport de nutriments à la progéniture du Scolyte peut représenter une quatrième fonction.

  • • Nous proposons que les associations Scolytes — Ophiostomatoïdes puissent être classées, en se basant sur la fréquence et la complexité de l’association et en prenant en compte l’agressivité de l’insecte. Nous montrons qu’il existe une étroite correspondance entre l’agressivité des insectes et la capacité de leur principale espèce fongique associée à stimuler les défenses de l’arbre hôte.

  • • Nous concluons en suggérant que la plupart des espèces de champignons envahissant l’aubier pourraient être des “tricheurs” qui ont profité de l’efficacité des relations entre les Scolytes et les espèces fongiques stimulatrices des défenses de l’arbre.

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  1. Laboratoire de Biologie des Ligneux et des Grandes Cultures UPRES EA 1207, Université d’Orléans, rue de Chartres, BP 6759, 45067, Orléans Cedex 2, France

    François Lieutier & Aurélien Salle

  2. Unité de Zoologie Forestière, INRA, 2163 avenue de la Pomme de Pin, CS 40001, 45075, Ardon, Orléans Cedex 2, France

    Annie Yart

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Lieutier, F., Yart, A. & Salle, A. Stimulation of tree defenses by Ophiostomatoid fungi can explain attack success of bark beetles on conifers. Ann. For. Sci. 66, 801 (2009). https://doi.org/10.1051/forest/2009066

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