Aurélien Sallé

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

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.(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.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.(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.(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 :(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 ;(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 ;(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.

Preference-performance relationship and influence of plant relatedness on host use by Pityogenes chalcographus L.

1 Pityogenes chalcographus L. (Coleoptera: Scolytinae) causes damage in European coniferous forests, primarily on Picea abies L. Karst., but is also recorded on other native and exotic Pinaceae species. Estimating the adequacy between adult preference and larval performance of this beetle among its host‐range, as well as the influence of plant taxonomic relatedness on these parameters, would provide useful information on the beetles ability to shift onto novel hosts. 2 Choice and no‐choice assays were conducted under laboratory conditions. Adult preference and larval performance parameters among two native (Pinus sylvestris L. and Picea abies) and three exotic north American [Pinus contorta Dougl., Picea sitchensis (Bong.) Carr. and Pseudotsuga menziesii Mirbel (Franco)] conifer species were measured. 3 Pityogenes chalcographus exhibited a significant positive relationship between preference and performance. Picea abies was both the preferred and the most suitable host species for larval development. The closest relative, P. sitchensis, was the second best choice in terms of preference and performance. Pseudotsuga menziesii occupied an intermediate position for both beetle preference and performance, and Pinus spp. were the least suitable hosts for beetle development. 4 Adult preference and larval performance ranking among hosts provides little support to the plant taxonomic relatedness hypothesis. Taxonomic relatedness could play a role on the diet breadth, although only at a limited scale, within the genus Picea. At higher taxonomic levels, other factors such as bark thickness might be decisive.

Size and shape changes of Ips typographus L. (Coleoptera: Scolytinae) in relation to population level

1 High intraspecific competition is known to occur during Ips typographus outbreaks, and is thought to be the main factor regulating epidemic populations by affecting beetle population productivity. However, little is known about the consequences of intraspecific competition on population quality during outbreaks, although it could have consequences on beetle population dynamics.

Exceptional plant penetration and feeding upon cortical parenchyma cells by the woolly poplar aphid.

Forty percent of aphids live wholly or partly on trees, most species being associated with leaves or petioles. Species able to exploit woody parts have either specific adaptations, such as extra long stylets that allow them to reach the phloem, or the ability to induce galls. The woolly poplar aphid, Phloeomyzus passerinii (Signoret) (Hemiptera: Aphididae), colonizes the trunks and base of the lower branches of mature poplars and causes cortical necrosis leading to the death of trees where infestation is heavy. Very little is known about the mode of feeding of P. passerinii. This study looked at the feeding behavior of P. passerinii on stem-cuttings of Populus x canadensis Moench using: (i) histological analyses of the feeding site and stylet pathway and (ii) electrical penetration graphs (EPG, DC) based on parthenogenetic apterous females on woody tissues. The histological and EPG results showed that stylets of P. passerinii penetrated into the plant tissues following a straight unbranched extracellular and intracellular pathway to reach the cortical parenchyma. Compared to EPGs for phloem sap feeding aphids, there were differences in the waveforms A and C whereas a new waveform Icp was described. Based on histological analyses and previous descriptions of EPG waveforms, correlations with the stylet tip position and aphid activities within bark tissues are discussed. A pathway and a sustained intracellular phase were distinguished, both occurring in the cortical parenchyma cells. The bark aphid feeding mode is discussed in relation to the damage caused and in terms of changes in the aphids diet.

Resistant poplar genotypes inhibit pseudogall formation by the wooly poplar aphid, Phloeomyzus passerinii Sign

Key messagePhloeomyzus passeriniican induce a pseudogall within the bark of susceptible poplar genotypes, while in resistant genotypes the induction seems to be impeded by lignification processes.AbstractPhloeomyzus passerinii is a major pest of poplar stands in Europe, North Africa and the Near East. This aphid feeds in the cortical parenchyma of different poplar species and hybrids, and can affect their growth and survival through unknown mechanisms. In some genotypes, however, resistance prevents either the settlement or the development of aphid colonies. For a better understanding of tree reactions to aphid probing, we compared the anatomical and biochemical modifications undergone within the bark of stem cuttings, after different delays of either aphid colonization or mechanical wounding. To assess how resistance may modulate tree reactions, the comparison was performed using three poplar genotypes exhibiting different resistance levels. In these three genotypes, mechanical wounding induced a similar, localized, wound periderm. In contrast, aphid colonization triggered more extended reactions, which differed among genotypes. In the susceptible genotype, aphids induced a reaction tissue, characterized after a month by thin-walled hypertrophied cells and a depletion of soluble phenolic compounds and starch. Anatomical features of this reaction tissue suggest that the aphid initiates a pseudogall in the cortical tissues of its susceptible host. In the resistant genotypes, however, the differentiation of the reaction tissue was totally or partially inhibited, probably because of extended lignification processes. The implications of a pseudogall induction on susceptible hosts’ physiology, and the impact of lignification on aphid development and behavior, are discussed.

Characterization of Antibiosis and Antixenosis to the Woolly Poplar Aphid (Hemiptera: Aphididae) in the Bark of Different Poplar Genotypes

ABSTRACT The woolly poplar aphid, Phloeomyzus passerinii (Signoret) (Hemiptera: Aphididae), is a major pest of poplar plantations in the Mediterranean basin and the Near East. Aphids colonize poplar trunks and feed upon the cortical parenchyma. Despite the economic importance of poplar, little is known about the mechanisms involved in poplar resistance to this pest. However, Populus x canadensis Moench genotypes show various levels of resistance to P. passerinii. This study has investigated the type of poplar resistance (antibiosis or antixenosis) by assessing aphid settlement, physiology (survival, development, and reproduction), and stylet penetration behavior (electrical penetration graph) on three P. x canadensis genotypes; ‘I214’ (susceptible), ‘Brenta’ (resistant), and ‘I45/51’ (intermediate). Because settlement was reduced, the highly resistant genotype Brenta exhibited surface antixenosis. In addition, nymphal survival was null on Brenta, and twice less adult aphid initiated a sustained intracellular phase in the cortical parenchyma of that genotype compared with the other two genotypes. Thus, Brenta also showed parenchyma-located antixenosis coupled with antibiosis characteristic. In contrast, P. passerinii had no difficulty to initiate a sustained ingestion in the cortical parenchyma of the intermediate genotype I45/51, but decreased fecundity and lower intrinsic rate of natural increase were clear expressions of antibiosis.

Effects of fertilisation on amino acid mobilisation by a plant‐manipulating insect

1. Phytophagous insects frequently manipulate their host‐plant to improve their immediate environment. This generally implies substantial modifications of host metabolism, and sometimes an alteration of nitrogen allocation within the host‐plant. However, the outcome of plant manipulation on amino acid or protein content can be modulated by environmental factors and host‐plant traits.

Effect of temperature on the reproductive success, developmental rate and brood characteristics of Ips sexdentatus (Boern.)

Global warming is predicted to enhance the development rate and increase the number of generations in multivoltine insects. For secondary forest pests, such as the pine bark beetle Ips sexdentatus, the resulting increase in population level could trigger more frequent outbreaks. However, this positive effect could be outweighed by a temperature‐dependent decrease in offspring quality. To test these hypotheses, we carried out a laboratory rearing experiment with maritime pine logs at six temperature regimes reproducing hourly fluctuations and averaging 12–25.5 °C. We estimated the thermal requirements for a complete development of the beetle and the number of offspring per female. The offspring quality was estimated using three traits: dry body weight, elytra length and lipid content. The minimum and maximum developmental threshold were estimated at 10.9 and 36 °C, respectively, and the thermal requirements for complete development were estimated at 517 degree‐days. We predicted a mean of two generations per year in southwestern France, although an additional generation could occur during warmer years. The number of offspring increased exponentially with temperature, although we observed a curvilinear response of offspring traits to temperature, with optima at 15–18 °C. This suggests that there are trade‐offs between productivity and quality of offspring. Global warming is therefore likely to result in higher number of generations of I. sexdentatus per year, with larger broods but of reduced fitness at high temperatures.

Native Sap-Sucker Insects in the Mediterranean Basin

The chapter provides information on 15 species of invasive sacking insects on forest trees in the Mediterranean basin. Four Psyllids and one Thaumastocorid bug develop on Eucalyptus spp. and are native to Australia, although all of them possibly arrived in the Mediterranean area via South America. Among the five Cinara spp. those which develop on cedar trees spread inside the Mediterranean area, two of the aphids are North American species and one is probably from China. The discussed scale insects, two Matsucoccus spp. and Marchalina hellenica extent their range inside the Mediterranean basin. Finally, we report on two tingid species (Corythucha spp.) both originate from North America. We review their biology, the injury they inflect, their spread, as well as their natural enemies and the required management.

Promises and challenges in insect-plant interactions

There is tremendous diversity of interactions between plants and other species. These relationships range from antagonism to mutualism. Interactions of plants with members of their ecological community can lead to a profound metabolic reconfiguration of the plants’ physiology. This reconfiguration can favour beneficial organisms and deter antagonists like pathogens or herbivores. Determining the cellular and molecular dialogue between plants, microbes, and insects, and its ecological and evolutionary implications is important for understanding the options for each partner to adopt an adaptive response to its biotic environment. Moving forward, understanding how such ecological interactions are shaped by environmental change and how we potentially mitigate deleterious effects will be increasingly important. The development of integrative multidisciplinary approaches may provide new solutions to the major ecological and societal issues ahead of us. The rapid evolution of technology provides valuable tools and opens up novel ways to test hypotheses that were previously unanswerable, but requires that scientists master these tools, understand potential ethical problems flowing from their implementation, and train new generations of biologists with diverse technical skills. Here, we provide brief perspectives and discuss future promise and challenges for research on insect–plant interactions building on the 16th International Symposium on Insect–Plant interactions (SIP) meeting that was held in Tours, France (2–6 July 2017). Talks, posters, and discussions are distilled into key research areas in insect–plant interactions, highlighting the current state of the field and major challenges, and future directions for both applied and basic research.