Rapid monoterpene induction promotes the susceptibility of a novel host pine to mountain pine beetle colonization but not to beetle-vectored fungi

Abstract

Chemical induction can drive tree susceptibility to and host range expansions of attacking insects and fungi. Recently, mountain pine beetle (Dendroctonus ponderosae Hopkins; MPB) has expanded its host range from its historic host lodgepole pine (Pinus contorta var. latifolia Douglas ex Loudon) to jack pine (Pinus banksiana Lamb) in western Canada. Beetle success in jack pine forests likely depends upon the suitability of tree chemistry to MPB and its symbiotic phytopathogenic fungi. In particular, how rapid induced defenses of jack pine affect MPB colonization and the beetle's symbionts is unknown. In the field, we characterized and compared differences in rapid induced phloem monoterpenes between lodgepole and jack pines in response to various densities of Grosmannia clavigera (Robinson-Jeffery and Davidson)-a MPB symbiotic fungus used to simulate beetle attack-inoculations. Overall, lodgepole pine had higher limonene and myrcene, but lower α-pinene, concentrations than jack pine. However, myrcene concentrations in jack pine increased with inoculation density, while that in lodgepole pine did not respond to density treatments. We compared the growth and reproduction of MPB's symbiotic fungi, G. clavigera, Ophiostoma montium (Rumford) von Arx and Leptographium longiclavatum Lee, Kim and Breuil, grown on media amended with myrcene, α-pinene and limonene at concentrations reflecting two induction levels from each pine species. Myrcene and α-pinene amendments inhibited the growth but stimulated the reproduction of G. clavigera, whereas limonene stimulated its growth while inhibiting its reproduction. However, the growth and reproduction of the other fungi were generally stimulated by monoterpene amendments. Overall, our results suggest that jack pine rapid induction could promote MPB aggregation due to high levels of α-pinene (pheromone precursor), a positive feedback of myrcene (pheromone synergist) and low levels of limonene (resistance). Jack pine is likely as susceptible to MPB-vectored fungi as lodgepole pine, indicating that jack pine induction will likely not adversely affect symbiont activities enough to inhibit the invasion of MPB into jack pine forests.

Nitrogen and Ergosterol Concentrations Varied in Live Jack Pine Phloem Following Inoculations With Fungal Associates of Mountain Pine Beetle

“…The differences in the results of this and the earlier study may be attributed to differences between host tree species in terms of their secondary chemical profiles, how fungi were introduced to trees (artificial inoculation vs. natural beetle colonization), and analytical methods undertaken to quantify the ergosterol concentrations. First, although these two tree species share many secondary compounds, their concentrations show large variation, which may differentially affect fungal growth ( Cale et al, 2017 ; Erbilgin, 2019 ; Wang et al, 2020 ). Second, in the current study, we quantified ergosterol concentration from individual fungal species, while the earlier study quantified ergosterol from trees colonized by MPB without assessing the relative concentrations from each fungus.…”

“…Six weeks later, we collected phloem tissue samples from lesions as well as non-infected phloem adjacent to lesions (about 4 cm above the lesions; “non-infected phloem” hereafter; Figure 1 ). During our sampling we observed that fungal inoculations created much longer lesions than mock inoculations, suggesting that our inoculations were successful ( Bonello et al, 2006 ; Cale et al, 2017 , 2019 ). In addition, we confirmed fungal species by subsampling tissues taken from lesions on each tree.…”

“…Bark beetles (Coleoptera: Curculionidae, Scolytinae) contain some of the most ecologically and economically important insect species of conifer forests due to their ability to kill a large number of trees during periodic outbreaks, with cascading consequences for ecosystem function ( Kurz et al, 2008 ; Bentz et al, 2010 ; Hicke et al, 2012 ; Seidl, 2014 ). Fungal symbionts associated with bark beetles can amplify the beetles’ damage by promoting successful host colonization and development ( Harrington, 2005 ; DiGuistini et al, 2007 ; Six and Wingfield, 2011 ; Six, 2012 ; Wang et al, 2013 , 2014 ; Therrien et al, 2015 ; Cale et al, 2017 ; Zhao et al, 2019 ). In particular, fungal symbionts can facilitate beetle nutrition by either serving as a direct dietary substrate (e.g., ergosterol), or indirectly concentrating host plant nutrients (e.g., nitrogen) ( Ayres et al, 2000 ; Bleiker and Six, 2007 ; Goodsman et al, 2012 ).…”

Phytochemicals as mediators for host range expansion of a native invasive forest insect herbivore

“…The defense response is usually induced by the inoculation of trees with an MPB‐associated fungus, and is measured by determining the concentrations of defense chemicals, mainly monoterpenes, in the phloem and necrotic tissues (i.e. lesions caused by infections by beetle symbiotic fungi) (Arango‐Velez et al ., ; Cale et al ., ; Erbilgin et al ., ).…”

Anatomical and Chemical Responses of Eastern White Pine (Pinus strobus L.) to Blue-Stain (Ophiostoma minus) Inoculation

“…Similarly, Raffa and Berryman [52] showed that β-myrcene, limonene and terpinolene in combination with αand β-pinene are directly toxic to D. frontalis adults in loblolly pine. The implication of a long-term (65 dpi) induced monoterpenes response can be both beneficial and deleterious to P. strobus; as induction of β-myrcene and β-pinene may promote beetle aggregation [53,54], fostering future beetle attacks. Additionally, as carbohydrate reserves fund monoterpene synthesis [47], prolonged monoterpene production can eventually deplete carbon availability necessary for tree growth.…”