Ecological Entomology (2011), 36, 425–434 DOI: 10.1111/j.1365-2311.2011.01283.x Tree-mediated interactions between the jack pine budworm and a mountain pine beetle fungal associate LINDSAY J. COLGAN andNADIR ERBILGIN Department of Renewable Resources, University of Alberta, Edmonton, Canada Abstract. 1. Coniferous trees deploy a combination of constitutive (pre-existing) and induced (post-invasion), structural and biochemical defences against invaders. Induced responses can also alter host suitability for other organisms sharing the same host, which may result in indirect, plant-mediated interactions between different species of attacking organisms. 2. Current range and host expansion of the mountain pine beetle (Dendroctonus ponderosae Hopkins; MPB) from lodgepole pine-dominated forests to the jack pine- dominated boreal forests provides a unique opportunity to investigate whether the colonisation of jack pine (Pinus banksiana Lamb.) by MPB will be affected by induced responses of jack pine to a native herbaceous insect species: the jack pine budworm (Choristoneura pinus pinus Freeman; JPBW). 3. We simulated MPB attacks with one of its fungal associates, Grosmannia clavigera Robinson-Jeffrey & Davidson, and tested induction of either herbivory by JPBW or inoculation with the fungus followed by a challenge treatment with the other organism on jack pine seedlings and measured and compared monoterpene responses in needles. 4. There was clear evidence of an increase in jack pine resistance to G. clavigera with previous herbivory, indicated by smaller lesions in response to fungal inoculations. In contrast, although needle monoterpenes greatly increased after G. clavigera inoculation and continued to increase during the herbivory challenge, JPBW growth was not affected, but JPBW increased the feeding rate to possibly compensate for altered host quality. 5. Jack pine responses varied greatly and depended on whether seedlings were treated with single or multiple organisms, and their order of damage. Key words. Boreal forest, Grosmannia clavigera, induced responses, jack pine budworm, jack pine, monoterpenes, mountain pine beetle, tree-mediated interactions. Introduction (Franceschi et al., 2005). Examples of these include resin ducts, stone cells, and a broad spectrum of stored secondary Coniferous trees have evolved both constitutive and inducible metabolites such as terpenoids, phenolics, and alkaloids. defence systems that deter or kill insects and inhibit or Induced responses are triggered by the threat of tissue exclude pathogens physically and/or chemically (Johnson damage and are deployed to increase tree defence (Franceschi & Croteau, 1987; Brignolas et al., 1998; Hudgins et al., et al., 2005). They include numerous anatomical changes, 2003; Lieutier et al., 2003, 2009; Franceschi et al., 2005; such as traumatic resin duct formation and the activation Eyles et al., 2007, 2010). Constitutive defences are general of polyphenolic parenchyma cells, as well as quantitative defences maintained by a tree that are present at the time and qualitative changes of secondary metabolites (Franceschi of attack to provide immediate resistance to an invasion et al., 2005). Induced responses may alter a host’s suitability for sub- Correspondence: Nadir Erbilgin, Department of Renewable Re- sequent organisms attacking the same host plant (Bonello sources, 442 Earth Sciences Building, University of Alberta, Edmonton et al., 2006). Consequently, host tree chemistry may mediate AB, T6G 2E3 Canada. E-mail: [email protected] the interactions among attacking organisms. There are many © 2011 The Authors Ecological Entomology © 2011 The Royal Entomological Society 425 426 Lindsay J. Colgan and Nadir Erbilgin examples of changes in conifer resistance (Raffa et al., 1998; Materials and methods Wallin & Raffa, 2001) and susceptibility (Annila et al., 1999; Krokene et al., 1999; Kosaka et al., 2001) after initial damage. Study system and justification These studies have documented that the induction of resistance MPB is the most destructive pest of pine forests in or susceptibility of plants depends on the organisms involved western North America and attacks mature trees in several (e.g. herbivores vs. pathogens), the organ of induction (e.g. species of Pinaceae, including lodgepole pine (Pinus contorta stem vs. foliage), and resource availability (Herms & Mattson, Douglas var. latifolia Engelman), (Wood, 1982). MPB carries 1992; Eyles et al., 2007). a variety of staining fungi that facilitate beetle establishment by Plant-induced responses also mediate interactions among disrupting transpiration and weakening tree defences, as well multiple organisms, such as herbivores and pathogens. Plant- as providing nutrition for larvae and teneral adults (Bleiker mediated indirect interactions between pathogens and herbi- & Six, 2007). For additional details of its lifecycle refer to vores can occur when the first coloniser alters the host plant Safranyik et al. (2010). in a way that affects the second coloniser that is often spa- Over the past decade, warmer winters and an abundance tially or temporally separated from the first. Previous stud- of hosts have allowed MPB to greatly expand its range into ies have documented that pathogen infection interferes with higher elevations and move eastward from lodgepole pine hormonal signalling defined as ‘cross-talk’ between defence forests west of the Rocky Mountains to lodgepole x jack pine pathways against pathogens (associated with salicylic acid) hybrid forests of northern Alberta (Carroll et al., 2006). It is and phytophagous insects (associated with jasmonic acid) expected that MPB will invade jack pine forests in the boreal (Hatcher et al., 2004; Beckers & Spoel, 2006). Cross-talk (Logan et al., 2003) as previous studies have established that can have different impacts on interacting organisms; pathogen the beetle (Cerezke, 1995) and its fungal associates can thrive infection can make a plant more or less susceptible to an in jack pine (Rice et al., 2007, 2008). This host and range insect. expansion is of great concern because once it establishes in The evolutionary history between trees and attacking jack pine forests, MPB has the potential to spread across organisms influences the outcome of host-mediated interactions Canada and invade eastern pine forests (Colgan & Erbilgin, (Tollrain & Harvell, 1999). If an exotic organism enters an 2010; Safranyik et al., 2010). ecosystem, both the exotic and native organisms could directly Winter temperatures in Alberta’s jack pine forests are interact through host availability and indirectly through host expected to initially limit MPB populations to low or endemic tree chemistry. Therefore, native organisms could influence levels (Regni´ ere` & Bentz, 2007; CFS, 2008). In its historical the survival and spread of the exotic organism, and thus its range, endemic beetle populations are constrained to attack invasion success. As a result, relationships between exotic trees with lowered defences such as those weakened by other and native organisms can be studied under the framework of insects and pathogens (Safranyik & Carroll, 2006). plant-mediated interactions. These investigations will become The JPBW is a defoliator that outbreaks periodically and increasingly important as more species expand their ranges is sympatrically distributed with its host jack pine. For owing to climate change. details of its lifecycle refer to McCullough (2000). Severe In the present study, we focused on the potential invasion defoliation of jack pine can result in growth reduction, top- of the North American boreal forest by an insect species, kill, and tree mortality (Kulman et al., 1963). As JPBW the mountain pine beetle, Dendroctonus ponderosae Hopkins herbivory does not usually result in tree mortality, jack pine (hereafter MPB), and its potential indirect interaction with defoliation may provide opportunities for MPB attack (Colgan a native herbivore, the jack pine budworm, Choristoneura & Erbilgin, 2010). Consequently, both insects could affect pinus pinus Freeman (hereafter JPBW) on jack pine, Pinus jack pine suitability for one another by inducing responses banksiana Lamb. We used one of the fungal associates of in host trees. As plant-mediated interactions depend on the mountain pine beetle, Grosmania clavigera Robinson-Jeffrey organisms and organs involved (Bonello, 2010), studying the & Davidson, as a proxy for MPB-induced changes on jack pine indirect interaction between JPBW and MPB on jack pine is because MPB has not yet established in jack pine stands. This important in understanding tree-mediated interactions between fungus was chosen for our experiments as it is well adapted a range-expanding exotic and a native species and potentially to cold temperatures and is likely to become more prevalent forecasting the risk of invasion of the boreal forest. in the fungal community of MPB in the boreal forest (Rice et al., 2008). Experiment design and data collection Our objectives were to (i) examine if the growth of JPBW or G. clavigera is affected by prior induction with the other A greenhouse experiment was conducted at the University organism; (ii) compare needle monoterpene responses to the of Alberta (Edmonton, AB, Canada) using jack pine seedlings, induction, challenge, and control treatments; (iii) explore the JPBW, and G. clavigera. In March 2009, 2-year-old jack pine relationship among host monoterpenes, JPBW growth, and seedlings were obtained from Boreal Horticultural Services