Elsevier

Fungal Ecology

Volume 45, June 2020, 100926
Fungal Ecology

Fungal symbionts of bark and ambrosia beetles can suppress decomposition of pine sapwood by competing with wood-decay fungi

https://doi.org/10.1016/j.funeco.2020.100926Get rights and content

Abstract

Bark and ambrosia beetles inoculate dying trees with symbiotic fungi. The effects of these fungi on wood decomposition are poorly understood. We determined the effects of three widespread Ascomycota symbionts and one introduced Basidiomycota symbiont on the decomposition of loblolly pine (Pinus taeda) sapwood. Ascomycetes caused <5% mass loss and no visible structural degradation, whereas the basidiomycete Flavodon ambrosius caused nearly 15% mass loss and visible structural degradation similar to free-living wood-decay fungi. Ophiostoma ips and Raffaelea fusca reduced white- and brown-rot decay through competition with Ganoderma curtisii and Phaeolus schweinitzii, respectively. The inhibitory effects of O. ips and R. fusca on decay were negated when co-inoculated with F. ambrosius suggesting that the spread of this invader could influence forest carbon cycles. In contrast to the predominant forest biology narrative, the common and widespread ophiostomatalean symbionts of bark and ambrosia beetles studied here appear to delay, rather than facilitate tree biomass recycling.

Introduction

Wood comprises as much as 98% of the living biomass in forests (Fittkau and Klinge, 1973) and is mostly composed of lignocellulose which requires non-enzymatic and specialized enzyme suites for biological decomposition. The ability to decompose wood is possessed primarily by fungi within the phylum Basidiomycota (Blanchette, 1991; Floudas et al., 2012). Decay fungi are essential to forest productivity and biodiversity because they release the immense stores of energy and nutrients bound in wood to the surrounding biological community (Rayner and Boddy, 1988). Because of the ubiquity of woody biomass world-wide, changing wood decomposition rates could have global effects on nutrient cycling and carbon sequestration (Floudas et al., 2012; Hibbett et al., 2016). Wood decomposition is modulated by ecological interactions between decay fungi and other organisms (Hulme and Shields, 1970; Boddy, 2000), and small changes in fungal colonization processes can lead to several-fold changes in decay rates (Fukami et al., 2010; Cline and Zak, 2015).

Wood-boring bark and ambrosia beetles are widely believed to facilitate biomass recycling by inoculating dead and dying trees with saprotrophic fungi including ambrosia fungi and occasionally wood-decay fungi (Miller et al., 2016; Ulyshen, 2016). These beetles comprise more than 7000 species in the weevil subfamilies Platypodinae and Scolytinae that thrive throughout tropical and temperate regions (Kirkendall et al., 2015). They are often the first insects to colonize the wood, entering before the tree has died and having major impacts on fungal community development within wood (Leach et al., 1934; Persson et al., 2011; Strid et al., 2014; Skelton et al., 2019). The beetles have various relationships with the fungi they carry, ranging from incidental commensalism, to highly co-evolved and reciprocally obligate mutualisms (Harrington, 2005; Hulcr and Stelinski, 2017). Some beetles have specialized glandular organs called mycangia for transporting and nourishing particular lineages of nutritional fungi and have become entirely dependent on a fungal diet (Francke-Grosmann, 1956; Batra, 1963; Hulcr and Stelinski, 2017). Likewise, some fungi have evolved complete dependence on these beetles for dispersal and colonization of wood tissues (Francke-Grosmann, 1956; Batra, 1963; Six, 2003; Harrington, 2005). The few species of beetles and symbiotic fungi that kill healthy trees and impact agricultural and silviculture interests have been the center of intense research efforts. In contrast, we know little about the ecological roles of the thousands of other beetles and their fungi that do not kill trees but are ubiquitous and abundant on every continent except Antarctica.

In the southeastern United States, the phloem of stressed, declining, or recently dead pines (Pinus spp.) is typically infested by native bark beetles in the genera Ips, Dendroctonus, Orthotomicus, and Hylastes, and the xylem is colonized by ambrosia beetles in the genera Xyleborus, Myoplatypus, and Gnathotrichus. These beetles are primarily associated with saprotrophic Ascomycota in the orders Ophiostomatales (e.g. Ophiostoma, Leptographium, and Raffaelea), and Saccharomycetales (e.g. Pichia, Candida, and Ambrosiozyma), and incidental associations with various other fungi are common (Harrington, 2005; Hofstetter et al., 2015; Hulcr and Stelinski, 2017; Skelton et al. 2018, 2019).

Beetle-associated Ascomycota can utilize some of the major chemical components of wood including structural polysaccharides, but available evidence indicates that they generally do not cause extensive structural degradation or wood mass loss. Most saprotrophic fungi, including beetle-associated fungi, express extracellular enzymes capable of degrading the major carbohydrate constituents of plant cell walls such as cellulose and hemicellulose (Blanchette, 1991). Such enzymes have been detected in mixed fungal communities associated with laboratory colonies of the ambrosia beetle Xyleborinus saxesseni (Licht and Biedermann, 2012), as well as pure cultures of the beetle-associated tree pathogens Ophiostoma ulmi and Ophiostoma novo-ulmi (Svaldi and Elgersma, 1982; Binz and Canevascini, 1996; Przybył et al., 2006), the ambrosia fungus Phialophoropsis (Lehenberger et al., 2019), ambrosia and non-ambrosial Geosmithia (Veselská et al., 2019), and are likely to occur in many other beetle-associated fungi. However, the structural carbohydrates of woody tissues are reinforced by an interspersed matrix of the structural polymer lignin. Carbohydrate-targeting enzymes cannot effectively decompose the carbohydrates of wood unless the lignin is decomposed, unbound, or modified, which requires specialized non-enzymatic and enzymatic processes borne by few fungal lineages, mostly in Basidiomycota (Blanchette, 1991; Worrall et al., 1997; Floudas et al., 2012; Hibbett et al., 2016). Consequently, relatively few fungi cause extensive wood decomposition. Congruently, experimental studies of common beetle-associated Ascomycota have shown little to no degradation of wood structure, marginal loss of wood hardness, and minimal mass loss (Miller and Elgersma, 1976; Seifert, 1993; Kasson et al., 2016), suggesting that these fungi depend on more labile carbohydrate sources such starches, sugars, and other extractives, rather than the structural elements that comprise the majority of wood biomass (e.g. Schirp et al., 2007). Saprophytic fungi that cannot decompose lignocellulose, including beetle-associates, may still access non-structural nutrients in the wood by spreading their hyphae through ray parenchyma cells and resin canals to become distributed in the sapwood. Although they do not decompose the woody cell wall, they can mechanically penetrate cell walls using fine penetration pegs (Eriksson et al., 1990).

Beetle-associated fungi could impede colonization and decomposition by more aggressive wood-decaying fungi by competing with pioneer decay fungi for labile carbohydrates or producing toxic secondary metabolites. It has been previously demonstrated that colonization of wood by non-beetle-associated Ascomycota reduces subsequent decay through competitive interactions with decay fungi (Hulme and Shields, 1970; Behrendt et al., 1995). Some of these species of Ascomycota have potential commercial applications for preventing wood rot (Schubert et al., 2008). Similarly, a recent field experiment utilizing beetle exclosure cages showed that high densities of ambrosia beetles caused reduced decay of pine sap wood, potentially as an effect of competition between their ascomycete symbionts and wood-decay fungi (Skelton et al., 2019). Ophiostomatales may also facilitate colonization of fungi that cannot tolerate extractives such as pitch and other resinous compounds in freshly exposed xylem. Ophiostomatales and some other early colonizing fungi not only tolerate these compounds but can decompose them over time (Blanchette et al., 1992).

The primary nutritional symbiont of beetles in the genera Ambrosiodmus and Ambrosiophilus is unusual among ambrosia fungi. It is a fungus in the phylum Basidiomycota that decomposes lignocellulose and causes extensive mass loss and softening of wood similar to known aggressive wood-decay fungi (Kasson et al., 2016). Several species of Ambrosiodmus are native to the southeastern USA, and at least three species are non-native. An Asian ambrosia beetle, Ambrosiodmus minor, was first detected in Florida by state monitoring efforts in 2011, and has since become one of the most frequently collected ambrosia beetle species across the state where it infests many species of hardwood and coniferous trees (Hulcr et al., 2018). Although there have been more than 50 species of non-native bark and ambrosia beetles to become established in the USA (http://www.barkbeetles.info; accessed Oct 15, 2018), A. minor is particularly likely to affect wood decomposition because of the combination of its increasing abundance and its symbiotic wood-decay fungus. Another common basidiomycete beetle-associate, Entomocorticium spp., could also contribute directly to wood decomposition. This is a primary nutritional fungus of several native species of two bark beetle genera that specialize on conifers, Dendroctonus and Pityoborus. The phylogenetic placement of Entomocorticium within the paraphyletic white-rot genus Peniophora (Hsiau and Harrington, 2003), and the production of extracellular cellulases and polyphenol oxidases suggest Entomocorticium may cause structural decomposition of wood (Hsiau and Harrington, 2003; Valiev et al., 2009). However, in situ observations of this fungus suggested that it does not cause any noticeable structural decomposition of sapwood (Whitney et al., 1987).

The objectives of this study were to examine the direct effects of native ascomycete associates, and the introduced basidiomycete associate on pine wood decomposition, and to assess secondary effects through competitive interactions with two common wood-decay fungi in pines of the southeastern USA. We hypothesized that native bark and ambrosia beetles can suppress early stages of decay by inoculating fresh wood with fungi that do not extensively decompose structural elements of wood, but instead compete with pioneer colonizing wood-decay fungi. We further hypothesized the inclusion of the non-native wood-decay ambrosia fungus Flavodon ambrosius could offset the inhibitory effects of native beetle-associated fungi on early decomposition through functional redundancy with free-living decay fungi.

Section snippets

Methods

Isolate Recovery and Identification: All beetle-associated fungal isolates were obtained from the University of Florida Forest Entomology Bark and Ambrosia Beetle collection and were originally isolated from pine-infesting bark and ambrosia beetles at the Austin Carey Experimental Research Forest near Gainesville, Florida, USA (Table 1). Isolation from live beetles and culture methods followed Skelton et al. (2018). Identification of beetle-associated fungi was based on BLASTn comparison of the

Results

Direct effects experiment: The introduced Asian basidiomycete, F. ambrosius, caused approximately three times more mass loss than any other beetle-associated fungus that was assayed (Fig. 1). All assayed fungi caused mass loss that was significantly greater than negative controls indicating that some fraction of wood biomass had been consumed by each fungus (Table 2). However, the ascomycete beetle-associated fungi (Ophiostoma, Raffaelea, and Ambrosiozyma) caused less than 5% mass loss on

Discussion

Bark and ambrosia beetles are widely believed to accelerate wood decomposition by introducing fungi during the early stages of saprotroph community assembly. However, the majority of fungi associated with these beetles are ascomycetes (Hofstetter et al., 2015; Hibbett et al., 2016; Hulcr and Stelinski, 2017), and the large majority of Ascomycota do not cause extensive wood decomposition under normal circumstances in most habitats (Floudas et al., 2012; Hibbett et al., 2016). Many Ascomycota,

Conclusions

The two common and widespread ophiostomatalean associates of bark and ambrosia beetles studied here may inhibit decay by competing with decay fungi. In contrast, the introduced basidiomycete ambrosia fungus F. ambrosius, causes decay similar to other well-known free-living white-rot fungi and nullifies the inhibitory effects of ascomycete beetle symbionts, suggesting that widespread introduction of this fungus and its vectors could significantly impact carbon turnover rates in forest

Acknowledgement

We thank Allan Gonzalez for producing interaction photographs. We also thank Cassie Newman who was an undergraduate student who assisted with the decay microcosm preparation. We thank Daniel Lindner at the USFS Center for Forest Mycology Research, Madison WI, for preserving and providing fungal isolates. We thank three anonymous reviewers and Peter Biedermann for helpful feedback during manuscript revision. The project was supported by the USDA Forest Service, Florida Forest Service, USDA-APHIS

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