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Cadophora Margaritata Sp. Nov. and Other Fungi Associated with the Longhorn Beetles Anoplophora Glabripennis and Saperda Carcharias in Finland

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Cadophora Margaritata Sp. Nov. and Other Fungi Associated with the Longhorn Beetles Anoplophora Glabripennis and Saperda Carcharias in Finland Antonie van Leeuwenhoek https://doi.org/10.1007/s10482-018-1112-y ORIGINAL PAPER Cadophora margaritata sp. nov. and other fungi associated with the longhorn beetles Anoplophora glabripennis and Saperda carcharias in Finland Riikka Linnakoski . Risto Kasanen . Ilmeini Lasarov . Tiia Marttinen . Abbot O. Oghenekaro . Hui Sun . Fred O. Asiegbu . Michael J. Wingfield . Jarkko Hantula . Kari Helio¨vaara Received: 25 January 2018 / Accepted: 7 June 2018 Ó Springer International Publishing AG, part of Springer Nature 2018 Abstract Symbiosis with microbes is crucial for obtained from Populus tremula colonised by S. survival and development of wood-inhabiting long- carcharias, and Betula pendula and Salix caprea horn beetles (Coleoptera: Cerambycidae). Thus, infested by A. glabripennis, and compared these to the knowledge of the endemic fungal associates of insects samples collected from intact wood material. This would facilitate risk assessment in cases where a new study detected a number of plant pathogenic and invasive pest occupies the same ecological niche. saprotrophic fungi, and species with known potential However, the diversity of fungi associated with insects for enzymatic degradation of wood components. remains poorly understood. The aim of this study was Phylogenetic analyses of the most commonly encoun- to investigate fungi associated with the native large tered fungi isolated from the longhorn beetles revealed poplar longhorn beetle (Saperda carcharias) and the an association with fungi residing in the Cadophora– recently introduced Asian longhorn beetle (Ano- Mollisia species complex. A commonly encountered plophora glabripennis) infesting hardwood trees in fungus was Cadophora spadicis, a recently described Finland. We studied the cultivable fungal associates fungus associated with wood-decay. In addition, a novel species of Cadophora, for which the name Cadophora margaritata sp. nov. is provided, was Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10482-018-1112-y) con- isolated from the colonised wood. tains supplementary material, which is available to authorized users. R. Linnakoski (&) Á R. Kasanen Á T. Marttinen Á I. Lasarov A. O. Oghenekaro Á H. Sun Á F. O. Asiegbu Á School of Forest Sciences, University of Eastern Finland, K. Helio¨vaara Joensuu, Finland Department of Forest Sciences, University of Helsinki, Helsinki, Finland A. O. Oghenekaro e-mail: riikka.linnakoski@luke.fi Department of Plant Biology and Biotechnology, University of Benin, Benin City, Nigeria R. Linnakoski Á J. Hantula Natural Resources Institute Finland (Luke), Helsinki, Finland R. Linnakoski Á M. J. Wingfield Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa 123 Antonie van Leeuwenhoek Keywords 1 New taxon Á Alien invasive species Á 2014). However, the diversity of fungi associated with Cadophora sp. Á Introduced species Á Insect–fungus most Cerambycidae remains to be investigated. symbiosis Á Longhorn beetles Á Vectored pathogen An example of a common but poorly known Cerambycidae is the large poplar longhorn (Saperda carcharias) (Fig. 1). The biology of the insect is not fully understood, and there are no previous reports of Introduction its symbiotic fungi. The beetle is considered as the most harmful pest of hybrid poplars and aspen A nutrient-poor wood tissue (xylem), lacking readily (Populus tremula) in Finland (Hallaksela 1999; available carbohydrates and proteins, is a challenging Va¨lima¨ki and Helio¨vaara 2007). The adult beetle niche to be exploited by other organisms. However, feeds on aspen leaves and lays eggs in basal parts of cerambycid beetles (Coleoptera: Cerambycidae) are the stems during August–September (Helio¨vaara et al. adapted to complete their long lifecycle in wood 2004). The eggs undergo overwintering for tissues. In this niche, symbiosis with microbes 10–11 months and the emerging larvae remain in the (including filamentous fungi and yeasts) has been tunnels for 2–4 years. During this period, larvae can considered to be crucial for their survival and devel- gnaw tunnels up to 1 m long in the xylem. These opment (Kukor et al. 1988; Schloss et al. 2006; tunnels are often surrounded by a characteristic dark Watanabe and Tokuda 2010; Scully et al. 2013). The brown colour expanding vertically 1–3 m, which role of the associated microbes can be considered as prevent the logs from being used in the mechanical directly nutritional, in which insect larvae cultivate wood industry. Part of the wood material gnawed by and feed on the fungi (Francke-Grosmann 1967), or the larvae is transported through their alimentary when either ingested fungal enzymes (Kukor and canals. Due to long larval period of development in the Martin 1986; Kukor et al. 1988) or endosymbiotic gut tunnels, it is likely that the poplar longhorn has microbes contribute to cellulose degradation (Uvarov interactions with a number of fungi during its life 1929; Kukor et al. 1988;Gru¨nwald et al. 2010; cycle. Watanabe and Tokuda 2010; Scully et al. 2013). These The Asian longhorn beetle (Anoplophora symbiotic fungi may also have other functional roles, glabripennis) is a serious forest pest native to China such as nitrogen and vitamin acquisition (Gibson and (Lingafelter and Hoebeke 2002) (Fig. 2). In its native Hunter 2009; Ayayee et al. 2014). range, the beetle is not considered as a pest in natural The association of Cerambycidae and fungi was forests. However, the beetle became a common pest in recognised relatively long ago (Uvarov 1929; Jurzitza China as a result of widespread planting of susceptible 1959; Riba 1977; Chararas and Pignal 1981; Nardon poplar (Populus sp.) hybrids (EPPO 2016). As an and Grenier 1989). In general, the modified colour and invasive species, A. glabripennis is a highly destruc- texture of the wood close to the larval tunnels indicate tive quarantine pest (EPPO 2016). The beetle is that symbiotic organisms are commonly involved in capable of infesting a wide range of deciduous trees, the diet of xylophagous insects. Many of the wood- including also healthy trees. The Asian longhorned inhabiting fungi and insect symbioses have long co- beetle has spread globally mainly in ineffectively evolutionary histories (Vega and Blackwell 2005), treated wooden packaging materials originating from recently supported by the observations of fungi and China. It was accidentally introduced first into North associated organisms successfully passing through the America (Haack et al. 1996; Hu et al. 2009), followed insect alimentary tract (Drenkhan et al. 2013, 2016). by several introductions into European countries The associations with Cerambycidae have arisen during the past two decades (Tomiczek et al. 2002; independently in distantly related fungal genera, He´rard et al. 2006, 2009; Haack et al. 2010), and representing examples of convergent evolution (Jones recently into Finland. et al. 1999). Cerambycidae are known to harbour a rich In several instances, baseline information on fungal assemblage of microbes in terms of taxonomic and associates of insects in their endemic environment is functional diversity (Gru¨nwald et al. 2010; Watanabe lacking. This hinders risk assessment measures in and Tokuda 2010; Scully et al. 2013; Ayayee et al. cases where a novel forest pest and/or pathogen is introduced. Novel insect–fungal interactions represent 123 Antonie van Leeuwenhoek Fig. 1 a Aspen (P. tremula) stand in Urjala, Finland, b, c the large poplar longhorn beetle (S. carcharias) adult and larvae, and d brown decay surrounding the beetle gallery on P. tremula an increased risk to forest health (Humble and Allen carcharias in its native host tree and environment, and 2006; Hulcr and Dunn 2011; Wingfield et al. 2016; with the introduced A. glabripennis infestation in Stenlid and Oliva 2016). Examples of devastating tree Finland. Our hypotheses were that the longhorn disease problems that have arisen from these associ- beetles are associated with specific fungi, which may ations are increasing in number (Lu et al. 2011; improve nutritional quality of the larvae facilitating Akbulut and Stamps 2012; Ploetz et al. 2013; Santini larval development inside the wood. Furthermore, we and Faccoli 2014; Wingfield et al. 2016). Recent hypothesised that differences in fungal species com- introductions of plant pathogens (Wingfield et al. positions between intact wood and wood colonised by 2016) suggest that latent microbial pathogens com- beetles would reflect the specific symbiotic fungi monly remain undetected in quarantine inspections. associated with each beetle. In addition, we hypoth- The aim of the study was to provide baseline esise that the introduced insect pest would establish information on fungal diversity associated with S. interactions with native fungal associates of 123 Antonie van Leeuwenhoek Fig. 2 The Asian longhorned beetle (A. glabripennis) adult and larvae, and brown decay surrounding the beetle gallery on B. pendula ecologically and taxonomically closely related insect tunnels with surface disinfected carpenter’s knife and species. surgical knife. Control isolations were made from the non-coloured, undamaged distal ends of the logs as described above. All samples were surface disinfected Materials and methods in sterile conditions with 70% ethanol (10 s) and 10% sodium hypochlorite (NaClO) (5 s) and finally washed Study areas and collection of samples four times with fresh sterile water. The
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