Fungivory and host associations of Coleoptera: a bibliography and review of research approaches

Abstract

Fungi and Coleoptera are among the most evolutionarily successful and diverse heterotrophic organisms in the world. Due to their unique adaptive capacities, fungi and beetles co-occur and interact in various terrestrial habitats. In addition to commensal and mutualistic fungus–beetle relations, combative interactions involve aggressors from both sides such as entomopathogenic fungi and fungivorous beetles. Fungivory, most commonly in combination with saprophagy and xylophagy, is characteristic of many families of Coleoptera. The resource-exploiting fungal mycelia are most frequently consumed by beetles together with the woody substrata. The focus of the present review is on Coleoptera with larvae or adults feeding on a primarily fungal diet: fruit bodies and spores.

Keywords:

• beetles
• mycophagy
• basidiomycetes
• polypores
• saproxylic

Introduction

Fungivory (mycophagy: Lawrence 1989) is feeding on mycelia, fruit bodies, or spores of fungi. Obligate or facultative fungivory is characteristic of many saproxylic (dead wood and coarse woody debris dependent) insects, which exploit the lignolytic and cellulolytic abilities of fungi to feed on mycelia and inhabit wood altered by fungi. At least six types of fungivory can be identified based on the life stages of the insect (larva and adult) and the fungus (spore, mycelium, and fruit body). Furthermore, fungivorous insects can be divided into consumers of living and of dead fungi (Yakovlev 1995). Lawrence (1989) separates micro- and macrophagy of fungivores based on the mouthpart morphology of beetles and the types of food sources. All types of trophic specialization can be found among the fungivores from mono- and oligophagy to the most common polyphagy – in an extreme case, an Australasian fungivore Cis bilamellatus invaded northern Europe using a broad range of fungal hosts (Orledge et al. 2010).

Associations between fungi and insects are among the most species-rich, diverse, and complex in terrestrial ecosystems. The unique adaptations and dispersal abilities of both fungi and insects result in a variety of interaction types. One of the main guilds is comprised of fungivorous beetles. The high species diversity of fungivores in distantly related phylogenetic clades of Coleoptera indicates a special role of fungi in the evolution of the largest order of living organisms. Fungivory in Coleoptera seems to have evolved independently several times (Crowson 1981).

The paleontological evidence of insect fungivory is scarce – large fruit bodies of the Basidiomycetes are unknown until the Early Cretaceous, but a recent discovery from amber in France suggests that macromycetes have served as a habitat for fungivorous insects since the Albian, ca 100 million years ago (Schmidt et al. 2010).

Although insects often consume mycelia together with their woody substrates, the focus of this review is on beetles selectively consuming fruit bodies and spores of fungi. Most of the publications on insect fungivory have dealt with fruit bodies, and the present review aims to summarise these studies and to identify future research directions. It is impossible to cover all references on this broad topic in a review article. Additional references can be found in the bibliography reviews by Fogel (1973a, 1973b), Jonsell (1999), and Komonen (2003a), Thunes (1993) tabulates the polypore–invertebrate interaction studies from 1920 to 1989 and Schigel (2009) from 1950 to 2008.

Fungi and coleoptera

Fungal fruit bodies and their spores provide beetles with patchy and often temporally unpredictable habitats and food sources, which are rich in carbohydrates (structural polysaccharides) and proteins, including all the amino acids necessary for insect development and growth (Lundgren 2009a).The temporal and spatial variability of these habitats is reflected in the speed of fungal growth and decomposition, predictability and yearly fluctuations in fructification, duration and stability of fruit bodies, phenology (Ryvarden 1991), and sporulation patterns. Fruit bodies, including hypogeous ones (Fogel and Peck 1975), offer both airborne and terrestrial colonizers a diversity of targets.

Among the insects attracted by fungi, the most species-rich taxa are Diptera and Coleoptera. Hammond and Lawrence (1989) provide a family-by-family review of fungivory in these orders. Moisture of the larval habitat may demarcate Diptera and Coleoptera – most fungivorous Diptera colonize agaricoid fungi and boletes, and beetles are able to attack dry and dense xylotrophic fungi, but this ecological border is fuzzy. There is little doubt that saprophagy and fungivory are ancestral types of feeding in Coleoptera (Lawrence 1989; Leschen 2000). Fungivory is found among the smallest beetles, Ptiliidae, especially Nanosellinae (Fogel & Peck 1975; Polilov 2008), including the smallest beetle in Europe Baranowskiella ehnstromi (Andersen et al. 2003). The adults of many Leiodidae species live off fungal spores, but larvae of these species feed on myxomycetes; similar changes of the food source after pupation is characteristic for other spore-feeders, including Sphindidae, Nitidulidae, and Latridiidae. Decaying fungi attract saprophagous beetles such as Silphidae, Hydrophilidae, Scarabaeidae, and Staphylinidae (Lawrence 1989). Staphylinidae, a vast and insufficiently studied family, also includes predators and specialized fungivorous species with unknown larval biology, such as Gyrophaena spp. (White 1977), Scaphidiinae (Ashe 1984), and Hoplandriini (Thayer et al. 2004). Many Staphylinidae, especially Aleocharinae (Lipkow & Betz 2005; Semenov 2007, 2008), are associated with agaricoid, e.g. Phanerota with Russula spp. (Ashe 1981), bolete and other ephemeral moist fungal habitats (Babenko & Bogatyreva 1981; Thayer 1987). Sporulating fruit bodies, masses of spores and anamorphic fungi covering decaying plant and fungal remnants, host specialized beetles from such families as Clambidae, Cryptophagidae, and Corylophidae. In European fauna, the most abundant polypore destructors are Anobiidae, Trogositidae, Erotylidae, Endomychidae, Tenebrionidae, Mycetophagidae, Tetratomidae, Ciidae, and Melandryidae (Schigel 2009). Most of the publications reviewed here are based on larval records and rearings, but a few studies have scrutinized the species-rich assemblages of adult Coleoptera, which are attracted by fungal fruit bodies of, for example, Polyporus squamosus (Klimaszewski & Peck 1987); Piptoporus betulinus and Fomes fomentarius (Thunes 1994); and Fomitopsis pinicola and Fomes fomentarius (Hågvar 1999; Økland 2002). Epps and Arnold (2010) found 72 morphospecies of Coleoptera occurring on 68 species of fungi.

Morphological adaptations to fungivory, in particular the mouthparts of insect larvae, were described in books by Peterson (1960), Gilyarov (1964), Striganova (1966), and Stehr (1991), and later studied by Kompantsev (1982), Kompantsev and Potockaya (1987), Kompantseva (1987a, 1987b), Hanley (2001), Leschen and Beutel (2001), Betz (2004), and Betz et al. (2003).

Ecology of fungus–beetle relationships

Structural differences between the fruit bodies of different species of fungi as hosts of fungivores and predictability and abundance patterns of fungi are contrasted by the quantity vs. quality hypotheses of insect polyphagy, seen as a risk-spreading strategy among fungivores. Fruit bodies of perennial polypores are more persistent than those of annual polypores, which in turn are more durable than those of agarics and boletes – the diversity–stability hypothesis may offer an explanation of species-richness patterns in different types of fungal fruit bodies (Hanski 1989). As in plant–herbivore systems, relationships between fungi and fungivores include grazing pressure, defensive mechanisms, e.g. secondary metabolites of fungi (Rohlfs et al. 2007), and dispersal. Fungal mycelia greatly influence the nutritional turnover, while the formation of fruit bodies and spores can be seen as species exit from the community. These stages of the fungal life cycle attract various beetle colonizers and consumers.

The parallels between phylogenies and systematic position of beetle and fungal taxa were drawn by Paviour-Smith (1960a), Lawrence (1973), Kompantsev (1984), and Jonsell and Nordlander (2004). Fungal host associations are used to confirm specific isolation of two Phanerota species (Ashe 1982). Analysing the beetle host-groups, Orledge and Reynolds (2005) combine original and literature data to cover 167 species of Ciidae in relation to genera of their fungal hosts. Ashe (1986b, 1987) correlates phylogeny and morphology of fungivorous Gyrophaenine Staphylinidae, while Leschen and Löbl (2005) discuss phylogeny and evolution of fungivory of Scaphisomatini, and Robertson et al. (2004) and Leschen and Buckley (2007) of Erotylidae.

High species diversity of beetles on sporulating fruit bodies and the difference in diurnal and nocturnal activities of the Coleoptera were revealed by Paviour-Smith (1965) and Nilsson (1997a). Numerous species of spore-attracted beetles have been recorded on perennial polypores or on the large fruit bodies of polypores (Hågvar 1999). The role of fungivorous insects as spore vectors has been poorly documented. The direct negative (destructive) impact of the fungivores on the fungal community by, for example, reducing the spore productivity has been shown in a number of cases (Shaw 1992; Guevara et al. 2000c).

Experimental and host chemistry studies

The role of host odours and volatiles in attracting beetles to fungal fruit bodies have been demonstrated by a number of experimental studies. Guevara et al. (2000b) studied Ciidae beetles attracted by fungi in the field, and experimentally supported the field observations on specialist and generalist Ciidae responding to the polypore odours. Thakeow et al. (2008) confirmed that Cis boleti respond to the volatile compounds of Trametes gibbosa.

The chemical composition of fungi as habitats for insects, and the biochemical aspects of fungus–insect interactions were studied by Martin (1979, 1992), Martin et al. (1981), Kukor and Martin (1987), Pacioni et al. (1990, 1991), Gallois et al. (1990), Abraham and Berger (1994), and Fäldt et al. (1999). Hanski (1989) argued that volatiles may explain the broad polyphagy of fungivores. The kairomone effect of fungal mycelia in beetle attraction to dead-wood was studied by Johansson et al. (2007b). Lopes-Andrade et al. (2003) experimentally demonstrated secretion of a sexual pheromone by the abdominal fovea of the fungivorous ciid beetle Xylographus contractus. Dentinger and Roy (2010) studied insect attraction by orchids that look and smell like neighbouring fungi in the Ecuadorian Andes. Belmain et al. (2002) discuss the differences in volatile odours with aging of the fungus, and Guevara et al. (2000a) demonstrates differences in the behavioural responses of Ciidae exposed to odour compounds of mature and young fruit bodies of Trametes versicolor.

Host chemistry and odours is a research field closely linked to dispersal studies. Starzomski and Bondrup-Nielsen (2002) explored the effect of movement on the metapopulation structure of Bolitotherus cornutus. Komonen (2008) studied the abilities of Ciidae to colonize Trametes, and confirmed that ciids are able to disperse for up to 1.5 km towards the odours of fungal fruit bodies.

Biogeography

The national faunas and mycotas are reasonably well known in Europe, but most countries lack checklists of fungus–beetle interactions covering an entire vegetation zone or a state. Exceptions include Ševčík (2003), who reviewed the insect associations with wood-decaying fungi in the Czech and Slovak republics and Schigel (2011a), who reviewed these in Finland. At the regional level, Ciid ecology is well-documented in southwestern Germany (Reibnitz 1999) and in Sweden (Östergötland–Västerbotten, Jonsell & Nordlander 2004). Atty (1983) reported fungal hosts of beetles in Gloucestershire, UK and Conrad (1992) documented the distribution of 16 fungivorous beetles in Germany. Rough distribution maps are available at http://data.gbif.org/species and other regional and global occurrence and observation databases on the internet. Habitat loss and fragmentation pose a threat to the stability of the fungus–insect systems – Jonsson and Nordlander (2006) confirm that colonization rates of fungivores are affected by distance from an old-growth forest reserve.

History of research and literature review

Early works, XVIII-XX century

The first documented evidence of beetle fungivory can be found in the insect species descriptions and are reflected in their nomenclature, such as Cis boleti (Scopoli 1763). Occasionally, the labels of the old museum specimens read “on fungi” or the host fungi were indicated for individual insect species, e.g. by Perris (1853, 1877). These, and publications through the early twentieth century, on fungus–beetle interactions, are difficult to compare with modern data because of revised taxonomy, jointly reported associations of larvae and adults, and missing indications of the museums where specimens are preserved. Associations between fungi and invertebrates became an increasingly popular study topic for mycologists and entomologists in the twentieth century: Saalas (1917, 1923), Lesne (1917), Falcoz (1927, 1930), Roubal (1927), Donisthorpe (1931, 1935a, 1935b), and Portevin (1934) were among the first in Europe to document host associations of saproxylic and fungivorous beetles.

1950s and the great monographs

In the post-war world, natural history research traditions were still prominent, and several voluminous publications with valuable information on species ecology were produced, beginning with Scheerpeltz and Höfler (1948) and Palm (1951, 1959). Benick (1952) reported that Polyporus squamosus hosts 246 species of beetles. Even though it is unlikely that all of these species are fungivorous, none of the agaricoid fungi are known to host as many invertebrate associates. However, the number of individuals on a single fruit body of a polypore is lower in comparison to the number on a fruit body of an agaric fungus (Rehfous 1955). Fungivorous larvae of Erotylidae in Japan were studied by Nobuchi (1954), while those of Bolitotherus cornutus in the USA were studied by Liles (1956).

Soon after the classic work of Benick (1952), who studied 1116 species (32,004 specimens) of fungicolous beetles in northern Germany, lengthy reports on fungus–beetle links went out of fashion in species interaction research, and were replaced by more narrowly focused ecological studies.

Cyrillic literature

Cyrillic literature remains difficult to interpret and access for the global scientific community, even though selected papers have been re-published in English (Krasutskii 2006, 2007). The information blockade of the former Soviet Union from the rest of the academic world delayed advances of the research methods. This isolation, however, had the positive side effect of preserving the natural history style in research, enabling the large-scale collection of species-specific information in Eurasia from European Russia (Logvinovsky & Holkina 1992; Nikitsky & Tatarinova 2002; Schigel 2002; Nikitsky & Schigel 2004), Ukraine (Nadvornaya & Nadvorniy 1991) and Belarus (Tsinkevich 1995, 1997a, 1997b, 1998, 1999, 2004) to Central Asia (Nikitsky & Kompantsev 1997) and the Russian Far East (Nikitsky & Kompantsev 1995). Logvinovsky (1980, 1985) focused on Anobiidae, Yuferev (1982) on Leiodidae, Nikitsky (1993) on Mycetophagidae, and Kompantsev (1982, 1984, 1988), Kompantsev and Potockaya (1987), and Kompantseva (1987a, 1987b, 1987c) studied various aspects of beetle fungivory. Krasutskiy (1990, 1992a, 1992b, 1994a–1994c, 1995, 1996a, 1996b, 1997, 2005) carried out a number of beetle fungivory studies in Western Siberia and the Urals.

Nikitsky et al. (1996, 1998) and Nikitsky and Semenov (2001) supply information on fungal and myxomycete hosts for many of the 439 beetle species recorded in Prioksko-Terrasny Nature Reserve south of Moscow. Hosts of Mycetophagidae from Russia and adjacent countries are qualitatively reported by Nikitsky (1993), while studies by Saluk (1989, 1991, 1995) focus on Latridiidae. Krasutskiy (2005) provides data on 208 fungicolous beetles and 89 species of host fungi found in the Urals and Transurals.

1960s–early 1990s

Starting from the 1960s, in fungus–insect ecology studies, descriptions and observations became gradually replaced by experiments designed to test specific ecological hypotheses. In particular, studies of Paviour-Smith (1960a, 1960b, 1963a, 1963b, 1965, 1966, 1968a, 1968b, 1969) are examples of clarity and elegance in study design and in reporting results in fungus–insect interaction research.

By the end of this era, species ecology information started to migrate from the research articles (Graves 1960, 1965; Miyatake 1960; Eisfielder 1961, 1963, 1970; Graves & Graves 1966; Roman 1970; Dajoz 1981, 1988; Conrad 1984) towards books (Koch 1989a; 1989b and other Ökologie volumes of Die Käfer Mitteleuropas). Fungus–beetle studies based on a single species of fungi (Harrington 1980; Tadros 1982; Klimaszewski & Peck 1987) or on a single species of beetle (Paviour-Smith 1964; Pace 1967; Conner 1988, 1989) became more common.

The new world

Biologically, neither fungi nor beetles justify the separation of the fungus–beetle research in the Americas and Australasia from the Old World studies. However, the preference towards the staphyliniform and tenebrionoid beetles, the true passion for Bolitotherus cornutus as a model species (which can be compared only to the Bolitophagus reticulatus obsession in Europe, see below) are the distinct characters of the scholar school in the New World.

Weiss (1920a–1920c, 1921, 1922, 1924), Weiss and West (1920, 1921) and Chagnon (1935) were among the US pioneers in this research field. In the 1960s–1970s, Lawrence published a number of studies on North American fungivorous beetles (1967a, 1967b, 1971, 1973). Judd (1957), Pielou and Verma (1968), Matthewman and Pielou (1971), Hammond et al. (2004), and Majka (2007) studied fungivorous beetles in Canada, and Ackerman and Shenfeldt (1973a, 1973b) in Wisconsin, Chandler (1991) in New Hampshire, Goodrich and Skelley (1993) in Illinois, and Dajoz (1996) in Arizona. Epps and Arnolds (2010) reported 72 beetle species from 15 families collected as adults from a remarkable number of 180 species of fungi in the Appalachian Mountains.

Leschen and Allen (1988) described larvae and fungal hosts of three Oxyporus species. Leschen (1990) reviewed the fungivory of tenebrionoid beetles in the eastern USA, Skelley et al. (1991) of North American Erotylidae, Hanley and Goodrich (1993, 1995) of the New World Oxyporinae, and Goodrich and Skelley (1994) reported host fungi of North American Tritoma spp. Cline and Leschen (2005) provide a checklist of North American Coleoptera associated with Peurotus ostreatus. Bolitotherus cornutus is undoubtedly the best-studied fungivore beetle in the western hemisphere (Teichert 1999; Teichert & Bondrup-Nielsen 2005), including such aspects as sexual selection (Conner 1988, 1989), habitat fragmentation (Kehler & Bondrup-Nielsen 1999), and movement dynamics (Starzomski 2000). The fungivorous habits of other individual beetle genera and species have also been reported (Leschen 1988a, 1988b; Klopfenstein & Graves 1989).

Navarrete-Heredia and Novelo-Gutiérrez (1990), Delgado-Castillo et al. (1993), Navarrete-Heredia and Galinda Miranda (1997), Guevara and Dirzo (1999), and Fierros-López (2006) studied the fungivores of Mexico. Gumier-Costa et al. (2003) and Graf et al. (2007) uncovered the associations of beetles and fungi in Brazil. Hawkeswood et al. (1997), Lawrence and Milner (1996), and Grove (2002) reported fungivorous beetles from Australia. Leschen (1994a), Osawa et al. (2011), and Kadowaki (2010c) explore fungivorous Coleoptera of New Zealand, in particular the spore-feeding beetles on Ganoderma (Kadowaki et al. 2011a–2011c).

1990s–2011, the European dead wood boom

By the end of the twentieth century, fungivory of beetles became a popular study topic in population and mathematical ecology (O'Connell & Bogler 1997; Thunes & Willasten 1997; Sverdrup-Thygeson & Midtgaard 1998). Concurrently, the value of dead wood as a biodiversity hotspot habitat was demonstrated (Ehnström 2001; Johansson et al. 2007a).

Several studies have been restricted to certain widespread or conspicuous fungi, such as Cryptoporus volvatus (Setsuda 1995; Kadowaki 2010a, 2010b), Ganoderma applanatum (Tuno 1999; Kadowaki et al. 2010), Amylocystis lapponica and Fomitopsis rosea (Komonen et al. 2000, 2001) or beetles, e.g. Bolitophagus reticulatus (Nilsson 1997b; Midtgaard et al. 1998; Sverdrup-Thygeson & Midtgaard 1998; Knutsen et al. 2000; Jonsson 2003), and Cis dentatus (Orledge & Ewing 2006). Ehnström and Axelsson (2002) reported 18 main fungal hosts for 26 polyporicolous beetles, and Schigel (2011a) reported 198 fungal hosts for 176 polyporicolous beetles. Associations between fungi and beetles have been studied in a number of doctoral theses (Thunes 1993; Midtgaard 1996; Nilsson 1997a; Tsinkevich 1997b; Jonsell 1999; Rukke 2000a; Sverdrup-Thygeson 2000; Jonsson 2002; Henneberg 2003; Komonen 2003a; Johansson 2006; Olsson 2008; Möller 2009; Schigel 2009).

Among the key findings from this period are that forest characteristics and human activities directly influence the presence and the numbers of Coleoptera species in polypores (Thunes & Midtgaard 1998). Økland (1995) identified factors influencing composition and species richness of fungivorous beetle communities: hyphal structure of a fungus, its hardness, durational stability, and insect mouthpart adaptations. Aggregation and frequency of occurrence can be used to measure the habitat preference caused by a combination of dietary and non-dietary (e.g. mate location) constraints (Jonsell & Nordlander 1995; Jonsson et al. 1997). Fossli and Andersen (1998) identified certain fungal genera or species preferred by beetles based on the densities of beetle individuals on fungi. Jonsell et al. (1998) argued that the presence of wood-decaying fungi is one of the most important factors in determining the fauna of saproxylic beetles. Thunes et al. (2000) reported an increase in the number of red-listed beetle species and more beetle species per unit volume of fruit bodies in areas rich in dead wood. Jonsell et al. (2001) studied the effect of host size, succession stage, height above the ground, and exposure to the sun on insect species compositions and community structure.

The increasingly important role of dead-wood-associated, or saproxylic (Speight 1989) organisms in biological conservation (Jonsson et al. 2001) and the improved informational flow through the internet are the likely reasons for the recent peak in research activity in this field. In the 1990s–2000s, at least 70 studies on saproxylic, including fungivorous, beetles and their fungal hosts were carried out in Europe in Denmark (Jørum 2002), in Estonia (Süda & Nagirniy 2002), and in Finland (Kaila 1993; Kaila et al. 1994, 1997; Siitonen 1994; Siitonen et al. 1996, 2001; Komonen 2001; Yakovlev et al. 2001; Komonen 2003b, 2003c; Komonen et al. 2003, 2004; Schigel et al. 2004, 2006; Komonen and Kouki 2005; Schigel and Toresson 2005; Schigel 2007, 2008, 2011a). Selonen et al. (2005) explore changes in species diversity of Finnish fungi and beetles caused by anthropogenic disturbance.

Fungus–beetle interactions became a popular study topic in Germany (Möller 2005), in Hungary (Bratek 1992), in Lithuania (Rimšaitė 2000), in Poland (Lik 2005; Lik & Barczak 2005), in Russia (Yakovlev 1995), in Slovakia (Franc 2001), in the UK (Orledge & Smith 1999; Guevara et al. 2000a–2000c; Alexander 2002), and in France (Freeman & Van Meer 2000; Emerit 2001; Artéro & Dodelin 2007; Bouget et al. 2007; Callot 2008; Callot & Reibnitz 2008; Ponel & Rose 2009; Rose 2010; Rose & Ponel 2010; Dodelin et al. 2011). In particular, Dodelin (2004, 2006a–2006c, 2007, 2011) provides detailed information on the individual beetle species and saproxylic communities in the French Alps.

Numerous fungus–insect interaction studies were carried out in Norway (Økland & Hågvar 1994; Økland 1995; Hågvar & Økland 1997; Fossli & Andersen 1998; Rukke & Midtgaard 1998; Andersen et al. 2000; Olberg & Andersen 2000; Rukke 2000b, 2002; Olberg et al. 2001; Sverdrup-Thygeson & Ims 2002) and in Sweden (Jonsell & Nordlander 1995, 2002, 2004; Jonsson et al. 1997, 2001, 2003a, 2003b; Sörensson 1997; Jonsell 1998; Jonsell et al. 1999, 2003; Jonsson and Jonsell 2003; Johansson et al. 2006). Thunes (1994), Thunes and Midtgaard (1998), Thunes et al. (2000) disclose beetles of Fomes, Fomitopsis, and Piptoporus in Norway and Jonsson and Nordlander (2006) of Fomitopsis in Sweden.

Books and meetings

Contemporary views on fungus–insect interactions are summarised in books and book chapters (Crowson 1981; Vega & Blackwell 2005; Lundgren 2009b). Beetle fungivory was an important topic of the international symposia that took place in 1980s in the USA (Wheeler & Blackwell 1984) and in the UK (Wilding et al. 1989). These edited volumes have become canonical sources of information for scholars.

The latest international symposia on fungus–invertebrate interactions, both covering also beetle fungivory, took place in 2010 (Ecological role of hyphal structures in interactions between fungi and other organisms, IX International Mycological Congress, Edinburgh, UK) and in 2011 (Insect–fungus interactions, XVI Congress of European Mycologists, Halkidiki, Greece). Selected proceedings of these two meetings were included in volume 3:1 of Mycology: an International Journal of Fungal Biology in 2012.

Summary and future prospects

Beetle–sporocarp interactions are attractive study systems due to their resource patchiness and temporal unpredictability. However, to the best of my knowledge, only a few research groups and individual experts, working at the University of Arizona, the Florida State University (USA), the University of Bath and Cardiff University (UK), Landcare Research (New Zealand), the Swedish University of Agricultural Sciences, the Moscow State University (Russia), and the University of Helsinki (Finland), are currently focused on beetle fungivory, to name a few research hotspots.

Within the time span of an average research project, the choices in studying the ecology of fungivorous insects are either to select a few model species and high numbers of samples and replicates (the strategy employed by most of the latest references in this review), or to aim at documenting species diversity and food web structure (Schigel 2011b). Even for a common polypore species, a sample size of some dozens of fruiting bodies would be needed to detect most of the Coleoptera species. Thunes et al. (2000) and Komonen (2003c) demonstrate species accumulation curves for the fungus–beetle systems.

The state of the field is somewhat paradoxical: the natural history style studies and reports are difficult to publish because funding for natural history projects is declining, and in many countries the species-specific expert knowledge is migrating from academia to mycological and entomological professional and amateur societies. Mathematical ecology and molecular biology research is commonly based on a single or a few model species systems. Presently and in the future, fungus–beetle interaction research may face the Arabidopsis-effect – a few model species are studied deeply, but the rest of diversity is practically not studied at all, for the reason that there are not enough experts and not enough training to secure the inflow of new students and identification of the research materials. DNA barcoding and molecular identification are freezing the species expertise at its present state and thus make it broadly and electronically available. However, the dynamism of taxonomy and gaps in the coverage and quality of the reference libraries of sequences call for the renaissance of natural history as a part of new molecular and mathematical biology. Dormant, yet invaluable ecological data from student works (Ollila 2005; Seitzman 2007; Kochetova 2008) and personal datasets need to be electronically published. For experiments and statistical analyses of communities to include tens of species of fungi and of fungivorous beetles, their associations need to be discovered and described.

The number of insect species associated with fungi in the UK was estimated by Paviour-Smith (1960a) as 600 species. The number of beetle species associated with polypores may reach 250–300 species in Finland (Schigel 2009). Similar figures are observed in the Moscow region, Russia: 261 beetle species, linked with 61 species of polypores (Nikitsky & Schigel 2004). Ehnström (2001) assumes that the numbers of insect species dependent on lignicolous fungi is underestimated. Some 300–400 species of polyporicolous beetles may be expected to be found in European boreal forests. The main methods of beetle fungivory research have been field collections and laboratory rearing, with more than 40 publications based on each approach. Less popular methods are trapping, field experiments, and lab experiments (Schigel 2009).

Even though taxonomies of both fungi and beetles are relatively well-developed, the interactions and life histories of individual species remain insufficiently studied, especially for threatened species. Most of the research of beetle fungivory has been based on the species assemblages of basidiomycetes with large fruit bodies (polypores, agaricoids, and boletes) and their beetles. The associations of Coleoptera with ascomycetes (Lawrence 1977) and other, e.g. coral (Leschen & Carlton 1996), minute (Hoebeke et al. 1987; Stribling & Seymour 1988), and especially microscopic fungi are waiting to be studied further. On the one hand, species and geographic coverage of the fungus–insect studies needs to be expanded, since most of the fungivory publications focus on the widespread and conspicuous taxa collected around campuses and biological stations, such as Fomes fomentarius and Fomitopsis pinicola with at least 29 and 23 studies respectively (Schigel 2009). On the other hand, more studies are needed to explore ecological processes and factors that influence fungus–insect systems (Hanski 1989), such as abiotic and biotic factors (Heard 1998), parasitism (Hilszczajski et al. 2005; Yorozuya 2006), predation (Ashe 1990), competition (Yamashita et al. 2007a), subsocial behaviour (Ashe 1986a; Leschen 1994b), and acoustic communication (Gilbert & Arrow 1924).

Species communities of fungivorous beetles inhabit the compact but structured fruit bodies, and share them with other arthropods (Takahashi et al. 2005), such as Diptera (Jakovlev 1994; Wertheim et al. 2000; Jakovlev et al. 2006; Yamashita et al. 2007b) and Lepidoptera, but also Collembola and mites (Makarova 2004). The role of beetles as vectors of fungi could be studied by examining spores in guts (Dodelin et al. 2005) and surfaces of beetles, using microscopy, isolation and culturing, and high-throughput sequencing methods. Mechanisms of host selection can be elucidated by designing field attraction and lab choice experiments. Spatial and temporal aspects of beetle fungivory are among the least studied topics, which include fungal growth and decomposition vs. succession of beetles, and the role of fruit body architecture in the co-existence and competition of fungivorous Coleoptera.

Acknowledgements

Many thanks are due to the organisers and chairs of the symposium “Ecological role of hyphal structures in interactions between fungi and other organisms” and the IX International Mycological Congress, Edinburgh, UK, in particular to Prof. Akira Suzuki, Prof. Xingzhong Liu, as well as to organizers of XVI Congress of European Mycologists, Halkidiki, Greece, especially to Prof. Stephanos Diamandis. Special thanks to the participants and speakers of the Insect-Fungus Interactions symposium during this congress: Lynne Boddy, Bryn Dentinger, Mary Jane Epps, Jevgeni Jakovlev, Seong Hwan Kim, Olga Kochetova, Mervi Laaksonen, Teresa Lino-Neto, Beatrice Senn-Irlet, Ximena Silva, Ellen Suurmeyer, Teresa Veselka, and their co-authors for sharing the interests and the great days together. This work was supported by ERC Starting Grant no. 205905 (PI Otso Ovaskainen), and the University of Helsinki provided travel support for attending the Congresses. I am grateful to Tuomo Niemelä for comments on an earlier version of the manuscript, to Phil Harrison and Eliezer Gurarie for language editing, and to Mary Jane Epps and Benoit Dodelin for bibliographic discoveries.