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Article Assemblages on Sporocarps on Dead : An Observation Aided by Squirrels

Yu Fukasawa

Graduate School of Agricultural Science, Tohoku University, 232-3 Yomogida, Naruko, Osaki, Miyagi 989-6711, Japan; [email protected]; Tel.: +81-229-847-397; Fax: +81-229-846-490

Abstract: Dead wood is an important habitat for both fungi and , two enormously diverse groups that contribute to forest . Unlike the myriad of studies on – rela- tionships, insect communities on ascomycete sporocarps are less explored, particularly for those in hidden habitats such as underneath . Here, I present my observations of insect dynamics on Biscogniauxia spp. on oak dead wood from the early anamorphic stage to matured teleomorph stage, aided by the debarking behaviour of squirrels probably targeting on these fungi. In total, 38 insect taxa were observed on Biscogniauxia spp. from March to November. The com- munity composition was significantly correlated with the presence/absence of Biscogniauxia spp. Additionally, Librodor (Glischrochilus) ipsoides, Laemophloeus submonilis, and Neuroctenus castaneus were frequently recorded and closely associated with Biscogniauxia spp. along its change from anamorph to teleomorph. L. submonilis was positively associated with both the anamorph and teleomorph stages. L. ipsoides and N. castaneus were positively associated with only the teleomorph but not with the anamorph stage. N. castaneus reproduced and was found on Biscogniauxia spp. from June to November. These results suggest that sporocarps of Biscogniauxia spp. are important to these insect   taxa, depending on their developmental stage.

Citation: Fukasawa, Y. Invertebrate Keywords: fungivory; insect–fungus association; Sciurus lis; Quercus serrata; xylariaceous ascomycetes Assemblages on Biscogniauxia Sporocarps on Oak Dead Wood: An Observation Aided by Squirrels. Forests 2021, 12, 1124. https:// doi.org/10.3390/f12081124 1. Introduction Dead wood is an essential component of biodiversity in forest ecosystems [1,2]. Fungi, Academic Editor: Simon Curling in particular, is a major group of saproxylic communities; they have a large impact on saproxylic communities due to their unique wood decay abilities [3], and their fruit bodies Received: 24 July 2021 and spores are important to the diet of a variety of , including [4], Accepted: 20 August 2021 [5], and [6,7]. A better understanding of the relationships between Published: 22 August 2021 fungi and saproxylic communities is critical to clarifying the mechanisms that maintain biodiversity in forest ecosystems. Publisher’s Note: MDPI stays neutral In terms of their diversity and function, insects are another major group present within with regard to jurisdictional claims in saproxylic communities [1]. Insects have intimate relationships with fungi as fungivores, published maps and institutional affil- vectors of fungal propagules, and foragers of wood decomposed by fungi [8]. Numer- iations. ous studies have investigated the insect communities present on fungal fruit bodies, the majority of which are basidiomycetes [5,9,10]. Host specificity [11–14], the evolution of host use [15], and spore dispersal [16–20] have been intensively studied for a variety of fungus–insect relationships. Furthermore, topics in general (e.g., coexisting pat- Copyright: © 2021 by the author. terns on patchy resources [21,22]) and applied ecology (e.g., effects of forest management Licensee MDPI, Basel, Switzerland. on ecological communities [23,24]) have also been investigated using the insect–basidiocarp This article is an open access article system. However, studies on the relationships between insect communities on ascomycete distributed under the terms and fruit bodies, a sister taxon of basidiomycetes which also produces macroscopic fruit bodies, conditions of the Creative Commons are quite limited, with examples of symbiotic associations in ambrosia [25], wood- Attribution (CC BY) license (https:// wasps [26], and fungus-growing [27] and insect , such as in the genera creativecommons.org/licenses/by/ Beauveria [28], Metarhizium [29], and Ophiocordyceps [30]. 4.0/).

Forests 2021, 12, 1124. https://doi.org/10.3390/f12081124 https://www.mdpi.com/journal/forests Forests 2021, 12, 1124 2 of 10

Quercus serrata is a deciduous oak that dominates low-elevation rural forests through- out Japan. In recent decades, a serious dieback of Q. serrata ( disease) resulted in huge amount of dead wood [31,32]. Therefore, evaluations of the biotic communities associated with Q. serrata dead wood is necessary to understand and predict biodiversity in areas affected by oak wilt disease. The symbiotic association between a pathogenic fungus, Raffaerea quercivora, and ambrosia beetles, Platypus querucivorus, which carry the propagules of the fungus in their mycangia, is well studied [33,34]. In addition, since Q. serrata logs are traditionally used for cultivating shiitake mushrooms (Lentinula edodes), several ascomycete that negatively affect the yield of shiitake mushrooms are known to occur on Q. serrata bed-logs [35]. The most famous ascomycete species is in the (including species formerly denoted as Hypocrea), which is an antago- nistic and/or mycoparasitic taxon and causes serious damage to shiitake cultivation [36]. Trichoderma spp. has an intimate relationship with gall midge belonging to the genus Camptomyia on shiitake bed-logs [37]. Despite recent advances in the studies of microscopic and pathogenic ascomycetes associated with insects, relationships between insects and other taxa in macroscopic ascomycetes in genera such as Biscogniauxia, , Diatrype, Graphostroma, and , which fruit on Q. serrata dead wood, are largely unknown. To investigate successive changes of fungal and insect communities and their inter- actions during of Q. serrata dead wood, I started a multi-year survey of 32 experimentally cut logs of Q. serrata in August 2015. In March 2016, I observed that a squirrel or squirrels frequently visited and intensively debarked the logs, where colonies of anamorphic ascomycetes were found to appear on the sapwood. Subsequently, a variety of insects were found on the ascomycetes throughout their changes from the anamorph to the teleomorph stage. In the present study, I describe the insect assemblages that were observed on the Q. serrata logs and their relationships with the different sexual stages of ascomycetes during a growing season.

2. Materials and Methods 2.1. Experimental Setup The present study was conducted in a secondary forest dominated by Q. serrata and Pinus densiflora in Kami town, Miyagi, Japan (38◦37.2 N, 140◦48.6 E). In 2016, the mean an- nual temperature at the nearest meteorological station at Kawatabi (38◦44.60 N, 140◦45.6 E) was 11.6 ◦C (3.2 ◦C in February to 28.7 ◦C in August), and the annual precipitation was 1537.5 mm. Snow covers the ground from November to March (Japan Meteorological Agency, available online: https://www.jma.go.jp/jma/indexe.html (accessed on 21 Au- gust 2021)). In August 2015, two Q. serrata were felled and cut into 32 logs with a length of 1 m each (diameter 3.4–24.5 cm). The logs were laid on the ground approximately 1 m from each other. I began observations of the logs’ surfaces (top and bottom) in March 2016, when the ground was still covered with snow, but the tops of the logs were visible. On 10 March 2016, at 6:30 a.m., I observed that a squirrel (Sciurus lis) approached the logs and tore off the bark using its teeth. I found Geniculosporium type anamorph of ascomycete on the sapwood surface where the bark had been removed by the squirrel (Figure1a). The surface of the anamorph was scratched overall (Figure1a,b). I found 76 portions of debarking by the squirrel on 15 out of the 32 logs (in 1–10 portions per log). The frequency of the presence of anamorphs on the debarked portion was 100%. The observations continued once per week until the end of November 2016, except for April and May. The frequency of squirrel debarking increased to over 50% (19/32 logs) in July 2016. From March to July, the anamorph layers gradually peeled off and teleomorphs appeared (Figure1c,d), which were identified as Biscogniauxia maritima and Biscogniauxia plana by Dr. Shuhei Takemoto from the University of Tokyo. ForestsForests 20212021, ,1212, ,x 1124 FOR PEER REVIEW 3 3of of 10 10

Figure 1. (a) Surface of a Quercus serrata log recently debarked by a squirrel. Powdery ascomycete Figure 1. (a) Surface of a Quercus serrata log recently debarked by a squirrel. Powdery ascomycete anamorphanamorph appears appears at at the the centre centre of ofthe the debarked debarked portion portion where where numerous numerous scratch scratch scars scars can be can ob- be served,observed, March March 2016. 2016. (b) Zoomed (b) Zoomed in picture in picture of the scratch of theed scratched anamorph anamorph surface, March surface, 2016. March (c) Grad- 2016. ual(c) peeling Gradual of peeling the anamorph of the anamorph surface (brown surface port (brownion) portion)and appearance and appearance of the teleomorph of the teleomorph surface (greysurface portion), (grey portion),June 2016. June (d)2016. Zoomed (d) Zoomedin picture in of picture teleomorph, of teleomorph, which was which identified was identified as Biscog- as niauxiaBiscogniauxia maritima maritima and Biscogniauxiaand Biscogniauxia plana by plana Dr. byShuhei Dr. Shuhei Takemoto Takemoto from the from University the University of Tokyo, of Tokyo, July 2016.July 2016.Scale Scalebars: 5 bars: mm. 5 mm.

2.2.2.2. Data Data Collection Collection Debarked,Debarked, anamorph, anamorph, and and teleomorph teleomorph areas areas were were measured measured every every month month (except (except for for AprilApril and and May) May) by by placing placing 1 1 cm cm grid grid squares squares on on the the log log surface surface and and counting counting the the number number ofof grid grid squares squares that that had had debarkation, debarkation, anamorphs, anamorphs, and and teleomorphs. teleomorphs. InsectsInsects that that were were observed observed on on the the log log surface surface were were recorded recorded every every week week (except (except for for AprilApril and and May) May) as as binary binary data data (presence/absenc (presence/absencee on each on each log). log).Insects Insects were wereidentified identified with referencewith reference to the to keys the keysand andnomenclature nomenclature of Ku ofrosawa Kurosawa et al. et al.[38], [38 Ueno], Ueno et etal. al. [39], [39], and and HayashiHayashi et et al. al. [40] [40] for Coleoptera;Coleoptera; IshikawaIshikawa et et al. al. [41 [41]] for for ; Hemiptera; and and Terayama Terayama et al. et [42al.] [42]for Hymenopterafor (ants). (ants). Identification Identification to the to species the species level waslevel difficult, was difficult, so several so several species specieswere identified were identified at genus, at genus, , family, and order and level.order Taxalevel. thatTaxa occurred that occurred on ≥20 on logs ≥20 werelogs wererecorded recorded as dominant as dominant taxa. taxa. 2.3. Data Analysis 2.3. Data Analysis All statistical analyses were conducted using R ver. 4.0.5 [43]. A generalised linear All statistical analyses were conducted using R ver. 4.0.5 [43]. A generalised linear model (GLM) was applied to explain the species richness of invertebrates. The diameter of model (GLM) was applied to explain the species richness of invertebrates. The diameter of the logs, position (top/bottom) on the logs, and anamorph and teleomorph areas on the the logs, position (top/bottom) on the logs, and anamorph and teleomorph areas on the log log surface were set as explanatory variables. A binomial distribution error was assumed, surfaceand alogit were link set functionas explanatory was used. variables. The log-transformed A binomial distribution surface area error of was the logsassumed, was set and as aan logit offset link term. function was used. The log-transformed surface area of the logs was set as an offset Theterm. relationship between invertebrate community composition and environmental factorsThe was relationship visualised between using non-metric invertebrate multi-dimensional community composition scaling (NMDS) and environmental with the vegan factorspackage was [44 visualised]. Similarities using of thenon-metric invertebrate multi-dimensional communities across scaling the (NMDS) logs were with calculated the ve- ganusing package the Raup–Crick [44]. Similarities similarity of the index invertebrate (vegdist command),communities and across this the matrix logs waswere used calcu- to lateddevelop using the the NMDS Raup–Crick ordination similarity plot (metaMDS index (vegdistcommand). command), The significance and this matrix of the was difference used toin develop community the NMDS composition ordination between plot the(metaMDS top and command). bottom positions The significance of the logs of was the deter- dif- ferencemined usingin community permutation composition multivariate between analysis the top of variance and bottom [45] withpositions 10,000 of permutationsthe logs was determined(adonis command). using permutation In addition, multivariate community analysis variance of between variance samples [45] with (calculated 10,000 permu- using tationsthe betadisper (adonis command)command). wasIn addition, compared community between thevariance top and between bottom samples positions (calculated using an

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using the betadisper command) was compared between the top and bottom positions using an analysis of variance (anova command). Finally, the significance of the effects of the en- vironmental variables on the invertebrate communities was determined using the envfit command; sampling month, diameter, anamorph percentage, and teleomorph percentage were set as environmental variables. A set of GLMs were applied to explain the occurrence of the three dominant inverte- brate species. The environmental variables that were detected to be significant using en- Forests 2021, 12, 1124 vfit (diameter, anamorph percentage, and teleomorph4 of percentage) 10 were set as explanatory variables. Binomial distribution errors were assumed. Logit link functions were used. analysis of variance (anova command). Finally, the significance of the effects of the en- vironmental variables on the invertebrate communities was determined using the envfit 3. Resultscommand; sampling month, diameter, anamorph percentage, and teleomorph percentage were set as environmental variables. TheA set ofmean GLMs were percentage applied to explain of the debarked occurrence of thearea three per dominant log inverte- was 10% in March, increased slightly brate species. The environmental variables that were detected to be significant using envfit from(diameter, June anamorph to July, percentage, and remained and teleomorph constant percentage) were therea set as explanatoryfter (Figure 2a). The tops of the logs were debarkedvariables. Binomial more distribution than bottoms errors were assumed. of the Logit logs. link functionsThe anamorph were used. area occupied almost all parts of the3. debarked Results area in March but decreased to zero by the end of July (Figure 2b). In con- The mean percentage of debarked area per log was 10% in March, increased slightly trast,from the June toteleomorph July, and remained constantarea was thereafter seldom (Figure2a). observed The tops of the logsuntil were June but greatly increased in July debarked more than bottoms of the logs. The anamorph area occupied almost all parts andof theoccupied debarked area almost in March butall decreasedparts of to zero the by deb the endarked of July (Figurearea2 b).until In November (Figure 2c). contrast, the teleomorph area was seldom observed until June but greatly increased in July and occupied almost all parts of the debarked area until November (Figure2c).

Figure 2. Percentage area of debarked (a), anamorph (b), and teleomorph (c) of Bisogniauxia spp. on FigureQuercus 2. serrata Percentagelogs. Grey and whitearea bars of show debarked the top and bottom(a), anamorph sides of the logs, respectively.(b), and teleomorph (c) of Bisogniauxia spp. on QuercusIn total,serrata 38 taxa logs. of insects Grey were and recorded white (Table S1).bars Coleoptera show wasthe the top largest and group bottom sides of the logs, respectively. and consisted of 28 taxa, followed by 4 taxa of Hemiptera and 3 taxa of . Archaeognatha, Hymenoptera, and Psocodea included one taxon each. The GLM indicated In total, 38 taxa of insects were recorded (Table S1). Coleoptera was the largest group and consisted of 28 taxa, followed by 4 taxa of Hemiptera and 3 taxa of Lepidoptera. Ar- chaeognatha, Hymenoptera, and Psocodea included one taxon each. The GLM indicated that insect diversity was negatively correlated with log diameter and positively correlated with teleomorph area (Table 1). The bottom sides of the logs had lower insect richness than the top sides.

Table 1. GLM results showing associations with insect species richness and log variables. Variable Estimate Diameter –0.03 ** Position (bottom) –0.34 ** Teleomorph 0.02 *

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that insect diversity was negatively correlated with log diameter and positively correlated with teleomorph area (Table1). The bottom sides of the logs had lower insect richness than Forests 2021, 12, x FOR PEER REVIEWthe top sides. 5 of 10 The observed insect communities were significantly correlated with sampling month, log diameter, and anamorph area (Figure3); however, the position on the logs (top/bottom) was not correlated with the insect communities. Among the recorded insect taxa, Librodor (Glischrochilus) ipsoidesAnamorph, Laemophloeus submonilis, and Neuroctenus castaneus– were observed on ≥20 logs and wered.f. thus (null) assigned as dominant taxa; these species 444 were not recorded in March but were frequentlyNull deviance recorded in June and July, particularly 814.12 on the top sides of the logs (Figure4). Althoughd.f. (residual)L. submonilis and L. ipsoides disappeared 441 by August and September, respectively,ResidualN. deviance castaneus remained until November. Additionally, 770.35 N. castaneus reproduced on the surfaceAIC of Biscogniauxia teleomorphs (Figure4c). The1517.1 GLM based on the data from July suggested that the occurrence of L. submonilis was positively associated with *the p

Figure 3. NMDS results showing the relationships between environmental variables and insect Figure 3. NMDS results showing the relationships between environmental variables and insect com- community dissimilarity on Quercus serrata logs. munity dissimilarity on Quercus serrata logs.

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Figure 4. Frequencies of Laemophloeus submonilis (a), Librodor ipsoides (b), and Neuroctenus castaneus (c) Figure 4. Frequencies of Laemophloeus submonilis (a), Librodor ipsoides (b), and Neuroctenus castaneus on Quercus serrata logs. Grey and white bars show the top and bottom sides of the logs, respectively. (c) on Quercus serrata logs. Grey and white bars show the top and bottom sides of the logs, respec- tively. Table 2. GLM results showing estimated coefficients between occurrences of the three dominant Tableinsect 2. species GLM andresults log showing variables. estimated coefficients between occurrences of the three dominant insect species and log variables. Variable Laemophloeus Librodor Neuroctenus VariableDiameter Laemophloeus 0.18 Librodor 0.32 * Neuroctenus 0.20 ** AnamorphDiameter area 0.97 0.18 * 0.32 1.17 * 0.20 –** AnamorphTeleomorph area 0.080.97 ** 1.17 0.24 * 0.51 – ** d.f. (null) 63 63 63 TeleomorphNull deviance area 0.0851.98 * 0.24 71.98 * 0.51 86.46 ** d.f.d.f. (residual) (null) 60 63 63 60 63 61 ResidualNull deviance deviance 24.4751.98 71.98 22.51 86.46 41.33 d.f. (residual)AIC 32.47 60 30.5160 6147.33 * p

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iomycetes) sporocarps on 18 April 2021 in Japan (the personal observation of Yu Fukasawa). Although it is unclear whether squirrel fungivore of xylariaceous ascomycetes is common, I found the same type of debarking on freshly felled oak logs approximately 8 km away from the study site in 2018 and again at the study site in February 2021 (Figure S1, the personal observation of Yu Fukasawa). Currah et al. [6] investigated the stomach contents of squirrels and flying squirrels in North America and found fragments of and Diatripaceae . However, again, basidiomycetes sporcarps constituted the majority of their gut contents. Xylariaceous ascomycetes may constitute a supplemental diet during the early spring when other fresh food sources are unavailable. Fungal spores contain a high percentage of nitrogen, but their digestibility is very low in squirrels [50]. Among the recorded insect taxa, almost all taxa except for Niponius osorioceps and Pheidole fervida belonged to families that include species reported to be fungivores [1,51,52]. More specifically, species belonging to , Cucujidae, Nitidulidae, Anthribidae, Monotomidae, Silvanidae, Corylophidae, and Biphyllidae are known as ascomycete eaters [51,53]. I even observed Lepidopteran larvae of unknown identity the surface of Biscogniauxia stromata. Tineoidea are known to have fungivorous habits, although they feed on basidiomycotan wood decay fungi [22,54]. Powell [55] reported that Lepidopteran species belonging to feed on the stromata of Hypoxylon occidentale (Xylariaceae, ). As shown through NMDS (Figure3), the presence of Biscogni- auxia spp. may strongly attract fungivorous insects and affect their community structure. Lee et al. [56] reported that stem canker caused by truncatum (Xylariaceae) on oak stem significantly increases invertebrate diversity in Korea, irrespective of the presence or absence of sap flow. In the present study, I identified three dominant insect species: Librodor ipsoides (Ni- tidulidae, Coleoptera); L. submonilis (Cucujidae, Coleoptera); and N. castaneus (Aradidae, Hemiptera)—they each had significant relationships with the occurrence of Bisocogni- auxia spp. (Table2). Although the gut contents of these species were not surveyed in the present study, it is highly likely that these three species were all fungivores and had intimate associations with Biscogniauxia spp. during their life cycle. Nitidulidae is a well- known fungivorous Coleoptera occurring in not only fungal fruit bodies but also in the sap flows of damaged trees, fermenting fruits, and pathological plant tissues—-such species probably have or pathogenic fungi as a normal and essential part of their diet [51]. Specifically, species in the genus Librodor are known as ‘sap beetles’ that forage and breed in fermented sap flow [57](referred as a genus Glischrochilus). L. ipsoides has also been found in the sap on Quercus acutissima trees in Japan, although its abundance is quite low compared with that of other sap beetles [58]. On the other hand, L. ipsoides has been found in the fruit bodies of a basidiomycete volvatus on Pinus densiflora in Korea [59], but it was not found in C. volvatus in Japan [22]. In the present study, I newly found L. ipsoides on Biscogniauxia spp. fruit bodies at a relatively high frequency (>30%; Figure4), indicating that the stromata and/or conidia of Biscogniauxia spp. are an important habitat of this species. Lawrence [60] reported observations of Prometopia sexmaculata (Nitidulidae) breeding in the stromata of Hypoxylon (Xylariaceae) on oak. Cucujidae are also known as Coleopteran ascomycete eaters. Species in the genus Laemophloeus have been frequently reported in association with ascomata, such as Daldinia, Tubercularia, Hypoxylon, and Biscog- niauxia (=Nummularia)[51]. Therefore, it is not surprising that I found L. submonilis on Biscogniauxia spp. (B. maritima and B. plana) in the present study, even though it is a newly found association in Japanese species. In Aradidae (Hemiptera), most species are fungivores [53,61] that feed on fungal hyphae, using their piercing-sucking mouthparts to suck the cell contents, and have adapted gut systems [62], but little is known about the fungal host association of most species, particularly for ascomycetes [53]. Most of the Aradidae species occur preferentially on dead wood during the early stages of decay, probably due to the presence of their dietary fungal species [53]. As such, outbreaks of some Aradidae species are closely associated with large dieback events, such as forest fires and pests. lugubris can appear immediately Forests 2021, 12, 1124 8 of 10

after forest fires, when they feed on Daldinia loculata (Lév.) Sacc. (Xylariaceae), a known fire-related ascomycete in boreal forests [63]. Similarly, large-scale wind throws and bark outbreaks in a Norway spruce forest in the Bavarian Forest in Germany, where dead spruce snags were intensively colonised by a basidiomycete Fomitopsis pinicola [64], provided a suitable habitat for Aradus obtectus [53]. In Japan, Q. serrata trees have recently suffered from oak wilt disease [65]. However, relationships between oak wilt disease and the occurrence of Biscogniauxia spp. are unclear. Fukasawa et al. [66] compared latent fungal communities within Q. serrata trunks in stands with or without the prevalence of oak wilt disease and did not detect Biscogniauxia spp. Parental care has been observed in Aradidae, during which the male safeguards the egg mass for several weeks, and parental care may be extended to the nymphal stage [53]. In the present study, I also observed that adults appeared to guard the mass of nymphs (Figure4). In addition, I observed many nymphs spraying (probably some chemicals) simultaneously from their tail when they were shaded by my hands. To summarise, I observed the insect communities on saproxylic Biscogniauxia spp. on oak dead wood during the transition from the anamorphic to teleomorphic stages; this was aided by debarking by squirrels. The presence of Biscogniauxia spp. significantly affected the insect communities. More specifically, the population dynamics of two Coleoptera and one Hemiptera dominant species revealed that Biscogniauxia spp. represents an important habitat in their life cycles.

Supplementary Materials: The following are available online at https://www.mdpi.com/article/ 10.3390/f12081124/s1. Figure S1: Another evidence of debarking of Quercus serrata log by squirrel targeting on ascomycete anamorph, Table S1: Insect taxa recorded in the present study. Funding: This research received no external funding. Acknowledgments: The author is grateful to Shuhei Takemoto for identification of Biscogniauxia spp. I also thank Chisato Kobayashi for letting me use our garden for my experiment. Conflicts of Interest: The author declares that they have no conflict of interest.

References 1. Stokland, J.N.; Siitonen, J.; Jonsson, B.G. Biodiversity in Dead Wood; Cambridge University Press: Cambridge, UK, 2012. 2. Seibold, S.; Bässler, C.; Brandl, R.; Gossner, M.M.; Thorn, S.; Ulyshen, M.D.; Müller, J. Experimental studies of dead-wood biodiversity—A review identifying global gaps in knowledge. Biol. Conserv. 2015, 191, 139–149. [CrossRef] 3. Rayner, A.D.M.; Boddy, L. Fungal Decomposition of Wood: Its Biology and Ecology; John Wiley & Sons: Chichester, UK, 1988. 4. Fukasawa, Y.; Hyodo, F.; Kawakami, S. Foraging association between myxomycetes and fungal communities on coarse woody debris. Soil Biol. Biochem. 2018, 121, 95–102. [CrossRef] 5. Hanski, I. Fungivory: Fungi, insects and Ecology. In Insect–Fungus Interactions; Wilding, N., Collins, N.M., Hammond, P.M., Webber, J.F., Eds.; Academic Press: London, UK, 1989. 6. Currah, R.S.; Smreciu, E.A.; Lehesvirta, T.; Niemi, M.; Larsen, K.W. Fungi in the winter diets of northern flying squirrels and red squirrels in the boreal mixedwood forest of northern Alberta. Can. J. Bot. 2000, 78, 1514–1520. 7. Elliott, T.F.; Elliott, K. consumption and dispersal of the Nothofagaceae associated ascomycete . Austral. Ecol. 2019, 44, 747–751. [CrossRef] 8. Schigel, D.S. Fungivory and host associations of Coleoptera: A bibliography and review of research approaches. Mycology 2012, 3, 258–272. [CrossRef] 9. Buxton, C.M.G. British Diptera associated with fungi. III. of all families reared from about 150 species of fungi. Entomol. Mon. Mag. 1960, 96, 61–94. 10. Elton, C.S. The Pattern of Communities; Methuen and Co.: Slingsby, UK, 1966. 11. Jonsell, M.; Nordlander, G. Host selection patterns in insects breeding in bracket fungi. Ecol. Entomol. 2004, 29, 697–705. [CrossRef] 12. Yamashita, S.; Hijii, N. The role of fungal taxa and developmental stage of mushrooms in determining the composition of the mycophagous insect community in a Japanese forest. Eur. J. Entomol. 2007, 104, 225–233. [CrossRef] 13. Nakamori, T.; Suzuki, A. Surface properties of the mushroom Strobilurus ohshimae result in food differentiation by collembolan species. Eur. J. Soil Biol 2008, 44, 478–482. [CrossRef] 14. Yamashita, S.; Ando, K.; Hoshina, H.; Ito, N.; Katayama, Y.; Kawanabe, M.; Maruyama, M.; Itioka, T. structure of the fungivorous insect community on bracket fungi in a Bornean tropical rain forest. Ecol. Entomol. 2015, 40, 390–400. [CrossRef] 15. Kobayashi, T.; Sota, T. Evolution of host use in fungivorous ciid beetles (Coleoptera: Ciidae): Molecular phylogeny focusing on Japanese taxa. Mol. Phylogen Evol. 2021, 162, 107197. [CrossRef][PubMed] Forests 2021, 12, 1124 9 of 10

16. Tuno, N. Insect feeding on spores of a bracked fungus, Elfvingia applanata (Pers.) Karst. (Ganodermataceae, Aphyllophorales). Ecol. Res. 1999, 14, 97–103. [CrossRef] 17. Kadowaki, K.; Keschen, R.A.B.; Beggs, J.R. No evidence for a Ganoderma spore dispersal mutualism in an obligate spore-feeding beetle Zearagytodes maculifer. Fung Biol. 2011, 115, 768–774. [CrossRef][PubMed] 18. Persson, Y.; Ihrmark, K.; Stenlid, J. Do bark beetles facilitate the establishment of rot fungi in Norway spruce? Fung. Ecol. 2011, 4, 262–269. [CrossRef] 19. Kitabayashi, K.; Tuno, N. Soil burrowing Muscina angustifrons (Diptera: ) larvae excrete spores capable of forming mycorrhizae underground. Mycoscience 2018, 59, 252–258. [CrossRef] 20. Seibold, S.; Müller, J.; Baldrian, P.; Cadotte, M.W.; Stursová, M.; Biedermann, P.H.W.; Krah, F.S.; Bässler, C. Fungi associated with beetles dispersing from dead wood—Let’s take the beetle bus! Fung. Ecol. 2019, 39, 100–108. [CrossRef] 21. Takahashi, K.H.; Tuno, N.; Kagaya, T. The relative importance of spatial aggregation and resource partitioning on the coexistence of mycophagous insects. Oikos 2005, 109, 125–134. [CrossRef] 22. Kadowaki, K. Species coexistence patterns in a mycophagous insect community inhabiting the wood-decaying bracket fungus . Eur. J. Entomol. 2010, 107, 89–99. [CrossRef] 23. Komonen, A.; Penttila, R.; Lindgren, M.; Hanski, I. Forest fragmentation truncates a food chain based on an old-growth forest bracket fungus. Oikos 2000, 90, 119–126. [CrossRef] 24. Komonen, A.; Kouki, J. Occurrence and abundance of fungus-dwelling beetles (Ciidae) in boreal forests and clearcuts: Habitat associations at two spatial scales. Anim. Biodiv. Conserv. 2005, 28, 137–147. 25. Joseph, R.; Keyhani, N.O. Fungal mutualisms and pathosystems: Life and death in the mycangia. Appl. Microbiol. Biotechnol. 2021, 105, 3393–3410. [CrossRef] 26. Pažoutová, S.; Srutka, P.; Holusa, J.; Chudickova, M.; Kolarik, M. Diversity of xylariaceous symbionts in Xiphydria woodwasps: Role of vector and a host . Fung. Ecol. 2010, 3, 392–401. [CrossRef] 27. Visser, A.A.; Ros, V.I.D.; de Beer, Z.W.; Debets, A.J.M.; Hartog, E.; Kuyper, T.W.; Læssøe, T.; Slippers, B.; Aanen, D.K. Level of specificity of species associated with fungus-growing termites: A phylogenetic approach. Mol. Ecol. 2009, 18, 553–567. [CrossRef] 28. Xiao, G.; Ying, S.H.; Zheng, P.; Wang, Z.L.; Zhang, S.; Xie, X.Q.; Shang, Y.; St Leger, R.J.; Zhao, G.P.; Wang, C.; et al. Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci. Rep. 2012, 2, 483. [CrossRef][PubMed] 29. Stone, L.B.L.; Bidochka, M.J. The multifunctional lifestyles of Metarhizium: Evolution and applications. Appl. Microbiol. Biotechnol. 2020, 104, 9935–9945. [CrossRef][PubMed] 30. Nikoh, N.; Fukatsu, T. Interkingdom host jumping underground: Phylogenetic analysis of entomoparasitic fungi of the genus Cordyceps. Mol. Biol. Evol. 2000, 17, 629–638. [CrossRef][PubMed] 31. Watanabe, N.; Okada, T.; Tomaru, N.; Nishimura, N.; Nakagawa, M. Forest dynamics of stands damaged by Japanese oak wilt in the Kaisho forest, Aichi Prefecture. J. Jap. For. Soc. 2016, 98, 273–278. [CrossRef] 32. Nishikawa, S.; Kubo, M.; Ozaki, Y. Mass mortality due to the spread of oak wilt disease in a 19-ha secondary Quercus serrata forest within Sambe Forest at Shimane University. Bull Fac. Life Env. Sci. Shimane Univ. 2018, 23, 21–26. 33. Endoh, R.; Suzuki, M.; Okada, G.; Takeuchi, Y.; Futai, K. Fungus symbionts colonizing the galleries of the ambrosia beetle . Microb. Ecol. 2011, 62, 106–120. [CrossRef] 34. Masuya, H.; Manabe, R.; Ohkuma, M.; Endoh, R. Draft sequence of quercivora JCM 11526, a Japanese oak wilt associated with the Platypodid beetle, Platypus quecivorus. Genome Announc. 2016, 4, e00755-16. [CrossRef] 35. Kobayashi, T.; Oguro, M.; Akiba, M.; Taki, H.; Kitajima, H.; Ishihara, H. Mushroom yield of cultivated shiitake (Lentinula edodes) and fungal communities in logs. J. Res. 2020, 25, 269–275. [CrossRef] 36. Tokimoto, K.; Komatsu, M.; Fukumasa-Nakai, Y. Establishing the selection method for the Lentinula edodes strains resistant to Trichoderma spp. Proc. Jpn. Acad 1994, 70, 112–116. [CrossRef] 37. Kim, J.Y.; Kwon, H.W.; Yun, Y.H.; Kim, S.H. Identification and characterization of Trichoderma species damaging Shiitake mushroom bed-logs infested by Camptomyia pest. J. Microbiol Biotechnol 2016, 26, 909–917. [CrossRef][PubMed] 38. Kurosawa, Y.; Hisamatsu, S.; Sasaji, H. The coleoptera of Japan in color Vol.III; Hoikusha: Tokyo, Japan, 1998. (In Japanese) 39. Ueno, S.; Kurosawa, Y.; Sato, M. The coleoptera of Japan in color Vol.II; Hoikusha: Tokyo, Japan, 1999. (In Japanese) 40. Hayashi, M.; Morimoto, K.; Kimoto, S. The coleoptera of Japan in color Vol.IV; Hoikusha: Tokyo, Japan, 2002. (In Japanese) 41. Ishikawa, T.; Takai, M.; Yasunaga, T. A Field Guide to Japanese Bugs: Terrestrial Heteropterans; Zenkoku Noson Kyoiku Kyokai: Tokyo, Japan, 2012; Volume 3. (In Japanese) 42. Terayama, M.; Kubota, S.; Eguchi, K. Encyclopedia of Japanese Ants; Asakura Shoten: Tokyo, Japan, 2014. (In Japanese) 43. R Core Team. R: A Language and Environment for Statistical Computing; The R Foundation for Statistical Computing: Vienna, Austria, 2021. 44. Oksanen, J.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’Hara, R.B.; Simpson, G.L.; Solymos, P.; Stevens, M.H.H.; Szoecs, E.; et al. Vegan: Community Ecology Package; R Package Version 2.5-7; 2020. Available online: https://cran.r-project.org/ web/packages/vegan/index.html. 45. Anderson, M.J. A new method for non parametric multivariate analysis of variance. Austral Ecol. 2001, 26, 32–46. 46. Ulyshen, M.D. Saproxylic Insects: Diversity, Ecology and Conservation; Springer: Cham, Switzerland, 2019. 47. McKeever, S. The biology of the Golden-mantled ground squirrel, Citellus lateralis. Ecol. Monogr. 1964, 34, 383–401. [CrossRef] Forests 2021, 12, 1124 10 of 10

48. Maser, C.; Maser, Z. Interactions among squirrels, mycorrhizal fungi, and coniferous forests in Oregon. Great Basin Nat. 1988, 48, 358–369. 49. Stadler, M. Importance of secondary metabolites in the Xylariaceae as parameters for assessment of their , phylogeny, and functional biodiversity. Curr. Res. Environ. Appl. Mycol. 2011, 1, 75–133. [CrossRef] 50. Cork, S.J.; Kenagy, G.J. Nutritional value of hypogeous fungus for a forest-dwelling ground squirrel. Ecology 1989, 70, 577–586. [CrossRef] 51. Crowson, R.A. The associations of Coleoptera with Ascomycetes. In Fungus-Insect Relationships; Wheeler, Q., Blackwell, M., Eds.; Columbia University Press: New York, NY, USA, 1984; pp. 257–285. 52. Katanoda, I.; Sato, Y.; Morita, S.; Okubo, H. Adult emergence and oviposition preference of longipennis for Chinese Quercus acutissima. Kyushu J. Res. 2005, 58, 105–108. (In Japanese) 53. Gossner, M.M.; Damken, C. Diversity and ecology of saproxylic Hemiptera. In Saproxylic Insects: Diversity, Ecology and Conservation (Zoological Monographs 1); Ulyshen, M.D., Ed.; Springer: Cham, Switzerland, 2018. 54. Powell, J.A.; Mitter, C.; Farrell, B. Evolution of larval food preferences in Lepidoptera. In Lepidoptera, Moths and Butterflies Volume 1: Evolution, Systematics, and Biogeography; Kristensen, N.P., Ed.; de Gruyter: Berlin, Germany, 1998; pp. 403–422. 55. Powell, J.A. bistriatella: A which feeds in an ascomycete fungus (Lepidoptera: Pyralidae). J. N. Y. Entomol. Soc. 1967, 75, 190–194. 56. Lee, Y.-B.; An, S.J.; Park, C.G.; Kim, J.; Han, S.; Kwak, Y.-S. Oak tree canker disease supports diversity in a natural ecosystem. Plant Path. J. 2014, 30, 43–50. [CrossRef] 57. Jacobsen, R.M.; Birkemore, T.; Sverdrup-Thygeson, A. Priority effects of early successional insects influence late successional fungi in dead wood. Ecol. Evol. 2015, 5, 4896–4905. [CrossRef][PubMed] 58. Yoshimoto, J.; Kakutani, T.; Nishida, T. Influence of resource abundance on the structure of the insect community attracted to fermented tree sap. Ecol. Res. 2005, 20, 405–414. [CrossRef] 59. Park, M.S.; Fong, J.J.; Lee, H.; Shin, S.; Lee, S.; Lee, N.; Lim, Y.W. Determination of coleopteran insects associated with spore dispersal of Cryptoporus volvatus. J. Asia-Pac. Entomol 2014, 17, 647–651. [CrossRef] 60. Lawrence, J.F. Coleoptera associated with an Hypoxylon species (Ascomycetes: Xylariaceae) on oak. Coleopt. Bull. 1977, 31, 309–312. 61. Seibold, S.; Bässler, C.; Baldrian, P.; Thorn, S.; Müller, J.; Gossner, M.M. Wood resource and not fungi attract early-successional saproxylic species of Heteroptera—An experimental approach. Insent. Conserv. Divers. 2014, 7, 533–542. [CrossRef] 62. Nardi, J.B.; Bee, C.M.; Miller, L.A.; Taylor, S.J. Distinctive features of the alimentary canal of a fungus-feeding hemipteran, Mezira granulata (Heteroptera: Aradidae). Arthropod Struct. Dev. 2009, 38, 206–215. [CrossRef][PubMed] 63. Wikars, L.-O. The wood-decaying fungus Daldinia loculata (Xylariaceae) as an indicator of fire-dependent insects. Ecol. Bull. 2001, 49, 263–268. 64. Vogel, S.; Alvarez, B.; Bässler, C.; Müller, J.; Thorn, S. The red-belted bracket (Fomitopsis pinicola) colonizes spruce trees early after attack and persists. Fung. Ecol. 2017, 27, 182–188. [CrossRef] 65. FFPRI. Naragare Boujo No Shintenkai; Forestry and Forest Products Research Institute: Tsukuba, Japan, 2015; ISBN 978-4-905304-48-7. (In Japanese) 66. Fukasawa, Y.; Matsukura, K.; Stephan, J.; Makoto, K.; Suzuki, S.N.; Kominami, Y.; Takagi, M.; Tanaka, N.; Takemoto, S.; Kinuura, H.; et al. Patterns of community composition and diversity in latent fungi of living Quercus serrata trunks across a range of oak wilt prevalence and climate variables in Japan. Fung. Ecol. 2021, in press. [CrossRef]