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Invertebrate Assemblages on Biscogniauxia Sporocarps on Oak Dead Wood: an Observation Aided by Squirrels

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Invertebrate Assemblages on Biscogniauxia Sporocarps on Oak Dead Wood: an Observation Aided by Squirrels Article Invertebrate Assemblages on Biscogniauxia Sporocarps on Oak Dead Wood: 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 insects, two enormously diverse groups that contribute to forest biodiversity. Unlike the myriad of studies on fungus–insect rela- tionships, insect communities on ascomycete sporocarps are less explored, particularly for those in hidden habitats such as underneath bark. Here, I present my observations of insect community 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 organisms, including protozoa [4], Accepted: 20 August 2021 invertebrates [5], and vertebrates [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 ecology (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 beetles [25], wood- Attribution (CC BY) license (https:// wasps [26], and fungus-growing termites [27] and insect pathogens, 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 (oak wilt 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 species 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 genus Trichoderma (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, Daldinia, Diatrype, Graphostroma, and Hypoxylon, which fruit on Q. serrata dead wood, are largely unknown. To investigate successive changes of fungal and insect communities and their inter- actions during decomposition 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 trees 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.
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