First Report of Six Macrofungi from Daecheongdo and Socheongdo Islands, Korea

Abstract

Daecheongdo and Socheongdo Islands are located in the West Sea of Korea, 210 km away from land, and are military border areas very close to North Korea, making them difficult to access. Although the ecosystem of the islands is relatively well preserved due to the lack of accessibility, research on fungi of the regions is insufficient. Therefore, we aimed to investigate indigenous fungi in these geographically and geopolitically constrained regions. A survey of the indigenous fungal diversity of the islands was conducted in 2018. All specimens were identified at the species level based on morphological and molecular analyses. Among them, six macrofungi—namely, Agaricus menieri, Crepidotus praecipuus, Dichomitus squalens, Hortiboletus amygdalinus, Melanoleuca friesii, and Trametes lactinea—were not previously reported in Korea. Considering that the proportion of unrecorded species is high in the survey area and period as well as the number of samples collected, similar research on adjacent islands may be necessary.

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First Report of Six Macrofungi from Daecheongdo
and Socheongdo Islands, Korea
Minkyeong Kim, Jin Sung Lee, Jae Young Park & Changmu Kim
To cite this article: Minkyeong Kim, Jin Sung Lee, Jae Young Park & Changmu Kim (2021): First
Report of Six Macrofungi from Daecheongdo and Socheongdo Islands, Korea, Mycobiology, DOI:
10.1080/12298093.2021.1970957
To link to this article: https://doi.org/10.1080/12298093.2021.1970957
© 2021 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group on behalf of the Korean Society of
Mycology.
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RESEARCH ARTICLE
First Report of Six Macrofungi from Daecheongdo and Socheongdo
Islands, Korea
Minkyeong Kim
a
, Jin Sung Lee
b
, Jae Young Park
c
and Changmu Kim
d
a
Microorganism Resources Division, National Institute of Biological Resources, Incheon, Korea;
b
Yurim Mushrooms, Asan-si,
Chungnam, Korea;
c
Qmyco, Kwanak-gu, Seoul, Korea;
d
Biological and Genetic Resources Assessment, National Institute of
Biological Resources, Incheon, Korea
ABSTRACT
Daecheongdo and Socheongdo Islands are located in the West Sea of Korea, 210 km away
from land, and are military border areas very close to North Korea, making them difficult to
access. Although the ecosystem of the islands is relatively well preserved due to the lack of
accessibility, research on fungi of the regions is insufficient. Therefore, we aimed to investi-
gate indigenous fungi in these geographically and geopolitically constrained regions. A sur-
vey of the indigenous fungal diversity of the islands was conducted in 2018. All specimens
were identified at the species level based on morphological and molecular analyses. Among
them, six macrofungi—namely, Agaricus menieri, Crepidotus praecipuus, Dichomitus squalens,
Hortiboletus amygdalinus, Melanoleuca friesii, and Trametes lactinea—were not previously
reported in Korea. Considering that the proportion of unrecorded species is high in the sur-
vey area and period as well as the number of samples collected, similar research on adjacent
islands may be necessary.
ARTICLE HISTORY
Received 23 February 2021
Revised 23 July 2021
Accepted 17 August 2021
KEYWORDS
Daecheongdo; indigenous
species; macrofungal flora;
Socheongdo; unrecorded
species
1. Introduction
Daecheongdo and Socheongdo Islands are located at
37460–37500north latitude and 124400–124450
east longitude. Both islands belong to Daecheong-
myeon, Ongjin-gun, Incheon in South Korea,
located approximately 210 km northwest of the city
of Incheon on the South Korean mainland and
approximately 40 km southwest of the Ongjin
Peninsula in North Korea. The Daecheongdo and
Socheongdo Islands have winter minimum tempera-
tures that are 10 C warmer, with 400 mm lesser
precipitation annually, and 1.79 m/s higher wind
speeds than inland at similar latitudes [1]. Natural
vegetation in Daecheongdo and Socheongdo islands
was destroyed before and after the Korean War,
1950. Since the 1970s, there has been no artificial
afforestation, and secondary forests have been
formed naturally with Carpinus turczaninoxii and
Quercus sp. [2]. Pine trees (Pinus densiflora) are
widely distributed across these islands, but Carpinus
turczaninovii and Camellia japonica dominate high
elevations. The geological properties of these islands
are unique and have a simple hierarchical structure.
The coastal dune vegetation is relatively well pre-
served because these islands have fewer tourists than
other South Korean islands. Some floristic studies in
these areas were conducted by Choi and Lee [3] and
Yang et al. [4], but research on fungi has rarely
been conducted. Vascular plant diversity and fungal
diversity are closely related in that the higher diver-
sity of vascular plants creates niches and microhabi-
tats for fungi and the presence of many ecotones
[5–6]. Through re-identification of the collected
specimens, it has been confirmed that 398 species of
plants inhabit Daecheongdo island [7]. Despite the
relatively small area (12.75 km
2
), the variety of
inhabiting plant species can lead to the assumption
that the fungal species will also vary. To secure, pre-
serve, and manage the genetic biological resources
of higher fungi in Korea, a research project was car-
ried out on Daecheongdo and Socheongdo Islands
with the support of the National Institute of
Biological Resources (NIBR) of the Ministry of
Environment. Through this study, six unrecorded
fungal species in the Korean peninsula were discov-
ered from these islands.
2. Materials and methods
To fully characterize the distribution of fungi on
these islands, regular surveys were conducted
between July and September 2018. Each specimen
CONTACT Changmu Kim snubull@korea.kr
These authors contributed equally to this work.
ß2021 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group on behalf of the Korean Society of Mycology.
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/),
which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
MYCOBIOLOGY
https://doi.org/10.1080/12298093.2021.1970957

was photographed, and their location of collection,
habitat, host, substrate and fruiting characteristics
were recorded onsite. The specimens were dried at
50 C for several days and stored at the NIBR. The
specimens were initially identified based on their
macro- and microscopic features, according to pub-
lished descriptions [8–16]. The taxonomic classifica-
tion and nomenclature of the species were assigned
using the Index Fungorum database (http://www.
index-fungorum.org). Measurements and drawings
were made using a Nikon Eclipse 80i microscope
(Nikon, Tokyo, Japan). For molecular identification,
genomic DNA was extracted from dried samples
using the AccuPrep Genomic DNA Extraction Kit
(Bioneer, Daejeon, Korea). The internal transcrip-
tion spacer (ITS) and partial nuclear large subunit
(nLSU) rDNA regions were amplified using the pri-
mers ITS5 [17] and LR3 [18] as described previously
[19]. DNA sequencing was performed using an ABI
3730XL sequencer (Macrogen, Seoul, Korea). The
resulting nucleotide sequences were proofread and
edited using jPHYDIT software [20]. A neighbor-
joining (NJ) phylogenetic analysis was implemented
by PAUP 4.0b10 [21] using the Jukes-Cantor correc-
tion. The robustness of the inferred NJ topologies
was tested using 1000 bootstrap replicates.
3. Results and discussion
The resulting nucleotide sequences were edited and
deposited in GenBank (accession numbers
MW578953–MW578964). Species identities were
confirmed by comparison with GenBank reference
sequences using BLASTn (Table 1), and an NJ
phylogenetic analysis was conducted (Figures 1
and 2). Based on both morphological and phylogen-
etic analyses, 103 fungal taxa were enumerated and
classified according to current taxonomy guidelines,
among which 27 unique families were represented,
consisting of 83 species within 51 genera. Among
these taxa, there were six species (Agaricus menieri,
Crepidotus praecipuus, Dichomitus squalens,
Hortiboletus amygdalinus, Melanoleuca friesii, and
Trametes lactinea) that have not been previously
reported in Korea (Figure 3). Agaricus menieri is
consumed in Saint-Brevin, France, but it is not
tasty, and therefore not highly valued [22].
Crepidotus praecipuus is recorded as an endemic
species of New Zealand, and this is the first time it
has been recorded outside of New Zealand (https://
inaturalist.nz). Dichomitus squalens is a white-rot
basidiomycete that produces diverse extracellular
enzymes for lignocellulose degradation and oxidative
enzymes to act on lignin [23–25]. The extracts from
cultivated Trametes lactinea significantly inhibit the
activities of lipoxygenase and hyaluronidase [26].
Table 1. Closest GenBank matches of 6 undescribed species in this study.
ITS rDNA nLSU rDNA
Species Voucher No. GenBank accession No. The closest GenBank taxa Identity (%) GenBank accession No. The closest GenBank taxa Identity (%)
Agaricus menieri NIBRFG0000502802 MW578953 Agaricus menieri 99 MW578959 Agaricus bisporus 98
Crepidotus praecipuus NIBRFG0000502861 MW578958 Crepidotus praecipuus 97 MW578960 Crepidotus tobolensis 99
Dichomitus squalens NIBRFG0000502804 MW578954 Dichomitus squalens 99 MW578961 Dichomitus squalens 99
Hortiboletus
amygdalinus
NIBRFG0000502792 MW578955 Hortiboletus rubellus 89 MW578962 Hortiboletus amygdalinus 99
Melanoleuca friesii NIBRFG0000502881 MW578956 Melanoleuca friesii 100 MW578963 Melanoleuca friesii 99
Trametes lactinea NIBRFG0000502816 MW578957 Trametes lactinea 100 MW578964 Trametes lactinea 99
2 M. KIM ET AL.

Also, Trametenolic acid B, one of the components
in T. lactinea, is reported to possess cytotoxic
activities, thrombin inhibiting effects, and the abil-
ity to inhibit gastric cancer cell viability [27].
Melanoleuca is a character-poor genus with similar
macroscopic characters and a morphology strongly
influenced by habitat conditions [28]. It is a taxo-
nomically confused genus based on similar mor-
phological factors. Three species (M. arcuata, M.
melaleuca, and M. verrucipes) have been reported
in Korea, and M. friesii is rarely reported world-
wide. From the results of various previous studies,
it seems necessary to study physiological activity
about these species. As a result of the re-
identification of plant specimens collected on
Daecheongdo island, 398 taxa were confirmed [7].
The plant species diversity and fungal diversity are
closely related, so higher plant diversity should
positively affect fungal diversity. Considering that
the proportion of unrecorded species is high given
the survey area, survey period, and a number of
specimens collected, similar research on adjacent
islands of the West Sea may be necessary. Also, the
results indicated that regional variables had a
greatereffectthanthenumberoftimesandfre-
quency of collection. This study showed that the selec-
tion and concentration of the research area can bring
more diverse species diversity results.
Figure 1. Neighbor-joining tree inferred from nuclear large subunit rDNA sequences of the six macrofungal species newly
recorded in Korea. Auricularia auricula-judae (AAURG25S) was used as outgroup. Bootstrap values exceeding 50% for nodes
are indicated. Samples from the present study are indicated in bold.
MYCOBIOLOGY 3

Figure 2. Neighbor-joining tree inferred from nuclear ITS sequences of six macrofungal species newly recorded in Korea. (A)
Agaricus menieri; (B) Crepidotus praecipuus; (C) Dichomitus squalens; (D) Hortiboletus amygdalinus; (E) Melanoleuca friesii;(F)
Trametes lactinea. Bootstrap values exceeding 50% for nodes are indicated.
4 M. KIM ET AL.

4. Taxonomy
Basidiomycota R.T. Moore
Agaricomycetes Doweld
Agaricales Underw.
Agaricaceae Chevall
Agaricus menieri Bon, Docums Mycol. 11 (no. 44):
28 (1981)
Pileus up to 12 cm in diameter, thick-fleshy, appla-
nate or slightly umbonate, smooth, fibrillose or finely
cracked, whitish, pale yellowish with a gray-pink shade,
eventually pale ochraceous. Margin even, often with
remnants of the veil. Lamellae free, thin, whitish-pink,
pale grayish pink, with pale, sterile edges. Stipe
10 2.5 cm, central, equal, tightly cylindrical to slightly
spindle-shaped, white but at first a pale brownish yel-
low, silky-fibrillose. Ring broad, apical, free-standing.
Taste slightly bitter. Spore print brownish. Basidiospores
6–7.7 4.4–5.6 mm, broadly ellipsoid, brownish, smooth,
and relatively large. Basidia 22–27.6 7.7–9mm, 4-ster-
igmate, clavate. Sterigmata 2–2.5 mmlong.
Remarks: A. menieri is a strictly sabulicolous spe-
cies, fruiting on sandy soil and coastal dunes.
Basidiomata of this species are often completely cov-
ered with sand.
Specimen examined: The specimen was collected
from the pine forest, Moraeul beach, Daecheongdo
Island, from the sandy soil of coastal dunes;
3748’56.91"N 12440’43.82"E, July 25 2018;
NIBRFG0000502802 (GenBank accession no. ITS:
MW578953, LSU: MW578959).
4.1. Crepidotaceae Singer
Crepidotus praecipuus E. Horak, CBS Biodiversity
Series 16: 44 (2018)
Pileus 10–70 mm, semicircular to flabelliform,
convex to plano-convex, laterally or almost laterally
attached to the substrate, with an incurved and,
later, even margin, with a surface that is minutely
tomentose-scaly with yellowish-brown to brown
fibrillose scales and a tough, elastic consistency.
Lamellae whitish, ochre-brown to cinnamon, moder-
ately crowded, with margins that are minutely fim-
briate, remaining whitish. Stipe absent. Spore print
yellowish brown. Basidiospores 6.3–7.8 5.1–6.6 mm,
ellipsoid, smooth, thick-walled, apex obtuse,
depressed, or occasionally mucronate. Basidia
26–33 7.6–9.3 mm, cylindrical-clavate, 4-spored.
Chelliocystidia 26–65 4–14 mm, clavate, cylindrical,
irregularly cylindrical. Pleurocystidia absent.
Remarks: C. praecipuus is characterized by
6.3–7.8 5.1–6.6 mm, ellipsoid, smooth, thick-walled
basidiospores. It is distinguished from closely related
species such as C. tobolensis, by spore quotient (C.
praecipuus: C. tobolensis ¼1.19–1.2:1.21–1.35) and
basidiomata size (C. praecipuus: C. tobolen-
sis ¼10–70 mm: 7-43 mm) [29].
Specimen examined: The specimen was collected
on Daecheongdo Island, from the branch of a dead
deciduous tree; 3749’0.97"N 12441’40.18"E,
September 4, 2018; NIBRFG0000502861 (GenBank
accession no. ITS: MW578958, LSU: MW578960).
Figure 3. Fruiting bodies and microscopic features of Agaricus menieri (A), Crepidotus praecipuus (B), Dichomitus squalens (C),
Hortiboletus amygdalinus (D), Melanoleuca friesii (E), and Trametes lactinea (F). (a) basidiospores; (b) basidia; (c) basidioles; (d)
cystidia; (e) pileipellis; (f) generative hyphae; (g) skeletal hyphae; (h) binding hyphae. The scale bars in the microscopic images
represent 10 lm.
MYCOBIOLOGY 5

4.2. Tricholomataceae R. Heim ex Pouzar
Melanoleuca friesii (Bres.) Bon, Docums Mycol.
9(no. 33): 67 (1978)
Pileus up to 5–6 cm in diameter, initially convex to
plano-convex; margin not surplus, incurred, never
fully extended; cuticle smooth to slightly venous;
brown. Stipe 6–70.6–0.9cm, cylindrical, generally
short and wide, robust, full, progressively widening
toward the base, brownish-white, pruinose. Scent
mild. Flavor slightly spicy. Basidia 16–29 6–8.6 mm,
clavate, 4-spored; Sterigmata 3.4 mm long; Basidiospore
whitish, slightly cream in color when dry;
7.6–8.8 4.3–5.3 mm, narrowly ellipsoidal to subcylin-
drical,warty.Cheilocystidia42–73 12–13 mm, lageni-
form, Pleurocystidia similar to cheilocystidia.
Remarks: M. friesii is distinguished by having
lageniform cystidia and brownish whitish pruin-
ose stipes.
Specimen examined: The specimen was collected
on Socheongdo Island, on soil; 3746’29.27"N
12445’19.62"E, September 5 2018; NIBRFG0000502881
(GenBank accession no. ITS: MW578956,
LSU: MW578963).
4.3. Boletales E.-J. Gilbert
Boletaceae Chevall.
Hortiboletus amygdalinus Xue T. Zhu & Zhu L.
Yang, in Wu, Li, Zhu, Zhao, Han, Cui, Li, Xu &
Yang, Fungal Diversity 81: 98 (2016)
Pileus 6.5 cm in diameter, hemispherical, convex
to applanate; surface always strong rugose, glabrous
and yellow-brown, red-brown. Context cream to
yellowish. Hymenophore adnate, sometimes
depressed around the stipe; surface yellow to dull
yellow, becoming ochraceous. Pores compound,
angular, 0.5–1 per mm; tubes concolorous with
hymenophoral surfaces, staining blue when injured.
Stipe 5 1.7 cm, subcylindrical; apical part yellow-
ish; basal part cream to dirty white; middle part
cream to brownish. Basidia 30–40 10–11 mm, cla-
vate, 4-spored; Basidiospores 9.3–10 4.9–5.6 mm
subfusiform to slender, brownish yellow, smooth.
Pleurocystidia scattered, 61–77 11–13 mm, fusoid-
ventricose to clavate with wider apex, thin-walled.
Pileipellis is yellowish brown, more or less broad-
ened and often incrusted hyphal elements, with
cylindrical terminal cells, 37–63 10–12 mm. Clamp
connections absent.
Remarks: H. amygdalinus is characterized by its
rugose pileus surface when young, eventually turn-
ing glabrous and rimose-diffract with age, unpleas-
ant odor, and relatively wider basidiospores.
Specimen examined: The specimen was collected
on Haeneomi gogae, Daecheongdo Island, from soil;
3748’28.88"N 12441’37.93"E, July 24, 2018;
NIBRFG0000502792 (GenBank accession no. ITS:
MW578955, LSU: MW578962).
4.4. Polyporales G€
aum
Polyporaceae Fr. ex Corda
Dichomitus squalens (P. Karst.) D.A. Reid,
Revta Biol., Lisb. 5(1–2): 150 (1965)
Basidiocarps pileate, effused-reflexed, imbricate or
resupinate, individual pilei, up to 3 cm wide, 1–7cm
long, tough and corky when fresh, hard when dry.
Upper surface white to cream, with a very thin
cuticle; margin white, narrow to glabrous. Pore sur-
face white to wood-colored, with age more yellowish
or discolored in light brown and gray shades, often
unevenly. Pores circular to angular, 4–5 per mm,
with thin dissepiments. Hyphal system dimitic; gen-
erative hyphae with clamps, thin-walled, hyaline,
1.5–4mm in diameter; binding hyphae predominant,
arboriform and usually dichotomously branched,
hyaline, thick-walled to solid, up to 7 mm in diam-
eter in the main stems, tapering down to thin whip-
like ends. Cystidia absent, with fusoid cystidioles
present, 16 4.5 mm. Basidia clavate, 4-sterigmate,
23–27 6–7mm, with a basal clamp. Basidiospores
cylindrical to oblong-ellipsoid, hyaline, thin-walled,
smooth, 9.5–11.8 3–4.4 mm.
Remarks: D. squalens is characterized by circular
to angular pores with 4–5 pores per mm.
Specimen examined: The specimen was collected
from the pine forest, Moraeul beach, Daecheongdo
Island, from the branch of a dead deciduous tree;
3748’56.91"N 12440’43.82"E, July 18 2018;
NIBRFG0000502804 (GenBank accession no. ITS:
MW578954, LSU: MW578961).
Trametes lactinea (Berk.) Sacc., Syll. fung.
(Abellini) 6: 343 (1888)
Basidiocarps dimidiate to semicircular, soft and
velvety to touch, mostly azonate, concentrically sul-
cate and zoned near the margin, white to cream,
eventually turning ochraceous. Margin weakly lobed,
obtuse and relatively thick, concolorous or paler
than the upper surface. Pore surface cream, ochra-
ceous to pale fulvous. Pores round to angular,
mostly 1.5–2 per mm, dissepiments thin to rather
thick, entire, tubes concolorous with the context,
1–10 mm long. The hyphal system, trimitic.
Generative hyphae clamped, hyaline and delicately
thin-walled, 1–4mm in diameter. Skeletal hyphae
abundant, hyaline to pale yellow, thin-walled, 3–8mm
wide in the tubes. Binding hyphae also abundant,
hyaline to pale yellow, thick-walled, arboriform to
coralloid, 1–7mm in diameter. Basidia
14–17.3 5.9–6.2 mm, clavate, 4-spored. Basidiospores
cylindrical-ellipsoid, 6–6.5 2.2–2.7 mm, smooth
and hyaline.
6 M. KIM ET AL.

Remarks: T. lactinea is recognized by soft velvety
azonate pileus, thick fruitbodies, relatively large
pores, and presence of interlocking hyphae.
Specimen examined: The specimen was collected
at the pine forest at Moraeul beach, Daecheongdo
Island, from the branch of a dead deciduous tree;
3748’56.91"N 12440’43.82"E, July 25 2018;
NIBRFG0000502816 (GenBank accession no. ITS:
MW578957, LSU: MW578964).
Disclosure statement
No potential conflict of interest was reported by
the author(s).
Funding
This study was supported by a grant from the National
Institute of Biological Resources (NIBR), funded by the
Ministry of Environment (MOE) of the Republic of Korea
[NIBR202002116 and NIBR202102107].
ORCID
Changmu Kim http://orcid.org/0000-0001-7405-8449
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