Notes on the fungal diversity in the Botanical Garden of the National Museum of Bosnia and Herzegovina

Abstract

Over the past three years, initial mycological studies have been carried out in the Botanical Garden of the National Museum of Bosnia and Herzegovina. As a result of these sporadic surveys, 22 different species of fungi were found, including Octospora pseudoampezzana, Xylaria oxyacanthae, Orbilia carpoboloides and Calathella eruciformis, which were recorded for the first time in Bosnia and Herzegovina. The aim of this study is to initiate scientific research on fungal occurrence and diversity in this urban floral oasis and thus also to improve national knowledge about the fungal species that inhabit such anthropogenic habitats. This work can also serve as an additional argument to emphasise the importance of botanical gardens in urban areas, and their contribution to the diversity of mycobiota in anthropogenic habitats in general.

Full text

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Notes on the fungal diversity in the
Botanical Garden of the National Museum
of Bosnia and Herzegovina
NEDIM JUKIĆ*, SMILJAN TOMIĆ & NIHAD OMEROVIĆ
Mycological Society MycoBH, Trg Zlatnih Ljiljana 34,
71000 Sarajevo, Bosnia and Herzegovina, info@mycobh.com
*Corresponding author e-mail: info@mycobh.com
Received: 25 September 2023; Accepted: 7 December 2023
Original scientic paper
UDK: 582.287.23 ( 497.6 Sarajevo ) “ 2021/2023 “
Abstract: Over the past three years, initial mycological studies have been carried out in the Botanical Garden of the
National Museum of Bosnia and Herzegovina. As a result of these sporadic surveys, 22 dierent species of fungi were
found, including Octospora pseudoampezzana, Xylaria oxyacanthae, Orbilia carpoboloides and Calathella eruciformis,
which were recorded for the rst time in Bosnia and Herzegovina. The aim of this study is to initiate scientic research
on fungal occurrence and diversity in this urban oral oasis and thus also to improve national knowledge about the
fungal species that inhabit such anthropogenic habitats. This work can also serve as an additional argument to em-
phasise the importance of botanical gardens in urban areas, and their contribution to the diversity of mycobiota in
anthropogenic habitats in general.
Key words: mycobiota, urban areas, botany, Sarajevo

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INTRODUCTION
Although man-made green spaces in the urban environ-
ment are mostly represented by parks and other landscaped
green areas, whose primary functions are to provide quality
space for recreation and relaxation, without any particular
interest for maintaining a high level of biodiversity, there are
also botanical gardens formed with the opposite intention,
i.e. designed to create small biodiversity oases deep within
urban centres.
Botanical gardens have multiple purposes in everyday
life: They can represent important refuges for the survival of
certain highly endangered endemic and/or rare plant spe-
cies; they provide great opportunities for multidisciplinary
scientic research that could provide a better understand-
ing of phyto-diversity in general; they are a great place for
education in situ; they provide a perfect setting for daily
relaxation, which is benecial for both physical and mental
health. They can also be a useful tool in biosecurity research
by serving as sentinel monitoring sites to detect threats
from pathogens and pests (Wondafrash et al., 2021). Their
high biological and conservational importance is indicated
by the fact that 31% of the total number of accepted and
currently known plant species grow in botanical gardens all
over the world (Antonelli et al., 2020).
Alongside trees and plants, botanical gardens are home
to other closely associated organisms that are usually much
less investigated than the ora itself. Such other organisms
occasionally become subject of inventory primarily on the
initiative of employed scientists or in the context of regular
institutional project activities (see, for example, Glushakova
& Kachalkin, 2017 for yeasts; Matveev et al., 2018 for slime
moulds; Wilkie, 2020 for lichens; Cathrine et al., 2022 for
arachnids, etc.).
The real value of inventory studies within botanical gar-
dens largely lies in the fact that they help us to determine
the true magnitude of biodiversity in these urban oases,
which brings us one step closer to ex situ conservation of
endangered and rare organisms, while at the same time al-
lowing us to closely monitor structural changes in biodiver-
sity levels through temporal observation and analysis of the
diversity of certain species.
Fungi, as an inevitable and crucial component of the
biodiversity of botanical gardens, had largely remained un-
der-studied in the past. With the exception of isolated earlier
individual studies (for example Currey, 1874), only recently
have signicant eorts been undertaken in terms of the my-
cological research of botanical gardens (Eckstein & Eckstein,
2009; Folcz & Börcsök, 2015; Kartika et al., 2018; Watling et
al., 2019; Kruse et al., 2020; Bradshaw et al., 2022). In Bos-
nia and Herzegovina, to date there has been no evidence of
mycological studies being carried out in botanical gardens.
On the other hand, the presence of taxonomic studies of rel-
ative signicance in similar anthropogenic habitats in urban
areas are worthy of note (Moravec, 1971; Jukić et al., 2018).
The Botanical Garden of the National Museum of Bosnia
and Herzegovina is located near the centre of Sarajevo, in
the oldest cultural and scientic institution in the state. The
garden itself is an object of special educational purpose, and
represents an important monument of natural and botani-
cal heritage.
Although it occupies a signicantly smaller area in com-
parison to other European botanical gardens (14,270 m2
according to Bečić et al. (2011)), the diversity of the plant
fund has gradually increased over the years, having reached
a maximum number of 3,000 dierent plant species (Šilić,
1988). Currently, however, ocial sources list much smaller
number of the plants (1,700 according to the National Mu-
seum’s own website).
The Botanical Garden was founded by the famous Aus-
trian botanist Karl Malý at the beginning of the 20th centu-
ry, and has undergone certain structural and physiognomic
changes over time. However, its main role as an invaluable
and an eective instrument of in situ teaching at dierent
levels of education remained unchanged.
A detailed overview of and insight into the diversity
and abundance of living plants in the Botanical Garden of
the National Museum of Bosnia and Herzegovina has been
provided by Šilić (1988) and Bečić & Ljujić-Mijatović (2010).
However, no other systematic and comprehensive inven-
tories of other taxonomic groups – including fungi – have
been conducted to date.
To (partially) address this issue, the authors conducted
such research, with the preliminary results presented here
representing the rst real insight into the diversity of fungi
in botanical gardens in Bosnia and Herzegovina.
MATERIAL AND METHODS
Six eld studies were carried out between 2021 and 2023
in the Botanical Garden of the National Museum of Bosnia
and Herzegovina, Sarajevo. The main focus of the research
was ascomycetous fungi, their ecology and diversity. At the
same time, seven species from the phylum Basidiomycota
were also recorded, mainly those that are easy to identify in
situ by recognizing relevant macro-characters.
The ascomata and basidiomata of the registered fungi
species were photographed both in situ and ex situ using
photographic equipment and a stereomicroscope. Macro-
photographs in situ were taken with a Canon 700D camera,
a 100mm f/2.8L Macro IS USM lens, a tripod and a Canon
Macro Ring Lite MR-14EX II, while ex situ macrophotographs
were taken with a Nikon SMZ445 stereo zoom microscope. A

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Nikon SE type 102 compound light microscope was used for
laboratory analyses and observation of micromorpholog-
ical characters. Photomicrographs were taken with a Sony
DSC-H2 camera.
Samples for microscopy were prepared by cutting fresh
fungal apothecia by hand using a razor blade, and, in the
case of very small apothecia, samples were taken with a
teasing needle.
The descriptions of macro- and micromorphological
characters are mainly based on the analysis of living struc-
tures of fresh collections (Baral, 1992) from the Botanical
Garden of the National Museum of Bosnia and Herzegovina,
and are combined with relevant literature data where indi-
cated.
All measurements were carried out in a tap water mount.
For each species analysed, 20 ascospores were measured to
determine their average length and width. The extreme val-
ues of measured ascospores and other structures are given
in parentheses. The ornamentation of the ascospores was
stained with lactophenol cotton blue (LCB); the presence or
absence of an iodine reaction in the apical part of the asci
was checked using Lugol’s solution (IKI); cresyl blue (CRB)
was used to highlight cytoplasmic inclusions such as spore
bodies in Orbiliomycetes and for staining the nucleus and
nucleolus in Sclerotiniaceae.
In order to dene the simple spore shape in accordance
with the Q value (length:width ratio of ascospores) the geo-
metric delimitation criteria from Kušan et al. (2014) were
used.
The abbreviation “FAMU” and the corresponding data-
base codes are given for each material deposited in the Fun-
garium of the Mycological Society MycoBH.
RESULTS
1. Arrhenia spathulata (Fr.) Redhead
Fig. 1 – j)
Among shoots of Tortula ruralis covering rocks, 20 Feb
2021.
2. Octospora gyalectoides Svrček & Kubička
Fig. 2 - d), f)
Rocky and base-poor site, probably on shoots of
Crossidium squamiferum, 14 Feb 2021, 07 Jan 2023,
N.J./070123-Y2; FAMU – 0959.
3. Octospora pseudoampezzana (Svrček) Caillet & Moyne
Figs. 1 - b), d); 3 - i), o), p), q)
Description: Ascomata apothecial, 1–4 (5) mm in diam.,
yellow-orange, orange to brown-orange; margin con-
spicuous and quite pronounced, rst whitish and silky,
later getting darker, nally in mature specimens be-
coming blackish; hymenium nely granulose. Asci cy-
lindrical, *250–340 × 22–28.7 m, 8-spored, uniseriate.
Ascospores *(19.7) 20.2–23.8 × (14.3) 14.5–15.9 (16.9)
µm, ellipsoid to broadly ellipsoid, containing one large
oil droplet, usually eccentric; ornamentation consists of
roundish isolated warts, evenly scattered over the spore
surface and of more or less the same diam. (0.5–1.0–1.2
µm). Paraphyses cylindrical, barely exceeding asci,
slightly enlarged in the upper part, *7–10 µm wide in
the apical part, containing light orange pigmentation.
Material examined: On shoots of Schistidium crassipi-
lum/ S. helveticum complex covering limestone rocks, 14
Feb 2021, 20 Feb 2021 & 07 Jan 2023, N.J./070123-Y1;
FAMU – 1389.
Notes: As stated in Eckstein & Eckstein (2009) and
Németh et al. (2022), host species is almost always
Schistidium crassipilum. Rare cases with Racomitrium
heterostichum as a host moss were reported in Eckstein
et al. (2020). First record for Bosnia and Herzegovina.
4. Ciboria amentacea (Balb.) Fuckel
Figs. 1 - e), g); 3 - b), c), g), h), l) r), s)
On fallen and buried male catkins of Corylus avellana,
apparently emerging from thali of Marchantia polymor-
pha, 20 Feb 2021, 28 Feb 2021 & 07 Jan 2023.
5. Auricularia mesenterica (Dicks.) Pers.
On the dead Ulmus sp. trunk, 20 Mar 2021 & 07 Jan 2023.
6. Xylaria oxyacanthae Tul. & C. Tul.
Fig. 1 – k)
Description: Stromata usually slender, simple or rarely
branched, 2–5 cm in height and up to 2–4 mm wide,
cylindrical, slightly enlarged in the upper part and often
laterally compressed. Apices nely pronounced, some-
times mammiform, pinkish-orange to orange-brown.
Middle part more whitish or greyish, while lower part of
stromata remains black or greyish-black
Material examined: On partially buried and mummi-
ed Crataegus monogyna fruits probably mixed with
excrements of Columba palumbus, 20 Mar 2021.
Notes: First record for Bosnia and Herzegovina. The ma-
terial was identied on the basis of the description of
relevant macro and micro characteristics from Kujawa &
Karasiński (2007) and Himani & Krishnappa (2020).
7. Piceomphale bulgarioides (Rabenh.) Svrcek
Figs. 1 - c); 3 - m), n)
On fallen Picea omorika cones, 20 Mar 2021. First record
of P. bulgarioides on Picea omorika in Bosnia and Herze-
govina.

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Figure 1. Some fungal species registered in the Botanical Garden of the National Museum of Bosnia and Herzegovina: a) Geopora
sumneriana under Cedrus libani; b), d) Octospora pseudoampezzana, bryophilous species on shoots of Schistidium crassipilum/ S.
helveticum complex; c) Piceomphale bulgarioides on cones of Picea omorika; e), g) Ciboria amentacea ascomata seemingly emerging
from the liverwort Marchantia polymorpha thalli; f), i) Ciboria coryli sharing the same habitat type with C. amentacea; h) Ciboria
rufofusca on fallen Abies alba cones; j) Arrhenia spathulata, bryophilous species; k) Xylaria oxyacanthae (anamorph) on buried seeds
of Crataegus sp.

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8. Ciboria coryli (Schellenb.) N.F. Buchw.
Fig. 1 - f), i)
On fallen and partially buried male catkins of Corylus
avellana, 28 Feb 2021.
9. Ciboria rufofusca (O. Weberb.) Sacc.
Fig. 1 - h)
On lying cone scales of Abies alba, 08 May 2022.
10. Geopora sumneriana (Cooke) M. Torre
Figs. 1 - a); 3 - j), k)
Under Cedrus libani, among the litter of needles, 08 May
2022.
11. Orbilia aurantiorubra Boud.
Figs. 2 - a); 3 - a), e)
On dead dry semi-decorticated twigs of Fraxinus sp.?,
08 May 2022.
12. Orbilia carpoboloides (P. Crouan & H. Crouan) Baral
Figs. 2 – b), c); 3 - d), f)
Description: Ascomata apothecial, 0.5–1.5 (1.8) m
wide., light rose-carneous, light ochraceous, yel-
low-ochraceous or orange-ochraceous, sometimes
slightly reddish, irregularly rounded or broadly ellipti-
cal, concave, with conspicuous margin usually made of
whitish “teeth” or mbriate hair tufts (Baral et al., 2020).
Asci cylindrical, *(62.4) 65.4–78.8 (79.7) × (4.9) 5.6–6.4
(6.7) µm, 8-spored, bi- or triseriate. Ascospores *(12.4)
12.5–15.6 (15.9) × (2.3) 2.3–2.8 (2.9) µm, fusiform to fu-
soid, rarely straight, more often slightly curved at the
base; spore body vermiform, barely enlarged at the
base, 4.2–7 µm in length. Paraphyses septate, quite
straight, or slightly exuous, mammiform to spathulate
(Baral et al., 2020), with more or less pronounced apical
narrowed part.
Material examined: On corticated part of dead twig of
undetermined deciduous tree, 08 May 2022.
Notes: First record for Bosnia and Herzegovina.
13. Propolis farinosa (Pers.) Fr.
Fig. 2 - i)
On dead deciduous twigs, 08 May 2022.
14. Pyrenopeziza rubi (Fr.) Rehm
Fig. 2 - h), j)
On dead Rubus sp. twig, 08 May 2022.
15. Xylaria carpophila (Pers.) Fr.
On fallen dead beechmasts, 08 May 2022.
16. Dacrymyces capitatus Schwein.
Fig. 2 - e)
On dead twigs of unknown deciduous tree, 08 May
2022.
17. Calathella eruciformis (P. Micheli ex Batsch) D.A. Reid
Description: Basidiomata cyphelloid, tubular in shape,
sometimes distinctly narrowed at the base or campan-
ulate, 0.5–1.5 mm wide and up to 2 mm high; outer side
and marginal region densely covered in long whitish
hairs, later becoming more ochre, grey to ochre-brown-
ish, surface more brownish; hymenial inner part
smooth, pale cream to ochre cream.
Material examined: On dead Populus sp. twigs, 07 Jan
2023, N.J./070123-Y3; FAMU – 1391.
Notes: First record for Bosnia and Herzegovina. The
material was identied based on the description of rel-
evant macro and micro characteristics from Halama et
al. (2019).
18. Xylaria longipes Nitschke
On remnants of unknown deciduous tree, 07 Jan 2023.
19. Schizophyllum commune Fr.
On dead Populus alba remnants, 07 Jan 2023.
20. Auricularia auricula-judae (Bull.) Quél.
On living Berberis sp. branches, 07 Jan 2023.
21. Candolleomyces typhae (Kalchbr.) D. Wächt. & A. Mel-
zer
Fig. 2 - g)
On decaying dead stem and/or leaves of Typha angusti-
folia, 25 Jun 2023, N.J./250623-Y1; FAMU – 1390.
22. Psilachnum inquilinum (P. Karst.) Dennis
On dead partially inundated stem of Equisetum hiemale,
25 Jun 2023, N.J./250623-Y2; FAMU – 1392.

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Figure 2. Some fungal species registered in the Botanical Garden of the National Museum of Bosnia and Herzegovina: a) Orbilia aurant-
iorubra on dead Fraxinus sp,? twig; b), c) Orbilia carpoboloides on dead twig of undetermined deciduous tree; d), f) Octospora gyalectoi-
des on shoots of Crossidium squamiferum; e) Dacrymyces capitatus on dead twigs of undetermined deciduous tree; g) Candolleomyces
typhae on decaying stem of Typha angustifolia; h), j) Pyrenopeziza rubi on dead Rubus sp. stem; i) Propolis farinosa on undetermined
deciduous twigs.

NOTES ON THE FUNGAL DIVERSITY IN THE BOTANICAL GARDEN OF THE NATIONAL MUSEUM OF BOSNIA AND HERZEGOVINA
GZM PN NS 40 | 13
Figure 3. Micro characters of some fungal species registered in the Botanical Garden of the National Museum of Bosnia and Herzegovina: a), e) Orbilia
aurantiorubra – a) asci and ascospores in CRB mount, e) *mature ascospores; b), c), g), h), l) r), s) Ciboria amentacea – b) *immature ascospores and asci, c)
*asci and ascospores in IKI mount, g) *apical apparatus of the asci in IKI mount, h) – *mature ascospores, l) *vertical section of the apothecia, r), s) asci and as-
cospores in CRB mount; d), f) Orbilia carpoboloides – d) *apical part of the paraphyses and asci, f ) *mature ascospores; j), k) Geopora sumneriana – *mature
ascospores; m), n) Piceomphale bulgarioides – m) *mature ascospores in IKI mount, n) *mature ascospores; i), o), p), q) Octospora pseudoampezzana – o)
*immature ascospores, i), p) *mature ascospores in LCB, q) *apical part of the paraphyses. Bars: l) – 50 μm; b), c), q) - 20 μm; a), d), f), i), j), k), o), p), r), s) – 10
μm; e), h), g), m), n) – 5 μm.

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DISCUSSION
Botanical gardens in urban areas should be considered
unique sources of biodiversity enrichment. These small ar-
eas represent a profound substitutional link between hu-
man and natural environments, especially in the modern
and accelerated lifestyles of today.
Diverse oristic components and structures, the hetero-
geneity of the ora, the vegetation of dierent bioclimates,
the combination of normally incompatible components, and
the special care and treatment of the plants are the cause
of the great and highly specic biodiversity in these small
“oases” and are also the main reasons for botanical gardens’
need to be one of the highest priorities in urban planning.
This short and narrowly focused mycological study clear-
ly shows that botanical gardens are highly interesting and
intriguing man-made habitat types, and should be recog-
nized as fungal diversity hotspots within contemporary ur-
ban areas. This has also been argued by other mycologists
in the past (Eckstein & Eckstein, 2009; Folcz & Börcsök, 2015;
Kartika et al., 2018; Kruse et al., 2020; Bradshaw et al., 2022).
A number of long-term studies and corresponding results,
such as those of Folcz & Börcsök (2015) are quite impressive
and show the true value of botanical gardens and their im-
portance for the biodiversity of fungi, and the conservation
of fungi in general.
Although botanical gardens are usually very limited in
space and may seem somewhat irrelevant factors in terms
of fungal diversity (or overall biodiversity) at the national, re-
gional and global level, it is quite the contrary. These islands
of biodiversity play a signicant role in enriching fungal
heterogeneity, on national and regional scales in particular.
Also, botanical gardens are the only locations where certain
species of fungi (or other organisms) with natural habitats
that are very distant from one another can be found living
together. As a result, they provide a great opportunity for
scientists around world to closely study and monitor dier-
ent types of organisms, but such studies should also be tak-
en with caution, due to the negative eects of outbreeding
depression on population persistence (Chen & Sun, 2018).
They can, however, provide ideal conservation environ-
ments for ex situ conservation of fungi (Folcz & Börcsök,
2015), with the results presented here going some way to
support this hypothesis. In addition, botanical gardens pro-
vide a wide range of mycological interpretation and educa-
tional activities, including those aimed at preserving fungal
diversity (Hu & Zhang, 2008).
Collections of Octospora pseudoampezzana, Xylaria oxy-
acanthae, Orbilia carpoboloides and Calathella eruciformis
from the Botanical Garden of the National Museum of Bos-
nia and Herzegovina represent the rst registered ndings
of these species in Bosnia and Herzegovina, and provide sol-
id arguments for emphasizing the important role that bo-
tanical gardens can potentially play in modern science. This
preliminary checklist of fungi from the Botanical Garden of
the National Museum of Bosnia and Herzegovina is arguably
only partial in nature, and minute projection of the overall
level of fungal diversity within this man-made habitat. It is
for this reason that the authors strongly outline the (largely
self-implied) need for continuation of this mycological re-
search.
ACKNOWLEDGEMENTS
We would like to thank Mirsad Sijarić (Director of the Na-
tional Museum of Bosnia and Herzegovina) for recognizing
the value of this research and giving us permission for its
undertaking. We deeply appreciate all of the support and as-
sistance given by Dejan Kulijer and Adnan Zimić, employees
of the National Museum of Bosnia and Herzegovina, without
which this study would not have been possible to complete.
The host mosses for bryophilous fungi were identied
and conrmed by Marko Sabovljević (Institute of Botany
and Botanical Garden – Faculty of Biology, University of Bel-
grade), for which we are immensely grateful.

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NOTES ON THE FUNGAL DIVERSITY IN THE BOTANICAL GARDEN OF THE NATIONAL MUSEUM OF BOSNIA AND HERZEGOVINA
16 | GZM PN NS 40
SAŽETAK
Botanički vrtovi općenito predstavljaju vrlo značajne oaze bioraznolikosti koje je stvorio čovjek i obično su prostorno smješ-
tene unutar same jezgre urbanih sredina. Njihova uloga danas je višestruka i nezamjenjiva. Oni prije svega služe za edukaciju
različitih interesenih grupa, pomažu pri ex situ konzervaciji ugroženih vrsta biljaka i drugih organizama te u značajnoj mjeri
obogaćuju biodiverzitet u urbanim zonama, gdje on inače, ne dolazi do izražaja. Botanički vrtovi su interesantna staništa i s
aspekta mikologije, prvenstveno zbog prisustva obilja vaskularne, ali i nevaskularne ore, odnosno brojnih biljnih vrsta koje
učestvuju u različitim tipovima interakcija s gljivama. O tome svjedoče pojedini naučni radovi u okviru kojih su obrađene ra-
zličite taksonomske skupine gljiva: Eckstein & Eckstein (2009) – briolne vrste, Folcz & Börcsök (2015) – više različitih skupina,
Kartika et al. (2018) – više različitih skupina, Watling (2019) – nelihenizirane vrste, Kruse et al. (2020) – više različitih skupina,
Bradshaw et al. (2022) – gljive porodice Erysiphaceae i dr. Ovim istraživanjem utvrđeno je prisustvo pojedinih vrlo značajnih i
rijetkih vrsta gljiva te je valorizovana pretpostavljena važna uloga botaničkih vrtova u raznolikosti gljiva u modernim urbanim
zonama. S druge strane, premda postoji više od 100 godina i sadrži izuzetno vrijedne zbirke briota, viših biljaka i dendroore,
Botanički vrt Zemaljskog muzeja Bosne i Hercegovine do danas nije bio predmet mikoloških istraživanja. U ovom radu su
prvi put prezentovani rezultati istraživanja diverziteta gljiva Botaničkog vrta Zemaljskog muzeja Bosne i Hercegovine koja su
realizovana u posljednje dvije godine. Kratka istraživanja su provođena u zimskim, proljetnim i ljetnim dijelovima godine, a
ukupno je u periodu februar 2021. – juni 2023. realizovano 7 istraživanja. Predmet ovih istraživanja bile su gljive odjeljka Asco-
mycota, ali su uporedo, u manjem obimu, registrovane i neke karakteristične i značajne vrste odjeljka Basidiomycota. Sav pri-
kupljeni materijal je naknadno laboratorijski obrađen u skladu s principima vitalne taksonomije, a radi ispravne determinacije
vrsta i registrovanja najbitnijih specijskih obilježja. U okviru provedenog seta istraživanja determinisane su 22 vrste gljiva, od
čega 15 vrsta iz odjeljka Ascomycota i 7 iz odjeljka Basidiomycota. Vrste Octospora pseudoampezzana, Xylaria oxyacanthae,
Orbilia carpoboloides i Calathella eruciformis zabilježene su prvi put u Bosni i Hercegovini. Za navedene vrste je u okviru rada
dat kraći deskriptivni opis koji sadrži podatke o najbitnijim morfološkim i mikrokarakteristikama.