ACTA MYCOLOGICA
Vol. 48 (2): 173–188
2013
DOI: 10.5586/am.2013.019
Dedicated to Professor Maria Ławrynowicz
on the occasion of the 45th anniversary
of her scientific activity
Species diversity and composition of fungal communities
in a Scots pine forest affected by the great cormorant colony
ERNESTAS KUTORGA1, REDA IRŠĖNAITĖ2, TATJANA IZNOVA1,
JONAS KASPARAVIČIUS2, SVETLANA MARKOVSKAJA2
and JURGA MOTIEJŪNAITĖ2
1
Vilnius University, Department of Botany and Genetics, M. K. Čiurlionio Str. 21/27
LT-03101 Vilnius, ernestas.kutorga@gf.vu.lt
2
Nature Research Centre, Institute of Botany, Laboratory of Mycology
Žaliųjų Ežerų Str. 49, LT-08406 Vilnius
Kutorga E., Iršėnaitė R., Iznova T., Kasparavičius J., Markovskaja S., Motiejūnaitė J.: Species
diversity and composition of fungal communities in a Scots pine forest affected by the great
cormorant colony. Acta Mycol. 48 (2): 173–188, 2013.
A Scots pine forest, affected by the great cormorant colony, was studied by plot-based
fungal survey method during the years 2010-2012 in Lithuania. Diversity and composition
of fungal communities were investigated at five zones that had been influenced by different
stages of breeding colony establishment: starting-point and almost abandoned cormorant
colony part (zones A and B), active part (zones C and D), and the edge of the colony (zone E).
The control zone G in undamaged by cormorants pine stand was assessed too. A total of 257
fungal species of ascomycetes including anamorphic fungi, basidiomycetes and zygomycetes
were recorded. Seven species were registered for the first time in Lithuania. Species richness
in the examined zones varied, lowest being in zones B (51 species), C (46) and D (73) and
almost twice as high in the zones A and E (129 and 120, respectively). The comparison of
fungal species compositions of different zones showed that their similarity was rather low
(SS: 0.22–0.59). The most obvious changes in the trophic structure of fungal communities in
the territory occupied by the bird colony were a strong decrease of mycorrhizal species, the
presence of coprophilous fungi on forest litter, and the appearance of host-specialized fungi
on alien and non-forest plants that have established in the disturbed forest.
Key words: Phalacrocorax carbo, Pinus sylvestris, fungi, checklist, Lithuania
INTRODUCTION
Colonies of piscivorous birds may become a source of excessive nutrient enrichment
by transferring organic matter from aquatic to terrestrial ecosystems thus leading
to extraordinary high levels of nutrients in soils and other substrates (Garcia et al.
174
E. Kutorga et al.
2002; Osono et al. 2006a; Breuning-Madsen et al. 2010; Kolb et al. 2010) and subsequent changes in whole ecosystem. A cumulative effect of ornithogenic disturbances in forests is tree death due to ammonia poisoning and formation of glades
densely overgrown by tall herbaceous plants as well as invasion of elders (Sambucus
spp.) which rapidly form dense shrub communities replacing dead forest in the postcolony areas (Żółkoś, Markowski 2006; Laiviņš, Čekstere 2008; Garcia et al. 2011).
Bird guano increases soil fertility and primary productivity of plants, however, due
to ammonia poisoning in the most active parts of the colony plant biomass is lower,
than in the areas abandoned by birds (Kolb et al. 2010).
Fungi, together with other ecosystem components react to these disturbances.
Though there is a number of studies dealing with reaction of fungi to the increase
of nutrient levels (e. g. Ohenoja 1988; Kårén, Nylund 1997; Wallenda, Kottke 1998;
Peter et al. 2001, Tarvainen et al. 2003; Edwards et al. 2004), effect of ornithogenic
disturbances is, however, much less studied. Ninomiya et al. (1993), SchoenleinCrusius et al. (1996) and Osono et al. (2002, 2006b) studied soil and forest floor
litter micromycetes in bird colonies, but their investigations were based on isolated
fungal cultures, not on fungal fructification, and therefore most of mycobiota groups
remained unstudied.
Continental subspecies of the great cormorant (Phalacrocorax carbo sinensis),
not known to be breeding in Lithuania since early 20th century, re-established themselves in the early nineties and their population has increased manifold during the
next decades, following the same pattern as elsewhere in Europe (Žydelis et al.
2002). The largest and oldest colony is located in an old-growth forest, part of a
protected area in Kuršių Nerija (Curonian Spit) National Park neighbouring with
a popular resort Juodkrantė. Rapidly expanding colony receives strong public attention mainly due to its impact on forest. In 2010, a project aiming to investigate
changes in the biotic and abiotic components of forest ecosystem induced by a cormorant colony was started. One of the reaserch objects was fungi belonging to various taxonomic and ecological groups. This paper presents data on species richness,
distribution and trophic groups of fungi recorded in the colony and its surroundings
under varying impact from the bird activity.
STUDY AREA
The study was carried out in the northern part of the Curonian Spit peninsula
(Lithuania). The climate in the Curonian Spit is an intermediate between marine
and continental with a mean annual precipitation of 725 mm and mean annual air
temperatures ranging from 16.6 to 16.8° C in June and August to –2.8 to –2.6° C in
January and February (Galvonaitė et al. 2007). Seventy percents of the Spit land is
covered by forests with prevailing conifers (80%). Small fragments of old growth
Pinus sylvestris forest can be found on parabolic dunes and only at Juodkrantė settlement. The soils of the old parabolic dunes consist of eluvial and illuvial parts, they
have characteristics of typical podzols (Morkūnaitė et al. 2011).
The present colony of great cormorants established in Juodkrantė old growth
forest in 1989 and expanded into so far the largest breeding colony in Lithuania.
Species diversity and composition of fungal communities
175
Now (together with a small, stable colony of grey herons (Ardea cinerea)) the great
cormorants occupy an area of forest more than 700 m long and 370 m wide, and
their colony currently counts over 3300 occupied nests (M. Dagys, pers. com.). At
present the colony is located throughout an upper part of the dune ridge (altitude
up to 34 m), down to dune slope terraces and a dune hollow (alt. 0–2 m). Upper part
of the colony originally was ca. 110 year-old and slope terraces – ca. 230 year-old
pine forest of Empetro nigri-Pinetum association, growing on nutrient-poor sandy
soil, while dune hollow was formerly occupied by 230 year- old pine and spruce forest developed on temporarily wet mesotrophic soils (Jončys, Paulaitis 1987). Now
on the dune slope P. sylvestris trees are dead or dying, in the dune hollow P. sylvestris
trees are dead and mostly fallen.
Eighteen permanent sampling plots (100 m2 each) for current investigation were
established in six zones (3 plots in each zone) that were chosen considering forest
type, age and slope exposition, and basing upon different activity of the bird colony:
A – the oldest part of the colony in the dune hollow: formerly a pine and spruce
forest on mesotrophic temporarily wet soil, coniferous trees are now dead, few
young Picea abies, Quercus robur, Betula pubescens are still alive but partly dried out,
a large part of the area is overgrown with tall herbs as well as Sambucus spp. shrubs,
standing and laying barkless pine deadwood is abundant but in places overshadowed
with herbs and bushes. Cormorant nests are absent or very few, but birds fly over the
area to feed in the Curonian Lagoon.
B – the oldest part of the colony on the dune terraces: no living trees, standing
dead P. sylvestris trees are mostly barkless, large amounts of dead wood – laying
and standing, litter composed of fine twigs, larger and smaller pine bark pieces,
fish scales and bones. Vegetation consists mainly of nitrophilic herbaceous communities with Sambucus spp. shrubs. Moss layer is absent, patches of bare soil
abound. Cormorant nests are absent or very few, but numerous birds roost and fly
over the area (Fig. 1B).
C – the most active part of the colony in the former oligotrophic pine forest with
the highest concentration of nests; pine trees are dead or dying but still with bark;
shrub layer consists of Sorbus aucuparia and Sambucus spp., sparse remaining Juniperus communis shrubs are dying; herb layer makes up to 10 % with predominantly
nitrophilic species; moss layer is absent, patches of bare soil present (Fig. 1C).
D – an inner edge of the colony with the most recent and still rather few nests in
an oligotrophic pine forest on the upper part of dune, trees alive, but their vitality is
reduced – crowns are thinner; shrub layer is thickened with Sorbus aucuparia, young
Sambucus spp , Juniperus communis appear weakened; herb layer is depauperized
due to extinction of some oligotrophic herbs, meso- and eutrophic species become
abundant, patches of bare soil appear; moss layer is thinned.
E – edge of the colony with very few, the most recent nests (as recent as 2011),
relatively undamaged by cormorants oligotrophic pine forest (association Empetro
nigri–Pinetum) on the upper part of dune with solitary mesotrophic and eutrophic
plants.
G – zone outside of colony, nests absent, closest nests are distanced approximately at 60 m. The stand is oligotrophic pine forest (association Empetro nigri–Pinetum)
on the upper part of dune, undamaged by cormorants. G-zone was interpreted as a
control zone in our study.
Species diversity and composition of fungal communities
177
Fig. 2. The overall number of species from the sampled zones A-E and G.
MATERIAL AND METHODS
Field sampling was undertaken from September 2010 until October 2012. Due to
the rapid colony expansion in 2011, the additional control plots (zone G) were established and studied since spring of 2012. The study plots were inspected thoroughly
three times a year: one visit in spring (May) and two visits in autumn (September–
October). Specimens of fungal species that were difficult to identify in situ were
collected for microscopic examination in the laboratory and identified following
routine mycological methods (Mueller et al. 2004). Latin names are given according to Index Fungorum (2013). Voucher specimens of the study are deposited in the
Herbaria of the Nature Research Centre, Institute of Botany (Vilnius) (BILAS) and
Vilnius University (WI).
Sørensen coefficient (Ss) was employed to evaluate the fungal species composition similarity between pairs of the sampled zones. It equals 2W/(A+B), where W is
the shared abundance and A and B are the sum of abundances in individual sample
units. PC-ORD ver. 6 statistical software (McCune, Mefford 1999) calculated a Sørensen distance (Sd) matrix and values of this matrix was converted to a similarity
matrix by substracting from one (similarity=1-Ss).
178
E. Kutorga et al.
RESULTS
Species richness and distribution. Altogether 257 species of fungi were recorded,
of which 240 were identified to species and 17 to genus level (Tab. 1). Ascomycetes
(including anamorphic fungi) made up 138 species (54% of all recorded), Basidiomycetes – 117 (45%), and Zygomycetes – 2 (1%). Seven species were registred
for the first time in Lithuania, namely Allophylaria fumosella, Dicranidion gracilis,
Jaapia ochroleuca, Junewangia globulosa, Scolecobasidium verruculosum, Triadelphia
heterospora, and T. uniseptata.
Table 1
Checklist of fungi collected in a Scots pine forest affected by the great cormorant colony
(+ – taxa recorded)
Abbreviations. Trophic groups: B – biotrophs, M – mycorrhizal fungi, S – saprobes, Sc – coprophilous
saprobes. Substrate types: b – bark, c – cones, h – herbs, l – leaves, lt – forest litter, n – needles, s – soil,
t – twigs (small branches less than 0.5 cm in diameter), w – wood (trunks, snags, stumps, branches, excluding twigs).
Taxa
Ascomycota including anamorphic fungi
Acremonium sp.
Acrogenospora sphaerocephala
Allophylaria fumosella
Alternaria alternata
Alternaria sp.
Anungitea continua
Arthrobotrys oligospora
Ascobolus foliicola
Ascocoryne cylichnium
Ascocoryne sarcoides
Aspergillus sp.
Bactrodesmium biformatum
Bactrodesmium pithoideum
Bactrodesmium traversianum
Blastophorum pini
Botrytis cinerea
Brachysporium britannicum
Brachysporium nigrum
Brachysporium obovatum
Brachysporium polyseptatum
Cacumisporium capitulatum
Calcarisporium arbuscula
Calycina conorum
Camposporium cambrense
Camposporium pellucidum
Cenangium ferruginosum
Chaetosphaeria callimorpha
Chaetosphaeria ovoidea
Chalara longipes
Chalara microchona
Chalara sp.
Cheiromycella microscopica
Chloridium cylindrosporum
Chloridium clavaeforme
Chloridium virescens var. virescens
Circinotrichum britannicum
Trophic groups/
substrate types
A
Sampling zones
B
C
D
E
G
S/lt(h,n)
S/w
S/lt(c,n)
S/lt(h)
S/lt(t)
S/lt(n)
S/lt(b,l,t)
Sc/lt(c,n,t),w
S/w
S/lt(c),w
S/lt(t)
S/lt(t)
S/lt(b,t)
S/lt(t)
S/lt(t)
S/lt(h)
S/lt(t)
S/lt(t)
S/lt(t)
S/lt(t)
S/lt(t)
S/lt(n)
S/lt(c)
S/lt(t)
S/lt(n)
B,S/lt(t)
S/w
S/w
S/lt(t)
S/lt(b,t)
S/lt(t)
S/lt(t),w
S/lt(t)
S/lt(t)
S/lt(t)
S/lt(n)
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179
Species diversity and composition of fungal communities
Cirrenalia sp.
Cladosporium herbarum
Cladosporium sp.
Clonostachys compactiuscula
Coniochaeta malacotricha
Conioscypha varia
Cyclaneusma minus
Dactylaria candidula
Dactylella sp.
Dendryphion comosum
Dendryphiopsis atra
Diaporthe eres
Dicranidion gracilis
Diplocladiella scalaroides
Diplococcum spicatum
Doratomyces asperulus
Endophragmiella eboracensis
Endophragmiella pinicola
Epicoccum nigrum
Erysiphe alphitoides
Erysiphe vanbruntiana
Fusarium sp.
Gonytrichum caesium var. caesium
Graphium putredinis
Hamatocanthoscypha laricionis
Harzia sp.
Heyderia pusilla
Heteroconium chaetospira
Hyalorbilia inflatula
Hyaloscypha aureliella
Hymenoscyphus fructigenus
Hysterium acuminatum
Hormiactella fusca
Iodophanus carneus
Junewangia globulosa
Keissleriella pinicola
Lachnellula pseudofarinacea
Lachnellula subtilissima
Lentithecium arundinaceum
Linodochium hyalinum
Lophodermium conigenum
Lophodermium pinastri
Mariannaea elegans var. elegans
Menispora ciliata
Mycothyridium vestitum
Mytilinidion mytilinellum
Mollisia cinerea
Monodictys putredinis
Monodyctis levis
Monotosporiella setosa
Nectria cinnabarina
Nitschkia cupularis
Oncopodiella hyperparasitica
Oncopodiella trigonella
Orbilia delicatula
Papulaspora cf. sepidonioides
Paratrichophaea albescens
Penicillium sp.
Periconia sp.
Pezicula eucrita
Phaeoisaria clematidis
Phaeostalagmus cyclosporus
S/lt(t)
S/lt(h)
S/lt(t)
S/lt(t)
S/w
S/lt(t)
B,S/lt(n)
S/lt(t)
S/lt(h,n,t)
S/lt(b,h,t)
S/lt(h)
S/w
S/w
S/lt(t)
S/lt(t),w
S/lt(b,t)
S/lt(t)
S/lt(t)
S/lt(n)
B/l
B/l
S/lt(t)
S/lt(t)
S/lt(t)
S/lt(c),w
S/lt(h),s
S/lt(n)
S/lt(t)
S/w
S/w
S/lt(c)
S/lt(t)
S/lt(t)
Sc/lt(c)
S/w
S/w
B,S/lt(t)
B,S/lt(t)
S/lt(h)
S/lt(n)
B,S/lt(n)
B,S/lt(n)
S/lt(t)
S/lt(t)
S/w
S/w
S/w
S/lt(t)
S/lt(t)
S/lt(t)
B,S/lt(t),w
S/lt(t)
S/w
S/lt(b,t)
S/w
S/lt(b,t)
S/lt(c),w
S/lt(h)
S/lt(h)
B,S/lt(c)
S/lt(b,t)
S/lt(b)
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180
E. Kutorga et al.
Phialocephala humicola
Phialograpium sp.
Pleurophragmium acutum
Pleurotheciopsis brambleyi
Pleurothecium recurvatum
Podosphaera aucupariae
Polyscytalum fecundissimum
Polyscytalum pini
Pseudospiropes obclavatus
Rhinocladiella sp.
Saccobolus versicolor
Scolecobasidium verruculosum
Scutellinia scutellata
Selenosporella curvispora
Septonema fasciculare
Sirococcus strobilinus
Sympodiella acicola
Spadicoides atra
Sphaeropsis sapinea
Sporidesmiella hyalosperma var. hyalosperma
Sporidesmium cf. pedunculatum
Sporidesmium sp.
Sporormiella leporina
Stachybotrys cylindrospora
Taneolella stricta
Tapesia strobilicola
Thysanophora penicillioides
Torula herbarum
Triadelphia heterospora
Triadelphia uniseptata
Trichocladium asperum
Trichoderma viride
Tridentaria sp.
Trimmatostroma betulinum
Trimmatostroma scutellare
Trimmatostroma sp.
Troposporella monospora
Verticicladium trifidum
Verticillium albo-atrum
Xylohypha ferruginosa
Basidiomycota
Amanita citrina
Amanita fulva
Amanita porphyria
Amanita vaginata
Amphinema byssoides
Antrodia sinuosa
Antrodia xantha
Armillaria mellea
Athelia decipiens
Auricularia aurica-judae
Baeospora myosura
Botryobasidium candicans
Botryobasidium obtusisporum
Botryobasidium subcoronatum
Botryobasidium vagum
Ceraceomyces cystidiatus
Clitocybe clavipes
Clitocybe metachroa
Clitocybe nebularis
Collybia butyracea
Collybia confluens
S/lt(t)
S/lt(b)
S/lt(t)
S/lt(b,t)
S/lt(t)
B/l
S/lt(t)
S/lt(n)
S/lt(t)
S/lt(t)
Sc/lt(c)
S/w
S/w
S/lt(t)
S/w
S/lt(c)
S/lt(n)
S/lt(t)
B,S/lt(b,c,n,t)
S/lt(h,t)
S/lt(t)
S/w
Sc/lt(h,t),w
S/lt(b,t)
S/lt(t)
S/lt(c)
S/lt(n)
S/lt(h)
S/lt(b,t)
S/w
S/lt(t)
S/lt(t,n),w
S/lt(t)
S/lt(t)
S/lt(t)
S/w
S/lt(n)
S/lt(n)
S/lt(h,n)
S/lt(t)
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M/s
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B,S/w
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181
Species diversity and composition of fungal communities
Coniophora arida
Cortinarius caperatus
Cortinarius cinnamomeus
Cortinarius sp.
Crucibulum laeve
Cystoderma amiantinum
Cystoderma carcharias
Dacrymyces stillatus
Flammulina velutipes
Fomitopsis pinicola
Galerina marginata
Galerina oedipus
Galerina triscopa
Galerina unicolor
Galerina vittiformis
Gymnopilus bellulus
Gymnopilus penetrans
Gymnosporangium sp.
Hyphoderma argillaceum
Hyphoderma obtusiforme
Hyphoderma pallidum
Hyphoderma praetermissum
Hyphoderma puberum
Hyphoderma subdefinitium
Hyphodontia alutacea
Hyphodontia alutaria
Hyphodontia aspera
Hyphodontia breviseta
Hyphodontia crustosa
Hyphodontia pallidula
Hyphodontia sambuci
Hypochnicium geogenium
Jaapia ochroleuca
Kuehneromyces mutabilis
Laccaria amethystea
Laccaria laccata
Lactarius quietus
Lactarius rufus
Lepista inversa
Lepista irina
Leucogyrophana mollusca
Marasmius oreades
Meruliopsis taxicola
Metulodontia nivea
Mucronella flava
Mycena epipterygia
Mycena filopes
Mycena flavescens
Mycena flavoalba
Mycena galericulata
Mycena galopus
Mycena haematopus
Mycena leptocephala
Mycena maculata
Mycena rorida
Mycena sanguinolenta
Mycena stipata
Mycena vitilis
Mycena zephirus
Oligoporus rennyii
Oligoporus sericeomollis
Paxillus involutus
S/w
M/s
M/s
M/s
S/w
M/s
M/s
S/w
S/w
S/w
S/w
S/lt
S/w
S/lt
S/lt
S/w
S/w
B/l
S/w
S/w
S/w
S/w
S/w
S/w
S/w
S/w
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S/w
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S/w
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S/s
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182
Phanerochaete sordida
Phlebia tremellosa
Phlebiella pseudotsugae
Phlebiella sulphurea
Pholiota flammans
Piloderma byssinum
Piloderma croceum
Pleurotus ostreatus
Pluteus atromarginatus
Pluteus cervinus
Postia caesia
Pseudohydnum gelatinosum
Pseudotomentella tristis
Radulomyces confluens
Resinicium bicolor
Russula emetica
Russula integra
Russula sanguinea
Russula sardonia
Russula vesca
Russula xerampelina
Schizopora paradoxa
Stereum sanquinolentum
Strobilurus esculentus
Stropharia aeruginosa
Tomentella lilacinogrisea
Trechispora cohaerens
Trechispora farinacea
Trichaptum fuscoviolaceum
Tricholomopsis rutilans
Tubulicrinis subulatus
Tylopilus felleus
Vesiculomyces citrinus
Xerocomus badius
Zygomycota
Mortierella sp.
Rhopalomyces elegans var. elegans
E. Kutorga et al.
S/w
S/w
S/w
S/w
S/w
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M/w
S/w
S/w
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S/lt(t)
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.
Species richness in the studied zones conspicuously varied. The highest numbers of
fungal species were recorded in zones A (129 species) and E (120) (Fig. 2), meanwhile species richness in zones B, C and D was about two times lower, 51, 46 and 73
species, respectively.
Distribution of individual fungal species varied strongly within the study area.
Majority of fungi occurred in one (119 species, 46%) or two zones (75 species, 29%).
Only 6 species (2% of all species) were found in all six zones – Arthrobotrys oligospora, Cladosporium herbarum, Endophragmiella pinicola, Sphaeropsis sapinea, Trichoderma viride and Tridentaria sp. Additionally, Erysiphe vanbruntiana and Nectria
cinnabarina were widespread and notably abundant in all zones within the area currently occupied by cormorant colony (zones A-E). Few more species, e.g. Trichocladium asperum, Torula herbarum and Oncopodiella trigonella, were widespread only in
strongly affected forest parts (zones A-D).
The fungal species compositions also differed between the zones. In general, the
comparison of species compositions of different zones showed that their similarity was
rather low (SS: 0.22-0.59) (Tab. 2). The highest similarity was between zones E and G
(0.59), the lowest – between zone G and zones A, B, C, D (SS: 0.22-0.27). Zones A, B,
C, D showed average similarity between each other (SS: 0.33-0.41), except for zones C
and D which were rather similar in fungal species compositions (0.57).
Species diversity and composition of fungal communities
183
Fig. 3. The percent proportion of fungal trophic groups from the sampled zones A-E and G.
Abbreviations of trophic groups as in Table 1.
Trophic structure of fungal communities. Fruiting fungi from main trophic groups
were present in the study area, however, the trophic structure of fungal communities
more or less differed between zones as well (Fig. 3). Only a minor difference in the
percent proportions of trophic groups was detected between scarcely affected forest
zone E and control zone G. Meanwhile, obvious disparity of trophic structure existed between the latter two zones and all the rest of study zones. In the zones B and D,
mycorrhizal species were not found, and their percentage was very low in the zones
A (2%; 3 species: Laccaria laccata, Lactarius rufus and L. quietus) and C (4%; 2 species from the genus Cortinarius) when compared with zones E (17%; 21 species) and
G (17%; 16 species). On the other hand, the percentage of wood-inhabiting fungi
was very high in the zones A and B (both 38%; 50 and 20 species, respectively), but
was rather modest in the zones C (14%; 7 species) and D (19%; 15 species). Four coprophilous species from the genera Ascobolus, Iodophanus, Saccobolus and Sordaria
were notably present on forest litter (not directly on excrements) in the zones B, C
and D, and showed appearance in the zone E.
In total, 15 species of biotrophic fungi were recorded, and the percentage of biotrophs per zone varied from 5% to 12%. Erysiphe vanbruntiana, Nectria cinnabarina,
Podosphaera aucupariae, and Sphaerospis sapinea were common on woody plants,
damaged by bird activity. Facultative biotroph N. cinnabarina strongly infected Sorbus aucuparia, Salix spp., Sambucus spp., Pinus sylvestris and Juniperus communis in
the zones A-D. Needles, bark of twigs and cones of P. sylvestris in the colony were
inhabited by Sphaeropsis sapinea, especially in the zones C and D. Rather common
pine needle-inhabiting endophytes were Cyclaneusma minus and Lophodermium
spp.
Saprobic fungi prevailed in all studied zones, however, their presence percentage was more conspicuous at the starting-point and active parts of the colony
184
E. Kutorga et al.
Table 2
Matrix showing similarity of fungal species compositions between pairs of sampled zones
A-E and G: values of Sørensen (SS) similarity coefficient
Zones
A
B
C
D
E
G
A
1
0.33
0.35
0.41
0.31
0.27
B
C
D
E
G
1
0.41
0.40
0.27
0.24
1
0.57
0.23
0.22
1
0.33
0.27
1
0.59
1
(zones A-D; 84-94%) compared to the only recently occupied and unoccupied by
cormorants forest parts (zones E and G; both 76%). Nearly half of all recorded
fungal species were forest litter decomposers (116 species). These saprobic fungi
inhabiting fallen leaves, needles, cones, small twigs, bark pieces and dead herbs
made up highest number of species in the zone A (69 species), but was lowest in
the zone B (25 species). The most frequent (appeared in at least five zones) litter
saprobes were Arthrobotrys oligospora, Chloridium virescens var. virescens, Cladosporium herbarum, Endophragmiella pinicola, Mycena sanguinolenta, Trichoderma viride, Tridentaria sp. and Verticillium albo-atrum. Notably, Oncopodiella
trigonella, Papulaspora cf. sepidonioides, Phaeoisaria clematidis, Pleurotheciopsis
brambleyi, Torula herbarum, Trichocladium asperum and Triadelphia heterospora
were common exclusively in the zones strongly affected by cormorants (A-D).
Only 3 species out of total 92 species inhabiting wood of trunks, snags, stumps
and large branches were recorded in at least five zones: Ascocoryne sarcoides,
Botryobasidium subcoronatum, and Trichoderma viride. Several wood-inhabiting
species, such as Keissleriella pinicola, Pluteus cervinus, Triadelphia uniseptata, and
Scolecobasidium verruculosum were common only in the zones strongly affected
by cormorants.
DISCUSSION
Our observations show that mycobiota in a Scots pine forest affected by the great
cormorant colony undergo gradual decline reaching extreme impoverishment in the
most active part of the colony. With diminishing influence of birds in the older parts
of the colony, the numbers of fungal species start to grow following changes of vegetation and substrates. However, substrates in the abandoned parts of the colony are
colonized mostly by different species than these of unaffected forest. Fungal species
compositions in recently (year 2011) nested forest (zone E, outer edge of the colony)
and in undamaged forest (zone G, control) are still rather similar and largely maintain widespread and specific species of pine forests of both the Curonian Spit (Kutorga et al. 2012) and the Baltic region. Meantime, the species richness is strongly
declining at the inner edge of the active colony part (zone D) and was conspicuously
(>2 times) decreased at the most active part (zone C). Same effect was observed at
the zone B. Species compositions of these zones also show obvious differences from
the little- or not affected forest parts.
Species diversity and composition of fungal communities
185
The highest number of fungal species (129) was recorded in the zone A. Apparent reason for that is abundance of herbaceous plants, shrubs and dead wood in
this zone in combination with more favourable humidity and light regime, type of
initial (pre-colony) vegetation and decreased present activity of birds (absence of
nests). Therefore in this zone high diversity of litter saprobes and wood-inhabiting
ascomycetes were found, among them Scutellinia scutellata, a moist wood and soil
preferring fungus (Schumacher 1990), recorded exclusively in the zone A. This
zone also harboured rich corticioid and polyporoid wood-inhabiting mycobiota,
agaricoid wood saprobes, such as Pluteus, Mycena, Galerina were common there
as well.
Trophic structure of fungal communities especially strongly reacted to the cormorant colony-induced disturbances. Mycorrhizal species were dramatically reduced by the bird activity, albeit not eliminated totally; a few species from the genera
Laccaria, Lactarius and Cortinarius fruited inside the colony. The change in vitality
of partner trees and in edaphic conditions are the key factors inducing a change
in diversity of mycorrhizal fungi. For example, the absence of fruiting mycorrhizal
fungi in the zone B apparently was due to the absence of living trees. In the zone A,
all pines were dead, but several surviving oak trees enabled a scarce fruiting of few
mycorrhizal species, such as an oak-specific Lactarius quietus. Extremely poor and
sporadic fruiting of mycorrhizal fungi in active part of the cormorant colony (zone
C) was mainly determined by excessive nutrients from bird droppings and to some
extent by the reduced vitality of trees. It is a documented fact that forest fertilization
reduce the activity of mycorrhizal fungi (Ohenoja 1978, 1988; Shubin 1988; Kårén,
Nylund 1997).
The wood-inhabiting fungi depend on amount and quality of dead wood and on
the way the tree die (Stenlid et al. 2008). In our study area the spatial and qualitative differences of dead wood were obvious among the zones. Thus corticioid Botryobasidium subcoronatum which occurred in almost all zones is regarded as host
generalist with no preference to wood decay stage and diameter (Stokland, Larsson 2011). Another corticioid, Hyphodontia sambuci, found only in zone A, have
host preference to Sambucus spp., nitrophilous plants alien in Lithuania. Polypore Oligoporus rennyi confined to medium decayed large-sized coniferous logs
frequently occurred in zone B where logs abounded. Apart from O. rennyi, fallen
pine trunks in zone B harboured a number of other corticioid and polyporoid
species growing on their undersides. Zones C and D lacked fallen large diameter
pine trunks and therefore bore very few wood-inhabiting basidiomycetes, mainly
Mycena species.
In all strongly cormorant-affected zones the stressed woody plants were severely
attacked by biotrophs, such as Nectria cinnabarina, Sphaeropsis sapinea, Podosphaera
aucupariae and Erysiphe vanbruntiana. The latter species together with a weak pathogen Auricularia auricular-judae occurred exceptionally on Sambucus nigra and S.
racemosa, shrubs that were abundant within the colony area.
Unusual substrate/lifestyle switches were noted for several fungus species in the
territory of the colony. Chaetosphaeria ovoidea, Diaporthe eres, Mycothyridium vestitum, Mytilinidion mytilinellum and Nitschkia cupularis usually inhabit dead branches
and twigs of various deciduous trees (Munk 1957; Ellis, Ellis 1997), but in the colony area they were recorded on Pinus sylvestris. In the most active parts of the bird
186
E. Kutorga et al.
colony coprophilous species Ascobolus foliicola, Iodophanus carneus, Saccobolus versicolor and Sporormiella leporina were found on various parts of Pinus sylvestris and
twigs of Sambucus nigra. Most of these fungi usually are common on dung of various
animals, though A. foliicola was also observed on plant remnants and I. carneus –
on decaying anthropogenic substrates (Kutorga 2000; Treigienė 2004). Similar substrate switches were noted for myxomycetes in the cormorant colony (Adamonytė
et al. 2013). Rare hyperparasitic species Oncopodiella hyperparasitica, which usually
inhabits fruit-bodies of Lasiosphaeria spermoides and Athelia epiphylla (Ellis, Ellis
1998), was found on decaying wood of P. sylvestris covered by cormorant excrements
during this study.
Several new species for Lithuania were found during this study. Discomycete
Allophylaria fumosella is little known and rarely collected, pine needles inhabiting
species in Europe, taxonomical position of which remains unclear (Carpenter 1981;
Minter 1981; as Phialina fumosella). Anamorphic ascomycetes Junewangia globulosa, Scolecobasidium verruculosum and Triadelphia uniseptata, which mainly occur
on decaying wood and bark of small branches are found worldwide on various substrates (Ellis, Ellis 1997). Triadelphia heterospora, is a worldwide rare anamorphic
ascomycete which originally was described from submerged balsa wood in South
America (Shearer, Crane 1971) and later found in rainwater collected from Sophora
japonica trees in Hungary (Gönczöl, Révay 2004). In our study it was recorded on
Pinus sylvestris wood in cormorant affected forest parts, in unusual for this species
non-aquatic habitat. Another rare anamorphic ascomycete Dicranidion gracilis was
first described on forest litter from Solomon Islands (Matsushima 1971). Basidiomycete Jaapia ochroleuca, which was found on fallen branch of pine in zone E, inhabits
decaying coniferous wood (Eriksson, Ryvarden 1976) and is sporadically found in
Nordic countries growing on medium-decayed wood with no preference for its dia
meter (Stokland, Larsson 2011).
CONCLUSIONS
This study of the mycobiota in the Scots pine forest affected by the colony of great
cormorants revealed that: 1) species richness of fruiting fungi is reduced in active
part of the colony, 2) the species compositions differed among the colony zones and
their similarity was rather low, 3) the main direct changes in the trophic structure of
fungal communities in the territory occupied by the cormorant colony are the strong
decrease of mycorrhizal species, the appearance of coprophilous fungi on forest litter and of specialized fungi on alien and non-forest plants. This inventory study is
critical to subsequent studies aimed at understanding as to how fungi function as
integral parts of disturbed ecosystems.
Acknowledgements. This study was funded by the grants (No LEK-23/2010, LEK-03/2012) from the Research Council of Lithuania. The authors thank to an anonymous reviewer for valuable comments.
Species diversity and composition of fungal communities
187
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