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Chapter 12
Biogeography and Ecology of Tulasnellaceae
Franz Oberwinkler, Darı
´o Cruz, and Juan Pablo Sua
´rez
12.1 Introduction
Schr€
oter (1888) introduced the name Tulasnella in honour of the French physicians,
botanists and mycologists Charles and Louis Rene
´Tulasne for
heterobasidiomycetous fungi with unique meiosporangial morphology. The place-
ment in the Heterobasidiomycetes was accepted by Rogers (1933), and later also by
Donk (1972). In Talbot’s conspectus of basidiomycetes genera (Talbot 1973), the
genus represented an order, the Tulasnellales, in the Holobasidiomycetidae, a view
not accepted by Bandoni and Oberwinkler (1982). In molecular phylogenetic
studies, Tulasnellaceae were included in Cantharellales (Hibbett and Thorn
2001), a position that was confirmed by following studies, e.g. Hibbett et al.
(2007, 2014).
12.2 Systematics and Taxonomy
Most tulasnelloid fungi produce basidiomata on wood, predominantly on the
underside of fallen logs and twigs. Reports on these collections are mostly
published in local floras, mycofloristic listings, or partial monographic treatments.
F. Oberwinkler (*)
Institut für Evolution und O
¨kologie, Universita
¨tTübingen, Auf der Morgenstelle 1, 72076
Tübingen, Germany
e-mail: franz.oberwinkler@uni-tuebingen.de
D. Cruz • J.P. Sua
´rez
Museum of Biological Collections, Section of Basic and Applied Biology, Department of
Natural Sciences, Universidad Te
´cnica Particular de Loja, San Cayetano Alto s/n C.P, 11
01 608 Loja, Ecuador
©Springer International Publishing AG 2017
L. Tedersoo (ed.), Biogeography of Mycorrhizal Symbiosis, Ecological Studies 230,
DOI 10.1007/978-3-319-56363-3_12
237
Cite: Oberwinkler F, Cruz D, Suárez JP. 2017. Biogeography and
ecology of Tulasnellaceae. Ecol. Stud. 230: 237-271.
Unfortunately, the ecological relevance of Tulasnella fruiting on variously decayed
wood or on bark of trees is not understood. It would appear plausible to assume that
Tulasnella species are involved in wood decay, and that they may function in
anamorphic stages as mycobionts in close by habitats. Therefore it seemed imper-
ative to include in this overview of tulasnelloid mycobionts also reports on
basidiomata.
Though some well developed Tulasnella species can be recognized in the field
by the experienced mycologist with some certainty, correct identification of the
genus was only possible microscopically in pre-molecular times. Most tulasnelloid
fungi were sampled by collectors interested in corticiaceous fungi, Reports on these
collections are mostly published in local floras, mycofloristic listings, or partial
monographic treatments. Some of these publications are used to document biogeo-
graphical patterns on continental scales (Table 12.1). Because of considerable
taxonomic difficulties and inaccuracies in traditional microscopic identification of
Tulasnella morphospecies, they cannot be used for an attempt to disentangle their
distribution areas. However, molecular data may help to overcome this bottleneck.
In several Tulasnella species the hymenial surface has a rosy to faintly viola-
ceous tint (Fig. 12.1). Basidiomata consist of a few basal hyphae with or without
clamps. Normally a simple but rarely considerably thickened hymenium is devel-
oped. Subhymenial structures may be lacking, and consequently single generative
hyphae produce meiosporangia. Such growth forms or developmental stages cannot
be detected in the field. These are only detected microscopically by chance,
growing on the surface of other fungi, especially their hymenia. The growth can
be intrahymenial, e.g. in T. inclusa (Gloeotulasnella i., Christiansen 1959), or,
rather exotically, parasitising on amoebae (T. zooctonica, Drechsler 1969).
The anamorphic stage of Tulasnella has been named Epulorhiza (Moore 1987), and
it has been often used in mycorrhiza studies. Since the concept “One fungus ¼one
name” was implemented at the International Botanical Congress XVIII, Melbourne,
July 2011 (McNeill and Turland 2011; McNeil et al. 2012), the name Epulorhiza
became synonymous. Nevertheless, articles dealing with Epulorhiza are included in our
review, even when it appears uncertain in several cases, whether or not Tulasnella is
involved. For the reason of taxonomic clarity in the following text, a short comment on
the Ceratobasidium-Rhizoctonia complex is included here. In various treatments, the
formal taxonomy of the so-called “form genus Rhizoctonia” has been dealt with
(e.g. Gonza
´lez Garcia et al. 2006; Yang and Li 2012). As pointed out by Oberwinkler
et al. (2013), the name Ceratobasidium can only be applied for Ceratobasidium
calosporum and the genera Koleroga,Oncobasidium,Uthatobasidium,and
Ypsilonidium have to be put under synonymy of Rhizoctonia. The latter one has priority
over Thanatephorus. Unfortunately, these taxonomic re-arrangements were widely
ignored in a recent paper by Go
´nzalez et al. (2016).
Micromorphological characteristics of Tulasnella species include unique basidia
with strongly swollen sterigmata (Fig. 12.1), also called epibasidia, which is a
misleading term. After meiosis in the basidium, haploid nuclei and the basidial
cytoplasm migrate through the sterigmata into the terminally developing basidio-
spores. In the basal position, the sterigmata become secondarily septate. Apically
238 F. Oberwinkler et al.
Table 12.1 Compilation of perfect stages of Tulasnellaceaespecies, arranged according to Fig. 12.2
Regions Europe Asia Af America Pac Aus
Subdivisions N W C E S te tr N C S
Species Spores ●
T. eichleriana Globose–elliptical ●● ●●●● ● ●
T. violea ●● ● ● ●
T. zooctonia ●●
T. cystidiophora ●● ●
T. pacifica ●
T. bourdotii ●●
T. subglobispora ●●
T. hyalina ●●
Pseudotulasnella
guatemalensis
●
T. guttulata
T. traumatica ●●
T. conidiata ●●
T. valentini Oblong–elliptical ●
Stilbotulasnella conidiophora ●
T. albida ●●●●●
T. pinicola ●● ●
T. thelephorea ●● ●●●
T. asymmetrica ●
T. pruinosa ●● ● ●
T. dissitispora Phaseoli-form-subcylin-
drical
●
T. tomaculum ●● ●●● ●●
T. andina ●
T. irregularis ●
T. fuscoviolacea ●●●
T. rubropallens ●● ● ●
T. griseorubella ●●
T. bifrons ●●
T. robusta ●
T. cruciata ●●
T. kirschneri ●
T. pallidocremea ●
T. balearica Sigmoid ●
T. deliquescens ●●
T. quasiflorens ●
T. curvispora Allantoid ●
T. permacra ●
T. allantospora ●● ● ● ● ●
T. danica ●● ●
T. saveloides ●● ●
T. aggregata ●
T. anguifera Spiral ●
T. interrogans ●●
T. falcifera ●
T. helicospora ●● ●
T. calospora Fusiform-subfusi-form ●●●● ●● ● ●
T. eremophila ●
T. kongoensis ●
T. brinkmannii ●
T. pallida ●● ●●●
T. echinospora ●● ●
●records arranged geographically. Ccentral, Eeast, Nnorth, Ssouth, te temperate, tr tropical, Wwest. Literature: Europe: Bresadola
(1903), Bourdot and Galzin (1927), Pearson (1928), Strid (1975), Torkelsen (1977), Hjortstam (1978), Wojewoda (1978, 1983, 1986),
Hauerslev (1989), Roberts (1992, 1993a, b, 1994a, b, 1996, 1999, 2003), Due~
nas (1996, 2001, 2005), Van de Put and Antonissen (1996),
Roberts and Pia˛tek (2004), Ordynets (2012), Kunttu et al. (2015), Polemis et al. (2016). Asia: Do
gan and Kurt (2016). Africa: Crous et al.
(2015). North America: Rogers (1933), Olive (1946). Central America: Roberts (2006). South America: Martin (1939), Lopez (1987),
Greslebin and Rajchenberg (2001), Cruz et al. (2011, 2014, 2016), Nouhra et al. (2013). Pacific area: Olive (1957), Bandoni and
Oberwinkler (1982). Australia: Warcup and Talbot (1967, 1971, 1980). Orig
12 Biogeography and Ecology of Tulasnellaceae 239
partly septate basidia have been reported for Pseudotulasnella guatemalensis
(Lowy 1964). Basidiospores germinate by hyphae or secondary ballistospores.
Dolipores with continuous parenthesomes are a constant ultrastructural feature in
Tulasnella (Fig. 12.1). However, parenthesomes could not be found in dolipores of
Stilbotulasnella conidiophora (Bandoni and Oberwinkler 1982). Other apparently
unique ultrastructural features include cell wall expansions filled with amorphous
matrix (Fig. 12.1). It is unknown whether this character is representative in all or
most of Tulasnella species. Morphological and ultrastructural characters were
indicative of a separate systematic position in former heterobasidiomycetous
fungi, but precise phylogenetic position of Tulasnella within Basidiomycota
remained unsettled.
There is a set of micromorphological characters in Tulasnella species, which
appear to be applicable for circumscribing taxa. However, even in the case of very
accurate microscopic work, there remains much uncertainty about the variability of
structural features. This explains at least partly why reliable species identification is
difficult and quite often questionable. This situation became strikingly evident,
when molecular analyses showed that morphospecies were often not verifiable or
included cryptic taxa (Taylor and McCormick 2008; Cruz et al. 2014). Whether the
finding of Linde et al. (2013) in Australian orchid mycorrhizae, that an eight-locus
analysis is broadly congruent with the solely ITS based result, can be generalized,
remains questionable. For taxonomic details and nomenclature of Tulasnella
Fig. 12.1 Tulasnella violea (a,d) and Tulasnella spp. (b,c): (a) hymenial surface, bar 5 mm; (b)
dolipore with continuous parenthesomes, bar 0.1 μm; (c) spirally growing hypha with cell wall
extensions (arrows), bar 2 μm; (d) section through basidiome with basidia and basidiospores, one
forming a secondary spore, bar 5 μm. From Oberwinkler (2012)
240 F. Oberwinkler et al.
species we refer to Cruz et al. (2014, 2016). Table 12.1 provides an overview about
the basic morphological features and distribution of Tulasnellaceae morphospecies.
12.3 Phylogenetic Position of Tulasnella
A sequence database for the identification of ectomycorrhizal basidiomycetes
included also Tulasnella (Bruns et al. 1998). Tulasnelloid orchid associates clus-
tered with good support within the cantharelloid clade. In an attempt to identify
single pelotons of Dactylorhiza majalis using single-strand conformation polymor-
phism and mitochondrial ribosomal large subunit DNA sequences, Kristiansen
et al. (2001) found two taxa, Tulasnella, and a second one, distantly related to
Laccaria. As sister of the Tulasnella cluster, Sebacina sp. was found, and both
together appeared in a neighbour position to cantharelloid fungi. An expanded
taxon set of basidiomycetes was used by Bidartondo et al. (2003) to resolve the
phylogenetic placement of Aneura (Cryptothallus) associated fungi (see Sect.
12.5.1). They were phylogenetically well supported with T. asymmetrica as a sister
taxon and T. obscura and T. calospora in the same clade. Similar results were
obtained by Kottke et al. (2003), focusing on the mycobiont of Aneura pinguis, and
Weiß et al. (2004) in an approach covering most of heterobasidiomycetous genera
sequenced at that time. Resupinate homobasidiomycetes were analyzed molecu-
larly by Binder et al. (2005), again fitting Tulasnella species to the cantharelloid
clade but without substantial support. The results of Moncalvo et al. (2006) in
analyzing the cantharelloid clade were also ambiguous concerning Tulasnella in
nuc-rDNA and RPB2 together with mtSSU genes. Shimura et al. (2009) sequenced
the Japanese Cypripedium macranthos mycobiont and found a weakly supported
sister relationship to Cantharellus spp. and related taxa, including Sistotrema sp., in
a very limited sampling. In a comprehensive analysis of publicly available
sequences of Ceratobasidiaceae s.l. and related taxa, Veldre et al. (2013) included
also some anamorphic tulasnelloid strains and T. cystidiophora. Both groups
clustered in a sister relationship and were positioned in the Cantharellales. Also
in the review on Agaricomycetes of Hibbett et al. (2014), the Tulasnellaceae are
included in the Cantharellales.
12.4 The Presumable Age of Tulasnella and Evolution
of Plant Associations
Taylor and Berbee (2006) dated Basidiomycota between 1489 and 452 Mya, the
huge timespan resulting from the uncertainty in determining the age of the asco-
mycetous fossil Paleopyrenomycites. A maximum age of the evolutionary root in
Marchantiophyta is calculated for 450 Mya by Clarke et al. (2011), 520–470 Mya
12 Biogeography and Ecology of Tulasnellaceae 241
by Cooper et al. (2012), and 475 Mya by Sun et al. (2014). In a detailed time scale,
Cooper et al. (2012) mark a divergence time of 100–50 Mya for Aneura pinguis and
A. mirabilis. It may be concluded that Tulasnella mycobionts share the same age of
their liverwort photobionts. The second calibration approach of Taylor and Berbee
(2006) was used by Garnica et al. (2016) to determine divergence times in
Sebacinales and other taxa of Basidiomycota. For Cantharellales they found
317–128 Mya with an average of 203 Mya. With some caution, a similar age
interval may be adopted for Tulasnellaceae. Orchids originated approximately
100–80 Mya before present (Givnish et al. 2015), thus indicating a similar age of
their mycobionts, including Tulasnella.
Yukawa et al. (2009) summarized the occurrence of ORM mycobionts in major
clades of the Orchidaceae. Tulasnellaceae were reported from Apostasioideae,
Vanillinae, Cypripedioideae, Disinae, Orchidinae, Goodyerinae, Prasophyllinae,
Diuridinae, Caladeniinae, Neottieae, Dendrobiinae, Malaxideae, Calypsoeae,
Pleurothallidinae, and Cymbidiinae.
12.5 Biotrophic Associations of Tulasnella
12.5.1 Tulasnella Associated with Liverworts
Liverwort mycobionts were examined in the course of an extensive study of
biodiversity in a tropical cloud forest in South Ecuador (Kottke et al. 2003). Aneura
pinguis was associated with Tulasnella species related to T. asymmetrica
(Fig. 12.2), while Jungermanniales (Lophozia spp. and Calypogeia muelleriana)
involved sebacinoid mycobionts. The same sequence group of T. asymmetrica
(AY152406) was recovered in a study on the enigmatic hepatic Aneura mirabilis
(as Cryptothallus mirabilis, Wickett and Goffinet 2008) mycobionts in Europe by
Bidartondo et al. (2003). Aneura mirabilis is a mycoheterotrophic liverwort and
specialized as an epiparasite on Tulasnella species that form ectomycorrhizae with
surrounding trees like Alnus glutinosa,Betula pubescens,Pinus pinaster,
P. muricata or Salix aurita and S. cinerea (Bidartondo et al. 2003). In a geograph-
ically strongly expanded study on liverwort-fungal symbioses, Bidartondo and
Duckett (2010) reported Aneuraceae-associated Tulasnella from Europe, North
and South America, East Asia and New Zealand.
Thallose European and Andean species of Aneuraceae (Metzgeriales) host
Tulasnella mycobionts of high diversity especially in the European samples
(Nebel et al. 2004; Pressel et al. 2010; Preußing et al. 2010). These interactions
were considered by Krause et al. (2011) as a model of early evolved symbiotic
associations. It is most likely that specific Tulasnella species occur together with
the hosts throughout their distribution range.
242 F. Oberwinkler et al.
Fig. 12.2 Dendrogram of Tulasnellaceae species inferred by Jaccard analysis of all available
structures from 48 taxa, including the new species Tulasnella andina and T. kirschneri. Names of
species presented in detail by Cruz et al. (2016) are written in bold. Seven groups are defined,
based on basidiospore morphology. Other characters are indicated by symbols: clamp connections
(unfilled circles), cystidia ( filled circles), chlamydospores ( filled stars). From Cruz et al. (2016)
12 Biogeography and Ecology of Tulasnellaceae 243
12.5.2 Ectomycorrhiza (EcM)
The ectomycorrhizal lifestyle in fungi, including Tulasnella, and dealing with
diversity, distribution and evolution, was reviewed by Tedersoo et al. (2010). In a
study on ectomycorrhizal liaisons between forest orchids and trees in the Bavarian
northern Frankenalb, Bidartondo et al. (2004) mention Tulasnella and tulasnelloid
fungi as “lineages that contain some ectomycorrhizal strains”, however, without
further explanation.
In a wet Tasmanian sclerophyll forest, Tedersoo et al. (2008a) report several
unidentified Tulansella species associated with Eucalyptus regnans (Myrtaceae),
Nothofagus cunninghamii (Nothofagaceae), and Pomaderris apetala
(Rhamnaceae). The authors mention that Tulasnella is commonly observed in
Tasmania but seldom recorded in the Northern Hemisphere as EcM mycobionts.
This comment appears hardly probable for the real ECM occurrence of Tulasnella,
but matches literature information at present. Nevertheless, when studying the
community composition of Picea abies and Betula pendula seedlings in three
Estonian old-growth forests, Tedersoo et al. (2008b) found that “ordination ana-
lyses suggested that decay type determined the composition of EcM fungal com-
munity in dead wood”. In fact, in this study, Tulasnella EcMs were verified for the
first time in the Northern Hemisphere besides the experimental synthesis study of
Bidartondo et al. (2003).
12.5.3 Tulasnella Orchid Mycorrhiza (OM)
In seed germination experiments of orchids, Bernard (1899, 1909) and Burgeff (1909,
1932, 1936) detected the importance of fungal mycobionts during the early develop-
mental stages. At that time, identification of the mycobionts was impossible. In
addition, Burgeff (1932) treated the biology of symbiosis in tropical orchids exten-
sively. After a review of OMs by Rasmussen (2002), Dearnaley (2007) updated new
publications in this field. The trophic relationships in orchid mycorrhizae, including
Tulasnellaceae, and their implications for conservation were summarized by Rasmus-
sen and Rasmussen (2007). In a review on mutualistic, root-inhabiting fungi of orchids,
Kottke and Sua
´rez (2009) compiled also reports of tulasnelloid mycobionts, some of
them associated with epiphytic tropical orchids. The complex of requirements of
germination and seedling establishment in orchids, including tulasnelloid mycobionts,
were comprehensively treated by Rasmussen et al. (2015). Sua
´rez and Kottke (2016)
summarized their overview on ORMs in tropical mountain forests in Ecuador that main
fungal partners, including Tulasnella, correspond to findings in other biomes. Partial
genome sequences of two Tulasnella mycobionts, originating from Australian
Chiloglottis and Drakaea orchid species, may allow to obtain insight in evolutionary
trends of tulasnelloid OM (Ruibal et al. 2013).
244 F. Oberwinkler et al.
12.6 Biogeography of Tulasnella
12.6.1 Europe
Europe has the most abundant records of Tulasnella as fruit-bodies and in molec-
ular identification events from plant roots (Fig. 12.3). Hadley (1970) reported no
specificity of Tulasnella calospora in symbioses tests with European orchids,
Coeloglossum viride,Dactylorhiza purpurella,Goodyera repens and the tropical
Cymbidium canaliculatum,Epidendrum radicans,Laeliocattleya cv., Spathoglottis
plicata, and considered it as a potential universal orchid symbiont. Dijk et al. (1997)
stated that “Epulorhiza repens has been isolated from a vast amount of terrestrial
orchids, and is considered a ubiquitous orchid endophyte”. Tulasnella was the
predominant mycobiont in 59 root samples of seven European and North American
Cypripedium species (Shefferson et al. 2005). In addition, mycorrhizal specificity
of 90 populations of 15 Cypripedium taxa across Europe, Asia, and North America
was quantified by Shefferson et al. (2007). The orchids were associated almost
exclusively with Tulasnellaceae mycobionts.
The mycobiont septal structure of native terrestrial French Dactylorhiza majalis
(Strullu and Gourret 1974) and Italian D. maculata,D. sambucina,andPlatanthera
bifolia (Filipello Marchisio et al. 1985) was studied with the transmission electron
microscope. They authors found dolipores with continuous parenthesomes, suggesting
Sebacina and/or Tulasnella mycobionts, which were finally identified by Andersen
(1990) as T. deliquescens and T. calospora, respectively. A remarkable experimental
approach was carried out by Smreciu and Currah (1989), who studied symbiotic and
asymbiotic germination of seeds of north temperate terrestrial orchids in Europe and
Fig. 12.3 Sampling localities for Tulasnella spp., extracted from literature. Tulasnelloid associ-
ates with liverworts are marked with green dots. Orchid mycorrhizae (red dots) summarize isolates
of Tulasnella from orchid roots and molecularly identified samples. Tulasnelloid ectomycorrhizae
are marked with yellow dots. Lignicolous (blue dots) means that basidiomata were collected on
wood
12 Biogeography and Ecology of Tulasnellaceae 245
North America. The European species included Dactylorhiza maculata,D. sambucina,
Epipactis palustris,E. purpurata,Gymnadenia conopsea,G. odoratissima,Neottia
nidus-avis,Nigritella nigra,andOrchis morio. It appears that mycobionts of these
mostly widespread orchids were predominantly tulasnelloid fungi, except in N. nidus-
avis and E. purpurata. Rasmussen and Rasmussen (1991) tried to identify experimen-
tally the environmental conditions for germination and seedling development in
D. majalis together with T. calospora. A stimulating effect of Tulasnella (Epulorhiza
repens)andRhizoctonia (Ceratorhiza sp.) on the growth of Dutch Dactylorhiza spp.
and Orchis morio was reported by Dijk and Eck (1995). Single-strand conformation
polymorphism and mitochondrial ribosomal large subunit DNA sequences were used
by Kristiansen et al. (2001) to identify T. deliquescens and Laccaria sp. as D. majalis
mycobionts from single pelotons. Various fungal strains, isolated from non orchid
sources were used to test symbiotic germination of British D. fuchsii (Salman et al.
2001). Besides Ceratobasidium cornigerum,alsoT. helicospora stimulated germina-
tion of the orchid seeds and promoted seedling growth. From a wetland of Bavaria,
Bidartondo et al. (2004) reported Tulasnella as a mycobiont of D. majalis. Unidentified
Tulasnella OM symbionts were found in D. baltica,E. atrorubens,andO. militaris in
Estonian mine tailing hills and pristine sites (Shefferson et al. 2008). Most likely the
seed germination experiments of the boreal-alpine D. lapponica, collected from the
Solendet Nature Reserve in Central Norway, were enhanced by tulasnelloid
mycobionts (Øien et al. 2008). In analyzing the mycobionts of five Dactylorhiza
species in Belgium, Jacquemyn et al. (2012) concluded that orchid rarity is related to
mycorrhizal specificity and fungal distribution. In an extensive study of 114 sampled
individuals from one to three populations of 14 species of Dactyorhiza in Belgium,
France, Italy, Portugal, Sweden and the United Kingdom, Jacquemyn et al. (2016b)
suggested that habitat-driven variation occurs in mycorrhizal communities in which
Tulasnella plays an essential role.
Tulasnelloid mycobionts of Epipactis palustris were reported from Northeast
Bavarian wetlands (Bidartondo et al. 2004). Multiple independent colonization
events of former lignite mining areas in Eastern Germany by E. palustris were
documented by Esfeld et al. (2008) and observed in different rockgarden areas of
Tuebingen Botanical Garden by the first author between 1975 and 1995 (unpubl). In
a comparative study of E. helleborine,E. neerlandica, and E. palustris in Belgium,
Tulasnella was only retrieved from the latter photobiont (Jacquemyn et al. 2016a).
In ten North American and European Goodyera species, Tulasnella was only found
in G. pubescens and G. repens in the USA (McCormick et al. 2004; Shefferson et al.
2010). In their study on carbon and nitrogen exchange in Goodyera repens, Liebel
et al. (2015) found Tulasnella and Ceratobasidium as the most frequent mycobionts
of the orchid species.
Fungi from the roots of the common terrestrial orchid Gymnadenia conopsea
included typical ORMs of the Tulasnellaceae and Ceratobasidiaceae as well as several
ectomycorrhizal taxa of the Pezizales (Stark et al. 2009). In this orchid, Te
ˇs
ˇitelova
´et al.
(2013) found evidence that polyploidization can be associated with a shift in their
tulasnelloid mycorrhizal symbionts. Among a variety of ascomycetous and
246 F. Oberwinkler et al.
basidiomycetous associates of Himantoglossum adriaticum, Tulasnellaceae were iden-
tified in two protected areas of Central Italy (Pecoraro et al. 2013).
Liparis loeselii and Hammarbya paludosa are wetland specialists associated
with tulasnelloid mycobionts in Hungary (Illye
´s 2011). In situ and in vitro germi-
nation of L. loeselii were studied by Illye
´s et al. (2005). They found Tulasnella
(Epulorhiza) and Ceratobasidium (Rhizoctonia) as mycorrhizal partners. Broader
samplings with Dactylorhiza incarnata,Epipactis palustris,Gymnadenia
conopsea,Ophrys oestrifera,Op. sphegodes, and Orchis militaris,Or. palustris,
and Or. purpurea indicated Tulasnella associations to prefer wetter habitats (Illye
´s
et al. 2009), or to tolerate a wide spectrum of water availability (Illye
´s et al. 2010).
Here, the question arises, what constrains the distribution of orchid populations
(McCormick and Jacquemyn 2014), a question that should better be modified into
what constrains the distribution of orchid-mycobiont associations. Recently
Jacquemyn et al. (2015b) reported Tulasnellaceae in the roots and the soil of the
green Neottia ovata (Listera ovata) in eastern Belgium. It is noteworthy to mention
that tulasnelloid mycobionts have not been found in the achlorophyllous N. nidus-
avis (e.g. Selosse et al. 2002).
The mycorrhizal fungal diversity of Orchis militaris, including tulasnelloid
associates, detected in some Hungarian habitats, is considered to be essential for
the wide ecological range of the orchid species (Ouanphanivanh et al. 2007). In a
multidisciplinary approach of the simultaneously investigated mediterranean
Orchis simia,O. anthropophora, and their hybrid O. bergonii, Schatz et al.
(2010) compared leaf growth, seed viability, emitted scent, and mycorrhizal species
and their rate of infection. The mycobionts were unidentified Tulasnella species.
Five Orchis species, O. anthropophora,O. mascula,O. militaris,O. purpurea, and
O. simia, sampled from the Netherlands to Italy by Jacquemyn et al. (2010),
contained a majority of Tulasnella mycobionts. In three closely related and hybrid-
izing species, O. anthropophora,O. militaris, and O. purpurea, the influence of
mycorrhizal associations on reproductive isolation of the orchids appeared to be of
minor importance (Jacquemyn et al. (2011a). Girlanda et al. (2011) reported
Tulasnella calospora mycobionts in the mediterranean meadow orchids Ophrys
fuciflora,Anacamptis laxiflora,O. purpurea, and Serapias vomeracea. In a com-
prehensive survey of 16 European and Mediterranean Orchis species, Jacquemyn
et al. (2011b) found dominating Tulasnella OMs from the Netherlands, Belgium,
France, Portugal, Italy, Cyprus, and Israel. For the persistence and rarity of A. morio
and Dactylorhiza fuchsii in Belgian habitats, Bailarote et al. (2012) suggested that
fungal diversity with dominating Tulasnella are not necessarily related. Studies
conducted in the Gargano National Park in southern Italy by Jacquemyn et al.
(2014, 2015a) comprised Anacamptis pyramidalis,A. (Orchis)morio,
A. papilionacea,Neotinea maculata,N. ustulata,Orchis anthropophora,
O. italica,O. pauciflora,O. provincialis,O. quadripunctata,Ophrys apulica,Op.
biscutella,Op. bombyliflora,Op. sphegodes,Op. sicula,Op. tenthredinifera,
Serapias bergonii,S. cordigera,S. lingua, and S. vomeracea. The mycobionts of
coexisting orchid species had distinct mycorrhizal communities and were predom-
inantly recruited by Tulasnella and Rhizoctonia (“Ceratobasidiaceae”). A broad
12 Biogeography and Ecology of Tulasnellaceae 247
spectrum of mycobionts, including Tulasnella, were found to be associated with
O. tridentata in Central Italy by Pecoraro et al. (2012). The temporal variation in
mycorrhizal diversity of A. morio from North Italian meadows was analysed by
Ercole et al. (2014). The fungi, manually isolated from pelotons, were common
Tulasnella in autumn and winter, the pezizacean clade very frequent in spring, and
Ceratobasidium more frequent in summer. In 16 Mediterranean orchid species of
the genera Anacamptis,Ophrys,Orchis, and Serapias, Pellegrino et al. (2014)
found 18 operational taxonomic units (OTUs) of Tulasnella and
“Ceratobasidiaceae”. Mycobiont analyses of the mediterranean Op. bertolonii
revealed Tulasnella as the dominant fungal partner (Pecoraro et al. 2015). The
fine-scale spatial distribution of OM fungi, including Tulasnella, in soils of host-
rich mediterranean grasslands of northern Italy was screened by Voyron et al.
(2016) and found to be extremely sporadic. The spatially tight dependency of
tulasnelloid associates of orchids was clearly documented in populations of
A. morio,Gymnadenia conopsea, and O. mascula in Southern Belgium (Waud
et al. 2016a). Also in Belgium, the majority of mycobionts of O. mascula and
O. purpurea appeared to be Tulasnella (Waud et al. 2016b).
Bidartondo et al. (2004) reported Tulasnella as mycobiont of Platanthera
chlorantha from the Bavarian Frankenalb. In a study on the evolution of endemic
Azorean orchids, also ORMs were analyzed, and T. calospora and Tulasnella spp.
were found in Platanthera species (Bateman et al. 2014). Kohout et al. (2013)
studied the fungal communities associated with Pseudorchis albida in the S
ˇumava
National Park, Czech Republic. The mycobionts of the orchid were four unnamed
Tulasnella strains. In protocorms of P. albida, also from this country, and in
Serapias parviflora from Sardinia, Tulasnella spp. were detected by St€
ockel et al.
(2014). Protocorms of the mediterranean orchid Serapias vomeracea were colo-
nized by Tulasnella calospora in an experimental study of Balestrini et al. (2014).
12.6.2 Temperate Asia
Whole rDNA analyses of roots and leaves of Bletilla ochracea from a mountain
near Guiyang in Guizhou Province, China, provided a high number of fungal OTUs,
dominated by ascomycetes (Tao et al. 2008). In addition, also Epulorhiza sp. could
be identified. Eom (2012) isolated T. calospora,T. irregularis, and Tulasnella
sp. from terrestrial Korean Bletilla striata,Calanthe discolor,Cymbidium
goeringii, and Pogonia minor. Eom (2015) identified T. calospora and Tulasnella
sp. in Cephalanthera falcata,C. longibracteata,Platanthera chlorantha, and
P. mandarinorum in Korea. Jiang et al. (2011) isolated Tulasnella spp. from
Changnienia amoena, an orchid distributed in various provinces of Central China.
Lee and You (2000) identified Tulasnella repens in the native Korean Cymbid-
ium goeringii. Korean species of Cymbidium were successfully inoculated with
Tulasnella repens by Lee et al. (2001). In a comparative study, Ogura-Tsujita et al.
(2012) tried to find a correlation in mycobiont’s association in Cymbidium during
248 F. Oberwinkler et al.
the evolution of autotrophy to mycoheterotrophy. Tulasnella dominated in the
autotrophic C. dayanum, were less frequent in mixotrophic C. goeringii and
C. lancifolium and absent in mycoheterotrophic C. macrorhizon and C. aberrans.
In five Korean terrestrial orchids, C. goeringii,Spiranthes sinensis,Calanthe
discolor,Bletilla striata, and Pogonia minor, Youm et al. (2012) identified
Tulasnella calospora,T. irregularis,T. sp., and Sebacina vermifera.
The mycobiont of the threatened orchid Cypripedium macranthos var.
rebunense, from Rebun Island northwest of Hokkaido was identified as Tulasnella
(Shimura et al. 2009). Mycobionts of six endangered slipper orchid species from
Southwestern China, Paphiopedilum micranthum,P. armeniacum,P. dianthum,
Cypripedium flavum,C. guttatum, and C. tibeticum, were identified as Tulasnella
spp. by Yuan et al. (2010). Hayakawa et al. (1999) isolated Tulasnella deliquescens
from naturally occurring protocorms, seedlings, and adult Japanese Dactylorhiza
aristata. Most of the OM fungi in Dendrobium fimbriatum and D. officinale from
Guangxi were identified as members of the Tulasnellaceae by Xing et al. (2013).
Tan et al. (2014) used their Tulasnella isolates of D. officinale from Yunnan to carry
out seed germination experiments. They found different interactive capacities in
two fungal strains.
As mycobionts of Epipactis thunbergii, Eom and Kim (2013) identified i. a.
T. calospora and Tulasnella sp. E. thunbergii and Habenaria radiata were colo-
nized by the ecologically adapted, associated with various mycobionts in manmade
wetlands in the Hiroshima Prefecture, Japan (Cowden and Shefferson 2013). While
a diverse suite of fungal symbionts was found in H. radiata,E. palustris was nearly
exclusively inhabited by Tulasnella spp. Based on the morphology and cultures of
isolates with anastomoses, Uetaka et al. (1999) identified Epulorhiza repens in the
Japanese terrestrial orchids Gymnadenia camtschatica,Platanthera tipuloides and
Pogonia japonica. In nine species of the genus Holcoglossum from Yunnan and
Guangxi, T. calospora and the anamorphic tulasnelloid Epulorhiza were found (Tan
et al. 2012). From different populations of Liparis japonica in Northeast China,
Ding et al. (2014) identified fungi of the T. calospora species group. In situ and
in vitro specificity between mycobionts and Spiranthes sinensis var. amoena was
analyzed by Masuhara and Katsuya (1994). The germination was mainly induced
by Tulasnella (as Rhizoctonia repens).
12.6.3 Subtropical and Tropical Asia
Apostasioideae are considered the basal group of the Orchidaceae (Chase et al.
2003). Five studied Apostasia species had Botryobasidium and Ceratobasidium
mycobionts, and the related Neuwiedia veratrifolia was associated with
Ceratobasidium and Tulasnella (Yukawa et al. 2009). Most of the mycobiont
isolates of Neuwiedia veratrifolia, collected in Borneo, could be assigned to
Tulasnella by Kristiansen et al. (2004).
12 Biogeography and Ecology of Tulasnellaceae 249
The mycobiont of the “Chinese King Medicine Orchid”, Anoectochilus
roxburghii, was identified as Epulorhiza sp. and was successfully used in
co-culture experiments to improve the growth of the host plant (Li et al. 2012).
Dan et al. (2012) found that eight of 42 OM fungal strains tested including three
Epulorhiza spp. enhanced the growth of the host plantlets. The endophyte promot-
ing the growth and contents of kinsenosides and flavonoids of A. formosanus was
identified as Epulorhiza sp. by Zhang et al. (2013). Likewise, in seven localities of
Taiwan, Jiang et al. (2015) isolated mycobionts of this medicinally used orchid. No
increase in orchid seed germination was found when Tulasnella strains were
applied that clustered in clade III of their study. Mycobionts of the Chinese
medicinal orchid Dendrobium officinale were identified as Epulorhiza sp. and
inoculation of the fungus resulted in promoted seedling growth (Jin et al. 2009).
For symbiotic seed germination of D. draconis and Grammatophyllum speciosum,
native orchids of Thailand, the anamorph of Tulasnella calospora proved to be most
effective to stimulate protocorm development (Nontachaiyapoom et al. 2011). In
contrast, Salifah et al. (2011) found that seed germination rates in this orchid were
best when co-cultured with Fusarium sp. Five Tulasnella isolates of four
Dendrobium species from Chiang Rai Province of Thailand showed different
promoting effects on seed germination (Swangmaneecharern et al. 2012). The in
situ seed baiting of the epiphytic D. aphyllum from the Xishuangbanna tropical
Botanical Garden in South Yunnan, studied by Zi et al. (2014), revealed Tulasnella
spp. as mycobionts. In contrast, Agustini et al. (2016) isolated Rhizoctonia-like
fungi from D. lancifolium var. papuanum and Calanthe triplicata from Papua,
which was considered of “Ceratobasidium” relationship. Khamchatra et al.
(2016a) isolated T. violea and Epulorhiza repens from the Thai epiphytic
D. friedricksianum. Under in vitro culture conditions, Wang et al. (2016) found
promoted D. catenatum seedling growth from Hainan with dual inoculation of
Epulorhiza and Enterobacter or Herbaspirillum bacteria.
Commercially grown Thai species and hybrids of Cymbidium,Dendrobium, and
Paphiopedilum were used by Nontachaiyapoom et al. (2010) for isolation of
mycobionts. They identified Tulasnella anamorphs. Tulasnella spp., isolated from
wild and horticulturally grown Cymbidium spp. in SW-China, were used to test
growth differences in co-cultures with C. hybridum, an important pot ornamental
orchid (Zhao et al. 2014a). In addition, deep sequencing-based comparative tran-
scriptional profiles of these photo- and mycobionts were carried out (Zhao et al.
2014b). The positive experiments were indicative for application in Cymbidium’s
commercial cultivation. Mycobionts of C. faberi,C. goeringii, and C. goeringii var.
longibracteatum, also from SW-China, included Tulasnella spp. (Huang and Zhang
2015). Yu et al. (2015) isolated and identified endophytes, and Tulasnella ORMs
from roots of C. goeringii and C. faberi.
The germination and development of the terrestrial Arundina chinensis,
Spathoglottis pubescens, and Spiranthes hongkongensis from various locations of
Hong Kong were found to be strongly stimulated by Epulorhiza isolates (Shan et al.
2002). Isolated E. repens from the Thai terrestrial S. plicata enhanced seed germi-
nation in vitro considerably (Athipunyakom et al. 2004a). From this orchid species
250 F. Oberwinkler et al.
of Papua, Sufaati et al. (2012) reported Tulasnella mycobionts. In a study on
mycorrhizal associations and root morphology of 31 terrestrial and epiphytic
orchids species of the Western Ghats, southern India, also S. spicata was included
(Sathiyadash et al. 2012). Regarding the mycobionts, there is only the single remark
that the orchids “had moniliform structures resembling those of Tulasnella
calospora (Epulorhiza repens) in the cortical and root hair cells”.
In the endangered epiphytic Thai slipper orchid Paphiopedilum villosum,
Tulasnella sp. could be identified as mycobiont (Khamchatra et al. 2016b). A highly
compatible Epulorhiza strain was used to demonstrate promotion of seed germina-
tion and protocrom development in Papilionanthe teres from Xishuangbanna,
South China (Zhou and Gao 2016). In seed germination and seedling development
of the Thai terrestrial orchid Pecteilis susannae, the incubation of Tulasnella
enhanced growth considerably (Chutima et al. 2011). Isolates from the tropical
orchids Arachnis sp., Arundina graminifolia,Dendrobium crumenatum,
Diplocaulobium enosmum,Oncidium hybr., Vanda hybr., and Spathoglottis plicata
in Singapore comprised both Sebacina and Tulasnella mycobionts (Ma et al. 2003).
Mycobionts isolated from pelotons of Calanthe rubens, Ca. rosea,Cymbidium
sinense,Cy. tracyanum,Goodyera procera,Ludisia discolor,Paphiopedilum
concolor,P. exul,P. godefroyae,P. niveum and P. villosum were identified as
Epulorhiza calendulina,E. repens,and Tulasnella sp. among multiple mycobionts
(Athipunyakom et al. 2004b). Suryantini et al. (2015) reported on Epulorhiza and
Tulasnella spp. associated with epiphytic Ca. vestita and Bulbophyllum beccarii
from West Kalimantan. Seed germination of the epiphytic, therapeutically valuable
orchid Coelogyne nervosa, endemic to south India, was higher when inoculated
with Epulorhiza sp. (Sathiyadash et al. 2014).
12.6.4 North America
Rhizoctonia anaticula was described by Currah (in Currah et al. 1987), based on
five isolates of native Alberta orchids, and later transferred into the tulasnelloid
anamorphic genus Epulorhiza (Currah et al. 1990). The same mycobiont was also
isolated from Calypso bulbosa and Platanthera obtusata sampled in various loca-
tions of Alberta (Currah and Sherburne 1992; Currah et al. 1988). The TEM
micrographs indicate tulasnelloid fungi (Currah and Sherburne 1992). Smreciu
and Currah (1989) recovered potentially high percentage of tulasnelloid
mycobionts in symbiotic and asymbiotic germination of seeds of north temperate
terrestrial orchids Amerorchis rotundifolia, Ca. bulbosa,Coeloglossum viride,
Corallorhiza maculata,Co. trifida,Cypripedium calceolus,Goodyera repens,
Platanthera hyperborea,P. obtusata, and P. orbiculata, four of them also occurring
in Europe. So far, it remains unsettled what Ceratobasidium cereale, a mycobiont
of G. repens, is (Peterson and Currah 1990). In germination experiments of
P. hyperborea seeds, mycobionts of uncertain taxonomic position, like Rhizoctonia
cerealis or Ceratorhiza goodyerae-repentis, were used (Richardson et al. 1992).
12 Biogeography and Ecology of Tulasnellaceae 251
The orchid–mycobiont association was studied in detail in Goodyera repens,a
terrestrial orchid of the eastern United States (McCormick et al. 2006). It was found
that protocorms and adult orchids were able to switch with closely related
Tulasnella fungi. In germination tests of seeds of Goodyera discolor,Liparis
liliifolia and Tipularia discolor, McCormick et al. (2012) used fungal strains
isolated from adult orchids and found that Tulasnella was involved in all cases.
Shefferson et al. (2005) detected Tulasnella spp. in root samples of Cypripedium
californicum,C. fasciculatum and C. montanum in California; C. candidum and
C. parviflorum in Illinois and Kentucky, C. guttatum in Alaska. Whitridge and
Southworth (2005) reported Tulasnellaceae associated with Cypripedium
fasciculatum, and with Piperia sp. One of the rarest North American terrestrial
orchids, Piperia yadonii, showed non-specific ORMs, including Tulasnellaceae
(Pandey et al. 2013). In Encyclia tampensis of South Florida, Zettler et al.
(2013), reported T. irregularis as mycobiont and essential fungal partner during
seed germination. The symbiotic germination of Spiranthes lacera, with a naturally
occurring endophyte, Ceratorhiza cf. goodyerae-repentis, and with Epulorhiza
repens was tested by Zelmer and Currah (1997). The orchid occurs in the eastern,
northern and central parts of North America. The symbiotic germination of
S. brevilabris showed Epulorhiza mycobionts, and the reintroduction of the endan-
gered orchid, native to Florida, was discussed by Stewart et al. (2003).
In an integrated approach to Rhizoctonia taxonomy, Mordue et al. (1989)
succeeded in taxonomically separating orchid isolates, i.e. tulasnelloid mycobionts
from other Rhizoctonia-like fungi. A key and notes for the genera of fungi,
mycorrhizal with orchids, and a new species in the genus Epulorhiza, was provided
by Currah and Zelmer (1992). Ceratorhiza pernacatena and Epulorhiza
calendulina were described as mycorrhizal fungi of terrestrial orchids in the
Canadian prairies by Zelmer and Currah (1995), tulasnelloid mycobionts at least
in one case. Epulorhiza inquilina was proposed for the mycobiont of the mature
orchids Platanthera clavellata,P. cristata and P. integrilabia in Canada (Currah
et al. 1997). For the propagation of the auto-pollinated terrestrial P. clavellata in the
southern Appalachians, Epulorhiza spp. strains were applied in vitro by Zettler and
Hofer (1998). In P. praeclara of midwestern prairies, Epulorhiza and Ceratorhiza
were found and used in symbiotic seed germination and coinoculations by Sharma
et al. (2003a, b). Also in the endangered Hawaiian endemic Platanthera
leucophaea,Epulorhiza was found as mycobiont (Zettler et al. 2005).
Seeds of the endangered epiphytic orchid Epidendrum nocturnum from Florida
were germinated in vitro with Epulorhiza repens (Massey and Zettler 2007; Zettler
et al. 2007). Mycorrhized seedlings could successfully be reintroduced in the
Florida Panther National Wildlife Refuge. Symbiotic seed germinations of three
semi-aquatic orchids, Habenaria macroceratitis,H. quniqueseta, and H. repens
from Florida had Epulorhiza mycobionts (Stewart and Zettler 2002). Later, in
H. macroceratitis, Stewart and Kane (2006) isolated six Epulorhiza strains.
Epulorhiza sp. was present in seed germination of H. repens in situ beyond its
range in southern North America (Keel et al. 2011).
252 F. Oberwinkler et al.
12.6.5 Central and South America
Unfortunately, in their study on basidiomycetous endophytes from the roots of
epiphytic orchids in La Selva, Costa Rica, Richardson et al. (1993) use the generic
names Moniliopsis and Ceratorhiza for the isolates. Though it is most likely that
Tulasnella is included in these fungi, verification is impossible. Otero et al. (2002)
isolated Rhizoctonia-like fungi inclusive of Tulasnella from orchids in Puerto Rico.
They included the epiphytic species Campylocentrum fasciola,C. filiforme,
Ionopsis satyrioides,I. utricularioides,Psychilis monensis,Tolumnia variegata,
and the terrestial Erythrodes plantaginea,Oeceoclades maculata, and Oncidium
altissimum. In Brazil, Epulorhiza epiphytica was isolated from mycorrhizal roots of
epiphytic orchids and described as a new tulasnelloid anamorph by Pereira et al.
(2003), and additional ORMs from neotropical orchids were characterized mor-
phologically and molecularly by Pereira et al. (2005b), and for Laeliinae by
Almeida et al. (2007).
Kottke et al. (2008) used sequence data of Tulasnella and other mycobionts to
interprete fungal networks between diverse photobionts, including epiphytic
orchids and Aneuraceae. Mosquera-Espinosa et al. (2010) studied 12 fungal isolates
of eight Colombian orchids and reported Ceratobasidium spp. as mycobionts.
However, a proper taxonomic identification was not achieved. Mycorrhizal net-
works with prominent Tulasnella OM mycobionts were considered to promote and
stabilize the neotropical mountain rain forest (Kottke et al. 2013). Cruz et al. (2014)
analyzed the variability of micromorphological features of basidiomata and the
genomic polymorphism of Tulasnella ORMs in South Ecuadorian orchid species of
the genera Elleanthus,Maxillaria,Pleurothallis,Prostechea, and Stelis. From five
terrestrial orchids of Co
´rdoba, Argentina, Aa achalensis,Cyclopogon elatus,
Habenaria hexaptera,Pelexia bonariensis, and Sacoila australis, Ferna
´ndez Di
Pardo et al. (2015) isolated various mycobionts, including Epulorhiza.Sua
´rez and
Kottke (2016) summarized main mycobionts, including Tulasnella, and their spec-
ificities in neotropical orchids of South Ecuadorian rain forests. In an Andean cloud
forest of South Ecuador, Sua
´rez et al. (2006) found that diverse tulasnelloid fungi
form mycorrhizae with epiphytic Pleurothallis lilijae,Stelis concinna,S. hallii, and
S. superbiens. A study of Sua
´rez et al. (2016) in Ecuador revealed that Teagueia
spp. were associated with members of Tulasnellaceae, corresponding to four OTUs.
All detected mycobionts had a wide geographical distribution.
Experiments for a symbiotic propagation to reintroduce endangered Mexican
terrestrial Bletia urbana,B. campanulata, and Dichromanthus aurantiacus were
carried out by Ortega-Larrocea and Rangel-Villafranco (2007), applying anamor-
phic Tulasnella strains. Ovando et al. (2005) isolated and screened endophytic fungi
from the roots of the epiphytic orchids Brassavola nodosa,Cattleya skinneri, and
C. aurantiaca from Tuzanta
´n, South Mexico. The isolated strains were assigned to
11 fungal genera. Eight strains, used for germination experiments, did not show any
promoting effects. However, three strains, including Epulorhiza, provided mycor-
rhizal characteristics in C. aurantiaca. A new tulasnelloid anamorph, Epulorhiza
12 Biogeography and Ecology of Tulasnellaceae 253
amonilioides, lacking monilioid hyphae in pure culture, was isolated from
Brassavola and Encyclia species and described by Almeida et al. (2014) from
Bahia, Brazil. When analyzing three sympatric epiphytic Cymbidieae, Cyrtochilum
flexuosum,C. myanthum, and Maxillaria calantha from two sites of South Ecua-
dorian mountain rain forests, Cevallos et al. (2016) concluded that these orchids
have site-adjusted OM communities with keystone mycobionts, including
Tulasnella. In testing seed germination and protocorm development of
Cyrtopodium glutiniferum from Brazil, Pereira et al. (2015) found promotion by
mycorrhizal fungi of the tulasnelloid anamorphs Epulorhiza spp. In roots of four
Vanilla species from Puerto Rico, Costa Rica and Cuba, Porras-Alfaro and Bayman
(2007) found mycobionts of Ceratobasidium,Thanatephorus and Tulasnella.
Epulorhiza spp. was isolated from various Brazilian Epidendrum species (Pereira
2009, Pereira et al. 2009, 2011a, b, 2014a). From the epiphytic E. stamfordianum,
Erycina crista-galli,andStelis quadrifida from Southeast Chiapas, Mexico,
Ceratorhiza and Epulorhiza mycobionts were reported by Cruz Blası
´(2007). Two
different Tulasnella species were found to be associated with South Ecuadorian
E. rhopalostele, an orchid preferably growing on dead trees (Riofrı
´o et al. 2013).
Populations of E. firmum in Costa Rica had highly diverse and spatially heterogeneous
mycobionts, including six Tulasnella strains (Kartzinel et al. 2013). The mycobionts of
E. secundum, a widespread Brazilian orchid, were identified as Tulasnella spp. by
Pereira et al. (2014a) and as T. calospora by Nogueira et al. (2014). In vitro seed
germination and protocorm development of Brazilian Oncidium flexuosum was studied
with mycobionts of Epulorhiza and Ceratorhiza, earlier isolated from this orchid
(Pereira et al. 2005a, c), and Da Silva Coelho et al. (2010) reported regeneration and
production of the fungal protoplasts.
Epulorhiza epiphytica was isolated from Polystachya concreta and the African
Oeceoclades maculata, naturalized in the Neotropics, by Pereira et al. (2005b).
Nine unnamed morphotypes of fungi, associated with O. maculata, were isolated
from the understory of Avocado in Brazil by Teixeira et al. (2015).
In the mycorrhizal association of the terrestrial Chilean orchid Bipinnula
fimbriata also tulasnelloid ORMs were present (Steinfort et al. 2010). Mujica
et al. (2016) found that mycorrhizal diversity, including Tulasnella, decreased in
habitats of B. fimbriata and B. plumosa with higher N, but increased with P
availability in B. fimbriata. Morphological and molecular characterization con-
firmed that Chilean Chloraea collicensis and C. gavilu mycorrhizal partners belong
to Tulasnella (Pereira et al. 2014b). In contrast, Atala et al. (2015) reported
mycobionts with possible Thanatephorus teleomorphs from the critically endan-
gered Chilean C. cuneata. However, the data presented cannot exclude tulasnelloid
associates. In a study by Herrera et al. (2016), in six Chloraea species and Bipinnula
fimbriata from Chilean Coastal Range and Andes. Tulasnella spp. were found as
dominating mycobionts. Fracchia et al. (2014) found promoted see germination
through tulasnelloid and Ceratobasidium-like fungi in Gavilea australis, an endan-
gered terrestrial orchid from south Patagonia.
254 F. Oberwinkler et al.
12.6.6 Africa
Martos et al. (2012) identified a bipartite network including 73 orchid species and
95 taxonomic units of mycorrhizal fungi across the natural habitats of Reunion
Island. 58 tulasnellaceous OTUs were found in 73 orchid species, thus representing
the most frequent OM mycobionts. In their study on the evolution of endemic
Azorean orchids, Bateman et al. (2014) reported also the mycorrhizal association of
Tulasnella aff. Calospora with Platanthera algeriensis in Morocco. Most of the
OM fungi of the Itremo region in the Central Highlands of Madagascar were
identified as Tulasnella (Yokoya et al. 2015). The symbiotic seedling development
of the terrestrial Cynorkis purpurea, also from the Itremo area, has been tested
experimentally by Rafter et al. (2016). Though epiphyte-derived Sebacina cultures
had the strongest influence, also Tulasnella appeared as an advantageous
mycobiont. Disa bracteata of South Africa was associated with Tulasnella spp. in
West and South Australia as in its country of origin (Bonnardeaux et al. 2007). In an
attempt to elucidate the impact of above- and belowground mutalisms in
South African orchid diversification, an irregular pattern of fungal associates,
including 35, unspecified Tulasnella individuals, were detected (Waterman et al.
2011). The authors concluded that “shifts in fungal partner are important for
coexistence but not for speciation” of the host plants.
12.6.7 Australia
When Warcup and Talbot (1967) succeeded to isolate and cultivate OM fungi from
terrestrial Australian orchids, and finally obtained perfect states of Rhizoctonias, a new
era of experimental mycology and especially of studies in symbiotic systems began.
Tulasnella calospora was found to be the perfect state of three cultures considered to be
Rhizoctonia repens. Isolates were obtained from South Australia (Acianthus exsertus,
Caladenia reticulata,Cymbidium canaliculatum,Dendrobium sp., Diuris longifolia,
D. maculata,andThelymitra antennifera). Tulasnella asymmetrica was described as a
new species and as mycobiont of Thelymitra luteocilium from the Australian Mt. Lofty
Range. In a second contribution of the authors (Warcup and Talbot 1971), the
description of Tulasnella asymmetrica was emended and further orchid hosts were
reported from the Mt. Lofty Range: Thelymitra aristata (also Cape Jervis),
T. grandiflora,andT. pauciflora. Additional hosts were Th. epipactoides (Eyre
Peninsula), and Dendrobium tetragonum from North Queensland. The basidial stage
of the morphotype of T. allantospora with clamps was obtained from Mt. Lofty isolates
of Corybas dilatatus, and basidiocarp samples without clamps were collected on fallen
Eucalyptus wood in the same locality. The perfect stage of T. violea developed from an
isolate obtained from Th. aristata, collected in Uley, Eyre Peninsula. Tulasnella
cruciata was introduced as new to science, isolated from the Mt. Lofty Range orchids
Acianthus caudatus and Th. pauciflora, while the strain of Th. fusco-lutea originated
12 Biogeography and Ecology of Tulasnellaceae 255
from Pomonal, Victoria. In the third joint effort of Warcup and Talbot (1980) to obtain
perfect states of OM mycobionts they succeeded with T. irregularis sp. nov., isolated
from Dendrobium dicuphum, sampled near Darwin, Northern Territory. In studying
the specificity of ORMs in Australian terrestrial orchids, Warcup (1971) reported that
Th. aristata is at least associated with three species of Tulasnella. In the “Orchids of
South Australia” (Bates and Weber 1990), T. calospora is listed as mycobiont in orchid
species of the genera Acianthus,Diuris,Orthoceras,andThelmytra. For the latter one
and Acianthus,alsoT. cruciata is mentioned. The symbiotic germination of some
Australian terrestrial orchids was analyzed by Warcup (1973) who reported that various
isolates of T. calospora differed markedly in the efficiency with which they stimulated
germination of the Diuris and Thelymitra photobionts. A close association of this
mycobiont with Diuris and Orthoceras orchids was confirmed by Warcup (1981).
The mycorrhizal specificity of D. fragrantissima with Tulasnella spp. and persistence
in a reintroduced population west of Melbourne was studied by Smith et al. (2007,
2010). In D. magnifica and Prasophyllum giganteum,T. calospora was found, and in
Pyrorchis nigricans isolates T. danica were identified (Bonnardeaux et al. 2007).
A narrow group of monophyletic Tulasnella symbiont lineages is associated
with multiple species of Chiloglottis in New South Wales and the Australian
Capital Territory (Roche et al. 2010). For Tulasnella OM species delimitation in
the Australian orchid genera Chiloglottis,Drakaea,Paracaleana and Arthrochilus,
Linde et al. (2013) used six nuclear loci, two mitochondrial loci, the photo- and
mycobiont association and sampling locations in an integrated approach. They
found that the Chiloglottis isolates belong to one species, and those from Drakaea
and Paracaleana to a sister taxon, a result in accordance with previous ITS
analyses. Boddington and Dearnaley (2009) reported a putative mycorrhizal
Tulasnella-like fungus in the tropical epiphytic Dendrobium speciosum of
Queensland. In studies of Drakaea species in Southwest Australia, Phillips et al.
(2011, 2014) found no evidence that Tulasnella specificity contributed to the rarity
of the orchids.
According to Brundrett (2007), most West Australian orchids studied have
highly specific mycorrhizal associations with fungi in the Rhizoctonia alliance,
most likely including Tulasnella spp. The nutrient-acquisition patterns of ORMs,
inclusive of Tulasnella, appear to explain the diversification in terrestrial orchids in
this biodiversity hotspot (Nurfadilah et al. 2013).
Milligan and Williams (1988) obtained 27 tentatively identified Tulasnella
calospora isolates from Microtis spp. at seven sites in the Sydney region. The
specificity of associations between M. parviflora and Epulorhiza spp. was studied
by Perkins et al. (1995). The compatibility webs of brief encounters, lasting
relationships and alien invasions of West Australian terrestrial orchids were studied
by Bonnardeaux et al. (2007), documenting that M. media, together with the
invasive Disa bracteata, had the most ORMs. Mycorrhizal preference apparently
promotes habitat invasion of M. media in Western Australia (De Long et al. 2013).
When studying the effects of endophytic fungi on New Zealand terrestrial
M. unifolia,Spiranthes novae-zelandiae, and Thelymitra longifolia, Frericks
256 F. Oberwinkler et al.
(2014) obtained Tulasnella calospora isolations and compared them with strains of
various geographical origins.
The rare subterranean, achlorophyllous orchid Rhizanthella gardneri from
western Australia lives in a more than triple association with autotrophic and
heterotrophic partners in which, apparently, two Tulasnella species are involved
(Warcup 1985). In a taxonomic study and an experimental approach to grow
Rhizanthella gardneri together with Melaleuca scalena (Myrtaceae), Bougoure
et al. (2009a, b) used as mycobiont an unidentified, so-called “Ceratobasidium”
with the positive result that 5% of carbon fed to Melaleuca as
13
CO
2
was transferred
to R. gardneri. Further studies are needed to clarify the taxonomy and whether
diverse mycobionts are involved in this association.
12.7 Conclusions
Our literature search for Tulasnella on a global scale confirmed that distribution
patterns are biased by sampling. Nevertheless, there is unequivocal documentation
that Tulasnella as a group and certain morphological species have global distribu-
tion. Furthermore, it appears obvious that the world-wide distribution of orchids
may reflect a similar occurrence of their mycobionts, for which Tulasnella species
play a crucial role. The same may be true for Tulasnella associates of certain
liverworts. In addition, lignicolous basidiomata of Tulasnella are reported from
collecting areas of mycologists, interested in corticioid fungi. Apart from these
restrictions, a more adequate interpretation of Tulasnella’s biogeography is the
distribution pattern of suited habitats which appear to occur in a nearly world-wide
range.
Acknowledgements We thank Leho Tedersoo for the invitation to contribute to the book on
Biogeography of Mycorrhizae, Roland Kirschner and two anonymous reviewers for critical
comments. Gratefully acknowledged are the copyright permissions for Fig. 12.1 (Staatliches
Museum für Naturkunde Karlsruhe), and Fig. 12.2 (J. Cramer in Gebr. Borntraeger
Verlagsbuchhandlung, Stuttgart).
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