Fungal Diversity (2012) 52:225–244
DOI 10.1007/s13225-011-0133-x
A first assessment of Galapagos basidiolichens
Alba Yánez & Manuela Dal-Forno & Frank Bungartz &
Robert Lücking & James D. Lawrey
Received: 30 May 2011 / Accepted: 9 August 2011 / Published online: 2 September 2011
# Kevin D. Hyde 2011
M. Dal-Forno : J. D. Lawrey
Department of Environmental Science and Policy,
George Mason University,
Fairfax, VA 22030-4444, USA
tiled thalli, when fertile with circular lines of basidiocarps
on its lower side. Dictyonema is distinguished by
filamentous cyanobionts and distinctly filamentous thalli
that are homomereous (i.e., not distinctly layered); all
species of Dictyonema s.str. have trichomes (filamentose
cyanobacterial photobionts) closely enveloped by fungal
cells of a jigsaw pattern. In D. sericeum thallus filaments
(i.e., individual fibrils) aggregate to form shelf-like structures
similar in appearance to polyporoid bracket fungi; basidiocarps develop in irregular patches on the lower side of these
shelves. In contrast, fibrils of D. schenkianum grow encrusting their substrate with irregularly to suberect trichomes,
occasionally bearing basidiocarps dispersed across the
thallus. Two other species in Galapagos show adpressed
growth form and are described here as new: Dictyonema
pectinatum, which is characterized by large parallel fibrils
with paler, papillate tips, and D. galapagoense, characterized
by thin trichomes of more squarrish elongate cells. The
genus Cyphellostereum is represented by two species: the
newly described C. imperfectum and an unnamed Cyphellostereum sp., both phenotypically similar to free-living
cyanobacterial filaments. Cyphellostereum imperfectum has
narrow photobiont filaments with irregular hyphal sheath
leaving interspaces; macroscopically it shows a bluish green
thallus with a distinct prothallus. Cyphellostereum sp. has a
rather uncommon basidiolichen appearance: thin sctytonematoid fibrils surrounded by straight fungal cells forming
shiny tufts. The new combination Cyphellostereum nitidum
is also proposed. The ecology and taxonomy of Galapagos
basidiolichens is briefly discussed and a key and short
descriptions of all species are presented.
R. Lücking
Botany, The Field Museum,
1400 South Lake Shore Drive,
Chicago, IL 60605-2496, USA
Keywords Census of Galapagos Biodiversity . Galapagos
Lichen Inventory . Acantholichen . Cora . Cyphellostereum .
Dictyonema
Abstract As part of an ongoing comprehensive inventory
of Galapagos lichens, a first assessment of the morphology
and anatomy of basidiolichens from the archipelago is
presented here. It is the basis for further studies of the
taxonomy, ecology and biogeography of this poorly
known group of lichens. Four genera, all in Hygrophoraceae, can be distinguished: Acantholichen, Cora, Cyphellostereum and Dictyonema. Both Acantholichen and Cora
are characterized by chroococcoid cyanobionts and a
heteromerous thallus with a distinct upper cortex and
photobiont layer. The monotypic Acantholichen pannarioides is entirely composed of small, branched, inflated
squamules that appear densely pruinose because their
cortical hyphae bear characteristically swollen, densely
spinose end cells (acanthohyphidia); this species has never
been observed fertile. The common Cora glabrata is
foliose, forming large, radially zonate, conch-like, often
A. Yánez : F. Bungartz (*)
Biodiversity Assessment, Charles Darwin Foundation (AISBL),
Puerto Ayora, Santa Cruz, Galapagos, Ecuador
e-mail: frank.bungartz@fcdarwin.org.ec
A. Yánez
Universidad Central del Ecuador,
Quito, Ecuador
226
Introduction
The Galapagos Lichen Inventory represents a unique effort
in assembling the worldwide first comprehensive account
of all lichen species for a tropical archipelago (Bungartz et al.
2010a). It is part of a large scale biodiversity inventory by
the Charles Darwin Foundation with the long-term goal to
establish a comprehensive Census of Life for the Galapagos
Islands. During the first phase of the project, a centralized
species register, the CDF Galapagos Species Checklist, was
established. This open access database is available online;
individual checklists are regularly updated and the most
recent versions can be downloaded directly from the website
(Bungartz et al. 2010b). Currently the site not only provides
taxonomic data, but also assessments whether species are
rare or threatened (i.e., IUCN red list status), if they are
native or introduced, and distribution maps and photos. For
the next phase it is planned to augment this taxonomic
register with additional, more detailed distribution and
abundance data, and descriptive and ecological information
such as invasive species risk assessments. The overall goal of
this census of Galapagos biodiversity is to build up a
centralized knowledge management system that efficiently
provides detailed information about all known Galapagos
species.
One major challenge of the Galapagos species inventory
is the fact that the majority of species diverse but
inconspicuous taxonomic groups like invertebrates or fungi
have traditionally received little attention. This bias needs
to be addressed by emphasizing inventories also of these
poorly known groups.
Until recently, the inventory of Galapagos lichenized
fungi focused on ascomycetes, since the majority of lichens
belong to this phylum (>99% if assuming a total number of
17,500 lichenized species, about 50 of which are basidiomycetes). Several treatments of ascolichens have already
been published (Aptroot and Bungartz 2007; Aptroot and
Sparrius 2009; Aptroot et al. 2008; Bungartz 2008;
Bungartz et al. 2008; Bungartz et al. 2009; Tehler et al.
2009). Here we now present the first overview of currently
known Galapagos basidiolichens.
The taxonomy of lichenized basidiomycetes continues to
be poorly resolved (Chaves et al. 2004). As mentioned,
they represent a rather small group within Basidiomycota;
less than 1% of lichens are basidiomycetes, an estimated
fifty species within ten genera (Lawrey et al. 2009). With
possibly more than twenty species, the basidiomycete genus
Dictyonema sensu lato represents the largest basidiolichen
group and, to date, Parmastro’s monograph still is the only
comprehensive “modern” treatment of the genus (Parmastro
1978). Parmastro (1978) adopted a relatively wide species
concept, emphasizing thallus anatomy and treating morphological differences largely as phenotypic variation.
Fungal Diversity (2012) 52:225–244
Chaves et al. (2004) challenged this concept, arguing that
further molecular analysis is necessary to assess if forms
recognized by Parmastro (1978) were not better recognized
as distinct species. They described two new species and
provided a key to a total of eleven different morphotypes
that generally show little if no transitional forms but
supposedly represent distinct morphological entities. Lawrey
et al. (2009) were the first to begin molecular studies of
Dictyonema and related basidiomycetes, both lichenized and
non-lichenized. They found a high concentration of lichenized basidiomycetes in one single family, the Hygrophoraceae, and their results demonstrated that at least three
distinct genera should be recognized within Parmastro’s
concept of Dictyonema s.l. (Cora, Dictyonema s.str., and
Cyphellostereum); the clade also includes the morphologically and anatomically unique, monospecific Acantholichen
pannarioides (Jørgensen 1998).
All these genera can reliably be distinguished by their
morphological, micromorphological and anatomical characteristics. They all associate with photobionts of the genus
Rhizonema, a previously unrecognized lineage of filamentous cyanobacteria (Lücking et al. 2009), which in Cora and
Acantholichen occur as “chroococcoid” packets of broken
down filaments, and in Dictyonema s.str. and Cyphellostereum maintain their filamentous structure (Parmastro refers to
these algal filaments as trichomes compared to the thallus
filaments, i.e., trichomes surrounded by their hyphal sheath,
which he calls fibrils).
According to Lawrey et al. (2009) the species distinguished here are placed into four genera: the monotypic
Acantholichen, Cora, Dictyonema and Cyphellostereum
(also known as the Dictyonema phyllogenum-group).
Methods
The Galapagos Archipelago comprises more than 123
oceanic islands, islets and large rocks that emerged from
the sea as a result of volcanic hot spot activity. Fourteen
islands are somewhat arbitrarily recognized because of their
size as the principal islands. As island groups they are
typically associated with numerous smaller islands, rocks
and islets within close proximity (Snell et al. 1996). The
climate of Galapagos is unusually dry and principally
dominated by the sea currents, with a hot and cool season
and prevailing winds from the south and southeast (Trueman
and d’Ozouville 2010). Largely as a result of climate,
prevailing winds and elevation, five principal vegetation
zones can be distinguished: coastal, dry, transition, humid,
and high altitude dry zone (Bungartz et al. 2009; Tye et al.
2002). On the southern side of the islands the humid zone is
typically much more extensive, whereas it is absent from low
islands and typically not well developed on the leeward sides
Fungal Diversity (2012) 52:225–244
227
of higher islands. Only on the highest volcanoes of Isabela
Island the humid zone transitions into a high altitude dry
zone above the cloud inversion layer (see, Trueman and
d’Ozouville 2010, Fig. 1).
As part of the Galapagos Lichen Inventory the following
islands have been visited, where all vegetation zones with
their principal lichen habitats have been surveyed: Isabela
(Volcán Sierra Negra, Volcán Alcedo, Volcán Darwin),
Santiago (incl. Rabida, Bartolomé), Santa Cruz (incl. Santa
Fé, Plaza Sur, Plaza Norte, Roca Gordon, Pinzón), Pinta,
Española, Floreana, and San Cristóbal.
Additionally some material from mainland Ecuador was also
examined for this study (collections by H. Jonitz and F. Nugra).
Herbarium collections of this inventory are deposited at
CDS; specimens from historic collections have also been
examined (COLO, CAS, FH, H, S, B). All specimens were
Fig. 1 a−c free living Scytonema (Jonitz 596); a growth aspect of
filaments (scale bar 3 mm); b−c filaments lacking a gelatinous sheath (scale
bar 15 μm). d−f Cyphellostereum imperfectum (Lücking 25588); d growth
aspect of thallus surrounded by white prothallus (scale bar 3 mm); e−f loose
hyphal sheath of sinous fungal cells wrapped around photobiont trichomes
(scale bar 30 μm). g−h Cyphellostereum sp. (Dal Forno 1182 B); g: growth
aspect of thallus with erect filaments (scale bar 2 mm); h−i closely bundled
trichomes loosely embraced by fungal hyphae (scale bars 15 μm)
228
examined with a Zeiss Stemi DV4 dissecting microscope and a
Zeiss Imager A1 compound microscope equiped with differential interference contrast. Macrophotos were taken with a Nikon
D300, 62 mm Nikkor Micro Lens and R1C1 macro flash
directly in the field, or using a Novoflex macro-table to take
images of herbarium specimens; for photographic magnifications higher than 1:1 an extension tube or Novoflex bellows was
used. For microphotos the compound microscope is equipped
with a phototube for the Nikon D300. Photos in the laboratory
were taken with Nikon Camera Control Pro 2; all photos are
databased with the program IDimager 5 using the Darwin Core
XML schema to embed collection and identification information
as metadata (http://wiki.idimager.com/index.php?title=Darwin
CoreXMP#.27.27.27Darwin_Core_XMP.27.27.27). Photos
were processed with Photoshop CS4.
Results
Overall Galapagos diversity of basidiolichens appears less
pronounced than on the South American continent. Several of
the morphotypes recognized by Chaves et al. (2004) were not
found in Galapagos, but with surveys being intensified and
focusing on humid highland vegetation we expect that more
species and forms may be added to this list. The following
species are reported here:
Acantholichen pannarioides, Cora glabrata, Cyphellostereum imperfectum, Cyphellostereum sp., Dictyonema galapagoense, Dictyonema pectinatum,
Dictyonema sericeum, and Dictyonema schenkianum.
Relatively frequently collected among the Galapagos
material are also specimens that consist of bundled cyanobacterial trichomes that are only very loosely associated with
hyphae. If these specimens represent lichenized forms is
presently not well understood.
Species descriptions
Free living filamentous cyanobacteria
Scytonema sp. (not lichenized)
Figure 1a−c; habitat: 5c−e
Filamentous cyanobacteria occasionally with false branching, composed of chains of elongated cylindrical, bluish green
cells, interspersed with colourless to pale yellowish, slightly
larger heterocytes have classically been referred to the genus
Scytonema. Until recently it was believed that these cyanobacteria occur both free-living and as a common lichen photobiont. Molecular studies now, however, suggested that most, if
not all superficially similar lichen cyanobionts belong to the
Fungal Diversity (2012) 52:225–244
genus Rhizonema, a distinctly separate clade of cyanobacteria,
more closely related to other cyanobacteria like Nostoc,
Anabaena, Fischerella, or Hapalosiphon than to Scytonema
itself (Lücking et al. 2009).
Material of free living Scytonema appears to be
characterized by individual trichomes lacking a gelatinous
sheath, not closely bundled or enveloped by hyphae; the
illustrations provided here (Fig. 1a−c) are from material
collected in Peru (see specimens examined).
Specimen examined: Ecuador: Galapagos: Isla Santa
Cruz, behind the park fence, close to the border of the National
Park, 0°39′56′′S, 98°19′31′′W, alt. 502 m, Miconia robinsoniana shrubland, on bryophyte, growing over Frullania sp. on
branches of Miconia, 23-Jun-2010, Dal-Forno, M. 1182 B
(CDS no. 45429). Peru. Loreto: San Martin de Tipishca,
4°41′36.1′′ S, 74°23′57.8′′, 115 m, Jonitz, H. 596 (GMUF).
Acantholichen P.M. Jørg., Bryologist 101(3): 444 (1998)
Thallus bluish gray, coarsely pruinose, squamulose, heteromerous, i.e. with a distinct upper cortex, photobiont layer and
medulla, lower cortex lacking; upper cortex with swollen
spinose cells (acanthohyphidia); photobiont Rhizonema, but
not filamentous (not forming trichomes), chroococcoid
(broken down into packets of 4–8(−10) cells; but lacking a
distinct gelatinous sheath), enveloped by paraplectenchymatous haustoria of enlarged cells that occasionally form an
almost jigsaw-like pattern, clamp connections not observed;
only one species currently known.
Acantholichen pannarioides P.M. Jørg., Bryologist 101
(3): 444 (1998).
Figure 2a−c; habitat: 5c−d
A very distinct species that can easily be recognized in the
field by its ± globular densely pruinose squamules. The
squamules have a characteristic bluish gray colour, but older,
necrotic parts become pale beige to orange. The characteristic
acanthohyphidia that cause the pruinose “appearance of an
unshaven skin”, if observed in the light microscope look like
“spiny clubs of Roman gladiators” Jørgensen (1998 p. 446).
These characteristic cells are otherwise known only known
from non-lichenized basidiomycetes. Lücking (2008) reports
that the species has soredia. In the Galapagos material rather
coarse granules can only rarely be observed on the lower side
of few squamules and it is not clear if these are true soredia
functioning as dispersal units (as widely known from lichenized ascomycetes). Since basidiocarps remain unknown it is
equally as easily conceived that the small squamules fracture
and are distributed as fragments.
Ecology & substrate: The species is most frequently found
overgrowing epiphytic liverworts, especially Frullania. It is a
rare species that was probably more common in the so called
“brown zone” of Galapagos humid highlands, a native
vegetation type characterized by Zanthoxylon fagara trees
and an abundance of brown liverwort mats forming thick
carpets covering branches and tree trunks. On Santa Cruz
Fungal Diversity (2012) 52:225–244
229
Fig. 2 a−c Acantholichen pannarioides (Bungartz 5593); a−b growth
aspect of squamules (scale bars 8 mm); c cross section through a squamule
with the upper cortex bearing acanthohyphidae and the photobiont layers
with packets of cyanobionts (scale bar 10 μm). d−f Cora glabrata;
d conch-shaped thalli on plant detritus (Bungartz 3983; scale bar 3 cm);
e thallus epiphytic on branches of the introduced guava tree (Psidium
guajava), associated with Frullania sp., Cladonia sp. and Peperomia
fraseri (Bungartz 6505; scale bar 5 cm); f herbarium specimen with
upturned lower side displaying basidiocarps (Yánez 1547; scale bar 1 cm);
g–j sections of thallus with basidiocarps (Yánez 1547); g upper cortex and
photobiont layer with packets of cyanobacteria (scale bar 10 μm); h thallus
section with basidiocarp on lowers side (scale bar 40 μm); i cross section
through basidiocarp with apical basidia (scale bar 20 μm); j tear-shaped
basidiospore (spore ca. 4×7 μm)
Island this vegetation type has become relatively rare and the
species is today more commonly found on Frullania mats on
introduced Cinchona pubescens.
Specimens examined: Ecuador: Galapagos: Isla San Cristóbal, Cerro San Joaquín, 0°53′49.5′′S, 89°30′47′′W, alt. 691 m,
upper Miconia belt with a few shrubs of Psidium guajava and
Pteridium arachnoideum in the understory, slope 30° SE, on
bark, among mosses on branches of Psidium guajava shrub,
24-Aug-2008, Truong, C. 1532 (CDS no. 39843); S-slope of
Cerro San Joaquín, in the highlands, 0°53′49′′S, 89°30′55′′W,
alt. 771 m, Miconia shrubland with Pteridium arachnoideum
and other ferns, few Psidium guajava shrubs, on bark,
230
branches and twigs of Miconia robinsoniana; sunny, wind- and
rain-exposed, 24-Aug-2008, Bungartz, F. 8577 (CDS no.
41223). −Isla Santa Cruz, abandoned farm behind El Puntudo,
0°38′25′′S, 90°19′57′′W, alt. 729 m, tall forest of Persea
americana, Cinchona pubescens and Scalesia pedunculata, on
bryophyte, growing over hepatics on trunk of Persea
americana, S-exposed; semi-shaded, 28-Oct-2010, Yánez, A.
1546 (CDS no. 45040); along the trail from Media Luna to El
Puntudo, 0°38′44′′S, 90°20′5′′W, alt. 726 m, Cinchona
pubescens forest with Pteridium arachnoideum in the understory, on bryophytes, on Cinchona pubescens, 05-Nov-2007,
Ertz, D. 11713 (CDS no. 37072); along trail from Bellavista to
El Puntudo, upper Cinchona forest, 0°39′002′′S, 90°20′42′′W,
alt. 684 m, dense forest of Cinchona pubescens, some life trees
but mostly dead trees due to erradiction, on bryophyte,
growing over Frullania sp., 23-Jun-2010, Dal-Forno, M.
1205 (CDS no. 44756), Dal-Forno, M. 1202 (CDS no.
44753), Dal-Forno, M. 1203 (CDS no. 44754), Dal-Forno,
M. 1204 (CDS no. 44755), Spielmann, A. 8265 (CDS no.
45426); alt. 733 m, Miconia belt, Cinchona pubescens forest
with few Miconia robinsoniana, Lycopodium sp., Pteridium
arachnoideum and other ferns, on bark, trunk of Cinchona
pubescens; sunny, wind- and rain-exposed, 08-Feb-2007,
Bungartz, F. 5593 (CDS no. 33035); cerca del Puntudo, 0°38′
46′′S, 90°20′48′′W, alt. 735 m, bosque de Scalesia pedunculata, sobre corteza, Scalesia pedunculata, altura al pecho, 23Feb-2007, Nugra, F. 400 (CDS no. 35155); eastern slope
below the summit of El Puntudo, 0°38′42′′S, 90°20′14′′W, alt.
780 m, open forest with Cinchona pubescens, Furcraea
hexapetala, on bark of Cinchona, 28-Feb-2006, Aptroot, A.
64679 (CDS no. 31253); near Puntudo, 0°38′39′′S, 90°19′27′′
W, alt. 850 m, on bryophyte, growing over Campylopus sp. on
the ground, 27-May-2005, Aptroot, A. 63215 (CDS no.
29948); near Puntudo, 0°38′41′′S, 90°20′13′′W, alt. 750 m,
on soil, 27-May-2005, Aptroot, A. 63214 (CDS no. 29947);
near the CDRS field-weather station below the summit of
Cerro Crocker, 0°38′35′′S, 90°19′42′′W, alt. 830 m, much
overgrown with dead Cinchona pubescens tree, on of dead
Cinchona pubescens trees, 28-Dec-2005, Bungartz, F. 3313
(CDS no. 26968); NE-slope of El Puntudo, 0°38′39′′S, 90°20′
74′′W, alt. 813 m, dwarf shrub vegetation with ferns and
Hypericum thesiifolium, lichen heath, scattered Cinchona
pubescens trees and open lava rocks, on bark of Cinchona
pubescens, semi-shaded, wind- and rain-sheltered, 10-Aug2008, Bungartz, F. 8152 (CDS no. 40798); path from Media
Luna to El Puntudo, near El Puntudo, 0°39′86′′S, 90°20′28′′W,
alt. 684 m, small Cinchona forest with Pteridium arachnoideum, grasses and some Miconia, on bryophyte, growing over
Frullania sp. on branch of Cinchona pubescens, sunny, 28Oct-2010, Yánez, A. 1533 (CDS no. 45026), Yánez, A. 1519
(CDS no. 45010); trail to El Puntudo N of the crossing with
Cerro Crocker, 0°38′38′′S, 90°20′5.5′′W, alt. 802 m, area
invaded by Cinchona pubescens, on bark of small Cinchona
Fungal Diversity (2012) 52:225–244
with mosses, 10-Aug-2008, Truong, C. 1148 (CDS no. 39459);
tras del Puntudo, ex finca de Don Benito, 0°38′46′′S, 90°20′48′′
W, alt. 732 m, plantaciones de plátano, yuca, piña dentro de un
bosque de Scalesia pedunculata de árboles muy grandes y
maduros, sobre corteza, Cinchona pubescens, altura al pecho,
03-Feb-2007, Nugra, F. 379 (CDS no. 35134); vía Media Luna,
lindero del del Parque Nacional Galapagos, 0°39′58′′S, 90°19′
28.5′′W, alt. 500 m, con árboles invasores de Cinchona
pubescens, sobre corteza, Psidium guajava, altura al pecho,
exposición NE, 23-Aug-2007, Nugra, F. 439 (CDS no. 36753);
vicinity of Academy Bay, Miconia belt, on bryophytes,
Frullania mats, 15-Feb-1964, Weber, W.A. s.n. (CDS no.
189094), Weber, W.A. s.n. (COLO); La Copa (= Media Luna),
on bryophytes, Frullania mats, 15-Feb-1964, Weber, W.A. s.n.
(CDS no. 188949). −Isla Santiago, 1 km Wof the eastern peak,
0°12′50′′S, 90°46′30′′W, alt. 800 m, hillside covered mainly by
herbaceous vegetation, Zanthoxylum snags, on bark of Psychotria, 02-May-1971, Pike, L.H. ID19–20 (CDS no. 97965);
along trail to summit above Santiago Bay, lava flow, 0°12′35′′S,
90°47′5′′W, alt. 895 m, dense stand of Zanthoxylum and
Psychotria, 04-May-1971, Pike, L.H. s.n. (CDS no. 255659);
along trail to summit of James Bay, lava flow, 0°12′35′′S, 90°
47′5′′W, alt. 895 m, dense stand of Zanthoxylum and
Psychotria, on bark, 04-May-1971, Pike, L.H. 2753 (CDS no.
97964); permanent plot # 11 Pampa dentro, 0°12′59′′S, 90°46′
41′′W, alt. 870 m, non-wooded summit pampa with Setaria
parviflora, Cyperus virens, Paspalum galapageium, Pityrograma calomelanos var. calomelanos, Rhynchospora nervosa,
Doryopteris palmata, Hyptis rhomboidea and open soil in
between, on bark of Zanthoxylum fagara, 24-Mar-2006, Aptroot, A. 65554 (CDS no. 32142). −Isla Isabela, Volcán Alcedo,
outer SE-exposed slope, ca. 100 m below the crater rim, 0°27′0′
′S, 91°5′55′′W, alt. 1,100 m, Pteridium arachnoideum and
Stachytarpheta cayennensis, scattered low shrubs of Tournefortia rufo-sericea and outcrops of basalt tuff in between, on
bryophytes, growing over hepatics on Zanthoxylum fagara, 07Mar-2006, Aptroot, A. 65187 (CDS no. 31771); outer SEexposed slope, ca. 100 m below the crater rim, 0°27′4′′S, 91°5′
50′′W, alt. 1,066 m, Pteridium arachnoideum, Paspalum
conjugatum with open soil in between, on bark of Zanthoxylum
fagara (ca. 8 cm in diam.); sunny, wind- and rain-exposed, 06Mar-2006, Bungartz, F. 4125 (CDS no. 28152).
Cora Fr., Syst. orb. veg. (Lundae) 1: 300 (1825)
Thallus foliose, of flattened, conch-shaped lobes, heteromerous, i.e. differentiated into a distinct upper cortex, photobiont
layer and medulla, lacking a lower cortex; photobiont Rhizonema, but not filamentous (not forming trichomes), chroococcoid (broken down into packets of 4–8(−10) cells; but lacking
a distinct gelatinous sheath), enveloped by parplectenchymatous haustoria of enlarged cells that occasionally form an
almost jigsaw-like pattern; basidiocarps corticioid, zonate when
well developed, i.e. associating into large circular bands on the
lower side of the conch-shaped lobes.
Fungal Diversity (2012) 52:225–244
Cora glabrata (Spreng.) Fr., Epicr. syst. mycol. (Upsaliae): 556 (1838) [1836–1838]
Figure 2d−j, habitat: 5a−b
≡ Thelephora glabrata Spreng., K. svenska VetenskAkad. Handl. 41: 51 (1820); Dictyonema glabratum
(Spreng.) D. Hawksw., Lichenologist 20(1): 101 (1988)
Thallus whitish gray when dry, olive to greenish gray when
wet, typically ± radially zonate, of large, conch-like, often tiled
lobes; cortex prosoplectenchymatous, moderately thick, of ±
loosely to tightly interwoven hyphae; upper surface smooth,
shiny, typically minutely rugged and of an “elephant skin”
appearance, but in parts also of less tightly interwoven hyphae
and there almost tomentose, clamp connections not observed.
Notes: The Galapagos material appears rather uniform
and it is unlikely that several distinct species are included in
this group.
Ecology & substrate: Cora glabrata is among the most
common Galapagos basidiolichens inhabiting a very wide
range of substrates, most commonly epiphytic, but relatively
frequent also on the ground between terricolous bryophytes
and in Cladonia heathlands.
Specimens examined: Ecuador: Galapagos: Isla Santa Cruz,
abandoned farm behind El Puntudo, 0°38′25′′S, 90°19′57′′W,
alt. 729 m, tall forest of Persea americana, Cinchona
pubescens and Scalesia pedunculata, on bryophyte, growing
over hepatics on branch of Persea americana; semi-shaded,
28-Oct-2010, Yánez, A. 1547 (CDS no. 45041); along trail
from Bellavista to El Puntudo, behind parking lot, 0°40′48′′S,
90°19′26′′W, alt. 469 m, secondary forest of Cinchona
pubescens and Psidium guajava, on bryophyte, growing over
Frullania sp. on branch of Psidium guajava; semi-shaded,
WSW-exposed, 23-Jun-2010, Dal-Forno, M. 1180a (CDS no.
44714); along trail from Bellavista to El Puntudo, behind the
park fence, close to the border of the National Park, 0°39′56′′S,
98°19′31′′W, alt. 502 m, Miconia robinsoniana shrubland, on
bryophyte, growing on Frullania sp., 23-Jun-2010, Dal-Forno,
M. 1197 (CDS no. 44729), Dal-Forno, M. 1187 A (CDS no.
47764), Dal-Forno, M. 1223 (CDS no. 44748), Dal-Forno, M.
1200 (CDS no. 44745), Dal-Forno, M. 1218 (CDS no.
44741), Dal-Forno, M. 1198 (CDS no. 44730), Dal-Forno,
M. 1196 (CDS no. 44728), Dal-Forno, M. 1195 (CDS no.
44727), Dal-Forno, M. 1194 (CDS no. 44726), Dal-Forno, M.
1201 (CDS no. 44746), Dal-Forno, M. 1207 (CDS no.
44731); along trail from Bellavista to El Puntudo, upper
Cinchona forest, 0°39′002′′S, 90°20′42′′W, alt. 684 m, dense
forest of Cinchona pubescens, some life trees but mostly dead
trees due to erradiction, on bryophyte, growing over and
among Frullania sp., 23-Jun-2010, Dal-Forno, M. 1199 A
(CDS no. 44752); along trail from El Puntudo to abandoned
farm of Don Benito, 0°38′34′′S, 90°20′7′′W, alt. 733 m, open
grassy area with Pteridium arachnoideum and few scattered
Zanthoxylum fagara trees, on bark, branches of Cinchona
pubescens; semi-shaded, wind- and rain-sheltered, 08-Feb-
231
2007, Bungartz, F. 5594 (CDS no. 33039); at the base of the
eastern slope below the summit of El Puntudo, 0°38′42′′S, 90°
20′14′′W, alt. 780 m, open forest with Cinchona pubescens,
with dense ground cover of Pteridium arachnoideum and
Polypodium polypodioides over basalt rocks, on rock, Eexposed front/slope of small crater ledge, between plant debris;
semi-shaded, somewhat sheltered, 28-Feb-2006, Bungartz, F.
3983 (CDS no. 27913); below El Puntudo, 0°38′40′′S, 90°20′
96′′W, alt. 762 m, Cladonia heathlands, on rock, growing over
and among Frullania sp., 28-Oct-2010, Bungartz, F. 8789
(CDS no. 45291), growing over Cladonia confusa on the
ground, 28-Oct-2010, Yánez, A. 1538 (CDS no. 45031),
growing over Campylopus anderssonii on front of boulder;
semi-shaded, 28-Oct-2010, Yánez, A. 1540 (CDS no. 45033);
línea del Parque Nacional Galapagos, cerca la vía Baltra, sector
Los Gemelos, 0°38′74′′S, 90°23′39′′W, alt. 570 m, bosque
perturbado de Scalesia pedunculata, con especies introducidas,
dominante la Scalesia pendunculata, sobre rocas de lava
basáltica, 30-Jun-2006, Nugra, F. 26 (CDS no. 32679); N of
Bellavista, path from parking lot to Media Luna, 0°39′46′′S,
90°19′36′′W, alt. 555 m, Miconia shrubland, on bryophyte,
growing over hepatics on branches of Miconia robinsoniana,
SW-exposed, 28-Oct-2010, Yánez, A. 1509 (CDS no. 45000);
N of Bellavista, path from parking lot to Media Luna, 0°39′46′′
S, 90°19′36′′W, alt. 555 m, Miconia shrubland, on bryophyte,
growing over hepatics on branches of Miconia robinsoniana,
SW-exposed, 28-Oct-2010, Yánez, A. 1508 (CDS no. 44999);
N of Bellavista, path from parking lot to Media Luna, 0°39′46′′
S, 90°19′36′′W, alt. 555 m, Miconia shrubland, on bryophyte,
growing over hepatics on branches of Miconia robinsoniana,
SW-exposed, 28-Oct-2010, Yánez, A. 1510 (CDS no. 45001),
Yánez, A. 1511 (CDS no. 45002), Yánez, A. 1513 (CDS no.
45004); N of El Puntudo, 0°38′29′′S, 90°20′1.7′′W, alt. 724 m,
open Cinchona pubescens stand with ferns and grasses, on
bark of Cinchona pubescens, 05-Nov-2007, Ertz, D. 11720
(CDS no. 37079); on the northwestern fork of the way from
the parking lot to Caseta, near Media Luna, 0°39′31′′S, 90°19′
42′′W, alt. 600 m, along a small stream, among several
different fern species, on rock, large basalt boulder covered by
thin soil, SE-exposed, shaded, wind and rain-sheltered by the
cover of Pteridium arachnoideum, 28-Dec-2005, Bungartz, F.
3322 (CDS no. 26988); path from Media Luna to El Puntudo,
near El Puntudo, 0°39′86′′S, 90°20′28′′W, alt. 684 m, small
Cinchona forest with Pteridium arachnoideum, grasses and
some Miconia, on rock, front of small rock, sunny, 28-Oct2010, Yánez, A. 1536 (CDS no. 45029); saddle between
Puntudo and Mt. Crocker, 0°38′41′′S, 90°19′57′′W, alt. 720 m,
on rock, 18-Apr-1976, Weber, W.A. s.n. (CDS no. ), Weber, W.A.
s.n. (CDS no. 10833); tras del Puntudo, ex finca de Don
Benito, 0°38′23.27′′S, 90°19′57′′W, alt. 732 m, plantaciones de
plátano, yuca, piña dentro de un bosque de Scalesia
pedunculata de árboles muy grandes y maduros, sobre
corteza, Psidium galapageium, altura al pecho, 28-Dec-
232
2006, Nugra, F. 250 (CDS no. 33166); vía Media Luna,
lindero del del Parque Nacional Galapagos, 0°39′58′′S,
90°19′28.5′′W, alt. 500 m, con árboles invasores de
Cinchona pubescens, sobre corteza, Psidium guajava,
altura al pecho, exposición NE, 23-Aug-2007, Nugra, F.
437 (CDS no. 36189); S. slope of the mountain, alt.
520 m, on ground, 09-Apr-1930, Svenson, H.K. 202 (CDS
no. 197196); trail from Bella Vista to La Copa (= Media
Luna), N of Academy Bay, alt. 270 m, on bark, sprawling
lower stems and branches of Miconia robinsoniana, 25Jan-1964, Weber, W.A. 107 (CDS no. 185827); trail from
Bellavista to La Copa (Media Luna), alt. 270 m, on bark
of sprawling lower stems and branches of Miconia
robinsoniana, 25-Jan-1964, Weber, W.A. s.n. (CDS no.
197200); vicinity of Academy Bay, on bark of Miconia,
17-Feb-1964, Schuster, R.O. 154 (CDS no. 189289);
vicinity of Academy Bay, alt. 540 m, on bark of Miconia,
15-Feb-1964, Itow, S. 36 (CDS no. 192190); below Cerro
Camote, alt. 370 m, on bark of Miconia robinsoniana, 15Feb-1964, Rick, C.M. s.n. (CDS no. 193407); La Copa (=
Media Luna), alt. 500 m, margin of a pool, 31-Jan-1964,
Itow, S. 6 (CDS no. 192186); La Copa trail (= Media Luna
trail), on bark, Miconia stems, 15-Feb-1964, Weber, W.A.
106 (CDS no. 192976); vicinity of Academy Bay, trail to La
Copa (= Media Luna), moist zone, on bark, various shrub
stems, 15-Feb-1964, Weber, W.A. 67 (CDS no. 190029). −Isla
Santiago, along trail to summit above Santiago Bay lava
flow, 0°12′35′′S, 90°47′5′′W, alt. 895 m, dense stand of
Zanthoxylum and Psychotria, 04-May-1971, Pike, L.H. 2750
(CDS no. 255664); along the trail from Cerro Gavilan to La
Central, 0°13′2′′S, 90°46′33′′W, alt. 890 m, artificial grassland caused by former grazing with Setaria parviflora,
Cyperus virens, Paspalum galapageium, Pityrograma calomelanos var. calomelanos, Rhynchospora nervosa, Doryopteris palmata, Hyptis rhomboidea and open soil in between,
on open soil between pasture grasses, on NW-exposed and
ca. 10° inclined slope; sunny, wind- and rain-exposed, 24Mar-2006, Bungartz, F. 4831 (CDS no. 29005), 0°12′59′′S,
90°46′41′′W, alt. 870 m, non-wooded summit pampa with
Setaria parviflora, Cyperus virens, Paspalum galapageium,
Pityrograma calomelanos var. calomelanos, Rhynchospora
nervosa, Doryopteris palmata, Hyptis rhomboidea and open
soil in between, on soil, 24-Mar-2006, Aptroot, A. 65557
(CDS no. 32145). −Isla Isabela, Volcán Sierra Negra, 01-Jan1983, Luong, T.T. s.n. (CDS no. 10887); along dirt road from
Puerto Villamil to crater of Sierra Negra, farmland, 0°50′
37.5′′S, 91°3′55′′W, alt. 579 m, Psidium guajava trees along
dirt road and at the edge of of a fenced off pasture, on
liverworts on upper side of Psidium guajava branches; semishaded, wind- and rain-sheltered, 09-Sep-2007, Bungartz, F.
6905 (CDS no. 36397); Cueva del Sucre, at the entrance
(parking), SE side of the, 0°50′32.5′′S, 91°1′36′′W, alt. 369 m,
abandoned farming areas with forest stands, flat, on bark,
Fungal Diversity (2012) 52:225–244
branches of Syzgium jambos, 15-Aug-2008, Herrera-Campos,
M.A. 10639 (CDS no. 40376); dirt road to Sierra Negra, 0°50′
35′′S, 91°3′55′′W, alt. 580 m, farming areas, forest patch of
Psidium guajava, slope 25° NE, on bark, branches of
Psidium guajava with mosses (with Cora glabrata), 14Aug-2008, Herrera-Campos, M.A. 10546 (CDS no. 40282);
Cueva Sucre, abandoned farm bought by the National Park,
0°50′34′′S, 91°1′39′′W, alt. 362 m, agricultural area, Syzygium
jambos trees and Coffea arabica shrubs along a trail, on bark,
dead branch of Syzygium jambos lying on the ground, semishaded, wind- and rain-sheltered, 15-Aug-2008, Bungartz, F.
8252 (CDS no. 40898). −Isla San Cristóbal, near Tres Palos,
on bark of Psidium, 22-May-1976, Lanier, J. s.n. (CDS no.
298408); S of summit San Joaquín alt. 336 m, on bark of
Psidium guajava, 23-Dec-1967, Weber, D. s.n. (CDS no.
255566); south of summit San Joaquín, alt. 336 m, farm area,
on bark of Psidium guajava, 23-Dec-1967, Weber, D. s.n.
(CDS no. 10876).
Cyphellostereum D.A. Reid , Nova Hedwigia, Beih. 18:
336 (1965)
Thallus principally filamentose, but not distinctly layered and thus always lacking a distinct differentiation into
cortex, photobiont layer and medulla (i.e., homomereous);
entirely composed of fibrils, i.e., photobiont trichomes
closely enveloped by a sheath of lichen hyphae with
cylindrical cells leaving interspaces (not merged in a jigsaw
pattern); basidiocarps (if known) cyphelloid, with dorsiventral flap and short stipe.
Cyphellostereum imperfectum Lücking, Barillas & Dal
Forno sp. nov.
Figure 1d−f; habitat: 5c−e
Mycobank no. MB 561988
Sicut Cyphellostereum phyllogenum sed hypothallo et
prothallo albo et hyphis in filamentis cyanobacteriarum
intricatis differt.
Holotype: Guatemala: Baja Verapaz: Biotopo del Quetzal,
road CA-14, 3 km SE of Purulha, Sendero Corto (Los
Helechos) trail; 15° 13′ N, 90° 13′ W, 1,600–1,800 m;
montane rain forest with Podocarpus oleifolius, Hieronia
guatemalensis, Oreomunnia guatemalensis, Ocotea spp.;
May 2008, Lücking & Rivas Plata 25511(F, holotype; BIGU,
isotype).
Thallus corticolous, appressed-filamentous, appearing
crustose, up to 5 cm diam., turquois-blue with distinct
white hypothallus and prothallus; prothallus closely appressed to substrate, effuse-byssoid. Photobiont a filamentous cyanobacterium (Rhizonema?), filaments loosely
attached to the hypothallus, more or less horizontally
oriented, unbranched or basally with true branching, bluegreen, wrapped in a dense sheath of 2–3 μm wide, hyaline
fungal hyphae; photobiont cells 7–10 μm wide and 3–6 μm
high, heterocytes sparse to abundant, hyaline, 5–7×5–
7 μm; hyphal sheath formed by densely arranged, irregular
Fungal Diversity (2012) 52:225–244
to strongly undulate, frequently branched hyphae mostly
oriented longitudinally and leaving small interspaces.
Hypothallus and prothallus formed by 2–3 μm wide,
hyaline, straight hyphae with perpendicular branching
pattern. Clamps not observed on the medullary hyphae.
Basidiocarps not observed.
Notes: This new species is known from the well-developed
type collection, as well as a small specimen found intermixed
with Dictyonema pectinatum from Galapagos. The narrow
photobiont filaments and the irregular hyphal sheath leaving
interspaces place this taxon in the Cyphellostereum clade
(Lawrey et al. 2009). Most similar in this clade is
Cyphellostereum nitidum (Lücking) Lücking comb. et stat.
nov. [Dictyonema phyllogenum f. nitidum Lücking, Flora
Neotropica 103: 785 (2008)], which also has a white
prothallus, but has strongly appressed photobiont filaments
with a more loose hyphal sheath. Cyphellostereum phyllogenum lacks a distinct hypo- and prothallus and its hyphal
sheath is also less dense compared to C. imperfectum.
Molecular data of the nuclear large subunit ribosomal DNA
(nuLSU) and the internal transcribed spacer (ITS) confirm
that the new taxon belongs in the Cyphellostereum clade and
is specifically distinct from both C. nitidum and C.
phyllogenum (Dal Forno et al. 2011, in prep). The hyphal
sheath of the new species reminds of the jigsaw-shaped cells
of the sheath found in Dictyonema s.str., but differs in that
the hyphae themselves are sinous and leave interspaces,
hence the epithet imperfectum.
Specimens examined: Ecuador: Galapagos: Isla Santa
Cruz, along trail from Bellavista to El Puntudo, behind the
park fence, close to the border of the National Park, 0°39′
56′′S, 98°19′31′′W, alt. 502 m, Miconia robinsoniana
shrubland, on bryophyte, growing on Frullania sp., 23Jun-2010, Dal-Forno, M. 1193 B (CDS no. 47767).
Cyphellostereum sp.
Figure 1g−i; habitat: 5c−e
Thallus filamentous, encrusting its substrate but becoming
subfruticose, since the long fibrils cluster together forming
shiny tufts; fibrils entirely composed of ca. 8–15 trichomes
loosely bundled together by sterile fungal hyphae, 1–2 μm
wide; each individual trichome enveloped by a distinct
hyaline gelatinous sheath of 10 μm wide, bundled fibrils ca.
50–80 μm in diam.; cyanobacterial cells elongate cylindrical,
in chains (Scytonema?), 6 μm wide and 8–9 μm high,
heterocytes not seen (absent?). Clamps not observed.
Basidiocarps not observed.
Notes: In Galapagos, all material of filamentous cyanobacteria with a scytonemoid micromorphology that has so
far been found appears to consist of closely bundled
cyanobacterial filaments with a distinct gelatinous sheath,
their individual cyanobacterial cells elongated cylindrical,
apparently entirely lacking heterocytes. All of these specimens form thick bundles of cyanobacterial filaments that
233
are sometimes very loosely held together by few hyphae
that are not easily observed among the bundles of
cyanobacterial filaments. Dictyonema phyllogenum f. defectum was recently described for a morphotype with a very
poorly developed fungal sheath (Lücking 2008). Figure 2
58 E–F in Lücking (2008), however, depicts cyanobacterial
trichomes that are not closely bundled as it is the case in the
Galapagos material. Also, trichomes of Dictyonema phyllogenum f. defectum are appressed rather than erect, as seen
in the Galapagos material. The Galapagos specimens grow
on a variety of substrates, one also found on leaves of the
endemic Miconia robertsoniana, but most were collected
on bryophytes. The micromorphology of these specimens is
quite similar, but not identical with free-living forms of
Scytonema, since Cyphellostereum sp. clearly presents
fungal sheath cells surrounding the cyanobacteria.
Ecology & substrate: All specimens from the humid
zone of the Santa Cruz highlands, in scrubland of the
endemic Miconia robinsoniana; these highlands are today
often invaded by Cinchona pubsecens, most specimens
were found on epiphytic liverworts overgrowing Miconia or
Cinchona, some also on leaves, bark or soil. Several
specimens were found growing with Cora glabrata.
Specimens examined: Ecuador: Galapagos: Isla Santa
Cruz, abandoned farm behind El Puntudo, 0°38′25′′S, 90°19′
57′′W, alt. 729 m, tall forest of Persea americana, Cinchona
pubescens and Scalesia pedunculata, on bryophyte, growing
over hepatics on trunk of Persea americana, S-exposed;
semi-shaded, 28-Oct-2010, Yánez, A. 1545 (CDS no. 45039),
Yánez, A. 1544 (CDS no. 45038); along trail from Bellavista
to El Puntudo, behind parking lot, 0°40′48′′S, 90°19′26′′W,
alt. 469 m, secondary forest of Cinchona pubescens and
Psidium guajava, on bryophyte, growing over Frullania sp.
on branch of Psidium guajava; semi-shaded, WSW-exposed,
23-Jun-2010, Dal-Forno, M. 1180b (CDS no. 44714);
Miconia robinsoniana shrubland, on leaf of Cinchona
pubescens, 23-Jun-2010, Spielmann, A. 8259 (CDS no.
45422); along trail from Bellavista to El Puntudo, upper
Cinchona forest, 0°39′002′′S, 90°20′42′′W, alt. 684 m, dense
forest of Cinchona pubescens, some life trees but mostly
dead trees due to erradiction, growing over and among
Frullania sp., 23-Jun-2010, Dal-Forno, M. 1199 B (CDS no.
45428), Dal-Forno, M. 1190 (CDS no. 44751); along trail
from Bellavista to El Puntudo, behind the park fence,
close to the border of the National Park, 0°39′56′′S,
98°19′31′′W, alt. 502 m, Miconia robinsoniana shrubland, on bark, twig, 23-Jun-2010, Dal-Forno, M. 1187 B
(CDS no. 47764); Media Luna, 0°39′35′′S, 90°19′44′′W,
alt. 600 m, Miconia belt, on soil, 27-May-2005, Aptroot,
A. 63219 (CDS no. 29953); N of Bellavista, path from parking
lot to Media Luna, 0°39′46′′S, 90°19′36′′W, alt. 555 m,
Miconia shrubland, growing over hepatics on branches of
Miconia robinsoniana, SW-exposed, 28-Oct-2010, Yánez, A.
234
1512 (CDS no. 45003); trail from Bellavista to Media Luna,
close to Ntl. Park boundary, 0°40′6′′S, 90°19′26′′W, farn area
with pastures and introduced trees, on bark, trunk of Cinchona
pubescens, 25-Jan-2006, Ziemmeck, F. 512 (CDS no. 27070);
along the road from Bellavista to Los Gemelos, 0°39′56′′S, 98°
19′31′′W, alt. 502 m, Miconia robinsoniana shrubland, growing
over Frullania sp., 23-Jun-2010, Dal-Forno, M. 1188 B (CDS
no. 47765).
Dictyonema C. Agardh ex Kunth, Syn. Plantarum, Quas in
Itinere ad Plagam Aequinoctialem Orbis Novi, Collegerunt
Al. de Humboldt et Am. Bonpland (Paris) 1: 1 (1822)
Thallus principally filamentose, but not distinctly layered
and thus always lacking a distinct differentiation into cortex,
photobiont layer and medulla (i.e., homomereous); entirely
composed of fibrils, i.e., photobiont trichomes closely
enveloped by a sheath of lichen hyphae, their cells growing
in a jigsaw pattern; at least in one morphotype (D. sericeum)
these fibrils soon associate into a distinct, two-dimensional
“foliose” thallus, forming shelf-like structures that bear a
superficial semblance with polyporalean bracket fungi,
basidiocarps corticioid (if known), i.e., irregular, pale whitish
beige areas of a dense pseudotissue lacking photobiont cells.
Dictyonema galapagoense Yánez, Dal Forno & Bungartz
sp. nov.
Figs. 3a−c; habitat: 5f
Mycobank no. MB 561986
Sicut Dictyonema schenkianum sed trichomata tenuis
cellulis algarum quadratis differt.
Type: Ecuador: Galapagos: Isla San Cristóbal, trail from
Cerro Pelado to El Ripioso, 0°51′41′′S, 89°27′39′′W, alt.
392 m, Psidium guajava forest with some old Hippomane
mancinella trees and dense understory of Rubus niveus,
Tournefortia rufo-sericea and Zanthoxylum fagara, on
bryophytes, growing over mosses on bark of Hippomane
mancinella, upper side of inclined branch (ca. 20 cm in
diam.), SW-exposed; semi-shaded, wind- and rainsheltered, 23-Aug-2008, Bungartz, F. 8517 (CDS no.
41163−holotype selected here!).
Thallus filamentous, encrusting its substrate; fibrils
loosely interwoven, irregularly suberect; composed of
photobiont trichomes with a densely paraplectenchymatous
fungal sheath of cells in a jigsaw pattern, sheath not
extending beyond the trichome apex; photobiont Rhizonema, trichomes uniseriate, thin, with their fungal sheath
less than 12,5 μm in diam., cyanobacterial cells square to
elongate-cylindrical, in chains. Clamps not observed.
Basidiocarps not observed.
Notes: Macroscopically identified by much thinner, often
brightly bluish green filaments that are typically not adpressed
to their substrate, but forming erect to suberect fibrils;
microscopically the photobiont trichomes are significantly
thinner (<to 12.5 μm) than all morphotypes of Dictyonema,
but they are still enveloped in a fungal sheath with the distinct
Fungal Diversity (2012) 52:225–244
Fig. 3 a−c Dictyonema galapagoense (Bungartz 8517, holotype); a b
growth aspect (scale bar 4 mm); b−c microphoto of trichomes with
squarrish cells and jigsaw-celled fungal sheath (scale bars 30 μm). d−f
Dictyonema pectinatum (Dal Forno 1170); d thallus margin (scale bar
5 mm); e ± parallel filaments appearing as if combed (scale 5 mm); f
trichomes sheathed by papillate fungal hyphae (scale bar 20 μm). g−l
Dictyonema schenkianum; g filaments closely wrapped around
Frullania sp., lacking basidiocarps (Bungartz 4127 B; scale bar
3 mm); h filaments loosely wrapped around Frullania sp., with
whitish basidiocarp squamules (Dal Forno 1209; scale bar 4 mm); i
basidiocarps developing from white, non-lichenized hyphae that must
not be confused with a prothallus (Dal Forno 1209; scale bar 2 mm);
j–l trichomes with fungal sheath of hyphae in a jigsaw pattern
(Bungartz 4127, Dal Forno 1225; Yánez 1534; scale bars 60 μm)
jigsaw pattern typical for Dictyonema s.str. Individual cyanobacterial cells that form the trichomes are also not as flattened
as in D. sericeum, more squarish to shortly elongatecylindrical. A distinct, compact prothallus is missing.
Ecology & substrate: Currently only known from a
single collection site, on San Cristóbal Island, in an old
Manzanilla (Hippomane mancinella) forests with many
large and mature trees. This forest, although recently
beginning to become more and more invaded by Rubus
nivea, is particularly diverse with many rare lichen species
and possibly represents an ancient forest fragment.
No additional specimens known.
Dictyonema pectinatum Dal Forno, Yánez & Lücking
sp. nov.
Figs. 3d−f; habitat: 5c−e
Mycobank no. MB 561987
Sicut Dictyonema schenkianum sed trichomata pectinata
in apicis papillatis differt.
Type: Ecuador: Galapagos: Isla Santa Cruz, along trail
from Bellavista to El Puntudo, behind parking lot, 0°40′48′′
S, 90°19′26′′W, alt. 469 m, secondary forest of Cinchona
pubescens and Psidium guajava, on bark of Psidium
guajava, 23-Jun-2010, Dal-Forno, M. 1170 (CDS no.
44705–holotype selected here!).
Thallus dark green, adpressed-filamentous, composed of
mostly parallel, as if “combed” blue-green cyanobacterial
filaments forming very long fibrils. The part that doesn’t
show the horizontal-flattened fibrils looks like an arachnoid
net of several layers of filaments. Thallus lacking a
distinctly delimited, marginal prothallus, but occasionaly
with pale areas of few, hyaline and loosely interwoven
hyphae of 6 μm wide. Cyanobacterial filaments bluegreen becoming yellow in the tips, which present
papillae; cells 16–21 μm wide and 5–9 μm high,
surrounded by a fungal sheath forming jigsaw puzzleshaped cells. Hyaline fungal sheath 5–9 μm wide (on
each side of the photobiont), not extending beyond the
apex of the photobiont trichomes. Heterocytes sparse to
abundant, yellow, 12–13×2–3 μm. Clamps not observed.
Basidiocarps not observed.
Fungal Diversity (2012) 52:225–244
235
236
Notes: The Galapagos material is rather uniform, growing
closely adpressed to smooth bark. It is not evident to which
extent this unusual growth may be substrate induced, but is
notable that this is the only species of Dictyonema s. str.
growing directly on bark in the Islands; also, the olive-gree
rather than blue-green color correlates with this unusual
morphology. Dictyonema pectinatum shows the characteristic
fungal sheath around the cyanobacterial filaments composed of
jigsaw puzzle-shaped cells, which confirm its position inside
the Dictyonema s. st. group. The most remarkable character of
this new species, not observed in Dictyonema schenkianum, is
the presence of horizontal filaments growing in the same
direction, as it has been combed, therefore the name epithet
pectinatum. Also, the conspicuously papillose apices of the
filaments (papillae formed by the hyphal sheath), in combination with the cyanobacterial filaments becoming paler towards
the tips, characterizes this new species.
Ecology & substrate: This unusual morphotype is only
known from four specimens growing on smooth bark of
introduced Guava (Psidium guajava).
Aditional specimens examined (paratypes): Ecuador: Galapagos: Isla Santa Cruz, along trail from Bellavista to El
Puntudo, behind the park fence, close to the border of the
National Park, 0°39′56.8′′S, 98°19′31.4′′, 502 m, Miconia
robinsoniana shrubland, on bark of Psidium guajava, 23-Jun2010, Dal-Forno, M. 1221 (CDS 44744), Dal-Forno, M.
1222 (CDS no. 44747); Dal-Forno, M. 1193 C (CDS no.
47766), Dal-Forno, M. 1188 A (CDS no. 44722).
Dictyonema schenkianum (Müll. Arg.) Zahlbr., Cat.
Lich. Univers. 7: 748 (1931).
Figs. 3g−l; habitat: 5a−e
≡ Laudatea schenkianum Müll. Arg., Hedwigia 30: 234
(1891); Dictyonema sericeum f. schen[c]kianum (Müll.
Arg.) Parm., Nova Hedwigia 29: 112 (1978). Note:
Parmastro (1978) erroneously used the spelling schenckianum for Dictyonema sericeum f. schenkianum
Thallus bluish to olive green, loosely encrusting its substrate,
fibrils irregularly interwoven, suberect to erect; hyaline fungal
sheath not extending beyond the apex of the photobiont
trichomes; thallus lacking a distinctly delimited, marginal
prothallus, but often with a loose to dense mat of whitish
hyphae, becoming visible where the photobiont is missing.
Corticioid basidiocarps are irregularly distributed across the
thallus and typically not associating into larger areas.
Notes: The Galapagos material shows considerable
morphological consistency. Chaves et al. (2004) suggest
that the development of a prothallus, length of fibrils or
presence and absence of basidiocarps may help to distinguish three different encrusting growth forms. However,
preliminary phylogenetic analysis suggests that the situation is even more complicated and that anatomical features
are also necessary to characterize species. The Galapagos
material differs slightly from the description in Lücking
Fungal Diversity (2012) 52:225–244
(2008) insofar as the fungal hyphae that form a fungal
sheath with jigsaw pattern are not papillate.
Ecology & substrate: Unlike Dictyonema sericeum this
crustose species is much more common and still quite
abundant throughout the humid native scrubland vegetation
of Miconia robinsoniana in the humid highlands of Santa
Cruz and San Cristóbal.
Specimens examined: Ecuador: Galapagos: Isla Pinta, on
top of the highest point of the, 0°35′3′′N, 90°45′12′′W, alt.
625 m, low and dense vegetation of ferns, grasses (Cyperus
andersonii), and Lycopodium sp., on plant debris & bryophytes, semi-shaded by vegetation, wind- and rain-exposed,
26-Feb-2007, Bungartz, F. 5746 (CDS no. 33400).−Isla Santa
Cruz, temporary Cinchona weather station, along the trail to
El Puntudo, 0°39′66′′S, 90°19′57′′W, alt. 698 m, Cinchona
pubescens stand with scattered Miconia robinsoniana, in
understory Pteridium arachnoideum dominant, on bryophytes, Frullania aculeata growing epiphytically on Cinchona pubescens branches, 28-Dec-2005, Bungartz, F. 3276
(CDS no. 26918); along trail from Bellavista to El Puntudo,
behind parking lot, 0°40′48′′S, 90°19′26′′W, alt. 469 m,
secondary forest of Cinchona pubescens and Psidium
guajava, on bark, 23-Jun-2010, Spielmann, A. 8264 (CDS
no. 45421); along trail from Bellavista to El Puntudo, behind
parking lot, 0°40′48′′S, 90°19′26′′W, alt. 469 m, secondary
forest of Cinchona pubescens and Psidium guajava, on
bryophyte, growing over Frullania sp., 23-Jun-2010, DalForno, M. 1177 (CDS no. 44711); path from Media Luna to
El Puntudo, near El Puntudo, 0°39′86′′S, 90°20′28′′W, alt.
684 m, small Cinchona forest with Pteridium arachnoideum,
grasses and some Miconia, on bark, trunk of Cinchona
pubescens; sunny, 28-Oct-2010, Yánez, A. 1534 (CDS no.
45027), along the road from Bellavista to Los Gemelos, 0°38′
12′′S, 90°23′46′′W, alt. 574 m, NNW-exposed road bank with
annual vegetation partially dry and died-back, and some lava
rocks along Scalesia pedunculata forest, on detritus, 12-Feb2006, Aptroot, A. 63899 (CDS no. 30455); on bryophyte,
growing over Frullania sp., 23-Jun-2010, Dal-Forno, M.
1178 (CDS no. 44712), Dal-Forno, M. 1171 (CDS no.
44706), Dal-Forno, M. 1185 (CDS no. 44715), Dal-Forno,
M. 1181 (CDS no. 44716), Dal-Forno, M. 1179 (CDS no.
44713), Dal-Forno, M. 1224 (CDS no. 44749), Spielmann,
A. 8261 (CDS no. 45420), Rivas Plata, E. 4081 (CDS no.
45152); on bryophyte, growing on mosses over bark, semishaded branches, 23-Jun-2010, Dal-Forno, M. 1174 (CDS
no. 44709); 0°39′56′′S, 98°19′31′′W, alt. 502 m, Miconia
robinsoniana shrubland, on bryophyte, growing over Frullania sp., 23-Jun-2010, Dal-Forno, M. 1219 (CDS no. 44742),
Dal-Forno, M. 1183 (CDS no. 44718), Dal-Forno, M. 1225
(CDS no. 44750), Dal-Forno, M. 1184 (CDS no. 44719),
Dal-Forno, M. 1186 (CDS no. 44720), Dal-Forno, M. 1182
A (CDS no. 44717), Dal-Forno, M. 1211 (CDS no. 44735),
Dal-Forno, M. 1215 (CDS no. 44739), Dal-Forno, M. 1214
Fungal Diversity (2012) 52:225–244
(CDS no. 44738), Dal-Forno, M. 1191 (CDS no. 44724),
Dal-Forno, M. 1212 (CDS no. 44736), Dal-Forno, M. 1210
(CDS no. 44734), Dal-Forno, M. 1208 (CDS no. 44732),
Dal-Forno, M. 1220 (CDS no. 44743), Dal-Forno, M. 1189
(CDS no. 44723), growing over Frullania sp. and fern
fronds, 23-Jun-2010, Dal-Forno, M. 1209 (CDS no. 44733);
along trail from Bellavista to El Puntudo, upper Cinchona
forest, 0°39′002′′S, 90°20′42′′W, alt. 684 m, dense forest of
Cinchona pubescens, some life trees but mostly dead trees
due to erradiction, on bryophyte, growing over Campylopus
anderssonii, 23-Jun-2010, Spielmann, A. 8249 (CDS no.
44757); along trail from Media Luna to El Puntudo, 0°38′43′
′S, 90°20′5′′W, alt. 733 m, Miconia belt, Cinchona pubescens
forest with few Miconia robinsoniana, Lycopodium sp.,
Pteridium arachnoideum and other ferns, on bryophyte,
growing over Frullania sp. on twigs of Cinchona pubescens;
semi-shaded, wind- and rain-exposed, 08-Feb-2007, Bungartz, F. 5592 (CDS no. 33034); 0°39′97′′S, 90°19′59′′W, alt.
724 m, upper Miconia belt with Pteridium arachnoideum,
largely invaded by Cinchona pubescens, growing over
Frullania sp. on branches of Cinchona, 10-Aug-2008, Clerc,
P. 08–109 (CDS no. 39963); Bellavista, near parking place
for trail to Media Luna, 0°40′10′′S, 90°19′22′′W, alt. 400 m,
on Frullania aculeata on Cinchona, 27-May-2005, Aptroot,
A. 63153 (CDS no. 29883); below El Puntudo, 0°38′40′′S,
90°20′96′′W, alt. 762 m, Cladonia heathlands, on bryophyte,
growing over Frullania sp. on the ground, 28-Oct-2010,
Yánez, A. 1539 (CDS no. 45032); between El Puntudo and
Cerro Crocker, ca. 100 m N off the main path, 0°38′40′′S,
90°19′58′′W, alt. 760 m, small cliff in dense Miconia
shrubland, on bryophyte, growing over Frullania sp. on
Cinchona trunk; sunny, 28-Oct-2010, Yánez, A. 1541 (CDS
no. 45035); N of Bellavista, path from parking lot to Media
Luna, 0°39′46′′S, 90°19′36′′W, alt. 555 m, Miconia shrubland, on bryophyte, growing over Frullania sp. on branches
of Miconia robinsoniana, SW-exposed, 28-Oct-2010, Yánez,
A. 1515 (CDS no. 45006), Yánez, A. 1507 (CDS no. 44998),
Yánez, A. 1514 (CDS no. 45005); near Puntudo, 0°38′41′′S,
90°20′13′′W, alt. 750 m, on bark of Cinchona pubescens, 27May-2005, Aptroot, A. 63192 A (CDS no. 29923); near
Puntudo, 0°38′41′′S, 90°20′13′′W, alt. 750 m, on bryophyte,
growing over mosses on soil, 27-May-2005, Aptroot, A.
63198 (CDS no. 29929); path from Media Luna to El
Puntudo, near El Puntudo, 0°39′86′′S, 90°20′28′′W, alt.
684 m, small Cinchona forest with Pteridium arachnoideum,
grasses and some Miconia, on Frullania sp. on branch of
Cinchona pubescens, 28-Oct-2010, Yánez, A. 1523 (CDS no.
45014), Yánez, A. 1527 A (CDS no. 45018), Yánez, A. 1520
(CDS no. 45011), Yánez, A. 1528 (CDS no. 45020), Yánez,
A. 1531 (CDS no. 45023), Yánez, A. 1516 (CDS no. 45007),
Yánez, A. 1517 (CDS no. 45008), Yánez, A. 1521 (CDS no.
45012), Yánez, A. 1518 (CDS no. 45009), Yánez, A. 1524
(CDS no. 45015); Steve Divine's Farm at the end of Tortoise
237
Road, off the main road to Baltra, Tortoise Territory, 0°40′8′′
S, 90°24′17′′W, alt. 364 m, open farmland with Cedrela
odorata, Persea americana, Citrus sp., on plant debris, over
lava, 23-Feb-2006, Aptroot, A. 64519 (CDS no. 31091),
Bungartz, F. 3956 (CDS no. 27838); temporary Cinchona
weather station, along the trail to El Puntudo, 0°39′66′′S, 90°
19′57′′W, alt. 698 m, Cinchona pubescens stand with
scattered Miconia robinsoniana, in understory Pteridium
arachnoideum dominant, on bryophytes, growing over
Frullania aculeata on Cinchona pubescens branches, 28Dec-2005, Bungartz, F. 3275 (CDS no. 26917); tras del
Puntudo, ex finca de Don Benito, 0°38′23′′S, 90°19′57′′W,
alt. 732 m, plantaciones de plátano, yuca, piña dentro de un
bosque de Scalesia pedunculata de árboles muy grandes y
maduros, sobre corteza, Psidium galapageium, altura al
pecho, 28-Dec-2006, Nugra, F. 252 (CDS no. 33168); sobre
hepaticas en corteza de Cinchona pubescens, altura al pecho,
25-Jan-2007, Nugra, F. 358 (CDS no. 35113). −Isla Isabela,
Volcán Alcedo, outer SE-exposed slope and crater rim, 0°27′
29′′S, 91°7′19′′W, alt. 1,089 m, tortoise pasture with scattered
trees (Tournefortia rufo-sericea, Zanthoxylum fagara), on
bark of Tournefortia, 05-Mar-2006, Aptroot, A. 65037 A
(CDS no. 31619); outer SE-exposed slope, ca. 100 m below
the crater rim, 0°27′4′′S, 91°5′50′′W, alt. 1,066 m, Pteridium
arachnoideum, Paspalum conjugatum with open soil in
between, on lichen, growing over lichen thallus on trunk of
Zanthoxylum fagara (ca. 8 cm in diam.); sunny, wind- and
rain-exposed, 06-Mar-2006, Bungartz, F. 4127 B (CDS no.
28155); Volcán Sierra Negra, along dirt road from Puerto
Villamil to crater of Sierra Negra, farmland, 0°50′38′′S, 91°3′
45.5′′W, alt. 550 m, abandoned Psidium guajava orchard
with few Inga sp. and dense understory of shrubs, fallen
trees, grasses and ferns, growig over hepatics on top of
Psidium guajava branches (ca. 5 cm in diam.); semi-shaded,
wind- and rain-sheltered, 09-Sep-2007, Bungartz, F. 6883
(CDS no. 36362); close to the southern crater rim, along the
trail to Alemania, 0°51′12′′S, 91°8′40.5′′W, alt. 1,055 m,
pampa of Pteridium arachnoideum, Pernettya howellii,
Lycopodium sp., and with occasional tree ferns (Cyathaea
weatherbyana) and Psidium guajava shrubs, dead & living
plants, growing over dead plant material and Lycopodium
and fern stems near the ground; shaded, wind- and rainsheltered, 16-Aug-2008, Bungartz, F. 8350 (CDS no. 40996);
La Cueva Sucre, abandoned farm bought by the National
Park, 0°50′34′′S, 91°1′39′′W, alt. 362 m, agricultural area,
Syzygium jambos trees and Coffea arabica shrubs along a
trail, on bryophyte, growing over Frullania sp. twigs in the
crown of a fallen Syzygium jambos tree; sunny, wind- and
rain-exposed, 15-Aug-2008, Bungartz, F. 8258 (CDS no.
40904); trail to Sierra Negra, 0°49′41′′S, 91°5′30′′W, alt.
967 m, Psidium guajava shrubland with Pteridium arachnoideum on the ground, slope 25° SE, plant debris &
bryophytes, growing over dead twigs with mosses on the
238
ground, 14-Aug-2008, Truong, C. 1239 (CDS no. 39550);
trail to Volcán Chico, along Sierra Negra crater, 0°49′48′′S,
91°5′18′′W, alt. 980 m, Psidium guajava shrubland with
Pteridium arachnoideum on the ground, slope 25° SW, on
bark, branches of Psidium guajava, 14-Aug-2008, HerreraCampos, M.A. 10560 (CDS no. 40297).
Dictyonema sericeum (Sw.) Berk., London J. Bot. 2: 639
(1843)
Figs. 4a−g; habitat: 4g−h, 5a−b
≡ Hydnum sericeum Sw., Nova gen. sp. pl.: 149 (1788);
Dictyonema sericeum f. sericeum (Sw.) Berk., London J.
Bot. 2: 639 (1843).
Thallus fibrils soon associating into large, shelf-like
brackets in appearance similar to polypolarean fungi; hyaline
fungal sheath extending far beyond the apex of the photobiont
trichomes, forming a white to pale beige fringe along the
margins of the shelf-like brackets; basidiocarps corticioid, not
distinctly zonate, associating into large, irregular areas on the
lower side of the shelf-like brackets.
Ecology & substrate: Where they occur the large brackets
of Dictyonema sericeum are very conspicuous. Like Acantholichen they might have been a native element of the
Galapagos lichen biota in the Zanthoxylon forests, where this
species is still found growing quite abundantly on some of
old Zanthoxylon tree trunks. Much more commonly the
species today inhabits secondary habitat like the extensive
guava forests (introduced Psidium guajava) in the upper
agricultural zone and along the crater rim of Volcán Sierra
Negra in southern Isabela. In Santa Cruz the species has only
recently been found in a fragmented old growth forest of the
endemic Scalesia pecdunculata, growing however, not on
the native trees, but in introduced Avocado trees.
Specimens examined: Ecuador: Galapagos: Isla San
Cristóbal, Cerro San Joaquín, 0°53′51′′S, 89°30′48.5′′W, alt.
681 m, upper Miconia belt with shrubs of Psidium guajava,
Rubus niveus and Pteridium in the understory, slope 45°
SSE, on bark, among mosses on branches of Psidium
guajava shrubs, 24-Aug-2008, Truong, C. 1533 (CDS no.
39844), Herrera-Campos, M.A. 449 (CDS no. 43340); NE of
El Junco, alt. 575 m, on bark of Psidium guajava, 21-Dec1967, Weber, D. s.n. (CDS no. 255569); Isla San Cristóbal, Sslope of Cerro San Joaquín, 0°53′49′′S, 89°30′55′′W, alt.
771 m, Miconia shrubland with Pteridium arachnoideum
and other ferns, few Psidium guajava shrubs, on bark,
branches and twigs of Miconia robinsoniana; sunny, windand rain-exposed, 24-Aug-2008, Bungartz, F. 8576 (CDS no.
41222). −Isla Santa Cruz, abandoned farm behind El
Puntudo, 0°38′25′′S, 90°19′57′′W, alt. 729 m, tall forest of
Persea americana, Cinchona pubescens and Scalesia
pedunculata, on bryophyte, growing over hepatics on branch
of Persea americana; semi-shaded, 28-Oct-2010, Yánez, A.
1550 (CDS no. 45044), Yánez, A. 1549 (CDS no. 45043),
Yánez, A. 1548 (CDS no. 45042); near summit, wet slope, on
Fungal Diversity (2012) 52:225–244
hepatics, 10-May-1932, Howell, J.T. 4 (CDS no. 194144),
Howell, J.T. 4 (CDS no. 197185), Howell, J.T. 4 (CDS no.
633897); vicinity of Academy Bay, above Horneman farm
on trail to La Copa, on bark of Miconia robinsoniana, 15Feb-1964, Weber, W.A. 33 (CDS no. 189029), Weber, W.A. 33
(CDS no. 193829); Bellavista, near parking place for trail to
Media Luna, 0°40′10′′S, 90°19′22′′W, alt. 400 m, on bark of
Miconia, 27-May-2005, Aptroot, A. 63148 (CDS no.
29878);. −Isla Santiago, 1 km W of the eastern summit, 0°
12′50′′S, 90°46′30′′W, alt. 800 m, dense tree fern forest in
ravine, 02-May-1971, Pike, L.H. ID20-3 (CDS no. 255984);
along trail to summit above Santiago Bay lava flow, 0°13′0′′
S, 90°47′30′′W, alt. 680 m, dense stand of Zanthoxylum and
Psychotria, 03-May-1971, Pike, L.H. ID21-1 (CDS no.
255996); along trail to summit of James Bay lava flow, 0°
13′0′′S, 90°47′30′′W, alt. 680 m, dense stand of Zanthoxylum,
Croton, Psychotria, 03-May-1971, Pike, L.H. ID21-1 (CDS
no. 104040); ridge 50 m N of Muñeco Rock outcrop, 0°12′
38′′S, 90°46′58′′W, alt. 860 m, S-exposed, steep basalt cliffs
of crater rim with ferns (Pityrograma calomelanos var.
calomelanos, Polypodium tridens, Doryopteris palmata,
Adiantum concinnum, Blechnum polypodioides) growing in
crevices, on bark of Zanthoxylum, 23-Mar-2006, Aptroot, A.
65523 (CDS no. 32112). −Isla Isabela, Volcán Alcedo, outer
SE-exposed slope, ca. 100 m below the crater rim, 0°27′4′′S,
91°5′50′′W, alt. 1,066 m, Pteridium arachnoideum, Paspalum conjugatum with open soil in between, on trunk of
Zanthoxylum fagara (ca. 8 cm in diam.), sunny, wind- and
rain-exposed, 06-Mar-2006, Bungartz, F. 4127 A (CDS no.
28154); on crater rim SE of hut, 0°27′35′′S, 91°6′43′′W, alt.
1,080 m, tortoise pasture with scattered trees (Tournefortia
rufo-sericea, Zanthoxylum fagara), on lava rock, 05-Mar2006, Aptroot, A. 64818 (CDS no. 31393); outer SE-exposed
slope, ca. 100 m below the crater rim, 0°27′0′′S, 91°5′55′′W,
alt. 1,100 m, Pteridium arachnoideum and Stachytarpheta
cayennensis, scattered low shrubs of Tournefortia rufosericea and outcrops of basalt tuff in between, on bark of
Zanthoxylum, 07-Mar-2006, Aptroot, A. 65186 (CDS no.
31770). −Volcán Sierra Negra, along dirt road from Puerto
Villamil to crater of Sierra Negra, farmland, 0°50′38′′S, 91°3′
45.5′′W, alt. 550 m, abandoned Psidium guajava orchard
with few Inga sp. and dense understory of shrubs, fallen
trees, grasses and ferns, on branches of Inga sp. (ca. 5 cm in
diam.), semi-shaded, wind- and rain-sheltered, 09-Sep-2007,
Bungartz, F. 6852 (CDS no. 36301); along dirt road from
Puerto Villamil to crater of Sierra Negra, farmland, 0°50′
37.5′′S, 91°3′55′′W, alt. 579 m, Psidium guajava trees along
dirt road and at the edge of of a fenced off pasture, on bark
of Psidium guajava branches; sunny, wind- and rainexposed, 09-Sep-2007, Bungartz, F. 6906 (CDS no. 36398);
close to the southern crater rim, along the trail to Alemania,
0°51′12′′S, 91°8′40.5′′W, alt. 1,055 m, pampa of Pteridium
arachnoideum, Pernettya howellii, Lycopodium sp., and with
Fungal Diversity (2012) 52:225–244
239
Fig. 4 Dictyonema sericeum; a shelf-like thallus similar in appearance to a
polyporoid bracket-fungus (Bungartz 4127 A; scale bar 3 cm); b growth
aspect overgrowing bryophytes on branch of Psidium guajava tree (Bungartz
6906; scale bar 6 cm); c lower side of “shelves” with basidiocarps (Bungartz
6906; scale bar 3 cm); d close-up of white fringe formed by fungal sheath
extending far beyond the trichomes within (Bungartz 6906; scale bar
0.5 cm); e−f trichomes wrapped in sheath of hyphae with jigsaw pattern
apically extending beyond the trichomes (Bungartz 6906; scale bars 60 μm);
g growth habit (Bungartz 4127 A; scale bar 10 cm); h habitat, remnant
Zanthoxylon trees at Volcán Alcedo, Isabela Island
occasional tree ferns (Cyathaea weatherbyana) and Psidium
guajava shrubs, on bark, branch of Psidium guajava; semishaded, wind- and rain-sheltered, 16-Aug-2008, Bungartz, F.
8363 (CDS no. 41009); dirt road to Sierra Negra, 0°50′35′′S,
91°3′55′′W, alt. 580 m, farming areas, forest patch of
Psidium guajava, slope 25° NE, on bark, branches of
240
Fungal Diversity (2012) 52:225–244
Fig. 5 Habitats of Galapagos
basidiolichens; a secondary
forest of introduced guava
(Psidium guajava) in the farm
zone of Sierra Negra, Isabela
Island provides a habitat rich in
Cora glabrata, Dictyonema
sericeum, and other Dictyonema species; b branch of
Psidium guajava ladden in
Cora glabrata (same locality as
previous photo; Bungartz 6905,
scale bar 5 cm); c view of El
Puntudo on Santa Cruz Island
in the Miconia-zone, invaded
by quinine (Cinchona pubescens), now representing
secondary habitat for Acantholichen pannarioides and
various Dictyonema species;
d same locality with Cinchona
pubescens trees; d view of the
Santa Cruz highlands from the
highest elevation Cerro
Crocker; e El Ripioso on San
Cristóbal Island, transition zone
forest with Manzanillo (Hippomane mancinella) close to the
type locality of Dictyonema
galapagoense
Psidium guajava with mosses (together with Cora glabrata),
14-Aug-2008, Herrera-Campos, M.A. 10545 (CDS no.
40281), Truong, C. 1275 (CDS no. 39586); near parking place
at start of foot path to the crater, 0°49′47.5′′S, 91°5′19′′W, alt.
939 m, open grazed woodland of shrubby Psidium guajava, on
bryophytes, on Frullania sp. on Psidium guajava branch;
shaded, wind- and rain-sheltered, 08-Sep-2007, Bungartz, F.
6849 (CDS no. 36297); South side of Sierra Negra crater, trail
to Alemania, 0°51′17′′S, 91°8′55′′W, alt. 924 m, vegetation
with Pteridium arachnoideum, invaded by a few small trees of
Psidium guajava, slope 15° SW, on Polypodium stems among
mosses on the ground, slope 15° SW, 16-Aug-2008, Truong,
C. 1259 (CDS no. 39570); viewpoint at southern edge of
Sierra Negra crater, 0°49′36′′S, 91°5′36′′W, alt. 1,005 m,
Psidium guajava shrubland with Pteridium arachnoideum on
the ground, slope 25° SW, on bark, branches of Psidium
guajava, 14-Aug-2008, Herrera-Campos, M.A. 10555 (CDS
no. 40291), Clerc, P. 08–166 (CDS no. 40020); near Santo
Tomas, alt. 200 m, on bark of Psidium guajava, 14-Jan-1968,
Weber, D. s.n. (CDS no. 255568); above Santo Tomas, between
“Los Tanques” and “La Torre”, alt. 500 m, on bark of Psidium
guajava, 14-Jan-1968, Weber, D. s.n. (CDS no. 10878); south
side of Sierra Negra crater, trail to Alemania, 0°51′17′′S, 91°8′
55′′W, alt. 924 m, vegetation with Pteridium arachnoideum,
invaded by a few small trees of Psidium guajava, on soil &
mosses, over basalt rocks, 16-Aug-2008, Clerc, P. 08–194 (CDS
no. 40048). −Isla San Cristóbal, NE of El Junco, alt. 575 m, on
bark of Psidium guajava, 21-Dec-1967, Weber, D. s.n. (CDS
Fungal Diversity (2012) 52:225–244
no. 10877); SE-slope of CerroSan Joaquín, shortly below the
summit, 0°53′52′′S, 89°30′49′′W, alt. 672 m, low vegetation of
Pteridium arachnoideum, other ferns, Cyathea weatherbyana,
Miconia robinsoniana, Psidium guajava shrubs and Furcraea
hexapetala, on bryophytes, growing over Frullania sp. on twig
of Miconia robinsoniana; sunny, wind- and rain-exposed, 24Aug-2008, Bungartz, F. 8581 (CDS no. 41227).
Key to Galapagos basidiolichens
1. Photobiont coccoid, i.e., Rhizonema trichomes broken
down into small fragments or distinct packets of cells
enveloped by±paraplectenchymatous haustoria; thallus
distinctly layered (heteromerous).....................................2
Photobiont filamentous, lichenized or not; thallus
filamentous, not layered, entirely composed of macroscopically discernible fibrils, encrusting its substrate or
dimidiate, i.e., aggregating into three-dimensional shelflike structures resembling polyporalean bracket fungi
(Dictyonema)....................................................................3
2. Thallus squamulose, very small, but occasionally
covering areas of up to 20 cm or more, of minutely
branched, ±swollen, globose squamules, less than 1 mm;
surface dull, even, azonate, densely pruinose because
their upper cortex is densely covered by inflated spinulose
cells (acanthohyphidia)...............................................
..............................................Acantholichen pannarioides
Thallus foliose, large, spreading up to 50 cm or more,
of conch-shaped, frequently tiled lobes, individual lobes
2–10 cm; surface smooth, shiny, rugulose, rarely ± fibrous
and in parts becoming hairy, typically distinctly radially
zonate cortex almost absent or of loosely or tightly
interwoven hyphae; always lacking spinulose cells
....................................................................Cora glabrata
3. Cyanobacterial trichomes without a gelatinous sheath and
not associated with lichen hyphae; free living filamentous
cyanobacteria..............................................Scytonema sp.
Cyanobacterial trichomes with a gelatinous sheath,
either loosely bundled by sparse hyphae or enveloped by a
tight, paraplectenchymatous hyphal sheath.....................4
4. Macroscopic filament surface roughened, dull, distinctly
lichenized, microscopically surrounded by a tight,
distinctly paraplectenchymatous fungal sheath of
individual cells enveloping photobiont filaments in
a jigsaw pattern........................................................5
Macroscopic filament surface smooth, shiny, not
appearing distinctly lichenized but more like nonlichenized cyanobacteria; hyphal sheath composed of
cylindrical cells leaving interspaces.........................
..........................................................................................8
5. Thallus dimidiate, forming large shelf-like structures with
a broad, pale fringe devoid of photobionts; individual
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thallus fibrils of intertwined hyphae that apically extend
well beyond the apex of the cyanobiont trichomes that
they envelop....................................................
........................................................Dictyonema sericeum
Thallus not dimidiate, of individual, undifferentiated
filaments, not aggregating, but encrusting their substrate;
individual thallus fibrils of intertwined hyphae that
apically do not extend beyond the apex of the cyanobiont
trichomes that they envelop............................................6
6. Thallus filaments dark brownish green, flattened and
strongly adpressed to their substrate, predominantly
growing parallel, as if combed; fibrils apically
papillose.................................................................
..................................................Dictyonema pectinatum
Thallus filaments bluish to olive green, not distinctly
flattened or adpressed to their substrate, but at least
some ± erect, irregularly intertwined; fibrils not
papillose........................................................................7
7. Thallus fibrils broad (>20 μm); individual cyanobiont
cells flattened, rectangular-cylindrical, like a “stack of
coins”....................................Dictyonema schenkianum
Thallus fibrils thin (<15 μm); individual cyanobiont
cells square to elongate-cylindrical, like a “chain”.
...............................................Dictyonema galapagoense
8. Macroscopic surface dark green, smooth, shiny, filaments forming thick, erect tufts, microscopically
cyanobiont filaments closely bundled into thick,
multi-seriate trichomes by few, loosely interwoven
hyphae............................................Cyphellostereum sp.
Macroscopic surface bluish green, with a distinct white
prothallus, appressed, microscopically cyanobiont filaments reminding a jigsaw pattern but with sinuous hyphae
leaving interspaces...........................................................
...........................................Cyphellostereum imperfectum
Discussion
The objective of this first assessment of Galapagos
basidiolichens is to establish a descriptive framework of
phenotypic variation as observed in specimens collected
during our inventory. Chaves et al. (2004) did already
recognize the significant phenotypical variation within
Dictyonema s.l. but hesitated to re-instate the genera Cora
and Dictyonema.
Macroscopically and microscopically the four genera
distinguished here are very well supported also by
molecular studies (Lawrey et al. 2009; Lücking et al.
2009) except for the possibly paraphyletic Dictyonema;
they are thus formally recognized here and they can
easily be distiguished by the following descriptive
characters:
242
The genus Acantholichen has acanthohyphidia, i.e.
swollen, spinulose cortical cells. Whether these are homologous to the papillose cells found in species of Dictyonema
is unclear. Both the foliose Cora and the squamulose
Acantholichen have distinctly layered thalli, with an upper
cortex, a photobiont layer, and a medulla, both lacking a
lower cortex. Their photobionts are broken down into short
fragments or groups of coccoid cells, not aggregated into
characteristic filaments, a micromorphological variation of
Rhizonema apparently induced by the mycobiont (Lücking
et al. 2009). In contrast, Dictyonema s.str. always grows
filamentous, where the characteristic Rhizonema filaments
are closely surrounded by a fungal sheath of paraplectenchymatous cells in a jigsaw pattern (Lücking 2008).
Although Dictyonema sericeum s.str. forms large shelves
of lobes somewhat reminiscent of the lobes of Cora, their
principally filamentous composition is still easily discernible, even macroscopically. Cyphellostereum is similar to
Dictyonema in general aspect but has an irregular hyphal
sheath with cylindrical cells leaving interspaces, and the
cyanobacterial trichomes are much narrower, morphologically suggesting a different photobiont although genetically
there appears to be no difference (Lücking et al. 2009).
The evidence presented here also strongly suggests
that the morphotypes distinguished by Chaves et al.
(2004) correspond to well delimited species, they are not
simple variation in growth forms. Intermediates between
these forms cannot be observed. Even if it cannot entirely
be ruled out that fibrils of substrate encrusting forms could
develop into the characteristic, shelf-like structures of D.
sericeum, the presence of corticioid basidiocarps already
on entirely undifferentiated crusts of D. schenkianum
indicates that these two morphotypes are not simply
developmental stages of the same species. Even if the
fibrils of both species are microscopically relatively
uniform both species are also microscopically distinct: in
D. sericeum s.str. the fungal sheath around the photobiont
filaments regularly extends far beyond the apex of the
trichomes and even in specimens that are macroscopically
not yet differentiated into distinct shelves, these colourless
fibrils are nevertheless visible at an early stage as a
distinct, pale white to beige fringe that must not be
confused with unlichenized hyphae of a prothallus. In D.
sericeum this fringe clearly develops at the apex of fibrils
and it is therefore not a developmental stage of nonlichenized hyphae from which lichenized filaments subsequently arise.
In the dichotomic key presented by Chaves et al. (2004)
the formation of a prothallus is also interpreted as an
important character. Dictyonema schenkianum lacks a
distinct prothallus. Instead its fibrils typically develop from
a poorly differentiated network of hyaline hyphae, but the
dense, stark-white prothallus observed in other species of
Fungal Diversity (2012) 52:225–244
Dictyonema is nevertheless absent. Instead this species is
very commonly fertile and its basidiocarps regularly
develop from non-lichenized hyphae. These whitish mats,
where the basidiocarps arise from non-lichenized hyphae
must not be confused with the prothallus mentioned in
Chaves et al. (2004).
In Galapagos both species are also ecologically distinct:
Dictyonema schenkianum is by far the most common
basidiolichen. It is widely distributed throughout the humid
zone, growing on a variety of substrates, but preferably on
bryophytes. Though common, it is possibly more typical
for less disturbed, native vegetation such as the Miconia
scrublands of Santa Cruz. In comparison, Dictyonema
sericeum s.str. is relatively rare and mostly found on
introduced trees; although the species at least in Santa Cruz
is known from fairly old forests, these sites are also highly
disturbed by non native tree species. In Isabela the species
is known from extensive forest of introduced Guava
(Psidium guajava), but it also has been found in fragments
of native Zanthoxylon forests.
Some specimens among the Galapagos material do not
fit well into the concept of D. schenkianum presented here.
They are crustose, formed by very closely adpressed fibrils
predominantly growing parallel, i.e., fibrils oriented mostly
horizontally, appearing as if “combed”. The four specimens
are comparatively darker, more brownish to olive brown
instead of the bright bluish green typical of fresh D.
schenkianum. Because the Galapagos specimens also grow
closely adpressed, they at first appear superficially similar
to D. membranaceum sensu Chaves et al. (2004), but their
fibrils are much longer and more distinctly parallel. Unlike
D. membranaceum sensu Chaves et al. (2004) these
Galapagos specimens are not epiphyllous. Microscopically
the specimens can be distinguished from D. schenkianum
by their pale tips with papillae. Revising a large quantity of
material from other countries of South and Central
America, we became convinced that no other material is
alike and therefore decided to publish the new species
Dictyonema pectinatum.
Another Galapagos specimen (Bungartz 8517) is described here as a new species of Dictyonema. It is
characterized by a micromorphology significantly different
from all other morphotypes of Dictyonema and it does not
fit into any one of the species recognized by Parmastro
(1978). It has fibrils that are much narrower (ca. 12 μm)
than any forms of Dictyonema and the individual photobiont cells of the trichomes are square to elongatecylindircal instead of flattened-rectangular. Although these
trichomes are thus similar to those found in Cyphellostereum (the Dictyonema phyllogenum-group), the species is
clearly characterized by a fungal sheath of the sericeumtype, i.e., it has trichomes tightly enveloped by cells in a
distinct jigsaw pattern.
Fungal Diversity (2012) 52:225–244
Surprisingly, two species of Cyphellostereum (the Dictyonema phyllogenum-group) were found in Galapagos. This
group has a different shape of hyphae, not the jigsaw pattern
around the cyanobacteria, but so far its characteristics are not
well established. Both species found in the islands present
quite different cell shapes: one having straight cells around
the thin scytonematoid cyanobacteria, and the other presenting a sinous shape with spaces between the cells around a
much thinner type of Rhizonema. Molecular studies are
being realised and already confirm the status of this unclear
group of basiodiolichens as a separated clade. However,
morphological evidence alone is insufficient to objectively
interpret these associations of hyphae and cyanobacteria and
no formal species name is established here.
As previously mentioned, the descriptive framework
presented here is a pre-requisite for a better understanding
of the ecology of Galapagos basidiolichens. Presently
ecology and distribution of Galapagos basidiolichens and
their origin, i.e., how they arrived in Galapagos, where else
on the South American continent related populations occur
−all these questions remain open. They are only possible to
address with a more extensive species inventory.
We now know that all Galapagos basidiolichens are
restricted to islands with a well developed humid zone,
such as Isabela, San Cristóbal, Santa Cruz, Santiago, and
Pinta. Few species venture from the lower humid zone into
the upper, still relatively humid transition zone, where they
all remain confined to the most humid habitats. Both
Acantholichen pannarioides and Dictyonema sericeum are
generally quite rare, both today have most commonly been
found in secondary forests of introduced trees. Nevertheless, it seems unlikely that these species represent recent
introductions. Had they arrived in Galapagos with their
phorophytes, one would expect these species to be equally
as abundant today as their now very wide-spread substrates.
Instead these lichens remain rare and their populations
show no signs of expanding as rapidly as their phorophytes.
A more logical explanation might be to interpret their
present distribution as remnants of populations that were
more common in natural, undisturbed forests. This would
also imply that these species were previously more
common and more widely distributed.
Both Acantholichen pannarioides and Dictyonema sericeum require high humidity and typically occur only in
habitats that are very humid, with the typical frequent fogs
of the Galapagos called “garúa”. In Galapagos they are
clearly much limited in their distribution, confined only to
the most humid habitats, rarely found below 500 m.
Throughout the humid zone D. schenkianum is clearly the
most common Dictyonema, it is most abundant especially
in the Miconia scrublands of Santa Cruz and San Cristóbal,
but present also in a variety of humid forests on other
islands. In comparison to all other basidiolichen species D.
243
schenkianum may have the largest ecological amplitude,
still found in forests that are not sufficiently humid for any
other species.
Overall Cora glabrata might be considered the least
specific of the Galapagos basidiolichens; it grows on almost
any substrate in open, relatively disturbed sites. Nevertheless, unlike D. schenkianum, the species requires a certain
amount of humidity and is therefore not as widely distribute
as D. schenkianum, still confined to areas with sufficient
rainfall or at least with regular occurrences of garúa.
Acknowledgements We thank Frauke Ziemmeck for managing the
cryptogam collection at CDS, helping with collecting, data entry and
curating of specimens. Successive Directors of Science at the Charles
Darwin Foundation have supported this project: Alan Tye, Mark
Gardener, and Rodolfo Martinez. We are further indebted to the
Galapagos National Park, especially its technical director Washington
Tapia for support and specimen export permits. The Census of Galapagos
Biodiversity and the CDF Checklist of Galapagos Species is supported by
several grants to the Charles Darwin Foundation (donors cited at http://
www.darwinfoundation.org/datazone/checklists/). A checklist of Galapagos lichens is regularly updated and available at http://www.darwin
foundation.org/datazone/checklists/lichens, where contributing scientists
are acknowledged. The lichen inventory continues to receive funds from
The Paul and Bay Foundations and the Erwin Warth Stiftung. In 2010
an international lichen workshop was held in Galapagos, supported by
two National Science Foundation (NSF) projects entitled “Neotropical
Epiphytic Microlichens - An Innovative Inventory of a Highly Diverse
yet Little Known Group of Symbiotic Organisms” (DEB 0715660 to
The Field Museum; PI Robert Lücking) and “Phylogenetic Diversity of
Mycobionts and Photobionts in the Cyanolichen Genus Dictyonema,
with Empasis on the Neotropics and the Galapagos Islands” (DEB
0841405 to George Mason University; PI James Lawrey, subcontract to
the Charles Darwin Foundation, local coordinator Frank Bungartz). The
latter grant continues to support the studies on basidiolichens in
Galapagos. We thank Harald Jonitz for specimens collected in
continental Ecuador available for this study. This publication is
contribution number 2041 f the Charles Darwin Foundation for the
Galapagos Islands.
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