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The new genus Jocatoa (Lecanoromycetes:
Graphidaceae) and new insights into subfamily
Redonographoideae
Authors: Miranda-González, Ricardo, Lücking, Robert, Barcenas-Peña,
Alejandrina, and Ángeles Herrera-Campos, María de los
Source: The Bryologist, 123(2) : 127-143
Published By: The American Bryological and Lichenological Society
URL: https://doi.org/10.1639/0007-2745-123.2.127
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The new genus Jocatoa (Lecanoromycetes: Graphidaceae) and new
insights into subfamily Redonographoideae
Ricardo Miranda-Gonza
´lez
1,2,5
, Robert L¨
ucking
3
, Alejandrina Barcenas-Pe˜
na
2,4
and Mar´
ıa de los ´
Angeles Herrera-Campos
2
1
Department of Botany and Plant Pathology, Oregon State University, 2082 Cordley Hall, Corvallis, OR 97331–2902,
U.S.A.;
2
Departamento de Bota
´nica, Instituto de Biolog´
ıa, Universidad Nacional Aut´
onoma de M´
exico. Apdo. Postal
70–3627, C. P. 04510, Ciudad de M´
exico, M´
exico;
3
Botanischer Garten und Botanisches Museum, Freie Universit ¨
at
Berlin, K¨
onigin-Luise-Straße 6–8, 14195 Berlin, Germany;
4
Science & Education, The Field Museum, 1400 South Lake
Shore Drive, Chicago, IL 60605-2496, U.S.A.
ABSTRACT.One new genus and two new species of Graphidaceae are described from tropical dry forests of
Mexico, based on morphological and molecular data of the mtSSU, nuLSU and ITS markers. The new
genus Jocatoa in subfamily Graphidoideae is described to accommodate the species Graphis agminalis
(syn.: Medusulina texana), previously known from Colombia and North America. The new genus
resembles Diorygma but differs by having simple paraphyses tips that do not form an epithecium. Jocatoa
agminalis is similar to Diorygma monophorum but differs by having larger ascospores, hypostictic and
stictic acids and by the type of paraphysis tips. In subfamily Redonographoideae, the two new species
Gymnographopsis corticicola and Redonographa parvispora are described, representing the first corticolous
species in the subfamily. Gymnographopsis corticicola is characterized by the smallest spores in the genus,
the presence of norstictic acid, and a rectangular perispore that appears to be a newly recognized
character state in fungi. Redonographa parvispora is characterized by warty periphysoids, small ascospores
with 3 transverse septa, and norstictic acid. It also frequently develops a rectangular perispore. We
present a phylogenetic analysis, based on the markers mtSSU, nuLSU and RPB2, that includes all the
genera in the family Graphidaceae, with available sequences, to accommodate the new genus and to
validate for the first time the position of Gymnographopsis. Diagnostic anatomical and ecological
characters are discussed for Redonographoideae. Gymnographopsis is newly reported to the Northern
Hemisphere.
KEYWORDS.Chamela Biological Station, lichen systematics, Mexico, North America, tropical dry forest,
rectangular perispore.
RESUMEN.Un nuevo g´
enero y dos especies nuevas de Graphidaceae son descritas del bosque tropical seco
de M´
exico, basa
´ndose en datos morfol ´
ogicos y moleculares de los marcadores mtSSU, nuLSU y ITS. Se
describe el nuevo g´
enero Jocatoa en la subfamilia Graphidoideae para acomodar a la especie Graphis
agminalis (sin.: Medusulina texana), conocida de Colombia y Norte Am´
erica. El nuevo g´
enero se asemeja
aDiorygma, pero difiere por tener las puntas de las para
´fisis simples y por no formar un epitecio. Jocatoa
agminalis es similar a Dior ygma monophorum, pero difiere por tener ascosporas ma
´s grandes, a
´cidos
hypoest´
ıctico y est´
ıctico y por el tipo de para
´fisis. En la subfamilia Redonographoideae, las dos nuevas
especies Gymnographopsis corticicola yRedonographa parvispora son descritas, representando las primeras
especies cort´
ıcolas en la subfamilia. Gymnographopsis corticicola se caracteriza por tener las esporas ma
´s
peque˜
nas del g´
enero, la presencia de a
´cido norest´
ıctico y por tener una perispora rectangular que parece
5
Corresponding author’s e-mail: mirandar_g@yahoo.com.mx
DOI: 10.1639/0007-2745-123.2.127
The Bryologist 123(2), pp. 127–143 Published online: April 7, 2020 0007-2745/20/$1.85/0
Copyright Ó2020 by The American Bryological and Lichenological Society, Inc.
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ser el reconocimiento de un nuevo caracter para hongos. Redonographa parvispora se caracteriza por tener
per´
ıfisis espinuladas, ascoesporas peque˜
nas con 3 septos transversales y a
´cido norest´
ıctico. Adema
´s,
tambi´
en presenta frecuentemente una perispora rectangular. Presentamos un ana
´lisis filogen´
etico, basado
en los marcadores mtSSU, nuLSU y RPB2, que incluye a todos los g´
eneros de la familia Graphidaceae,
con secuencias disponibles, para acomodar al nuevo g´
enero y para validar por primera vez la posici ´
on
filogen´
etica de Gymnographopsis. Se discuten caracteres anat ´
omicos y ecol ´
ogicos diagn ´
osticos para
Redonographoideae. Gymnographopsis se reporta por primera vez para el hemisferio norte.
PALABRAS CLAVE.Estaci ´
on de Biolog´
ıa Chamela, sistema
´tica de l´
ıquenes, M´
exico, Norte Am´
erica, bosque
tropical seco, perispora rectangular.
^^^
Graphidaceae is the second largest family of liche-
nized fungi, after Parmeliaceae (L¨
ucking et al.
2017a). The family contains only crustose lichens,
is predominantly tropical and subtropical, and
associates with trentepohlioid or very rarely tre-
bouxioid algae (Kraichak et al. 2015). Staiger (2002),
Frisch et al. (2006) and Mangold et al. (2008) laid
the bases for the current classification of the family
and triggered several new studies. Recent molecular
work showed that Graphidaceae includes three core
subfamilies: Fissurinoideae, Graphidoideae and Re-
donographoideae (L¨
ucking et al. 2013; Lumbsch et
al. 2014a; Mangold et al. 2008; Rivas Plata et al.
2013); a fourth subfamily, Gomphillaceae (Rivas
Plata et al. 2012) has been shown to be sister to
Graphidaceae (Jaklitsch et al. 2016; Kraichak et al.
2018). Of the three subfamilies, Graphidoideae is
further divided into seven tribes that contain most
of the species of the family and the previously
separated Thelotremataceae (Lumbsch et al. 2014a;
Rivas Plata et al. 2012).
Recently, Kraichak et al. (2018) proposed to
divide Graphidaceae into four families, Diploschista-
ceae, Fissurinaceae, Graphidaceae s.str. and Thelo-
tremataceae, based on the approach of temporal
banding which attempts to harmonize rank-based
taxa through their evolutionary age. This approach
has been rejected, for various reasons (L¨
ucking 2019):
(1) by using a single criterion, the temporal banding
approach does not properly reflect evolutionary
histories across the different kingdoms of life and
not even between closely related clades; (2) taxon
sampling in Graphidaceae was incomplete and early
diverging lineages such as subfamily Redonographoi-
deae and several orphaned lineages in subfamily
Graphidoideae, which would have resulted in addi-
tional families, were either omitted or ignored, such
as Platythecium; (3) while Fissurinaceae, Graph-
idaceae and Thelotremataceae represent natural taxa,
the family Diploschistaceae merged three unrelated
groups that do not form a supported clade in other
phylogenetic studies and hence represents a highly
artificial taxon; (4) the proposed classification has
little information content with regard to phenotypic
variation and disparity and the reinstated families
Graphidaceae and Thelotremataceae have little in
common with the traditionally separated families
under these names, making any effort to reinstate
these families to preserve their use futile. In the
present paper, we therefore continue to use Graph-
idaceae in the sense of L¨
ucking et al. (2017a), which is
also supported by our updated family-wide phyloge-
netic analysis, which contradicts the topology ob-
tained by Kraichak et al. (2018).
Presently, Graphidaceae includes c. 2100 known
species in 79 genera (L¨
ucking et al. 2017a), and it is
expected to have another 1500 undescribed species
(L¨
ucking et al. 2014). The relations within the family
are relatively well known and only nine of the
accepted genera have not yet been sequenced
(Amazonotrema,Anomalographis,Anomomorpha,
Byssotrema,Diaphorographis,Gymnographopsis,Kal-
bographa,Polistroma and Thecographa; nomencla-
ture follows L¨
ucking et al. 2017a,b, except as noted).
Nonetheless, the position of many small genera like
Aggregatorygma or Schistophoron are not resolved
with support, some of the larger genera like
Acanthothecis,Fissurina and Phaeographis, are not
monophyletic, and some species like Graphis
agminalis Nyl. and Medusulina texana M¨
ull. Arg.
are of unknown generic affinity (L¨
ucking et al.
2017b; Lumbsch et al. 2014a; Rivas Plata et al. 2013).
L¨
ucking et al. (2014) predicted that just the
tropical part of Mexico would have 429 species of
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Graphidaceae. Herrera-Campos et al. (2014) count-
ed 175 species registered for the whole country,
including both published and unpublished data.
Mexico is currently considered to be one of the
world hotspots for undescribed species of Graph-
idaceae, with recent papers (Barcenas-Pe˜
na et al.
2014, 2015; Herrera-Campos et al. 2019) marking
the start of modern studies in this group in Mexico.
In this paper we describe a new genus in
subfamily Graphidoideae and two new species in
subfamily Redonographoideae from tropical dry
forests of Mexico. We obtained, for the first time,
sequence data of the genus Gymnographopsis, which
had been predicted to belong in subfamily Redo-
nographoideae (L¨
ucking et al. 2013). To accommo-
date the new genus and to test the inclusion of
Gymnographopsis in that subfamily, we reconstruct-
ed an updated three-gene phylogeny of Graph-
idaceae that included representatives of all the
genera in the family with available sequences.
METHODS
Study area.All new taxa and new sequences
were obtained from samples collected in or around
the Chamela-Cuixmala Biosphere Reserve located 2
km inland from the Pacific Coast of Mexico (1058W,
208N). All samples were found in tropical dry forests
sensu Holdridge (1967) and Olson et al. (2001),
sometimes referred to as seasonally dry tropical
forest (Bullock et al. 1995). The forests in the study
area are characterized by a warm sub-humid climate
with summer rains (Garc´
ıa 2004), and an extended
dry season during which more than 95% of the
plants lose their leaves completely. The wet season is
marked by a fast greening of the canopy which is the
product of short and intense rains intercalated with
dry periods. The mean annual precipitation is highly
variable, ranging from 340 to 1329 mm and with a
mean of 800 mm (1983–2015 period), of which
86.8% falls between the months of June and
October. The area has a strong oceanic influence
that maintains mean monthly values of relative
humidity above 75% year-round, with mean annual
temperature of 24.68C. (Garc´
ıa-Oliva et al. 2002;
Maass et al. 2002, 2018; Sa
´nchez-Azofeifa et al.
2013). Lichen communities cover most of the bark
of most trees and are typically represented by
crustose groups in the families Arthoniaceae,
Graphidaceae and Pyrenulaceae, while species of
macrolichens are few, rare, and usually limited to
the canopy (Herrera-Campos et al. 2017, 2019;
Miranda-Gonza
´lez 2012).
Anatomical studies.Specimens were studied at
Oregon State University using standard techniques
in an Olympus SZ61 dissecting microscope and an
Olympus BX41 compound microscope, both con-
nected to a NIKON D5300 digital camera. Sections
were mounted in tap water. KOH and IKI reagents
were used at 10% and 0.3% respectively following
Bungartz (2002). All anatomical measurements were
made in tap water. Morphological characters of
lirellae follow terminology in L¨
ucking (2009). Thin
layer chromatography (TLC) was performed with
solvents A and C using the standard techniques in
Culberson & Johnson (1982) and Orange et al.
(2010).
Taxon sampling.The phylogenetic analysis was
based on data from Lumbsch et al. (2014a) and
supplemented with sequences from Kalb et al.
(2004), Staiger et al. (2006), Rivas Plata et al.
(2013), Kraichak et al. (2013), L¨
ucking et al. (2013),
Lumbsch et al. (2014b), and new sequences
generated in this study. We included a total 273
sequences of mtSSU (122), nuLSU (99) and RPB2
(52) for 122 ingroup species, with representatives
from all the genera of Graphidaceae currently
published in GenBank, as well as all the available
species of Diorygma (Supplementary Table S1). No
new sequences of the RPB2 marker were generated
in this study, but given its good representation in
GenBank for Graphidaceae, it was included in the
multi-locus phylogenetic analysis.
DNA extraction, PCR, and sequencing.One or
two lirellae per sample were detached and washed in
acetone for five minutes. Total DNA was isolated
using the Sigma-Aldrich REDExtract-N-Amp Plant
PCR Kit (St. Louis, MO, U.S.A.) following the
manufacturer’s instructions, except only 15 lLof
extraction buffer and 15 lL of dilution buffer were
used per sample. The whole ITS and portions of
mtSSU and nuLSU were amplified and sequenced
using the following primers: ITS1F/ITS4 (Gardes &
Bruns 1993; White et al. 1990), mrSSU1/mrSSU3R
(Zoller et al. 1999), and AL2R/LR6 (Mangold et al.
2008; Vilgalys & Hester, 1990) respectively. If
samples were old or the PCR was problematic the
following primer combinations were used: ITS1F/
ITS86R for ITS1, ITS86F/ITS4 for ITS2 (Gardes &
Miranda-Gonza
´lez et al.: New genus Jocatoa in Graphidaceae and insights into subfamily Redonographoideae 129
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Bruns 1993; Op De Beeck et al. 2014; Turenne et al.
1999; White et al. 1990), and mrSSU1/mrSSU2R for
mtSSU (Zoller et al. 1999).
Each 10 lL PCR reaction consisted of 5 lL R4775
Sigma-Aldrich REDExtract-n-Amp PCR Ready Mix,
0.5 lLofeachprimer(10lM), 3 lLwater,and1lL
undiluted DNA. The PCR cycling conditions for ITS
were: 958C for 5 min, followed by 35 cycles of 958C
for 30 s, 528Cfor45s,and728Cfor105s,followedby
728Cfor5min.ThePCRcyclingconditionsfor
mtSSUandnuLSUwere:958C for 5 min, followed by
35 cycles of 958Cfor1min,538C(formtSSU)or578C
(for nuLSU) for 1 min, and 728C for 105 s, followed
by 728Cfor10min.2lLofeachPCRproductwas
visualized on 1.5% TBA agarose gel stained with
GelRed (Biotium). Single bands were cleaned directly
from PCR products with ExoSAP-IT tfor PCR
product cleanup (Affymetrix, Santa Clara, CA,
U.S.A.). If double bands appeared the rest of the
PCR product was gel extracted and cleaned with
GELase (Epicentre Biotechnologies, Madison, WI,
U.S.A.) following manufacturer’s instructions.
Samples were sequenced at Eurofins MWG
Operon LLC (Louisville, KY, U.S.A.). Each 12 lL
reaction consisted of 2.4 lL primer (at 10 lM), 2 lL
undiluted PCR product cleaned with ExoSAP and
7.6 lL water or 2.4 lL primer (at 10 lM) and 9.6 lL
DNA cleaned with GELase.
Phylogenetic analysis.New sequences were
edited in Geneious 8.1.9 (Kearse et al. 2012). All
sequences of mtSSU, nuLSU, and RPB2 were aligned
independently using the GUIDANCE2 server (Sela et
al. 2015) with the multiple sequence alignment
algorithm MAFFT (Katoh & Standley 2013). Unre-
liable columns were removed using a cutoff of 0.6.
Introns were visually identified and removed. The
final alignment is available as Supplementary Table
S2. A maximum likelihood (ML) analysis of all
markers partitioned by marker was performed using
the RAxML-HPC BlackBox 8.2.10 (Stamatakis 2014),
with 450 bootstrapping replicates as automatically
determined by RAxML using a saturation criterion.
Furthermore, a Bayesian analysis was performed
using MrBayes 3.2.6 (Huelsenbeck & Ronquist
2001), with two independent runs of three million
generations each, resampling every 1000 trees, 25%
burn-in, and heated chains of 0.2. Both analyses were
done with the GTR GAMMA model and run on the
Cipres Gateway server (Miller et al. 2010). Single
marker analyses were also performed to visually test
for topological incongruence. The final ML tree was
plotted using FigTree 1.4 (Rambaut & Drummond
2012) and edited in Photoshop CS6.
RESULTS
Phylogenetic analysis.Atotalof23new
sequences were generated for this study (Table 1).
The combined data set consisted of 124 OTU’s and
2866 unambiguously aligned characters, 939 from
mtSSU, 982 from nuLSU and 945 for RPB2,of
which 789, 812, and 673 respectively were phyloge-
netically informative (Supplementary Table S2).
The combined Maximum Likelihood and Bayesian
analysis (Fig. 1,Supplementary Figure S1) recov-
ered the three subfamilies and 7 tribes as supported
branches presented in Lumbsch et al. (2014a), with
the exception of the tribes Graphideae and Wirthio-
tremateae that did not reach threshold support
Table 1. GenBank accession numbers of the new sequences generated in this study. – indicates missing data. * indicates holotypes. All samples from
Mexico (all specimens in MEXU).
Species Voucher ITS mtSSU nuLSU
Gymnographopsis corticicola* Miranda 1158 – MK776937 –
G. corticicola Miranda 4567 MK776871 MK776935 MK776866
G. corticicola Miranda 4729 MK776872 MK776936 MK776867
Jocatoa agminalis Miranda 2040 MK776873 MK776938 –
J. agminalis Miranda 3080 MK776874 MK776939 –
J. agminalis Miranda 4744 MK776875 MK776940 MK776868
J. agminalis Miranda 4745 MK776876 MK776941 MK776869
Redonographa parvispora Miranda 1099 MK776877 – –
R. parvispora* Miranda 1128 MK776878 – –
R. parvispora Miranda 4558 MK776879 MK776942 –
Schistophoron tenue Herrera-Campos et al. 77 MK776880 MK776943 –
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values. The new sequences of Gymnographopsis were
positioned as sister to Redonographa in subfamily
Redonographoideae, which was anticipated by
L¨
ucking et al. (2013), although the type species has
not yet been sequenced. The new genus and
combination Jocatoa agminalis clustered with high
support as sister to Schistophoron and is unrelated to
the monophyletic Diorygma clade. Sequences of ITS
were obtained for all new specimens; unfortunately,
we could not include them in the analysis because
sequences of Graphidaceae for this marker are
extremely underrepresented in GenBank. Nonethe-
less, we made the new ITS sequences available
because the ITS is the recommended genetic
barcode for fungi (Schoch et al. 2012) and is useful
for phylogenetic, environmental, floristic and eco-
logical studies. We encourage other researchers to
include the ITS marker in their studies.
Figure 1. Phylogeny of the family Graphidaceae based on a Maximum Likelihood analysis of the markers mtSSU, nuLSU and RPB2. Support values are
shown as numbers if Maximum Likelihood bootstrap values 70 and as bold branches if Bayesian posterior probabilities 0.95. Bold names show new
sequences from this study. For collapsed branches refer to Supplementary Figure S1.
Miranda-Gonza
´lez et al.: New genus Jocatoa in Graphidaceae and insights into subfamily Redonographoideae 131
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The recovered topology within Graphidaceae
matches that of earlier studies (L¨
ucking et al. 2013;
Lumbsch et al. 2014a; Rivas Plata et al. 2013) but was
found in partial conflict with the topology obtained
by Kraichak et al. (2018) and used for their proposed
reclassification of Graphidaceae into four families.
The two clades in accordance between these studies
were subfamily Fissurinoideae (Fissurinaceae sensu
Kraichak et al. 2018) and tribe Thelotremateae in
subfamily Graphidoideae (Thelotremataceae sensu
Kraichak et al. 2018). Differences were found in the
position of Platythecium, which has generally been
recovered within tribe Graphideae in subfamily
Graphidoideae (Graphidaceae s.str. according to
Kraichak et al. 2018) but outside that clade in the
latter study, and in the placement of tribes Dip-
loschisteae, Leptotremateae, Ocellularieae, and Wir-
thiotremateae, which were united into a single family,
Diploschistaceae by Kraichak et al. (2018) but in all
other analyses, including the present, formed three
unrelated clades. Our phylogenetic analysis also
confirmed the placement of tribe Acanthothecieae
and the genera Aggregatorygma and Phaeographopsis
as additional lineages likely unrelated to any of the
families proposed by Kraichak et al. (2018). We
consider this topology a strong argument to maintain
Graphidaceae in the sense of L¨
ucking et al. (2017a).
TAXONOMY
Gymnographopsis corticicola R.Miranda, Herrera-
Camp. & L¨
ucking, sp. nov.Fig. 2
MYCOBANK MB 834676
ITS BARCODING SEQUENCE ACCESSIONS: MK776871,
MK776872 (paratypes).
Differing from other species of Gymnographopsis in
being corticolous, having smaller ascospores (15–
18 33–5 lm), and containing norstictic acid.
TYPE: MEXICO. JALISCO: La Huerta Mun., Chamela-
Cuixmala Biosphere Reserve, Estaci ´
on de Biol-
og´
ıa Chamela, between trails Chachalacas and
Camino Antiguo del Sur, mature tropical dry
forest, 1982905300 N, 1058203300 W, elev. 107 m, on
bark of Loncharpus sp., Jun. 2009, R. Miranda-
Gonza
´lez 1158 (holotype: MEXU!).
Description.Thallus crustose, corticolous, epi-
peridermal, continuous to rimose, ecorticate,
whitish green to pale grey, with a black prothallus
present at contact lines with other lichens. Photo-
biont trentepohlioid, in a continuous layer sur-
rounded by small crystals that appear beige to
salmon in polarized light and that dissolve in KOH.
Ascocarps abundant, lirelliform, immersed to
erumpent, straight to curved, rarely branched,
0.2–1.2 30.1–0.2 mm; thalline margin raised above
disc, complete to lateral, whitish grey; disc initially
concealed, but in mature lirellae exposed and open
(Fig. 2B), black to light brown. Exciple not striate,
laterally light brownish, apically brownish to black
and sometimes appearing carbonized, POL–, 10–30
lmwide,inyoungascocarpsforminganopenroof
on top of the hymenium (Fig. 2F)thatlaterrecedes
as the ascocarps mature; hymenium hyaline, not
inspersed with oil droplets, embedded in a
gelatinous matrix, sparsely anastomosed, 45–75
lm high, I–; periphysoids short, smooth to slightly
verrucose, originating in the inner exciple from
about the upper third of the hymenium to the
inner tip of the exciple, embedded in a gelatinous
matrix, 7.5–16 lm long; epihymenium not differ-
entiated; epithecium absent; hypothecium hyaline
yellowish, 12–24 lm deep. Ascospores 8 per ascus,
hyaline, mostly with 3 transverse septa but some
with up to 5 septa, very rarely with 1 longitudinal
septum, oblong, 12.5–18 33–5 lm, I–, frequently
with a rectangular gelatinous perispore of up to
3(–5) lmthick.
Chemistry.Norstictic (major) and connorstictic
(minor) acids.
Etymology.The epithet ‘‘cortici-cola’’ combines
two words from Latin, cortex, genitive corticis (bark)
and the suffix -cola (inhabitant of), in reference to
the substrate as it is so far the first species in the
subfamily Redonographoideae known to grow on
bark.
Ecology and distribution.Gymnographopsis
corticicola has only been found in the mature
tropical dry forest of the Chamela-Cuixmala Bio-
sphere Reserve. It is a frequent species in the study
area, generally associated with the main trunk of
trees of the genus Lonchocarpus and less frequently
with Bursera cf. exelsa, Cordia alliodora,Erythrina
lanata,Forchhammeria pallida,andHeliocarpus
pallidus.
Remarks.Gymnographopsis corticicola is super-
ficially similar to species of the genera Diorygma
and Thalloloma, but these genera have Iþviolet
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spores and lack periphysoids. The closely related
genus Redonographa differs by its complete to
laterally carbonized exciple and by the nature of the
periphysoids, which grow from the inside of the
excipulum in Gymnographopsis and from the
outside of the excipulum in Redonographa.Only
two other species are known in the genus
Gymnographopsis:G. chilena Dodge (1966) and G.
latispora Egea & Torrente (1996), both from the
southern hemisphere, saxicolous, with much larger
ascospores, longer lirellae, and without norstictic
acid. The new species is therefore tentatively
assigned to the genus Gymnographopsis,butthe
differences with the other two species, which have
not been sequenced, suggest that a third, unrecog-
nized genus might be involved.
Additional specimens examined.MEXICO.
JALISCO: La Huerta Mun., Chamela-Cuixmala Bio-
Figure 2. Gymnographopsis corticicola.A–C. Habit showing lirellae, note open discs in B and aggregate lirellae in C. D. Ascospores with rectangular
perispore and apical folds. E. Section of a mature lirella showing periphysoids. F–G. Section of an immature lirella in water and KOH respectively. H.
Section of a mature lirella. Scale: A–C 1 mm; D 10 lm; E–H40lm. Specimens: A R. L ¨
ucking 25090;B,E,HR. Miranda-Gonza
´lez 4365;CR. Miranda-
Gonza
´lez 4729;D,F,GR. Miranda-Gonza
´lez 4367.
Miranda-Gonza
´lez et al.: New genus Jocatoa in Graphidaceae and insights into subfamily Redonographoideae 133
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sphere Reserve, Estaci ´
on de Biolog´
ıa Chamela, on
Chachalacas trail, elev. 60 m, on bark of unknown
tree, Jun. 2008, R. L ¨
ucking 25090, on bark of
Erythrina lanata,Lonchocarpus spp., and unknown
trees, Jun. 2009, R. Miranda-Gonza
´lez 1105, 1121,
1680, 1681, 1685, 4365, 4366, 4367, on bark of
unknown tree, Jun. 2014, R. Miranda-Gonza
´lez
4567; ibid.; near Hornitos stream, 250 NE of the
end of Eje Central road, elev. 73 m, on bark of
Cordia alliodora,Forchhammeria pallida,Lonchocar-
pus sp., and an unknown tree, Jun. 2009, R.
Miranda-Gonza
´lez 795, 1570, 1574, 1581, 4369; ibid.;
on Tej ´
on trail, elev. 57 m, on bark of Bursera cf.
exelsa, Apr. 2010, R. Miranda-Gonza
´lez 2103, 2122,
on bark of unknown tree, Sep. 2011, A. Barcenas-
Pe˜
na 4616, 4618, on bark of unknown tree, Aug.
2014, R. Miranda-Gonza
´lez 4729. (all specimens in
MEXU).
Redonographa parvispora R.Miranda, Barcenas-
Pe˜
na & L¨
ucking, sp. nov.Fig. 3
MYCOBANK MB 834675
ITS BARCODING SEQUENCE ACCESSIONS: MK776878
(holotype), MK776877, MK776879 (paratypes).
Similar to Redonographa galapagoensis but with
smaller, 3-septate ascospores, longer lirellae,
lateral to complete excipular carbonization, and
corticolous habit.
TYPE: MEXICO. JALISCO: La Huerta Mun., Chamela-
Cuixmala Biosphere Reserve, Estaci ´
on de Biol-
og´
ıa Chamela, between trails Chachalacas and
Camino Antiguo del Sur, mature tropical dry
forest, 1982905100 N, 1058203000 W, elev. 136 m, on
bark of Piptadenia constricta, Jun. 2009, R.
Miranda-Gonza
´lez 1128 (holotype: MEXU!).
Description.Thallus crustose, corticolous, epi-
peridermal, rimose, ecorticate to weakly corticate,
whitish grey, with a black prothallus present at
contact lines with other lichens. Photobiont trente-
pohlioid, in a continuous layer surrounded by small
crystals that appear beige in polarized light and that
dissolve in KOH, as well as insoluble coarse crystals.
Ascocarps abundant, lirelliform, erumpent to prom-
inent, mostly curved to sinuous, sparsely branched,
1–7 30.2–0.3 mm; thalline margin complete but
thin above and giving the impression of pruinose
discs, concolorous with the thallus; disc concealed,
black. Exciple laterally to completely carbonized,
POL–, 20–50 lm wide, not striate, covering most of
the hymenium, with short and warty periphysoids
originated from the carbonized exciple and specially
abundant towards the outside of it; hymenium
hyaline, not inspersed with oil droplets, embedded
in a gelatinous matrix, 60–90 lmhigh,I–;
paraphyses simple to anastomosed near the excip-
ulum; epihymenium not differentiated; epithecium
absent; hypothecium hyaline, 45–90 lm deep.
Ascospores 8 per ascus, ellipsoid, hyaline, with 3
transverse septa, 10–15 32.5–4.5 lm, I–, frequently
with a rectangular gelatinous perispore of up to 3
lm thick.
Chemistry.Norstictic (major) and connorstictic
(minor) acids.
Etymology.The epithet refers to the ascospores,
which are the smallest among the species of this
genus with transverse septation.
Ecology and distribution.Redonographa parvis-
pora has only been found in the mature tropical dry
forests of the Chamela-Cuixmala Biosphere Reserve.
It is a rare species in the study area. Most specimens
were found on the main trunk of trees of Piptadenia
constricta.
Remarks.The corticolous Redonographa parvis-
pora is characterized by having warty periphysoids,
small and narrow spores with three transverse septa,
and norstictic acid. The only other species in the
genus with warty to verrucose periphysoids is the
saxicolous Redonographa galapagoensis Bungartz &
L¨
ucking, which has larger submuriform ascospores,
and mostly rounded lirellae. The only species in the
remarkably similar but unrelated genus Carbacan-
thographis, with norstictic acid as major lichen
product is Carbacanthographis induta (M¨
ull. Arg.)
L¨
ucking, but this species has ascospores up to 70 lm
long (L¨
ucking et al. 2009). Carbacanthographis
marcescens (F´
ee) Staiger & Kalb sometimes have
traces of norstictic acid but its major lichen product
is salazinic acid, and the species further differs in its
muriform ascospores (Staiger 2002).
Redonographa parvispora shares the warty pe-
riphysoids and the corticolous habit with the genus
Carbacanthographis in the Graphidoideae. As these
two characters are traditionally used to distinguish
between these genera, the new species would appear
to belong in Carbacanthographis,however,we
described it in Redonographa for two reasons: First,
the available sequences of ITS and mtSSU support
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its position in Redonographoideae (Fig. 1), of the
two genera available in the subfamily, Redonographa
shares with the new species the excipular carbon-
ization and the periphysoids type. Second, the
rectangular perispore is similar to the one of
Gymnographopsis corticicola in the same subfamily,
a character that to our knowledge has never been
reported for fungi. Perispores are common in some
genera of lichenized fungi, but typically their outline
follows that of the spore wall.
Unfortunately, the samples of Redonographa
parvispora were difficult to sequence and only three
sequences of ITS and one short sequence of mtSSU
were successful. From the available sequences of
Redonographa in GenBank there is none of ITS and
only one of mtSSU from R. chilensis. This resulted in
few phylogenetically informative characters and lack
ofmolecularsupportfortheinclusionofR.
parvispora in Redonographa. To avoid unnecessary
taxonomic changes, we refrained from describing a
new genus and tentatively assigned the new species
to Redonographa. A future analysis with more
sequences will be needed to solve this problem.
A Brazilian collection referred as ‘‘KALB 28829
(systematic position unclear)’’ in Staiger & Kalb
(1999) is remarkably similar to R. parvispora,
sharing the lateral to completely carbonized exciple,
warty and short periphysoids, ascospores size and
septation pattern, and norstictic acid as major lichen
product. It only differs in the spore’s cell lumina,
which are somehow interconnected in Kalb’s
illustration, and in the form of the perispore, which
Figure 3. Holotype of Redonographa parvispora (R. Miranda-Gonza
´lez 1128). A–B. Habit showing lirellae. C. Section of lirella showing complete
excipular carbonization. D. Section of lirella showing lateral excipular carbonization. E. Verrucose periphysoids in KOH. F. Ascospores with rectangular
perispore. G. Ascospores with perispore pushed towards one side. H. Biseriate ascospores in asci. Scale: A–B 1 mm; C–E40lm; F–H10lm.
Miranda-Gonza
´lez et al.: New genus Jocatoa in Graphidaceae and insights into subfamily Redonographoideae 135
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is a typical oval shape (Fig. 4 in Staiger & Kalb
1999). Nonetheless, given their scarce material these
differences may be just an artifact. As we did not
examine Kalb’s collection, we are not sure if R.
parvispora and KALB 28829 are conspecific. There-
fore, we refrain from extending the distribution of
R. parvispora to Brazil.
Additional specimens examined.MEXICO.
JALISCO:LaHuertaMun.,Chamela-Cuixmala
Biosphere Reserv e, Estaci ´
on de Biolog´
ıa Chamela,
near B ´
uho trail, elev. 83 m, on bark of unknown
tree, Nov. 2008, A. Barcenas-Pe ˜
na 2006, 2007,
2008, 2011;ibid.;betweentrailsChachalacasand
Camino Antiguo del Sur, elev. 136 m, on bark of
Piptadenia constricta,Jun.2009,R. Miranda-
Gonza
´lez 1099, 1134, 1135; ibid.; on Chachalacas
trail, elev. 98 m, on bark of unknown tree, Jun.
2014, R. Miranda-Gonza
´lez 4558.(allspecimensin
MEXU).
WORLDWIDE KEY TO THE KN OWN SPECIES OF SUBFAMILY
REDONOGRAPHOIDEAE IN GRAPHIDACEAE
1. Exciple laterally to completely carbonized; periphysoids mostly
forming from the top external area of the carbonized exciple
and not embedded in a gelatinous matrix; norstictic acid
present ................................................................. (Redonographa)2
1. Exciple not carbonized, sometimes apically brownish black and
appearing carbonized; periphysoids mostly forming from the
inner part of the exciple and embedded in a gelatinous matrix;
norstictic acid present or not......................... (Gymnographopsis)6
2. Periphysoids verrucose to warty; ascospores less than 6 lmwide
... 3
2. Periphysoids smooth; ascospores more than 7 lm wide.............. 4
3. Ascospores submuriform, 5–6 transverse and 1–2 longitudinal
septa, 15–20 34–5 lm; exciple completely carbonized; lirellae
short to rounded; disc often partially open; saxicolous habit;
Galapagos................................................................. R. galapagoensis
3. Ascospores with 3 transverse septa, 10–15 32.5–4.5 lm; exciple
lateral to completely carbonized; lirellae elongated; disc con-
cealed; corticolous habit; western Mexico................ R. parvispora
4. Ascospores with 3–7 transverse septa, 20–28 38–11 lm; lirellae
unbranched to sparsely branched; exciple lateral to completely
carbonized; Californian peninsula (U.S.A., Mexico) and Gala-
pagos.............................................................................. R. saxorum
4. Ascospores submuriform, 18–25 38–11 lm; lirellae frequently
branched to stellate; exciple lateral or completely carbonized;
Chile.................................................................................................... 5
5. Lirellae stellate-branched to pseudostromatic; exciple com-
pletely carbonized; ascospores 18–25 38–10 lm, 3–5
transverse and 0–2 longitudinal septa, with regular cell lumina
(graphidoid) .............................................................. R. chilensis
5. Lirellae irregularly branched and bent; exciple laterally
carbonized; ascospores 18–22 39–11 lm, 4–5 transverse and
1–2 longitudinal septa, with irregular cell lumina (astrothe-
lioid) .......................................................................... R. saxiseda
6. Ascospores 15–18 33–5 lm; lirellae to 1 mm long; norstictic acid
present in thallus; corticolous habit; western Mexico.... G. corticicola
6. Ascospores larger than 20 38lm; lirellae longer than 1 mm;
norstictic acid lacking; saxicolous habit; southern hemisphere ... 7
7. Ascospores 20–26 310–12 lm; lirellae 2–3 mm long; with an
unknown substance of the stictic acid complex; northern Chile . . .
...................................................................................................... G. chilena
7. Ascospores 20–31(–37) 312–16(–18) lm; lirellae 0.8–1.5 mm
long; no substances detected by TLC; South Africa... G. latispora
Jocatoa R.Miranda, gen. nov.Fig. 4
MYCOBANK MB 834677
A new genus in the family Graphidaceae, subfamily
Graphidoideae, tribe Graphideae, differing from
Diorygma in that the paraphysis tips are simple,
thin and do not form an epithecium. Thallus
ecorticate; ascocarps solitary to pseudostromatic;
excipulum not carbonized; spores muriform, Iþ
strongly violet; chemistry of the stictic acid complex.
Type species:Jocatoa agminalis (Nyl.) L¨
ucking,
Herrera-Camp. & R.Miranda.
Etymology.The genus is named in honor of the
late Prof. Jos´
eCastillo Tovar (1935–2012), for
educating the current generation of Mexican
mycologists and for introducing the first author to
the study of lichens.
Remarks.The new monospecific genus strongly
resembles species of Diorygma in the ecorticate thallus,
spore type, chemistry, and in the laterally branched
and anastomosed paraphyses that are embedded in a
thick gelatinous matrix. Nonetheless, in Diorygma the
paraphysis tips are reticulately branched, anastomosed
and thickened, which form a clear epithecium (Kalb et
al. 2004), while in the new genus the paraphyses tips
are simple, thin and do not form an epithecium. The
genus Glyphis differs by having a heavily carbonized
exciple with dark brown paraphysis tips intermingled
with brown granules.
The younger names of genera that are synonyms
with Diorygma (Type Diorygma hieroglyphicum) are:
Solenographa (Type Diorygma confluens), Glaucina-
ria (Type Diorygma poitaei), and Cyclographina
(Type Diorygma pruinosum). Of these, D. poitaei
and D. pruinosum cluster in a monophyletic group
with D. hieroglyphicum.Diorygma confluens has not
been sequenced yet, but it differs from the new
genus in the carbonized exciple and in the presence
of the epithecium. As the genus Jocatoa is outside
the Diorygma clade (Fig. 1), none of those names are
available.
136 The Bryologist 123(2): 2020
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Figure 4. Jocatoa agminalis.A–D. Habit showing lirellae. E. Section of lirella showing anastomosed paraphyses towards the exciple. F. Section of lirella
showing tips of paraphyses in KOH. G. Muriform ascospore. H. Section of lirellae showing uncarbonized excipulum (appearing black due to presence of
abundant crystals that dissolve in KOH). Scale: A–D 1 mm; E–G40lm; H 100 lm. Specimens: A A. Lindig 143 (isotype of Graphis agminalis,G); B J. W.
Eckfeldt 56A (holotype of Medusulina texana); C, F R. Miranda-Gonza
´lez 2040;DR. Miranda-Gonza
´lez 5005;E,G,HR. Miranda-Gonza
´lez 5004.
Miranda-Gonza
´lez et al.: New genus Jocatoa in Graphidaceae and insights into subfamily Redonographoideae 137
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The type species of Jocatoa was previously
included in Medusulina, a polyphyletic genus no
longer recognized and loosely characterized by
having aggregate lirellae, carbonized excipulum
and muriform ascospores (L¨
ucking 2013; Zahl-
bruckner 1926). However, the name is no longer
available because its type species, Medusulina nitida,
belongs in Fissurina (Staiger 2002). Medusulina was
previously believed to be the hyaline ascospore
counterpart of Sarcographa (M¨
uller 1894) or close to
Glyphis but with muriform ascospores (Zahlbruck-
ner 1926). Besides Fissurina and the new genus
Jocatoa, another species previously described in
Medusulina is now a member of Redonographa
(L¨
ucking et al. 2013). None of these genera are
particularly close to Sarcographa or Glyphis, al-
though these last two genera together with Jocatoa
belong in the same tribe, Graphideae.
Jocatoa agminalis (Nyl.) L¨
ucking, Herrera-Camp. &
R.Miranda, comb. nov.Fig. 4
MYCOBANK MB 834678
”Graphis agminalis Nyl., Ann. Sci. Nat., Bot., S´
er. 5
7: 334 (1867); ”Graphina agminalis (Nyl.)
Zahlbr., Cat. Lich. Univers. 2: 394 (1923); TYPE:
COLOMBIA. Near Magdalena River, elev. 100
m, on bark, 1863, A. Lindig 143 (holotype: H-
NYL 7602!; isotypes: BM!, G!, M!).
¼Medusulina texana M¨
ull. Arg., Bull. Herb. Boissier
2: 93 (1894); TYPE: U.S.A. TEXAS: Brownsville, on
bark, 1881, J.W. Eckfeldt 56A (holotype: G!).
Description.Thallus crustose, corticolous, epi-
peridermal, ecorticate, light yellowish brown to
olive-green, sometimes not continuous and then
with endoperidermal parts but always well devel-
oped near the ascocarps, UV–, with a black
prothallus present at contact lines with other
lichens. Photobiont trentepohlioid, in a continuous
layer surrounded by small crystals that appear beige
in polarized light and that dissolve in KOH, as well
asinsolublecoarsecrystals.Ascocarpsabundant,
lirelliform to rounded, erumpent, straight to
curved, unbranched when young to stellate or in
groups forming white to cream-colored pseudos-
tromata, individual lirellae 0.2–1.5 30.2–0.25 mm,
in groups up to 1 cm long; thalline margin lateral,
raised above disc, concolorous with the thallus;
disc black to brown black, sometimes with
remnants of thallus that give the impression of
coarse pruina, immersed, exposed when mature
but sometimes partly covered by the thalline
margin. Exciple not striate, hyaline to light brown,
with small crystals and a granular appearance
POLþthat originates from the thallus margin,
22–30 lm wide; hypothecium hyaline 30–50 lm
deep; hymenium hyaline, not inspersed with oil
droplets, embedded in a strong gelatinous matrix,
175–250 lm high, I–, epihymenium golden brown,
with a granulose appearance; paraphyses simple to
anastomosed specially towards the exciple, tips
simple and not swollen, periphysoids absent.
Epithecium absent. Ascospores 1 per ascus, hyaline,
strongly muriform, ellipsoid, inner cells larger than
peripheral cells, (110–)150–192(–217) 3(45–)50–
70(–85) lm, Iþstrongly violet, frequently with a
hyaline gelatinous perispore.
Chemistry.Hypostictic, stictic, cryptostictic,
and constictic acids, plus three unknown substances
with Rf 5–6 (solvent A) and Rf 5 (solvent C) that
react UVþred and white on TLC plates before the
acidþheat treatment.
Ecology and distribution.In the study area this
species is mostly found in the mature tropical dry
forests of the Chamela-Cuixmala Biosphere Reserve,
but one depauperate sample (R. Miranda-Gonza
´lez
3080) was found in a secondary forest in an area
surrounding the Reserve. It is a rare species in the
study area, found on the main trunk of the
phorophytes Apoplanesia paniculata,Cordia allio-
dora,Thouinia paucidentata, and in the canopy of
Amphipterygium adstringens. The species was previ-
ously known from the type locality of Graphis
agminalis in Colombia, a low altitude interandine
dry valley along the Magdalena River, and from the
type locality of Medusulina texana in Brownsville,
Texas (M¨
uller 1984). Further collections (not seen
by us) are registered in the Consortium of North
American Lichen Herbaria (CNALH) from Louisi-
ana (USA) and Tamaulipas (Mexico) (Accessed
through Consortium of North American Lichen
Herbaria (CNALH) Data Portal, http//:lichenporta-
l.org/portal/index.php, 2018-07-16). Thus, through-
out its range, J. agminalis appears to be a corticolous
species associated with dry forest and semi-arid
areas.
Remarks.Jocatoa agminalis is overall similar to
Diorygma monophorum (Nyl.) Kalb, Staiger & Elix,
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which has smaller ascospores (105–165 335–60
lm), anastomosing paraphysis tips, lacks stictic
acid, and does not have aggregate ascocarps.
Notably, D. monophorum was described as having
a slightly different nature of the paraphyses, as
hardly anastomosing, thinner towards the tips and
forming a mostly distinctly developed epithecium
(Kalb et al. 2004), which might be explained by the
observation that in many species of Diorygma, only
the paraphyses lateral to the excipulum show
distinct anastomoses. The original description of
Medusulina texana by M¨
uller (1894) and subse-
quently the treatment by Fink (1935) mention
soredia for this taxon; however, neither the type
collection nor our samples have soredia, so this
possible referred to the crumbling remnants of the
thallus margins of the ascomata.
Additional specimens examined.MEXICO.
JALISCO: La Huerta Mun., Chamela-Cuixmala
Biosphere Reserve, Estaci ´
on de Biolog´
ıa Chamela,
on Tej ´
on trail, elev. 57 m, on bark of Apoplanesia
paniculata, Jun. 2009, R. Miranda-Gonza
´lez 1451,
2040,onbarkofThouinia paucidentata, May 2015,
R. Miranda-Gonza
´lez 5004,onbarkofApoplanesia
paucidentata, Jun. 2015, R. Miranda-Gonza
´lez
5005, on bark of fallen branch from canopy of
unknown tree, Dec. 2015, R. Miranda-Gonza
´lez
4745;ibid.;onEjeCentralroad430m,elev.62m,
on bark of fallen branches from the canopy of
Amphipterygium adstringens, Dec. 2015, R. Miran-
da-Gonza
´lez 4744; ibid.; Surrounding areas of the
Chamela-Cuixmala Biosphere Reserve, Ejido Cai-
ma
´n, elev. 72 m, on bark of Cordia alliodora,Sep.
2010, R. Miranda-Gonza
´lez 3080.(allspecimensin
MEXU).
DISCUSSION
Subfamily Redonographoideae.Our phyloge-
neticanalysisincludesforthefirsttimesequences
of a species that can be assigned to the genus
Gymnographopsis, supporting its inclusion in
subfamily Redonographoideae. Traditionally, the
only two genera in this subfamily were separated
bythepresenceofnorsticticacidandlateralto
complete excipular carbonization in Redonographa
versus absence of norstictic acid and an uncar-
bonized exciple in Gymnographopsis (L¨
ucking et al.
2013). With the description of G. corticicola in this
paper,thepresenceofnorsticticacidisnolongera
good character to distinguish these genera. We
propose instead to emphasize the nature of the
periphysoids and excipular carbonization. In
Gymnographopsis, the periphysoids are embedded
in a gelatinous matrix and originate from the inner
part of the exciple; in the case of Gymnographopsis
corticicola, the periphysoids start to appear at the
upper third of the hymenium and extend towards
the tip of the exciple. In Redonographa the
periphysoids are not embedded in a gelatinous
matrix and mostly originate from the top and
outer part of the carbonized exciple, similar to
Carbacanthographis.
This is the first report of the genus Gymnogra-
phopsis for the Northern Hemisphere, with previous
localities being in northern Chile (Dodge 1966) and
South Africa (Egea & Torrente 1996). The whole
subfamily Redonographoideae is known to occur
only on subtropical and tropical coastal areas with a
dry season. Except for the South African G. latispora,
all species occur along the coast of the Pacific Ocean
(L¨
ucking et al. 2013). Our study area near the Pacific
Coast of Mexico fits the known ecology of the
subfamily.
Interestingly, the new species Gymnographopsis
corticicola and Redonographa parvispora are the only
species in Redonographoideae that are corticolous.
It was hypothesized by L¨
ucking et al. (2013) that the
common ancestor of Graphidaceae was corticolous
and from the wet tropics, and thus, that the peculiar
saxicolous ecology and subtropical-dry habitat of
the subfamily Redonographoideae evolved second-
arily within the subfamily. The inclusion of cortico-
lous species in both genera further supports the idea
of a derived association with rock substrates in
Redonographoideae. However, these new species
represent a problem for the previous concept of the
subfamily, because being saxicolous was considered
an important diagnostic character. Currently Re-
donographoideae is only separated from other
subfamilies by its tendency to occupy subtropical
and tropical coastal dry habitats and else by forming
a separate clade on a long branch near the base of
Graphidaceae.
Our samples of both Gymnographopsis cortici-
cola and Redonographa parvispora have a peculiar
rectangular shaped perispore with apparent folds at
both ends (Figs. 2D and 3F-G). In some spores the
ends of the perispore are reduced and the tips of the
spore protrude from the perispore, perhaps to start
Miranda-Gonza
´lez et al.: New genus Jocatoa in Graphidaceae and insights into subfamily Redonographoideae 139
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germination. Even though the presence of this
perispore is frequent, not all spores show it, but
this variability is typical of other perispore-produc-
ing species, as in Opegrapha and Rhizocarpon.We
currently do not know if the perispore is correlated
with the maturity of the spores. This type of
perispore has not been reported for fungi before
and may represent a unique character of Redonog-
raphoideae. If this is the case, it could be useful as a
diagnostic character of the subfamily, as well as to
distinguish Redonographa form the very similar but
unrelated genus Carbacanthographis.
Subfamily Graphidoideae.Our phylogenetic
analysis agrees with Kalb et al. (2004) in that
Diorygma forms a monophyletic clade when
Thalloloma is included (Rivas Plata et al. 2013).
Nonetheless, of the 71 species of Diorygma
(L¨
uckingetal.2017a),onlyahandfulhavebeen
sequenced, including the type species of both
genera. Our analysis clearly shows that the new
genus Jocatoa does not belong in the Diorygma
clade. Given that Diorygma is a large genus and that
both G. corticicola and J. agminalis could easily pass
as Diorygma species, we expect some of the current
species of Diorygma to fall outside the Diorygma
clade. We also expect that the genus Jocatoa will
remain monospecific for only a short period of
time. On the other hand, Jocatoa differs from
species of Diorygma in the dense thallus cortex,
with the exception of D. erythrellum which,
however, has a different type of cortex, and hence
its placement outside Diorygma is not entirely
surprising.
The new genus Jocatoa is here recovered as sister
to Schistophoron, a mazaediate genus that was
isolated within the tribe Graphideae. Nadvornikia
is the only other truly mazaediate genus in Graph-
idaceae, where it originated independently of its
occurrence in Schistophoron (Lumbsch et al. 2014b).
Nadvornikia was recently determined to include two
non-mazaediate species in a paraphyletic assembly
near N. hawaiiensis (Medeiros et al. 2017). However,
the differences between Schistophoron and Jocatoa go
beyond the mazaediate ascocarp and they should
not be considered congeneric, also given the
reciprocally monophyletic topology in combination
with long branches leading to each genus. Apart
from forming mazaedia, Schistophoron is distin-
guished by prominent to sessile lirellae and
ascospores that are brown, with submuriform to
transverse septation, up to 15 310 lm, and non-
amyloid. Jocatoa, on the other hand, has immersed
to erumpent lirellae and ascospores that are hyaline,
strongly muriform, larger than 150 350 lm, and
strongly amyloid (violet). Amyloid ascospores were
found to be conserved at the generic and even tribe
level within the tribe Graphideae and most of the
subfamily Graphidoideae (Lumbsch et al. 2014b).
However, the difference between Jocatoa and
Schistophoron in almost every conceivable character
shows that the placement of clades with unique
features cannot be predicted by phenotype.
The two new species introduced in this paper
depend strongly on undisturbed tropical dry forests.
This ecosystem suffers from constant anthropogenic
pressures and it is considered among the most
threatened in the world (Janzen 1988; Miles et al.
2006). In Mexico, tropical dry forests have a high
conversion rate to use in agriculture, and most of
the forested area in the country is heavily fragment-
ed and disturbed (Portillo-Quintero & Sa
´nchez-
Azofeifa 2010; Trejo & Dirzo 2000). Given that only
1.1% of the total extent of this ecosystem in Mexico
is under protection (Sa
´nchez-Azofeifa et al. 2009),
we consider the two new species described here to be
vulnerable, especially Redonographa parvispora,
which was found to be a rare species with a very
limited distribution inside the study area.
ACKNOWLEDGMENTS
Financial support for the first author was provided by CONACYT
(Reg. 217222) and SEP (scholarship BC-2239. Este art´
ıculo se ha
realizado con el apoyo de beca de la Secretar´
ıa de Educaci ´
on P ´
ublica
y del Gobierno Mexicano). Funding for field work was granted to
M. A. Herrera Campos by PAPIIT-UNAM (project IN225808) and
CONABIO (Project JF157). The participation of RL in the project,
in addition to fieldwork, was supported by two grants from the
National Science Foundation: Neotropical Epiphytic Microlichens –
An Innovative Inventory of a Highly Diverse yet Little Known Group
of Symbiotic Organisms (DEB-715660 to The Field Museum; PI R.
L¨
ucking) and ATM – Assembling a Taxonomic Monograph: The
Lichen Family Graphidaceae (DEB-1025861 to The Field Museum;
PI T. Lumbsch, CoPI R. L¨
ucking). We are grateful to Jorge Vega
(Director at the time of the study) and the personnel of Chamela
Biological Station for logistic support and to the Posgrado en
Ciencias Biologicas, UNAM. Bruce McCune kindly reviewed an
early version of the manuscript. We would like to thank the
personnel of the herbaria MEXU and OSC for facilitating loans for this
study, as well as James Lawrey and an anonymous reviewer for
useful suggestions on the manuscript. The curator at G, Philippe
Clerc, kindly and swiftly provided the type material of Medusulina
texana for study. The personnel of the herbaria BM,Hand Mkindly
hosted the second author during his visits.
140 The Bryologist 123(2): 2020
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Supplementary documents online:
Supplementary Table S1. GenBank accession
numbers of all sequences used in this study.
Supplementary Table S2. Final concatenated
alignment of the genetic markers mtSSU, nuLSU
and RPB2 for the 124 OTUs used in this study.
Supplementary Figure S1. Phylogeny of the
family Graphidaceae showing collapsed branches
from Fig. 1. Based on a Maximum Likelihood
analysis of the genes mtSSU, nuLSU and RPB2.
Support values are shown as numbers if Maximum
Likelihood bootstrap values 70 and as bold
branches if Bayesian posterior probabilities 0.95.
Miranda-Gonza
´lez et al.: New genus Jocatoa in Graphidaceae and insights into subfamily Redonographoideae 143
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