Stigmidium epistigmellum (Mycosphaerellaceae), a lichenicolous fungus from maritime Caloplaca in North America

Abstract

A lichenicolous fungus, Stigmidium epistigmellum (Nyl. ex Vouaux) Kocourk. & K. Knudsen, is re-described from maritime Caloplaca species from the western coast of North America and compared with other Stigmidium species on Caloplaca hosts.

Full text

Stigmidium epistigmellum (Mycosphaerellaceae), a lichenicolous
fungus from maritime Caloplaca in North America
JANA KOCOURKOVA
´
National Museum, Department of Mycology, Va
´clavske
´na
´m. 68, Praha 1, CZ-115
79 Czech Republic
e-mail: jana_kocourkova@nm.cz
KERRY KNUDSEN
The Herbarium, Department of Botany and Plant Sciences, University of
California at Riverside, Riverside, CA 92521-0124, U.S.A.
e-mail: kk999@msn.com
ABSTRACT.A lichenicolous fungus, Stigmidium epistigmellum (Nyl. ex Vouaux) Kocourk. &
K. Knudsen, is re-described from maritime Caloplaca species from the western coast of
North America and compared with other Stigmidium species on Caloplaca hosts.
KEYWORDS.California, Pharcidia epistigmella,Stigmidium cerinae,Stigmidium johnii,
Opegrapha physciaria, parasitism.
¤¤¤
Stigmidium Trevis. is a genus of mostly lichenicolous
fungi comprising over 83 binominals (Mycobank
2008) currently included in Mycosphaerellaceae
(Myconet 2008). The type species is S. schaereri (A.
Massal.) Trevis., a lichenicolous species occurring on
the sterile thalli of Solorina species. Part of the genus,
including those species formally included in
Pharcidia epicymatia, has recently been revised (Roux
& Triebel 1994). The genus is not monophyletic
(Calatayud & Triebel 2003). The majority of species
have perithecioid ascomata, periphyses and
pseudoparaphyses originating from the upper wall of
the ascomatal cavity, lack interascal filaments and
have hyaline 1-septate ascospores. The Stigmidium
psorae group has interascal filaments and will
probably be removed from the genus (Calatayud &
Triebel 2003). From North America 19 species are
currently reported (Esslinger 2007).
In this paper we make the new combination and
re-describe Stigmidium epistigmellum, a species of
Stigmidium s. str. from western North America,
lichenicolous on several species of Caloplaca which
share maritime habitats.
METHODS
Specimens have been examined using standard
microscopical techniques. Hand-made sections were
studied in water and 10% KOH [K]. Amyloid reactions
were tested in Lugol’s iodine with and without pre-
treatment with KOH [K/I]. Chromatic reactions were
tested with 1% solution of brilliant cresyl blue (BCr).
Ascospore measurements were made in water with
accurancy of 0.5 mm and given in the form
‘‘(minimum–) mean minus standard deviation–mean–
mean plus standard deviation
(–maximum)’’ and followed by the number of
measurements (n); the length/breadth ratio of
ascospore is indicated as l/b and given in the same way.
Macro and microphotographs were taken with a
digital camera Olympus C5050 on Olympus SZX 9
The Bryologist 112(3), pp. 578–583 0007-2745/09/$0.75/0
Copyright E2009 by The American Bryological and Lichenological Society, Inc.

Stereomicroscope and Olympus BX 50 (to 31250)
fitted with a Nomarski differential interference
contrast.
Stigmidium epistigmellum (Nyl. ex Vouaux)
Kocourk. & K. Knudsen, comb. nov. Fig. 1
Pharcidia epistigmella Nyl. ex Vouaux, Bull. Soc.
Mycol. France 28: 235. 1912; Mycoporellum
epistigmellum Hasse, Contrib. U.S. Natl. Herb.
17: 13. 1913, syn. nov. Type: U.S.A. CALIFORNIA:
Los Angeles County, Santa Monica Mountains,
on apothecia of Placodium festivum [5Caloplaca
luteominia], 1897, Hasse 915 (HOLOTYPE,H-NYL,
no. 382).
Description. Ascomata perithecioid, half
immersed in the host areoles or squamules or in
apothecia of the host in loose groups of 3–10 or
more, causing large pathogenic infections, eventually
causing bleaching and destruction of the host
(Fig. 1A), black, globose to subglobose, ostiolate, 80–
100(–120) mm high, 80–90(–120) mm wide.
Vegetative hyphae hyaline, 2–3 mm wide, branching,
septate, cells 5–7 mm long, BCr+bluish-violet and I–.
Ascomatal wall (Fig. 1B) dark brownish-black in
upper 1/5–4/5, lighter brown or reddish brown in
lower 4/5–1/5, but still dark even in thin sections,
never hyaline, 6–8 mm thick, slightly thicker (to
15 mm) in ostiolar area, of 2–4 cell layers, textura
angularis, cells mostly 6–9(–10) 33–5 mm in optical
section, some cells more angular on outer surface of
the wall, 6–7 36–7 mm. External periphyses sensu
Roux and Triebel (1994) visible as a dense fringe
when viewed from above (Fig. 1C), derived from
ascomatal wall, brown, mostly 2 mm wide, septate,
cells 3–5 mm long, of 2–4 cells, 15–20 mm long.
Hamathecium of pendent pseudoparaphyses (type
‘‘b’’ ) sensu Roux and Triebel (1994) (Fig. 1D)
originating from the upper wall of ascomatal cavity,
easily seen in immature ascomata, hyaline,
branching, 12–17 mm long, 1.5–2.5(–3) mm wide,
septate, of 3 cells, cells 5–7 mm long, but rarely visible
in mature ascomata when asci fully developed,
apparently breaking off and dissolving in the
hymenial gel. Lacking interascal filaments. Hymenial
gel I–, K/I–, BCr–. Asci (Fig. 1E, F) originating from
lower wall of ascomatal cavity, fissitunicate, narrowly
saccate, endoascus thickened in upper 1/3, sessile or
shortly stipitate, 8-spored, with ascospores
distichously arranged, 40–50 310–15 mm, I–,
endoascus BCr+violet. Ascospores (Fig. 1G, H)
1-septate, hyaline, not constricted or slightly
constricted, cells usually equal in length, but upper
one sometimes becoming wider, (14.5–)15.8–17.45–
19.1(–21.5) 3(3.5–)3.9–4.2–4.7(–5.0) mm, (n540),
l/b (3.2–)3.7–4.1–4.5(–5.0); epispore BCr+violet;
perispore BCr+intense blue. Conidiomata pycnidial,
ca. 30–35 mm diam., wall entirely dark brown;
conidiogenous cells cylindrical, 3.5–5.5 32–5 mm;
conidia 3–4 30.5–1.0 mm.
Substrate and ecology. On thalli and apothecia
of maritime species of Caloplaca (C. bolacina,C.
luteominia var. luteominia,C. ludificans,C. rosei)on
sandstone, granite, shale and volcanic rock. But in
same microhabitats S. epistigmellum has not yet been
found on other maritime Caloplaca species, for
instance C. marina subsp. americana and C. stantonii.
So far all known hosts are endemic to western North
America (Arup 1992a, b, 1993, 1995a, b). When the
fungus is present on the host, infection is often
abundant.
Distribution. Along coast of western North
America from Mexico (Baja Sur) to central California
(San Luis Obispo County) and on Guadalupe Island
(Mexico) and the Channel Islands (U.S.A.,
California) at elevations from just above sea level to
360 m on Santa Rosa Island.
Discussion. Stigmidium cerinae Roux & Triebel
was described from Austria, Germany, Italy and
Switzerland on the apothecia of Caloplaca cerina var.
chloroleuca (Roux & Triebel 1994). It was reported
from North America by Cole and Hawksworth
(2001), although Triebel and Ca
´ceres (2004)
expressed caution about some of the North American
reports: ‘‘As there exist at least two further
possibilities of still undescribed species of Stigmidium
occurring on thalli and apothecia of Caloplaca that
might also be found in the Sonoran Desert region,
the identification of Stigmidium on Caloplaca at the
species level is often regarded as uncertain.’’
Stigmidium epistigmellum differs from S. cerinae
in habitats (maritime vs. alpine), hosts, larger
ascomata [80–100(–120) mm high, 80–90(–120) mm
wide vs 50–70 345–70 mm], pseudoparaphyses (type
‘‘a’’) sensu Roux and Triebel (1994), and larger
Kocourkova
´& Knudsen: Stigmidium on maritime Caloplaca 579

Figure 1. Stigmidium epistigmellum (Knudsen 8795,PRM 910296). A. Strongly infected host thallus. B. Section of ascoma. C.
Surface view of an ascoma showing ostiole with fringe of external periphyses. D. Hamathecium of pendent periphysoids seen in
immature ascoma. E, F. Young asci in different stages of development showing thickened thollus and apical beak. G, H. Mature
ascospores. Scales: A 550 mm, B, C 520 mm, D–G 510 mm.
580 THE BRYOLOGIST 112(3): 2009

ascospores [(14.5–)15.8–17.45–19.1(–21.5) 3(3.5–)
3.9–4.2–4.7(–5.0) mm vs. (9.0–)10.0–11.2–12.5
(–13.0) 33.0–3.4–4 mm].
Two other Stigmidium species have been
reported from Caloplaca. We agree with Halici and
Hawksworth (2007) that S. caloplacae Alstrup &
Olech on C. cerina (Alstrup & Olech 1996) is
probably best treated as a synonym of S. cerinae. Its
ascospore size is practically the same as S. cerinae and
thus clearly smaller than those of S. epistigmellum.
The recently described species S. johnii Halici & D.
Hawksw. (Halici & Hawksworth 2007) occurs at high
altitude (2680 m) on an unidentified yellow-orange
Caloplaca on calcareous rock in Turkey. It differs
from S. epistigmellum in having wider ascospores, the
widest in the genus, 5–6.5 mm vs. 4.1–4.6(–5) mmin
S. epistigmellum.Stigmidium johnii also has overall
shorter ascospores than S. epistigmellum, (12.5–)
13.0–16.5 mm vs. (14.5–)15.8–17.45–19.1(–21.5) mm.
We have revised the material reported as
Stigmidium cerinae (Cole & Hawksworth 2001) from
southern California. In the specimen Bratt 9353
(SBBG) from Santa Barbara Island, determined by Cole
as S. cerinae (Cole & Hawksworth 2001), no
ascospores could be observed, but macroscsopically it
resembles S. epistigmellum. Another specimen from
Santa Barbara Island, Bratt 5141 (SBBG) was reported
as Opegrapha physciaria (Nyl.) D. Hawksw. on
Caloplaca rosei (Cole & Hawksworth 2001). It was
later determined by D. Ertz as S. cerinae s. lato. This
is a typical specimen of S. epistigmellum in which
occur no mature ascospores but immature
ascospores to 15.5 mm are very common. We found
no Opegrapha ascomata nor did Ertz and Egea
(2008). Hawksworth’s identification of Stigmidium
cerinae on Caloplaca luteominia from Baja California
(Wetmore 75720) is here also revised as S.
epistigmellum.
Specimens on a maritime Caloplaca species seen
from Point Lobos in Monterey County in California
(Imshaug 17750,MIN) and specimens on C. rosei
supplied by Bruce McCune from Oregon (McCune
17355 &Rosentretter 8439,HB.MCCUNE), as well as a
specimen from Iran on Caloplaca marina (Vondra
´k
3367,CBFS) possibly belong to a separate taxon with
shorter and narrower ascospores, 10–15 33mm, or
are poorly developed specimens of S. epistigmellum.
The Oregon specimens may have a different kind of
infection, blackening the host. Unfortunately, these
specimens were not well developed and no mature
ascospores were seen.
Stigmidium epistigmellum increases the number
of Stigmidium species reported from North America
to 20 (Esslinger 2007). Stigmidium cerinae and
Opegrapha physciaria should be removed from the
California checklist (Tucker & Ryan 2006).
Opegrapha physciaria does occur in Mexico on
Xanthoria species (Ertz & Egea 2008) and may be
collected in the future in California. The report of S.
cerinae from North America is now only based on
Wetmore 77785 on Caloplaca trachyphylla collected in
Nebraska (MIN) (Cole & Hawksworth 2001), a
specimen the authors reported had broader
ascospores than the description of S. cerinae. We
examined the specimen but could find no mature
ascospores.
Stigmidium epistigmellum was validly described
by Vouaux (1912) as Pharcidia epistigmella Nyl. from
a Hasse collection from California but the ascospore
size of 11–14 33.5–4.5 mm represents his
measurements of poorly developed ascospores in the
holotype. Vouaux (1912) described Pharcidia
epistigmella var. meizospora Vouaux with ascospores
14–19 34.5–6 mm on a specimen from Puebla,
Mexico, on the apothecia of Placodium, collected by
Fr. Nicolas. The holotype was not seen but the
mature ascospore size is wider than in the holotype
of Pharcidia epistigmella var. epistigmella. Based on
Nylander’s notes, Hasse published Mycoporellum
epistigmellum Hasse (1913) for the same taxon.
Hasse’s concept of the species includes other species
of Stigmidium on Acarospora.
Selected specimens examined. MEXICO.BAJA
CALIFORNIA SUR: W of San Ignascio, on areoles of
Caloplaca bolacina on shale, 30 V 1974, Nash 8940
(SBBG); GUADALUPE ISLAND: on W coast of island on
Fondeadrae del Oeste, near light on N-facing slopes
above the ocean, 28u589500N, 118u189500W, 80 m,
on apothecia of Caloplaca luteominia var. luteominia,
1 I 1996, Wetmore 75803 (MIN); BAJA CALIFORNIA NORTE:
Punta Santo Tomas SW of Ensenade, on ridge above
ocean, 31u339200N, 116u419200W, 20–100 m,
apothecia and areoles on Caloplaca rosei, 30 XII 1995,
Wetmore 75720 (MIN). U.S.A. CALIFORNIA: Los Angeles
Kocourkova
´& Knudsen: Stigmidium on maritime Caloplaca 581

Co., San Clemente Island, on rock in spray zone on
coast SW of old airfield, on apothecia of Caloplaca
bolacina, 30 IX 1996, Bratt 9648 (SBBG), Santa
Catalina Island, above Ripper’s Cove, N side of
island, on areoles and apothecia of Caloplaca
bolacina, 25 X 2000, Bratt 11887 w/ D. Knapp (SBBG),
Santa Monica, near Old Soldier’s Home, on
Caloplaca luteominia, X 1897, Hasse 951 (NY), City of
Los Angeles, Griffith Park, Royce Canyon, E end of
the Santa Monica Mountains, 34u089290N,
118u189260W, 263 m, on apothecia of Calopaca on
rock slab, 10 II 2005, Knudsen 2351 w/ Ochoa et al.
(PRM 910000, HB.ETAYO), Sullivan’s Canyon, Santa
Monica Mountains, on Caloplaca luteominia, 1913,
Hasse (FH); Santa Barbara Co., San Miguel Island,
Channel Islands Natl. Park, Nidever Canyon, across
first barranca NW of station, on apothecia of
Caloplaca luteominia, 22 VII 1995, Bratt 9061 (SBBG),
E of summit of Green Mountain, 34u019510N,
120u229520W, 146 m, on apothecia of Caloplaca
luteominia, 23 VI 2006, Knudsen 6683 (PRM 910002),
Santa Rosa Island, beach near East Point,
33u569450N, 119u589180W, 13 m, on areoles and
apothecia of Caloplaca bolacina on consolidated
volcanic ash, 17 VIII 2007, Knudsen 8868 w/ Werth &
Chaney (UCR), near Black Mountain in pass along
main road on S side of ridge and hilltop, 33u589450N,
120u049300W, 320 m, on areoles and apothecia of
Caloplaca bolacina, 1 I 1994, Wetmore 73532 (MIN); W
of radar station hill, on N-facing roadcut and hill,
33u569450N, 120u079300W, 460 m, on thallus and
apothecia of Caloplaca ludificans, 2 I 1994, Wetmore
73705 (MIN), along Burma Road, 33u569400N,
120u079040W, 462 m, on sandstone rocks, on
apothecia of Caloplaca luteominia, 20 VII 2007,
Kocourkova
´& Knudsen (PRM 909118), Sandy Point,
34u009040N, 120u149500W, 13 m, on Caloplaca
luteominia on caliche, 16 VIII 2007, Knudsen 8795 w/
Chaney & Werth (PRM 910296, FH,H,HB.DIEDERICH,
HB.LENDEMER,M,SBBG,UCR,UPS), upper Lobos
Canyon, near road crossing, 34u009180N,
120u059300W, 5 m, on thallus and apothecia of
Caloplaca bolacina, 16 X 2006, Knudsen 7592 w/
Baguskas (PRM 848909), above tributary of Water
Canyon, below Wreck Road, 33u589400N,
120u29250W, 142 m, on thallus and apothecia of
Caloplaca luteominia, on granite rock, 18 VII
2007, Kocourkova
´& Knudsen (PRM 909266), on
apothecia of Caloplaca bolacina, 19 VII 2007,
Kocourkova
´& Knudsen (PRM 909432); San Luis
Obispo Co., Avila Beach, near Point Bouchon,
Diablo Canyon Power Plant, on apothecia of
Caloplaca luteominia, 10 X 1995, Tucker 34227 w/
Bratt et al. (SBBG), San Simeon, San Simeon State
Park, coast SE of state park headquarters,
35u389210N, 121u109230W, 3 m, on apothecia of
Caloplaca luteominia, 10 I 2007, Knudsen 8216 (PRM
857263 & 910001, UCR); Ventura Co., San Nicholas
Island, N side, Sandspit Canyon, on apothecia of
Caloplaca luteominia, 13 II 1993, Bratt 8146 (SBBG),
Santa Barbara Island, Channel Island Natl. Park, on
trail to North Peak, 152 m, on apothecia of Caloplaca
rosei, 28 I 1986, Bratt 5141 (SBBG), Cave Canyon,
61 m, on apothecia of Caloplaca bolacina, 5 V 1996,
Bratt 9353 (SBBG).
ACKNOWLEDGMENTS
We thank Paul Diederich and Javier Etayo for their reviews of
this paper. We thank Sarah Chaney for facilitating our
collection of lichenicolous fungi on Santa Rosa Island and San
Miguel Island, The California Mediterranean Research Learn-
ing Center for their financial support, Ellen Bloch (NY), Imke
Schmitt (MIN), Michaela Schmull (FH), Shirley Tucker (SBBG),
Jan Vondra
´k(
CBFS) and Bruce McCune (Oregon State
University) for supplying additional specimens, and Giles
Waines, director of UCR, for his consistent support. The work of
J. Kocourkova
´was financially supported by a grant from
Ministry of Culture of the Czech Republic (MK0000237201).
LITERATURE CITED
Alstrup, V. & M. Olech. 1996. Lichenicolous fungi from the
Polish Tatra Mountains. Fragmenta Floristica et
Geobotanica 41: 747–752.
Arup, U. 1992a. Caloplaca marina and C. rosei, two difficult
species in North America. The Bryologist 95: 148–160.
———. 1992b. Caloplaca stantonii sp. nov. and its relationship
to Caloplaca bolacina and other lobate to squamulose
species in North America. The Bryologist 95: 449–457.
———. 1993. Caloplaca luteominia and C. bolanderi in western
North America. The Bryologist 96: 463–470.
———. 1995a. Eight species of Caloplaca in coastal western
North America. The Bryologist 98: 92–111.
———. 1995b. Littoral species of Caloplaca in North America:
a summary and key. The Bryologist 98: 129–140.
Calatayud, V. & D. Triebel. 2003. Three new species of
Stigmidium s. l. (lichenicolous ascomycetes) on Acarospora
and Squamarina. Lichenologist 35: 103–116.
582 THE BRYOLOGIST 112(3): 2009

Cole, M. S. & D. L. Hawksworth. 2001. Lichenicolous fungi,
mainly from the USA, including Patriciomyces gen. nov.
Mycotaxon 77: 305–338.
Ertz, D. & J. M. Egea. 2008 [2007]. Opegrapha.In T. H. Nash
III, C. Gries & F. Bungartz (eds.), Lichen Flora of the
Greater Sonoran Desert Region 3: 255–266. Lichens
Unlimited, Arizona State University, Tempe, AZ.
Esslinger, T. L. 2007. A cumulative checklist for the lichen-
forming, lichenicolous and allied fungi of the continental
United States and Canada. North Dakota State University,
http://www.ndsu.nodak.edu/instruct/esslinge/chcklst/
chcklst7.htm (first posted 1 Dec 1997, most recent update 2
Apr 2007), Fargo, ND. Accessed 1 Oct 2007.
Halici, G. M. & D. L. Hawksworth. 2007. Two new species of
lichenicolous fungi from Turkey. Lichenologist 5: 439–443.
Hasse, H. E. 1913. The lichen flora of southern California.
Contributions from the United States National Herbarium
17: 1–132.
Mycobank. 2008. www.mycobank.org Accessed Apr 2008.
Myconet. 2008. www.fieldmuseum.org/myconet Accessed Apr
2008.
Roux, C. & D. Triebel. 1994. Re
´vision des espe
`ces de
Stigmidium et de Sphaerellothecium (champignons
liche
´nicoles non liche
´nise
´s, Ascomycetes) correspondant a
`
Pharcidia epicymatia sensu Keissler ou a
`Stigmidium
schaereri auct. Bulletin de la Socie
´te
´Line
´enne de Provence
45: 451–542.
Triebel, D. & M. E. S. Ca
´ceres. 2004. Stigmidium.In T. H. Nash
III, B. D. Ryan, P. Diederich, C. Gries & F. Bungartz (eds.),
Lichen Flora of the Greater Sonoran Desert Region 2:
703–707. Lichens Unlimited, Arizona State University,
Tempe, AZ.
Tucker, S. & B. D. Ryan. 2007. Revised catalog of lichens,
lichenicoles, and allied fungi in California. Constancea 84
(http://ucjeps.berkeley.edu/constancea/84/). Accessed on 1
Oct 2007.
Vouaux, L. 1912. Synopsis des champignons parasites de
lichens. Bulletin de la Socie
´te
´Mycologique de France 28:
1–32, 209–256.
ms. received January 14, 2008; accepted December 9, 2008.
Kocourkova
´& Knudsen: Stigmidium on maritime Caloplaca 583