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Studia botanica hungarica 48(1), 2017
Hungarian Natural History Museum, Budapest
Studia bot. hung. 48(1), pp. 21–32, 2017
DOI: 10.17110/StudBot.2017.48.1.21
NEW OR LITTLE KNOWN EPIPHYLLOUS LIVERWORTS,
XXI. RADULA CAMERUNENSIS SP. NOV.
RADULACEAE, JUNGERMANNIOPSIDA
Tamás P
Institute of Biology, Eszterházy Károly University,
H–3301 Eger, Pf. 43, Hungary; colura@upcmail.hu
Pócs, T. (2017): New or little known epiphyllous liverworts, XXI. Radula camerunensis sp. nov.
(Radulaceae, Jungermanniopsida). – Studia bot. hung. 48(1): 21–32.
Abstract: e new epiphyllous sp ecies Radula camerunensis was discovered in the high rainfal l area
of the lowlands of SW Cameroon, as host of the new parasitic ascomycete Epibryon platycarpum
Döbbeler et T. Franke. As all the investigated species of the former section Epiphyllae proved to
be monophyletic, belonging to the same subclade of subgenus Metaradula in a recent molecular
investigation, the status of Radula sect. Epiphyllae is tenable. e new species di ers from all other
members of sect. Epiphyllae by its long stalked discoid gemmae.
Key words: Bryoparasitic fungi, Cameroon, discoid gemmae, Radula, sect. Epiphyllae
INTRODUCTION
Peter Döbbeler, renowned specialist of bryoparasitic fungi, called my at-
tention to an epiphyllous Radula species hosting a new species of ascomycetes,
Epibryum platycarpum Döbbeler et T. Franke (D 2016). e new as-
comycete occurred exclusively on this host and was absent on Radula accida
Lindenb. et Gottsche, which occurred on the same phanerogamic leaves. e spec-
imens were collected from the high rainfall area in the lowlands of SW Cameroon
by assilo Franke, biologist and producer of natural history lms. e Radula
host species had peculiar discoid gemmae with several rows of smaller cells along
their margin. Investigating the specimen, I found other unique features as well
and concluded that it belonged to a hitherto unknown epiphyllous Radula species.
e leaf-inhabiting Radula species were classi ed by S (1884–1885)
in the subgenus Acroradula (now subgenus Radula), and by C (1939, as
nomen nudum) in the separate sect. Epiphyllae Castle ex Grolle (G 1970).
Y (1979) followed the classi cation of Castle. S (1980a) in a
phylogenetic study considered Castle’s classi cation arti cial, claiming that the
sect. Epiphyllae was polyphyletic and included advanced representatives of dif-
ferent groups. He described within the group of epiphyllous Radula species three
PÓCS, T.
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Studia bot. hung. 48(1), 2017
new sections (Evansiae, Mammosae, Acuminatae) and within sect. Acuminatae
three new subsections (Stenocalyces, Ya n oe l l a e , Acuminatae). Sect. Epiphyllae
Castle ex Grolle emend. R. M. Schust., thus, became restricted to only two spe-
cies, R. accida and R. pseudo accida E. W. Jones. In Schuster’s classi cations of
the former Epiphyllae, sect. Evansiae and sect. Mammosae are never gemmiparous
while the subsections of sect. Acuminatae and the two species of sect. Epiphyllae
are all gemmiparous. e species of the subsect. Stenocalices, subsect. Ya n o e l l a e ,
and sect. Epiphyllae have marginal gemmae, while those of subsect. Acuminatae
have super cial gemmae.
Molecular genetic investigations by D et al. (2011) did not support
Schuster’s 1980 classi cation. ey established that all investigated species of
sect. Epiphyllae are a monophylum and constitute a subclade of subgenus Meta-
radula R. M. Schust. (S 1984). ey also supplied a new diagnosis for
subg. Metaradula, which had several defects, stating among others that lobule
insertion is parallel to stem, directed to stem apex (valid only for part of the spe-
cies) and that caducous leaves and gemmae are absent (which is not true for the
majority of the members of sect. Epiphyllae). Schuster’s original diagnosis of
subg. Metaradula seems to be more appropriate.
As the new species from Cameroon has marginal gemmae, I compared it
with the gemmiferous species from the sect. Epiphyllae. One of them, the Amero-
African Radula accida has very elaborate, funnel shaped, ‘ ying saucer’ like
gemmae, while all others have simple, at or slightly convex discoid gemmae ei-
ther in the plane of leaf lobe or perpendicular to it (Fig. 1B–F). In the new species
the gemmae are slightly convex and in the plane of leaf lobe. e striking feature
of the new species is the elongated stalk cell of the gemmae, developing mostly
on the antical margin (Fig. 1A).
e asexual reproduction of bryophytes by means of gemmae has been
studied in details by many authors since G (1898, 1930), C (1910),
and B (1911). S (1980b) described in detail the development of
complex, funnel form gemmae of Radula accida, observed earlier by G
(1930). R and B (2004), discussing the gametophytic characters
of the genus, showed that discoidal gemmae can be one or two cells thick, and
that granular and roughly spherical gemmae occur in Radula javanica Gottsche.
Only few authors, e.g. S (1910), paid attention to the development of
simple discoid gemmae in the genus. He established that in Radula complanata
gemma development starts with a protruding marginal leaf cell. Subsequently,
the projecting portion is cut o by a wall. e inner cell is regarded as a stalk,
the outer becomes the mother cell of the gemma. In the case of R. complanata
the shape of the discoid gemma is quite irregular. A er many cell divisions, when
the gemma is ready to be separated, schizolytic splitting takes place in the wall
NEW OR LITTLE KNOWN EPIPHYLLOUS LIVERWORTS, XXI 23
Studia bot. hung. 48(1), 2017
Fig. 1. Comparison of the gemma stalk of di erent Radula species with marginal gemmae in sect.
Epiphyllae. – A = Radula camerunenis Pócs et Döbbeler, from the type. B = Radula assamica Steph.
C = Radula nymanii Steph. D = Radula stenocalyx Mont. E = Radula tjibodensis K. I. Goebel. F =
Radula yanoella R. M. Schust.
PÓCS, T.
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Studia bot. hung. 48(1), 2017
between the stalk and the cells of the leaf. D (1938) showed the oc-
currence of a great variety of discoid gemmae in Radula and described the type
of gemma occurring in the majority of sect. Epiphyllae, being regularly orbicular
with smaller marginal cells in some cases.
e stalk cell in the gemmiferous species of sect. Epiphyllae is rounded,
square or even compressed parallel to the leaf margin. In the new species, how-
ever, the stalk cell is elongate, already in juvenile stage, elevating the developing
gemma above the leaf margin.
RESULTS
Radula camerunensis Pócs et Döbbeler, sp. no.
(Figs 2–5)
Diagnosis: Radula camerunensis di ers from the other gemmiferous spe-
cies of sect. Epiphyllae by its discoid gemmae having elongate stalk cells, which
elevate the gemmae above the leaf margin. In addition, the new species has ligu-
late, forward directed lobules, without a pronounced mammilliform ventral sac.
Type: Cameroon, Southwest Province: Bimbia-Bonadikombo Forest Res-
erve (Mabeta-Moliwe Forest Reserve), lowland rainforest at sea level, with 5000
mm annual precipitation, epiphyllous, hosting the bryoparasitic ascomycete
Epibryum platycarpum Döbbeler et T. Franke, which, being small, does not af-
fect the growth of its host. Radula camerunensis thrives together with Radula
accida, Cololejeunea pusilla, and Cololejeunea microscopica var. a icana, none of
them infected by the fungus. Coll.: assilo Franke, 27.11.2000, Döbbeler No.
8784 (holotype: EGR, isotype: NY, under the fungal name of Epibryum platycar-
pum, paratypes from the same collector, locality, and date: Döbbeler No. 8779,
M; 8780 (holotype of E. platycarpum, M); No. 8789, TUR ; No. 8778, B).
Description: In herbarium olive green, forming several cm2 large colonies
on living leaves of phanerogams, sometimes covering their whole surface. Many
cases mixed with other epiphyllous liverworts, but easy to distinguish by the
o en developing, stalked discoid gemmae. Shoots irregularly branching, up to
10–20 mm length and 1.4–1.8 mm width. Stem width 50–64 µm, in section 4–5
cells wide with 4 thin-walled medulla cells surrounded by 8–12 cortical cells with
moderately thickened outer walls (Fig. 1B). is stem structure is typical for sect.
Epiphyllae according to J (1977), belonging to his type ‘5’. Cell walls pale
yellowish brown pigmented. Leaves moderately imbricate, lobe broadly ovate
with widely rounded apex, 1–2.4 × 0.8–1.8 mm, nearly plane, dorsal base arching
and with about ¼ of lobe length crossing the stem, dorsal base decurrent. Median
cells 17–25, basal 25–40, marginal 8–10 × 6–10 µm, their wall thin with small
NEW OR LITTLE KNOWN EPIPHYLLOUS LIVERWORTS, XXI 25
Studia bot. hung. 48(1), 2017
trigones and intermediate thickenings. Oil bodies already disintegrated in the
examined samples. Cuticle smooth. Keel straight or slightly curved, about ¼ of
lobe length. Lobule broad ligulate or triangular, 320–480 µm long with obtuse
apex, at about half of its length fused and directed parallel to the stem, without
large mamilliform ventral sac. It has only a dot-like (30–40 µm diameter) rhizoid
initial area with small (4–6 µm) cells giving origin to the short (35–70 µm), radi-
ally arranged, colourless rhizoids o en dichotomic at their end. Other median
cells 14–20 × 12–16 µm, marginal cells 10–16 × 4–6 µm.
Dioicous. Male gametoecia on apex of the mean stem and side branches,
o en forming a raceme at shoot ends. Male spikes up to 2 mm length and 0.4
mm width, consisting of 10–20 pairs of slightly falcate, 280 µm long and 240 µm
wide bracts with hypostatic lobules almost equalling the lobe length. e male
spike sometimes ends in a normal leafy shoot. Female gametoecia on shoot apex
or branches, usually with one innovation. Perichaetial leaves not specially dif-
ferentiated. Perianth very narrowly conical, trumpet shaped, 1–2 mm long and
0.3–0.6 mm wide at its undulate mouth. e lower 3/5 of perianth built up of
several layers, subtended by a stem-perigynium with cells of the outer wall ob-
long rectangle or sigmoid, 30–50 × 10–20 µm, while the upper 2/5 of perianth
is unilayered with irregular, near isodiametric cells of 16–30 × 10–20 µm size.
Sporophyte consists of a 2–2.5 mm long seta and a narrow cylindrical capsule,
with 600–750 µm long and 40 µm wide valves with 4–8 rows of 80–160 µm long
and 12 µm wide, elongate, brown pigmented cells in their outer walls.
Vegetative reproduction by discoid gemmae, developing at the antical mar-
gin of leaf or rarely on the male bract lobe. eir stalk cell from the beginning
of its growth already elongate, slightly widens upwards, 25–36 µm long, keep-
ing away the gemma from the lobe margin. e gemmae reach on the mother
plant 250–400 µm diameter but detached, mature gemmae 560–640 × 600–640
µm, reaching the size of smaller leaves, somewhat reniform, having shallowly
notched base at the insertion point of stalk, which nally detaches from the body
of gemma. Supposedly the gemmae continue their growth a er detachment, as
this large size never occurs until they are attached to the leaf. Mature gemmae
slightly convex (under pressure of coverslip they crack) and in the plane of the
leaf lobe; in cross section they are generally unilayered but here and there can be
two cells thick. e median cells are isodiametric, polygonal, 13–25 µm diameter
while 5–8 rows of marginal cells are smaller, quadrate, only 6–12 µm, forming a
rim around the large celled, 12–18 cells wide interior part. In cross section the
median cells are much higher than the marginal ones, hence the gemma is thin-
ning towards its margin. Unfortunately, I was not able to observe germinating
gemmae except one, which gave birth to another, sprouting gemma.
PÓCS, T.
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Studia bot. hung. 48(1), 2017
Fig. 2. Radula camerunensis Pócs et Döbbeler. – A = Habit, ventral view, and two detached, en-
larged gemma. B = Stem, transversal section. C = Lobe base, with the rhizoid initial area compar-
ing its small cells with those of the lobe and lobule. D = Median transversal section of a disciform
gemma not yet released from the lobe margin. E = Outer layer of the lower part of perianthium. F=
Single layer of the upper part of perianthium. All drawn from the type.
NEW OR LITTLE KNOWN EPIPHYLLOUS LIVERWORTS, XXI 27
Studia bot. hung. 48(1), 2017
Fig. 3. Radula camerunensis Pócs et Döbbeler. – A = Habit, ventral view. B = Leaf, ventral view. C =
Median lobe cells. D and E = Stalked gemmae on the antical lobe margin. Al l drawn from the type.
PÓCS, T.
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Studia bot. hung. 48(1), 2017
Fig. 4. Radula camerunensis Pócs et Döbbeler. – A = Margin of a detached gemma. B = Young
gemma and gemma initials on t he antical lobe margin. C = Mature, already detached gemma. Being
concave, cracked when attened under the pressure of coverslip. D = Stalked base of a maturing
gemma. E = Raceme on a shoot end formed by male branches. F = Part of a male branch. All drawn
from the type.
NEW OR LITTLE KNOWN EPIPHYLLOUS LIVERWORTS, XXI 29
Studia bot. hung. 48(1), 2017
Fig. 5. Radula camerunensis Pócs et Döbbeler. – A = Male branch with a gemma bearing enlarged
lobus. B = Capsule valves. C = Perianth mouth. D = Relatively small, young perianth. All drawn
from the type.
PÓCS, T.
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Studia bot. hung. 48(1), 2017
DISCUSSION
According to our present knowledge sect. Epiphyllae Castle ex Grolle con-
tained 13 species, if we do not mention other facultative epiphyllous species as
Radula lindenbergiana Gottsche et C. Hartm. (P 1982) in the Caucasus Mts
or Radula cavifolia Hampe ex Gottsche et al. From the 13 epiphyllous Radula 3
lack gemmae, while 10 are gemmiferous, including the recently described neo-
tenic, semi-thalloid Radula yanoella R. M. Schust. and R . aguirrei R. M. Schust.
(C 1939, G 1970, S 1980a, 1991) from the Neotropics
and the Asian Radula grandilobula Promma et Chantanaorrapint (P
and C 2015). With the description of the new species R.
camerunensis Pócs et Döbbeler, the number of species in sect. Epiphyllae is raised
to 14. According to the traditional view sect. Epiphyllae belonged to subgenus
Acroradula Spruce (present subg. Radula), according to recent molecular investi-
gations (D et al. 2011) to subg. Metaradula R. M. Schust. D et al. also
showed that the gemmiferous members of sect. Epiphyllae are a monophylum,
forming a separate subclade of subg. Metaradula characterized also by the pres-
ence of gemmae and their highly reduced stem anatomy (J 1977). As the
investigated species of the former section Epiphyllae proved to be monophyletic,
within the same subclade of subgenus Metaradula according to recent molecular
investigation, the status of Radula sect. Epiphyllae is tenable. Among the gem-
miferous members of the Epiphyllae the new species is unique by its elongated
stalk cell, which elevates the discoid gemmae above the lobe margin (in the plane
of lobe). e large median cells of the gemma are surrounded by several rows of
smaller and thinner marginal cells. is characteristic is shared with Radula tji-
bodensis and with R. nymanii, but its ligulate, forward directed lobule di erenti-
ates the new species from them. In addition, the gemmae of R. tjibodensis are per-
pendicular to the lobe surface and those of R. nymanii are developing on the ven-
tral (postical) lobe margin (S et al. 2016, Fig. 2). erefore, the taxonomic
position of the new species seems to be quite separate from the other members
of Epiphyllae. e host speci city of the parasitic ascomycete supports this. It is
interesting that the new African species is morphologically closest to two Asiatic
species. is may re ect the importance of stochastic long range dispersal in the
Epiphyllae (e.g. P et al. 2016) and suggest that greatly restricted distribu-
tion does not necessarily mean lower diversi cation rates.
Conservation aspects: As the bryo ora of Cameroon is poorly known,
mostly from old German collections, the discovery of the new species does not
come as a surprise. However, as the lowland forests in West Africa are very much
decimated, the coincidence of a new ascomycete exclusively parasitising a new
NEW OR LITTLE KNOWN EPIPHYLLOUS LIVERWORTS, XXI 31
Studia bot. hung. 48(1), 2017
species of liverworts is noteworthy and may indicate the richness and unique-
ness of the habitat. Bimbia-Bonadikombo Community Forest Reserve in the high
rainfall area of the Southwest Province of Cameroon near Limbe town has been
known for its high biodiversity with eight threatened vertebrate species includ-
ing chimpanzees, and merits special attention and a high level of protection. Due
to the surrounding population pressure, it will not be an easy task, but promising
measures have already been taken (N and T 2016).
***
Acknowledgements – I am very grateful to Dr Peter Döbbeler (Ludwig-Maximilians-Univer-
sität München, Department Biologie I, Systematische Botanik und Mykologie) calling my atten-
tion to the new Radula species and providing material for study. anks are due also to Prof. S.
Robbert Gradstein (Muséum d’Histoire Naturelle, Laboratoire de Cryptogamie, Paris) for amend-
ments and useful suggestions on the manuscript.
Összefoglaló: Peter Döbbeler mikológus (München), a mohalakó mikrogombák ismert ku-
tatója hívta fel a gyelmemet egy érdekes epiphyll (levéllakó) Radula fajra a kameruni sík vidé-
ki esőerdőkből, assilo Franke gyűjtéséből. Ez a Radula faj a kizárólagos gazdanövénye az ál-
tala leírt, tudományra új Epibryon platycarpum Döbbeler et T. Franke mohaparazita gombának
(D 2016), bár vele együtt egy másik Radula faj is tömegesen előfordul ugyanazokon a le-
veleken. Anyagát tanulmányozva ez a faj Radula camerunensis Pócs et Döbbele r néven, mint a tudo-
mányra új faj került leírásra. Az új faj egyedülálló tulajdonsága a Radula fajok között, hogy discoid
gemmáinak (vegetatív szaporító testek) nyélsejtje megnyúlt és a gemmát eltartja a levélke szélétől.
Ezáltal a 14., trópusi esőerdőkben élő epiphyll Radula faj vált ismertté. A közelmúltban végzett mo-
lekuláris vizsgálatok (D et al. 2011) igazolták C (1939) nyomán G (1970) felfogá -
sát a mono letikus Epiphyllae szekció önállóságáról és létjogosultságáról, szemben Schuster későb-
bi (S 1980a) felfogásával, aki ezt az egységet poli letikusnak tartotta és számos szekció-
ra bontotta. A mai felfogás szerint az Epiphyllae szekció a Metaradula R. M. Schust. alnemzetségbe
tartozik (D et al. 2011), bár e szerzők Epiphyllae diagnózisának megfogalmazása hibás.
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