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BFNA Title: Jubulaceae |
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XX. JUBULACEAE H. Klinggräff John
J. Atwood Plants lacking red-purple pigments, forming patches
or mats; branches
intercalary from sides of stem immediately behind leaf or terminal at ventral base of leaf and replacing
the lobule, the resulting half-leaf inserted on stem and branch, the primary
branch appendages mostly undivided, rarely bifid, unmodified; without
flagella. Lateral leaves alternate, asymmetrically 3-fid, with an incubous dorsal lobe and two modified ventral
lobes (lobule and stylus). Ventral
leaves 2-lobed. Rhizoids
clustered near base of ventral leaves.
Specialized asexual reproduction absent [multicellular discoid gemmae
present on margins of dorsal lobes or plants with caducous
lobules]. Gynoecium terminal on
stem or primary branch.
Perianth subtended by 1--2 subfloral, terminal innovations, not
replacing the ventral lobe of the bract, well-developed, dorsiventrally
compressed, with two lateral keels and one keel on ventral face, mouth
abruptly contracted to a short beak, perigynium absent. Spores finely papillose. Genera 3 (1 in the flora). North America, Mexico,
West Indies, Central America, South America, Europe, Asia (including Indonesia),
Africa (including Madagascar), Atlantic Islands, Indian Ocean Islands,
Pacific Islands, Australia. The
once broadly circumscribed Jubuloideae is treated
by several molecular
phylogentic studies (Ahonen
2004; Heinrichs et al. 2005, 2007; Forrest et al. 2006) as comprising three
families: the Jubulaceae, Frullaniaceae, and Lejeuneaceae. However, the recognition of some genera within
these families, as well as the deposition
of genera with both frullaniaceous
and lejeuneaceous characters, remains controversial (Schuster
1992; Gradstein et al. 2003; Larraín et al. 2015).
The three families share asymmetrically divided, bifid or trifid leaves; rhizoids in fascicles from the base of the ventral leaves; sporophytes enclosed by a stalked calyptra and beaked
perianth; spheroidal capsules with bistratose walls; and vertically aligned elaters
attached to the capsule valve (Crandall-Stotler et al. 2009). The Jubulaceae
and Frullaniaceae differ morphologically from the Lejeuneaceae in the shape and insertion of the lobules on
mature shoots, where most genera have helmet- or sac-shaped lobules
that are attached
to the dorsal lobe along a narrowly enrolled postical margin that is scarcely attached to the stem. The lobules can be
contiguous or remote from the stem, and in a parallel, sub-parallel, oblique,
or wide-spreading position to the stem. By comparison, genera in the Lejeuneaceae
have pocket-shaped lobules that are broadly attached along the postical margin
of the dorsal lobe, are broadly inserted
on the stem,
and are in a perpendicular
position to the stem. The Jubulaceae differs morphologically from the Frullaniaceae
in several respects. The Jubulaceae have pale, gray to blue-green
colored plants that lack the red-purple pigments often associated with
the Frullaniaceae. At terminal branch origins, the dorsal half-leaf is inserted
partly on the stem and branch,
with the initial branch appendages mostly undivided, lanceolate or
sub-triangular, and unmodified. In the Frullaniaceae, the
dorsal half-leaf is inserted on the stem. It is
rarely inserted on the stem and branch. The primary branch appendages are
bifid or trifid, and mostly galeate
or saccate, although in a few species they can sometimes be explanate, lanceolate
or sub-triangular. Lastly, the spores in the
Jubulaceae have a finely papillose ornamentation, and lack rosettes of tubercles
that are characteristic of spores in the Frullaniaceae. SELECTED REFERENCES Ahonen, I. 2004. Molecular phylogeny of
liverwort order Porellales (Marchantiophyta,
Jungermanniopsida).
In: B. Goffinet, V. C. Hollowell, and R. Magill, eds. Molecular Systematics
of Bryophytes. Monogr. Syst. Bot. Missouri Bot. Gard. 98: 169--188. Crandall-Stotler, B., R. E. Stotler, and D. G. Long. 2009. Phylogeny and
classification of the Marchantiophyta. Edinburgh J.
Bot. 66: 155--198. Forrest, L. L., E.
C. Davis, D. G. Long, B. J. Crandall-Stotler, A. Clark, and M. L.
Hollingsworth. 2006. Unraveling the evolutionary history of the liverworts (Marchantiophyta): multiple taxa, genomes and analyses.
Bryologist 109: 303--451. Gradstein,
S. R., M. E. Reiner-Drehwald, and H. D. Schneider. 2003. A phylogenetic
analysis of the genera of Lejeuneaceae (Hepaticae).
Bot. J. Linnean Soc. 143: 391--410. Heinrichs, J., S. R. Gradstein, R. Wilson,
and H. Schneider. 2005. Towards a natural classification of liverworts (Marchantiophyta) based on the chloroplast gene rbcL.
Cryptog.,
Bryol. 26: 215--233. Heinrichs, J., J.
Hentschel, R. Wilson, K. Feldberg, and H.
Schneider. 2007. Evolution of leafy liverworts (Jungermanniidae,
Marchantiophyta): estimating divergence times from
chloroplast DNA sequences using penalized likelihood with integrated fossil
evidence. Taxon 56: 31--44. Larraín, J., B. Carter, B. Shaw, J. Hentschel,
L. S. Strozier, T. Furuki,
J. Heinrichs, B. Crandall-Stotler, J. Engel, and M. von Konrat. 2015. The
resurrection of Neohattoria
Kamim. (Jubulaceae, Marchantiophyta): a six decade systematic conflict
resolved through a molecular perspective. PhytoKeys
50: 101--122. Schuster, R. M. 1992. The Hepaticae and Anthocerotae of North America
East of the Hundredth Meridian, Vol. 5. Field Museum of Natural
History, Chicago. 1--854. 1.
JUBULA Dumortier, Comment. Bot., 112, 1822 * [Latin juba, mane, hairs, alluding to the
numerous, vertically aligned elaters attached to the capsule
valve] Plants prostrate, loosely attached to substrate,
irregularly pinnately or bi-pinnately branched, vegetative branches intercalary,
sporadic and abbreviated, or terminal with an associated sub-orbicular dorsal
half leaf. Stem 8--15 cells wide in cross section, undifferentiated,
or with a single layer of thick-walled epidermal cells, and several layers of
thin-walled cortical cells, all 20--30 \um; rhizoids few, brownish, branched.
Lateral leaves inserted along an elongated,
almost longitudinal line, imbricate,
complanate or convex when dry, mostly complanate
when wet; antical margin slightly expanded and extending across stem;
lobules folded under the larger dorsal lobe and attached by a slightly enrolled,
stalk-like, postical margin, attached to the stem by a curved line of cells, parallel or sub-parallel to the
stem, when inflated ovoid or cylindric,
constricted at the mouth, opening
pointed toward shoot base, when explanate, lanceolate and acuminate, margins
somewhat reflexed; stylus filamentous, 1--2 cells, terminated by a slime papilla, located
between lobule
mouth and stem; marginal and
median cells of dorsal lobe
subquadrate to isodiametric, basal cells more elongate, all thin-walled, intermediate thickenings absent, trigones small, concave-sided; oil bodies granular,
spherical, or ellipsoidal. Ventral leaves distant to
contiguous, [narrow] orbicular, or elliptical, lobes narrow or broad, sinus
narrowly to broadly acute, base short- to long-decurrent [cuneate].
Sexual condition autoicous [rarely dioicous]. Androecia
mostly arising on spicate, Bryopteris-type
lateral branches [sometimes on short capitate
branches], consisting of 4--18 pairs of imbricate,
unequally 2-lobed bracts and bracteoles, each containing 1--2 antheridia. Gynoecia consisting of
one pair of keeled, subequally 2-lobed bracts and
bracteoles that are longer and wider than the vegetative leaves, bract dorsal
lobe longer and wider than bract lobule, stylar
tooth absent, bracteole free from bract, 2-fid, lobe apices acute to
acuminate, sinus margins plane or reflexed, margins entire to ciliate;
perianth emergent, obovoid, smooth; gynoecia with 1--4 archegonia. Foot indistinguishable. Seta
non-articulate, in transverse section
with a row of cells in outer layer, and four cells in inner layer. Capsule
2-stratose, the inner layer with reticulate cell wall thickenings, the outer
layer with nodular thickenings in cell wall angles, splitting into four,
strongly reflexed, hyaline valves. Elaters attached parallel to the
sporophyte, monospiral. Spores polyhedral,
pale brown, tan, or greenish. Species 5 (1 in the flora).
North America; Mexico; West Indies; Central
America; South America; Europe; Asia (including Indonesia); Africa (including
Madagascar); Atlantic Islands; Indian Ocean Islands; Pacific Islands;
Australia. Jubula and Frullania are the only two
liverwort genera in North America with inflated, helmet- or sac-shaped
lobules. However, despite this superficial similarity, the genera are
unlikely to be confused. Jubula frequently
has both
intercalary and terminal vegetative branches, whereas intercalary branching in Frullania is rare or associated with
damaged stems.
Furthermore, the dorsal lobes in Jubula are inserted
on the stem along an elongated,
longitudinal line, while in Frullania the insertion is shorter, subtransverse or oblique. Jubula also has an inconspicuous and reduced, sometimes
absent stylus, terminated by a slime papilla.
The stylus in Frullania is
generally more prominent, ranging from uniseriate to
lamellate, although it can occasionally be reduced in some species. In
addition, the androecia in Jubula mostly arise on spicate Bryopteris-type
branches, and have bracts and bracteoles throughout their length. In Frullania the
androecia are sessile or terminal on abbreviated or elongate Frullania-type
branches. The bracts can be few to numerous, but the bracteoles are only
found at the androecial base. The gynoecia of Jubula have a pair of bracts
and a bracteole in a single floral series, whereas the gynoecia in Frullania are
arranged in 2--5 series of pairs of bracts and bracteoles. Lastly, Jubula grows predominantly on
rocks in North America, although it has occasionally been collected on tree
bark, sandy soil, and as an epiphyll on leaves under very wet conditions. By
comparison, most North America Frullania species are epiphytic on tree trunks, branches
or twigs. While Frullania
may also occasionally inhabit rocks, the species usually occur in
considerably more mesic to xeromorphic conditions than Jubula. SELECTED REFERENCES Basile, D. V. 1964. The sporophyte of Jubula pennsylvanica.
Bryologist 67: 164--170. Crandall-Stotler, B. and W. R. Guerke 1980. Developmental anatomy of Jubula Dum. (Hepaticae).
Bryologist 83: 179--201. Guerke, W. R. 1978. A monograph of the genus Jubula
Dumortier. Bryoph. Biblioth.
17: 1--118. 1. Jubula hutchinsiae (Hooker) Dumortier, Comment. Bot., 112. 1822 Jungermannia hutchinsiae Hooker, Brit. Jungermann., Pl. 1, 1--2. 1812 Plants 1--2 cm x 1--1.8 mm. Stems 140–200 \um wide. Lateral leaves dorsal lobe ovate
to oblong-ovate, 0.6--1.1
x 0.6--0.9 mm, apex frequently decurved, [margins irregularly toothed or
spinose-dentate];
inflated lobules 0.2 x 0.2 mm [with appendage on external margin of
lobule mouth];
marginal cells 14--20 \um, median
cells 20--30 x 14--22 \um, basal cells 24--38 x 22--34 \um, oil-bodies 4--7 per cell, 6--10 x 2--5 \um. Ventral
leaves [margins spinose-dentate]. Gynoecia dorsal lobe oblong-ovate, 0.8--1.2 x
0.5--0.6 mm, apex acute to apiculate [or ciliate], margins entire [or irregularly toothed to spinose-dentate], lobule ovate-lanceolate, 0.6--1.2 x 0.4--0.5 mm, apex acute to acuminate,
margins entire [or spinose-dentate], sharply keeled, bracteole broadly
obovate, 1.0--1.6 x 0.8--1.2 mm; perianth 0.9--1.5 x 0.7--1.0 mm. Seta 1.2--2.8 mm. Capsule subglobose, blackish brown. Elaters
200--345 x 9--12 \um, reddish brown. Spores 20 x 30 \um. Subspecies 6 (2 in the flora). The genus Jubula contains
several morphologically variable species. The most widely-distributed of
these, J. hutchinsiae, is comprised of six
subspecies, two of which occur in North America. These two closely allied
taxa have been regarded as species (Evans 1905), subspecies of J. hutchinsiae (Verdoorn 1928), or subspecies of J. pennsylvaniva (Clark & Frye
1945; Guerke 1978; Schuster 1992), depending on
which morphological characters are emphasized. Based on unresolved sister
relationships among other Jubula taxa, as well as their overlapping morphologies, Pätsch et al. (2010) argued that the
North America representatives be treated as subspecies of J.
hutchinsiae.
Further justification for this rank was found by Konstantinova and Vilnet (2011),
who demonstrated variable and overlapping values in nuclear and chloroplast DNA sequences between taxa. 1. Dorsal
lobe margins mostly apiculate, sometimes bluntly acute, entire or with a few
ciliate teeth; lobules occasionally with a single projecting cell on external margin of mouth;
ventral leaves 3 or more times the stem
width, margins often with ciliate teeth or angulations............................................................. 1a.
Jubula hutchinsiae
subsp. bogotensis 1. Dorsal
lobe margins mostly rounded or bluntly acute, sometimes apiculate, entire;
lobules with smooth external
margin of mouth; ventral leaves
1--3 times the stem width, margins entire, rarely with angulations or ciliate
teeth........................................................................ ...................................................................................................................................... 1b. Jubula hutchinsiae subsp. pennsylvanica 1a. Jubula hutchinsiae
subsp. bogotensis (Stephani) Verdoorn, Ann. Crypt. Exot. 1: 215 1928 Jubula bogotensis
Stephani,
Sp. Hepat. 4: 687. 1911 Lateral leaves
dorsal lobe apex abruptly constricted, apiculate with a short tooth consisting of 2--4
slightly elongated cells, sometimes bluntly
acute, margins entire or with a few ciliate teeth, 1--3 cells long; inflated lobule sometimes with a projecting
cell on the external margin
of the mouth. Ventral leaves
0.4--0.6 x 0.6--0.7 mm, lobes with spiniform apices consisting of 2--4 slightly elongated
cells, margins commonly with 1--3 spinose teeth on each side, sometimes
entire. In
wet and shaded, north-facing crevices or under ledges; moderate elevations (200--1000 m); Ark.; Mexico; West Indies; Central America
(Costa Rica, Panama); South America. Jubula hutchinsiae
subsp. bogotensis was first reported from
North America by Schuster (1992) based
on a single
Arkansas specimen (Washington County, Anderson
12262). Since then, a few specimens at MO, originally determined as subsp.
pennsylvanica, have been discovered from
additional Arkansas counties. Some
populations from southeastern North America
have apiculate
dorsal lobe apices, ventral leaves that are approximately 3 times the width
of the stem, and more or less entire leaf margins. These
intermediate plants are morphologically comparable to robust expressions of
subsp. pennsylvanica
(see Schuster 1992: 282, fig. 822) as well as weak expressions of subsp.
bogotensis (see Verdoorn
1928: 217). Schuster (1992) noted that the Arkansas material might represent
a weak expression of subsp. bogotensis due to the lack of diagnostic
characters frequently observed in Neotropical subsp. bogotensis specimens. Typical subsp.
bogotensis,
like subsp.
hutchinsiae,
has discoid gemmae on the dorsal lobes as well as an elongate appendage on
the external margin of the lobule mouth. The Arkansas plants lack gemmae as
well as the lobule appendage, although some lobules have a distinct projecting cell on the mouth’s external margin. DNA sequencing is
needed to determine the affinity of these plants with Neotropical
populations. 1b. Jubula hutchinsiae
subsp. pennsylvanica (Stephani) Verdoorn, Ann.
Crypt. Exot. 1: 215. 1928. Frullania
pennsylvanica Stephani, Hedwigia 22:
147. 1883; J. hutchinsiae
var. sullivantii Spruce Lateral leaves dorsal
lobe apex rounded, bluntly acute, or apiculate with uniseriate tip, margins
entire; inflated lobule
with smooth external margin of the mouth. Ventral leaves 0.3--0.5 x 0.2--0.6 mm, with acute or
acuminate apices, margins mostly entire or occasionally with blunt
angulations or a ciliate tooth. In
deep, shaded crevices on damp soil or dripping rock walls; low to moderate elevations (0--1500 m); N.S.; Ala, Ark., Conn., Ga., Ill., Ind., Ky., Maine, Md., Mass., Mo.,
N.C., N.H., N.J., N.Y., Ohio, Okla., Pa., S.C., Tenn., Tex., Va., Vt.,
W.Va.; reported from Asia. Jubula hutchinsiae subsp. pennsylvanica is characterized by ovate to
oblong-ovate dorsal lobes with mostly rounded or acute, sometimes apiculate
apices. Furthermore, the leaves of subsp. pennsylvanica
have more or less
entire margins, compared to the more
irregularly toothed or spinose-margined leaves of subsp. hutchinsiae. This character has sometimes been used to
justify the recognition of two distinct species, despite intermediate
expressions of subsp. pennsylvanica having
weakly toothed leaf margins, and nearly entire
leaved expressions of subsp. hutchinsiae. A molecular phylogeny of Jubula (Pätsch et al.
2010) found that subsp. pennsylvanica and subsp.
bogotensis are closely allied, a result suggested earlier by Guerke (1978) through his examination of morphological
and phytogeographic evidence. Schuster (1992) noted that
compared to subsp. pennsylvanica, some
Neotropical specimens of subsp. bogotensis appear to be morphologically similar to subsp. hutchinsiae. Material for both of these
subspecies share toothed leaf margins, dorsal lobe gemmae, and lobule
appendages. In subsp. pennsylvanica, dorsal
lobe gemmae and appendaged lobules are consistently
absent. Conversely, subsp. pennsylvanica appears to be morphologically similar to the
newly described subsp. caucasica
from western Asia (Konstantinova
& Vilnet 2011). The two subspecies differ
slightly in the extent of their ventral leaf decurrencies. Although Schuster
(1992) reported that subsp. pennsylvanica may
have more numerous oil bodies per cell than that of subsp. hutchinsiae, the number of oil bodies observed
here and by Guerke (1978) overlaps with that
reported for subsp. hutchinsiae. SELECTED REFERENCES Clark, L. and T. C. Frye. 1945. Jubula pennsylvanica.
Bryologist 48: 127--130. Evans,
A. W. 1905. Notes on New England Hepaticae,—III. Rhodora
7: 52--58. Konstantinova, N. A. and A. A. Vilnet.
2011. Jubula hutchinsiae
subsp. caucasica
subsp. nov. Arctoa 20: 227--238. Pätsch, R., J. Hentschel, R. Linares-Palomino, R. -L. Zhu, and J.
Heinrichs. 2010. Diversification and taxonomy of the liverwort Jubula Dumort. (Jungermanniopsida: Porellales) inferred from nuclear and chloroplast DNA
sequences. Syst. Bot. 35: 6--12. Verdoorn, F. 1928. Über einige amerikanische Frullaniaceae. De Frullaniaceis
II. Annales Cryptog.
Exot. 1: 213--220. |
