BFNA Title: Jubulaceae
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.