BFNA Title: Calypogeiaceae
Date: Feb. 24, 2023
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Bryophyte Flora of North America, Provisional Publication
Missouri Botanical Garden
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38. CALYPOGEIACEAE Arnell

Patricia M. Eckel

Plants forming thin mats. Branches either intercalary from axils of underleaves or replacing ventral half of a leaf; ventral intercalary stolons with reduced leaves from axil of underleaf lacking; tips of branches sometimes tapering to flagella. Leaves alternate, obliquely inserted, incubous, plane, simple or very shallowly 2-lobed or 2-dentate, otherwise entire. Underleaves large, 2(--4)-lobed, occasionally with a strong lateral tooth on both sides. Rhizoids usually confined to base of underleaf, sometimes (in Eocalypogeia) also on underside of stem. Specialized asexual reproduction occasional, by ellipsoidal 1--2-celled gemmae on reduced leaves at attenuated shoot apices. Gynoecium on a short ventral branch, without subfloral branches. Perianth absent. Perigynium a deep, subterranean, conspicuous, fleshy marsupium.

Genera 6 (3 in the flora), species ca. 50 (10 in the flora). Nearly cosmopolitan in most continents, imperfectly circumtropical, with a high number of species in the neotropics; Greenland, Mexico, West Indies, Central America, North and South America, Europe, Eurasia, Africa, Atlantic Islands, Indian Ocean Islands, Pacific Islands, Australia.

The family Calypogeiaceae is distinct in the field, lacking secondary pigments and having a delicate, pale, translucent whitish to bluish or yellow-green color, the shoots flat to the substrate, the lateral leaves obliquely to widely spreading, rounded and without lobes or other ornamentation (sometimes minutely cuspidate or 2-dentate), incubously imbricated on the stem like scales, the insertion often so oblique as to be parallel to the stem. The underleaves are large, with abundant rhizoids tufted only in an elliptical area at their base, and with gemmae frequent at the ends of erect, gemmiparous branches. The sexuality of all North American species of the three genera in the family is autoicous, except dioicous in Calypogeia suecica. In most species, antheridia may also be found in the female inflorescences (paroicous).

Additional important features of Calypogeiaceae include: stem cortical and medullary cell-layers essentially undifferentiated, the cortical variously slightly larger or slightly smaller. Androecia on separate short ventral branches, spicate, of several to many pairs of tiny, reduced 2--3-lobed concave bracts, each bract containing 1 (occasionally 2--3) obovate to ellipsoid antheridia, stalk 1--2- seriate, the whole smaller than the underleaf in length. Sporophyte with the seta elongate, epidermal cells somewhat larger than internal ones; capsule elongate-cylindric (ovoid in one species), rupturing to the base into 4 linear to lingulate, parallel-sided and spirally twisted valves (in one species nearly straight), the wall 2-stratose, outer layer in 8--16 rows of cells; elaters moderately wide in 2(--3) narrow bands; spores 8--16 (--17) /um, finely granular-verruculose.

The family Calypogiaceae is included in the subtribe (Lepidoziinae) together with the Lepidoziaceae. All members of both families have incubous lateral leaf insertions, and rhizoids restricted to rhizoid initial areas at the base of the underleaves. Lepidoziaceae alone, however, have microphyllous, geotropic flagellae (stolons) as a dominant feature, and large bracts and bracteoles associated with a distinct fusiform perianth. Calypogeiaceae has only tiny, vestigial bracts on short ventral branches as it develops a pendant fleshy, rhizoid-covered pouch-like perigynium (marsupium) hidden and more or less buried in the substrate. Asexual reproduction in Lepidoziaceae is at most by caducous leaves (some stems with defoliated areas), but never with erect-ascending gemmiparous stems in an otherwise prostrate shoot as in Calypogeiaceae.

More importantly for identification, genera in the Lepidoziaceae have lateral leaves that are nearly always conspicuously 2--4-lobed or dentate, whereas species in the Calypogeiaceae essentially lack lobes, and although the leaves terminate in one or more minute teeth, the margins are otherwise never dentate. Sources of confusion occur mostly with the genus Bazzania of the Lepidoziaceae, whose apical leaf lobes in some species are short (less than 1/5 the leaf length). Bazzania species will commonly have intercalary microphyllous root-like flagella or stolons, the lateral leaves possess 2--3 distinct asymmetrical apical teeth, and fertile plants regularly produce strongly bracted perianths. Branching in Bazzania, alone in the Lepidoziaceae, is furcate (pseudodichotomous or Y-shaped) whereas branching in the other Lepidoziaceous genera, as well as in the Calypogeiaceae, is typically pinnate (ventral intercalary)—except the single species in Eocalypogeia, which is also pseudodichotomous. Bazzania leaves have large and bulging stellate trigones, whereas Calypogeiaceae seldom has these, or these less distinct.

Such generalized oil body characteristics of species in this family described below are derived from the published literature, illustrations and photographs, as these organs had disappeared in the dried herbarium specimens on which the following treatment is based. Deterioration of oil bodies in freshly collected material may be delayed by immediate refrigeration and prompt study (David Wagner, personal communication).

SELECTED REFERENCES

Bakalin, V.A. 2007. Liverworts of Kamchatka: The results of study. In Proceedings of the VII International Scientific Conference “Conservation of Biodiversity of Kamchatka and Coastal Waters,” Petropavlovsk-Kamchatsky, Russia, 28–29 November 2007; pp. 6–14.

Damsholt, K. 2013. The Liverworts of Greenland. Nordic Bryological Society, Lund, Sweden.

Frye, T. C. and L. Clark. 1946. Calypogeia. Hepaticae of North America, part IV. p. 678--687. Vol. 6 (4). University of Washington Publications in Biology, University of Washington Press, Seattle, Washington.

Hong, W. S. 1990. The Family Calypogeiaceae in North America West of the Hundredth Meridian. Bryologist 93: 313--318.

Stotler, R. E. and D. K. Crotz. 1983. On Mnium trichomanis Linnaeus (Hepatophyta). Taxon 32: 64--75.

Stotler, R. E. and B. Crandall-Stotler. 2017. A synopsis of the liverwort flora of North America north of Mexico. Ann, Missouri Bot. Gard. 102: 574--709.

1. Plants yellow to dark green, opaque, strongly chlorophyllose; shoots with branching mostly lateral and pseudodichotomous (furcate); rhizoids from underleaf bases and also scattered on stems; leaf cell cuticle verruculose-striolate, not smooth, leaf cells with conspicuous trigones; oil-bodies finely granular, opaque, gray-brown; marsupia appearing stalked, shortly ovoid-oblong with few rhizoids, shallowly subterranean; capsule oblong-ovoid, dehiscing into 4, nearly straight valves; gemmae absent. 1. Eocalypogeia, p. XX

1. Plants pale- to grayish to bluish green, translucent, weakly chlorophyllose; shoots in most species with branching normally all ventral-intercalary (pinnate); all rhizoids from underleaf bases only, none from stem cells; leaf cell cuticle verruculose-striolate or smooth, leaf cells generally lacking conspicuous trigones (except in two species); oil-bodies finely or mostly coarsely segmented, granular or botryoidal, hyaline, colorless or blue; marsupia appearing sessile, cylindric, densely rhizoidous, deeply subterranean; capsule cylindric, dehiscing into 4 spirally twisted valves; typically gemmiferous.

2. Stems appearing transversely flattened (elliptical) in section, usually of 4--6 cell rows dorsally, 4--6 cell rows ventrally, only 5--6 cells high, laterally bounded on each side by a single row of larger, hyaline cells (to which leaves are attached), cell cuticle verruculose-striolate; lateral leaf apices regularly sharply 2-dentate; underleaves 2-fid, sometimes four-lobed (bis-2-fid),  cleft to within 1 (--2) cells of rhizoid initial area, lobes acuminate; lateral underleaf outer margins uniformly armed with small, narrow, sharp teeth at the base 1--2 (--3) cells long on each margin; oil bodies spherical to broadly ovoid, composed of minute spherules (ca. 1--1/3 /um) .. 2. Asperifolia, p. XXX

2. Stems terete to elliptical in section, usually of 6 - 8 (9--14) or more cell rows dorsally, 8--10 cell rows or more ventrally, 7--9 (10) cells high, laterally bounded on each side by 2--3 rows of cells approximately the same size (to which leaves are attached); cuticle essentially smooth; lateral leaf apices entire or weakly 2-dentate; underleaves mostly 2-lobed to entire; cleft to within 2--6, to 7--14 cells of rhizoid initial area, lobes (if any) broad and more or less obtuse to acute, lateral underleaf margins entire or with short, broad, blunt teeth on one or both margins; oil-bodies linear or ellipsoidal, composed of large spherules (ca. 1.5--4 /um) except in one species.…  …3. Calypogeia, p. XXX

1. EOCALYPOGEIA (R. M. Schuster) R. M. Schuster, Fragm. Florist. Geobot. 40: 861. 1995 * [Greek eos, of the dawn, and Calypogeia, alluding to an inferred primitive state]

Metacalypogeia subg. Eocalypogeia R. M. Schuster, Hepat. Anthocerotae N. Amer. 2: 107. 1969

Plants yellow to deep green, opaque and firm, strongly chlorophyllose. Stems terete to elliptical in section, usually of (6--) 9--13 or more cell rows dorsally, 9--12 cell rows or more ventrally, 6--9 cells high, laterally bounded (at point of attachment of the leaf) on each side by 2--3 rows of cells approximately the same size to which leaves are attached. Shoots relatively small; simple or sparsely branched, with branching generally lateral and pseudodichotomous (furcate), often terminal, replacing the central half of a lateral leaf (Frullania type lateral branches); abbreviated sexual branches ventral intercalary. Rhizoids from stem cells scattered along stem, especially with age, and also abundant in sharply defined areas at bases of underleaves. Lateral leaves contiguous to moderately imbricate, narrowly ovate-lanceolate to ovate-triangular, slightly falcate, apex distinctly narrowed to the tip, normally bluntly acute, occasionally broadly and asymmetrically 2-dentate. Underleaves transverse, distant, small, equaling the stem width, normally 2-fid, sinus acute, lobes bluntly triangular to rounded, margins undulate, entire or sometimes with a blunt or rounded angulation or tooth at one or both sides. Leaf cells ca. (23-)25--32(--40) x 35--40(--50) /um midleaf, generally thin-walled, with conspicuous trigones, cuticle verruculose-striolate especially near base of leaf, some apical cells transversely elongate forming a weak border. Oil-bodies ovoid to ellipsoid, finely and minutely granular, opaque, gray-brown. Specialized asexual reproduction by gemmae absent. Sexual condition autoicous, antheridia may also be found in the female inflorescences (paroicous). Marsupia appearing stalked, the branch bearing at least 1--2 pairs of leaves, shortly ovoid-oblong with few rhizoids, shallowly subterranean; capsule oblong-ovoid, dehiscing into 4, nearly straight valves.

Species 2 (one in the flora): North America, Eurasia (e Siberia), Asia (Japan, Korea, Thailand), Pacific Ocean Islands (Hawaiian archipelago).

S. Hattori (1957) established the subgenus Metacalypogeia segregated from Calypogeia based on differences in oil body and cuticular structure. H. Inoue (1959) elevated Metacalypogeia to generic status, emphasizing the oblong, nearly straight capsule valves and their outer layer wall ornamentation. Eocalypogeia was in turn separated from Metacalypogeia as a subgenus (R. M. Schuster 1969) by the autoicous sexual condition, pseudodichotomous, lateral branching (Frullania-type), the granular-botryoidal oil-bodies, the rhizoids on both underleaf bases and scattered along the stem, elongated primitive gynoecial branches, and perigynial and capsule shape. Metacalypogeia subg. Eocalypogeia R. M. Schuster was then given generic rank (R. M. Schuster and N. A. Constantinova 1996) as Eocalypogeia (R. M. Schuster) R. M. Schuster, containing two species, with one in the flora, the other Asian.

Eocalypogeia in the flora region is associated with basic rocks and basiphilous species in calcareous wet fens and limestone ledges, unlike the more acidic substrates favored by species of Calypogeia which never grow directly on calcareous substrata.

SELECTED REFERENCES:

Hattori, S. 1957. Hepaticae of Hokkaido. II. Rishiri and Reben Islands. J. Hattori Bot. Lab. 18: 75--92;

Inoue, H. 1959. On Metacalypogeia, a new genus of Hepaticae. J. Hattori Bot. Lab. 21: 231--235.

Schuster, R. M. and N. A. Konstantinova. 1996. Studies on the distribution of critical Arctic/Subarctic hepaticae with special reference to taxa found in Russia. Lindbergia 21:. 26--48.

1. Eocalypogeia schusterana (S. Hattori & Mizutani) R. M. Schuster, Fragm. Florist. Geobot. 40: 861. 1995

Metacalypogeia schusterana S. Hattori & Mizutani, Misc. Bryol. Lichenol. 4: 121. 1967

Plants thin, flat. Leafy shoots small, (1--)1.4--1.6 mm wide. Leaves slightly asymmetrically longer than wide, apices entire or emarginate to rarely shortly asymmetrically 2-dentate, strongly narrowed. Underleaves divided 0.4--0.6 of length to the rhizoid initial area, lobes bluntly triangular, obtuse or rounded, sinus V-shaped, lateral margins rounded, midline from base of sinus to rhizoid-initial area in a series of (1--) 2--5 cells, rhizoid initial area not prominent, not colored, underleaf not or slightly decurrent, cuticle more or less roughened (verruculose-striolate). Leaf cells at midleaf rather large, trigones sometimes bulging, apical marginal cells sporadically isodiametric among tangentially strongly elongated cells forming an obscure border. Oil-bodies present in all cells in fresh material, grayish to brownish when fresh or dry. Specialized asexual reproduction by gemmae absent.  

Damp, black humus and thin soil over or directly on bare basic rocks, small, steep ravines or crevices in limestone cliff ledges, stony slopes of knolls, wet shrub-grass-moss tundra, calcareous fens; 0--900 m elevation; Greenland; Nfld. and Labrador (Nfld.), N.W.T., N.S., Que., Yukon; Alaska; Asia (e Siberia).

Plants of Eocalypogeia schusterana are obscurely shiny or weakly glistening when dry (R. M. Schuster 1969) whereas they glisten as if varnished in species of Calypogeia; only in Asperifolia sullivantii, Calypogeia integristipula (except on the margins), and C. neesiana are they dull. The cuticle of Eocalypogeia is striolate-verruculose, especially at the leaf bases, although smooth in nearly all species of Calypogeia, and weakly striolate-papillose in A. sullivantii. In Calypogeia, no species has consistently distinct trigones except C.sphagnicola and C. suecica.

Although gametangia are frequent, the sporophytes of this rare plant are known only from the type locality (R. M. Schuster and N. A. Konstantinova 1996). Since no mature capsules of the species are known, the structure of the capsule epidermis has not been determined. The epidermal cells of the capsule wall in Metacalypogeia (Hatt.) Inoue with which the genus Eocalypogeia was joined (as a subgenus), are distinctive as the long axis of the cells and their ornamentation are transverse, not longitudinal, a feature which may be anticipated in mature capsules in the genus Eocalypogeia.

Eocalypogeia schusteriana superficially resembles Calypogeia sphagnicola, notably in its small size (< 2 mm wide), but especially in the often lateral pseudodichotomous and terminal Frullania-type branching, but the latter species is shining and translucent (not only obscurely shining and opaque, as in E. schusterana), and pale whitish to yellowish green (not deep green), with gemmae usually produced at the ends of gemmiparous shoots (rather than never with gemmae). Calypogeia sphagnicola has isodiametric cells on the apical margin of the lateral leaves (not with an obscure border of elongate cells). The substrate of C. sphagnicola is typically Sphagnum mats in acidic situations, rather than the calcareous mineral, substrates of Eocalypogeia schusteriana.

In northern regions, Eocalypogeia schusterana might be confused with Bazzania tricrenata (Wahlenberg) Trevisan due to similar deep opaque green color, frequent terminal pseudodichotomous branching of the Frullania-type and distinct trigones on leaf cells. These species can be told apart when fertile—Eocalypogeia with a marsupium, Bazzania with a 3-angled perianth. Sterile specimens of Bazzania often have three lobes in the leaf apex (Eocaypogeia mostly one). Bazzania tricrenata displays intercalary microphyllous rootlike stolons, but not Eocalypogeia; stem sections of Bazzania show a thick epidermis and epidermal layer of cells thicker-walled than the smaller medullary cells, whereas in Eocalypogeia all the cells are leptodermous and virtually undifferentiated. Rhizoids are sparse at underleaf bases in Bazzania, but occur in dense masses in Eocalypogeia schusterana.

2. ASPERIFOLIA (R. M. Schuster) Bakalin & Maltseva, Plants 11(7, 983): 34. 2022 * [Latin asper, rough, and folius, leaved, alluding to slender and regularly toothed apices of the lateral leaves]

Calypogeia subg. Asperifolia R. M. Schuster, Hepat. Anthocerotae N. Amer. 2: 115. 1969 (replaced synonym: Calypogeia [unranked] Asperifoliae Warnstorf)

Plants a clear to whitish or yellowish green, translucent, weakly chlorophyllose. Stems appearing flattened in section, usually of 4--6 cell rows dorsally, 4--6 cell rows ventrally, only 5--6 cells high, laterally bounded on each side by a single row of larger, hyaline cells (to which leaves are attached); cortical cells somewhat to distinctly larger than medulla cells. Shoots relatively small, usually less than 2 mm wide, with branching normally all ventral-intercalary; abbreviated sexual branches ventral intercalary. Rhizoids from stem cells absent, rather sparse from defined areas only at the bases of underleaves. Lateral leaves distant to contiguous to slightly imbricate, narrowly to broadly ovate to oblong-elliptic; longer than wide, apices narrowly, sharply and uniformly symmetrically 2-dentate, teeth subparallel in our species. Underleaves transverse, distant, small (about equaling the stem width), often four-lobed (bis-2-fid) to within 1 (--2) cells of rhizoid initial area weakly rhizoidous, rhizoid initial area weak vs. distinct, of 3-4 rows of smaller cells, sinus broadly lunate, lobes acuminate, margins uniformly armed with small, narrow, sharp teeth at the base 1--2 (--3) cells long, on each outer margin. Leaf cells large, ca. 30--60 x 50--80 (--89) /um, thin-walled, trigones lacking, verruculose-striolate, apical cells isometric. Oil-bodies spherical to broadly ovoid, granular, composed of minute spherules (ca. 1--1/3 /um), translucent, hyaline. Specialized asexual reproduction by gemmae frequent, 1--2-celled, from reduced leaves and underleaves of the apices of erect, tapered shoots. Sexual condition monoicous (in ours) or indeterminate-dioicous. Marsupia appearing sessile, leafless, cylindric, densely rhizoidous, deeply subterranean; capsule cylindric, dehiscing into 4 spirally twisted valves.

Species 3 (one in the flora): North America, Europe, Asia (Vietnam).

R. M. Schuster (1995) recognized the subgenus Asperifoliae (Warnstorf) K. Müller, which included Calypogeia arguta Nees & Montange and C. sullivantii Austin, for the North American flora mostly based on structural differences in the epidermal characteristics of the capsule valves, stem structure, underleaves, and oil bodies. In the subgenus Asperifoliae, none but the two species reported here were accepted worldwide by L. Söderström et al. in 2016.

Species of the genus Asperifolia display a flattened stem section containing fewer cells with a lateral row of enlarged cells at the leaf insertion, with differences in underleaves and oil body configuration as defined in the key to the genera. Cells of the species of the genus display a cuticle that is distinctly verruculose-striolate. The bistratose structure of the epidermis of the capsule is distinctive between the two genera. The axis of the external cells in both genera is longitudinal. In Asperifolia, the external cells are about as wide as the cells of the inner layer, whereas in Calypogeia the epidermal cells are twice as wide. In Asperifolia, the entire capsule is made up of 64 longitudinal cell rows, in Calypogeia, 32. Each capsule divides into four linear valves, and in Asperifolia each valve has 16 longitudinal rows of cells divided into four groups of 4 longitudinal cells each (16:4). In Calypogeia each valve is made up of 8 longitudinal rows, these divided into four groups of 2 (8:2). In the capsule of Asperifolia, each fourth longitudinal wall is thin and lacks thickenings, whereas in the capsule of Calypogeia the longitudinal walls alternate, one thin, the next thick, or else all of the walls are thickened. Capsule valve morphology was not given for Asperifolia indosinica (V. A. Bakalin et al. 2022).

Asperifolia arguta (Nees & Montagne) A.V. Troitsky, Bakalin & Maltsevais here excluded as it was reported (as Calypogeia arguta Nees & Montagne) from a single collection from the flora area, adventive in a greenhouse in Philadelphia, Pennsylvania (A. Evans 1907b) and cited for the North American flora by T. C. Fry and L. Clark (1946) but never naturalized or occurring in additional natural or greenhouse situations. The dioicous Asperifolia arguta is a European species with widely divergent apical lateral leaf teeth. Asperifolia sullivantii is monoecious with apical teeth nearly parallel. R. M. Schuster (1969) indicated A. sullivantii was “doubtfully specifically distinct” from A. arguta, separated most importantly by sexuality, although T. C. Fry and L. Clark (1946) reported A. sullivantii as dioicous, and Schuster himself indicated (with a question mark) that the species may be “sometimes dioecious” (R. M. Schuster 1969). The sexual condition of the third species reported for the genus, Asperifolia indosinica Bakalin & Troizky, was not described by the authors (V. A. Bakalin et al. 2022).

Exceptionally, Calypogeia sphagnicola shares capsule wall morphology with Asperifolia in that the epidermal cell layer of each valve also has cells in 16 rows (not 8, as in. Calypogeia) (R. M. Schuster 1969). Hence 64 longitudinal cell rows occur for the entire capsule (not 32). But whereas in Asperifolia every fourth longitudinal wall is thin walled, in C. sphagnicola, the thin walls alternate with thickened ones, as in Calypogeia.

SELECTED REFERENCES:

Bakalin, V. A., Y. D. Maltseva, F. Müller, K. G. Klimova, V. S. Nguyen, S. S. Choi, and A, V. Troitsky. 2022. Calypogeia (Calypogeiaceae, Marchantiophyta) in Pacific Asia: Updates from molecular revision with particular attention to the genus in North Indochina plants. Plants 2022, 11(7), 983; https://doi.org/10.3390/plants11070983, pp. 1--56.

Evans, A. W. 1907. Notes on New England hepaticae---5. Rhodora 9: 56--60, 65--73, pl 73.

Frye, T. C. & L. Clark. 1946. Calypogeia. Hepaticae of North America, part IV. p. 678--687. Vol. 6 (4). University of Washington Publications in Biology, University of Washington Press, Seattle, Washington.

Söderström, L., A. Hagborg, M. von Konrat, S. Bartholomew-Began, D. Bell, L. Briscoe, Elizabeth Brown, D. C. Cargill, D. P. da Costa, B. J. Crandall-Stotler, E. D. Cooper, G. Dauphin, J. Engel, K. Feldberg, D. Glenny, S. R. Gradstein, X. Hu, J. Heinrichs, J. Hentschel, A. L. Ilkiu-Borges, T. Katagiri, N. A. Konstantinova, J. Larraín, D. Long, M. Nebel, T. Pócs, F. Puche, E. Reiner-Drehwald, M. Renner, A. Sass-Gyarmati, A. Schäfer-Verwimp, J. G. Segarra-Moragues, R. E. Stotler, P. Sukkharak, B. Thiers, J. Uribe, J. Váňa, J. Villarreal, M. Wigginton, L. Zhang & R. Zhu. 2016. World checklist of hornworts and liverworts. (29 Jan 2016). PhytoKeys 59: 1--828.

1. Asperifolia sullivantii (Austin) A. V. Troisky, Bakalin & Maltseva. Plants 11(7, 983): 35. 2022

Calypogeia sullivantii Austin, Hepat. Bor.-Amer., 19 (no. 74b). 1873

Plants thin, flat, translucent, pale to typically deeper and pure green, as single shoots, in patches, or loose mats. Leafy shoots small 1.2--1.8(--2.1) mm wide. Lateral leaves ovate to broadly ovate, longer than wide, leaf apex narrowed, never entire, uniformly sharply, narrowly 2-dentate on all leaves, the segments long, ending in a 2--3-celled tip from a generally 2--4 celled base, the teeth normally nearly parallel; leaf cells midleaf thin-walled, 40 x 60(--80) /um; apical marginal cells isodiametric or nearly so, not forming a border of tangentially elongate cells; oil-bodies present in all cells in fresh material, essentially colorless fresh or dry. Underleaves deeply divided 4/5--5/6 their length to rhizoid initial area, lobes acuminate to acute, subulate, with one or more 1--2-celled strongly divergent teeth , sinus narrowly rounded to crescentic (i.e. with teeth slightly convergent at their tips), lateral margins uniformly armed midlobe with a small, sharp tooth, midline from base of sinus to rhizoid-initial area in a very short series of 1(--2) cells; rhizoid initial area not prominent, not colored, small, transversely oval-oblong; underleaf somewhat decurrent; cuticle weakly striate-papillose. Specialized asexual reproduction by gemmae frequent. Sexual condition autoicous. 

Mostly acidic, deeply shaded mineral substrates, including damp rocks, loamy, clayey, silty, stony soils and peats, sides of wet ditches, creek bottoms banks, thin soil on damp sandstone outcrops and ledges, rock crevices and cave floors; 0--628 m elevation; N.S.; Ala., Ark., Conn., D.C., Del., Fla., Ga., Ky., Ill., La., Maine, Md., Mass., Miss., Mo., N.H., N.J., N.Y., N. C., Ohio, Okla., Pa., R.I., S.C., Tenn., Va., W.Va.; West Indies.

Specimens previously identified as Calypogeia arguta in N. America are Asperifolia sullivantii (R. M. Schuster 1969). Lateral leaves are distant to slightly imbricate; are small (rudimentary) near the shoot base and increase in size upwardly. The leaves are attached laterally on each side of the apparently flattened stem along a single row of enlarged, hyaline cortical cells, hence the stem appearing narrowly winged. Lateral leaf apices not falcate, not or slightly decurrent. The cells at the leaf attachment to the stem are therefore much larger than the adjoining cortical cells as the internal cells of the medulla are smaller. The underleaves are uniformly bis-2-fid or 2-fid and are armed with a narrow lateral tooth at the marginal base. The plants, as in C. integristipula and C. neesiana, are not nitid, but dull.

Oil bodies are coarsely granular, whereas in all species of Calypogeia they are composed of coarsely botryoidal globules, except in C. peruviana. Calypogeia peruviana, whose range overlaps in the southeastern United States, also has sharply 2-dentate lateral leaf apices and narrow teeth on the lateral margins of the underleaves, but the 2-dentate teeth are short and are widely separated forming a rounded, obtuse sinus, the leaf cells are smaller (to 39 /um), the underleaf lobes are broad and blunt, there are no inflated cells at the lateral leaf insertion, the overall cells are smooth. The oil bodies in C. peruviana are vivid blue when fresh and are also composed of numerous small, almost granulose segments.

3. CALYPOGEIA Raddi, conserved name., Jungermanniogr. Etrusca, 31. 1818 * [Gk. calyx, cup, and hypogaeus, subterranean, alluding to buried sac (marsupium) holding the sporophyte]

Plants closely prostrate to ascending when gemmiparous; bluish green or whitish green, usu. translucent and delicate, weakly chlorophyllose. Stems terete to elliptical in section usually of 6--8(--14) or more uniformly sized cell rows dorsally, and 8--10 uniformly-sized cell rows or more ventrally, 7--9(--10) cells high, laterally bounded on each side by 2--3 cell rows approximately the same size (at point of attachment of the leaf), as the other cells; cortical cells somewhat larger than the medulla cells. Leafy shoots variable, (0.8--)2--3(--4) mm wide, in most species with branching normally all ventral-intercalary (pinnate); abbreviated sexual branches ventral intercalary. Rhizoids from stem cells absent, sparse to abundant in usually clearly defined linear to subobicular areas at bases of underleaves. Lateral leaves distant to imbricate, narrowly to broadly ovate, ovate-elliptic to ovate-triangular, falcate at apex or not; apices rounded and entire to pointed, or weakly and regularly 2-denticulate. Underleaves transverse to elongate, variously distant, contiguous to imbricate, mostly large (equaling or to 4 x the stem width), orbicular to retuse, 2-fid to irregularly bis-2-fid to within a rather long line of 2--6(--14) cells of rhizoid initial area, lobes in divided underleaves broadly to narrowly obtuse to acute, their sinuses variously rounded to acute, margins entire or generally with blunt or in one species sharp teeth on one or both sides. Leaf cells 30--60 x 45--90 /um midleaf, thin-walled, trigones lacking or distinct in two species, cuticle essentially smooth, apical cells isodiametric or in two species tangentially elongate apical marginal cells forming a weak border. Oil-bodies linear or ellipsoidal, mostly composed of large spherules (ca.1.5--4 /um) or minute-granular in one species, translucent, hyaline or two species deeply blue when fresh. Specialized asexual reproduction by gemmae frequent, from reduced leaves and underleaves of the apices of erect, tapered shoots. Sexual condition autoicous, often paroicous, but one species dioicous. Marsupia appearing sessile, leafless, cylindric; capsule cylindric, dehiscing into 4 spirally twisted valves.

Species ca. 40 (8 in the flora): nearly cosmopolitan; Greenland, Mexico, West Indies, North America, Central America, South America, Eurasia, Africa, Atlantic Islands, Indian Ocean Islands, Pacific Islands (New Zealand, New Caledonia), Australia (Tasmania).

The current definitive taxonomic treatment of the genus in North America is restricted to the East (R. M. Schuster 1969). Recent attempts to evaluate the genus in the West are hampered by lack of critical study in those regions, most current identifications relying on Frye, T. C. and L. Clark (1946) and Schuster’s 1969 evaluations of eastern populations. Such limited attempts to describe western species include Hong (1990), Doyle, W. T. and R. E. Stotler (2006), V.A. Bakalin  (2012)  and V. A. Bakalin et al.  (2022).  

The full distribution of some species is also unknown due to recent nomenclatural revisions. Although the genus is quite distinctive, its species are difficult to tell apart due to extensive intergrading of morphology (polymorphism) not only between species but throughout the ecological gradations of moisture and exposure, and immaturity and maturity of individual collections. R. M. Schuster (1969) has cast doubt as to the viability of many earlier treatments of the family and indeed of identified collections residing in herbaria, preferring field identifications where living growth factors may be taken into account. Records earlier than Schuster’s 1969 treatment relied on earlier nomenclature and were found to be problematic, and the application of names difficult, as was best addressed in the paper by R. E. Stotler and D. K. Crotz (1983). Present nomenclature for the genus in the flora follows R. E. Stotler and B. Crandall-Stotler (2017).

Calypogeia occurs from sea-level to alpine but is absent from deserts and high, cold Arctic regions. It is found on acidic to neutral substrates, and unlike Eocalypogeia, is a calcifuge. Species are terrestrial, growing on organic or inorganic mineral clays to silty soil and rocks, on rotten logs in deep forest, with dependable moisture, in usually very wet sites, but not aquatic, sometimes among other bryophytes including Sphagnum hummocks in peatland, avoiding low humidity, high temperatures and high light intensity.

Species of Calypogeia display a rounded (not flattened) stem section with more constituent cells, lacking a lateral row of enlarged cells at leaf insertion. All of the species in the genus in North America are typically smooth-celled and lack a distinct verruculose cuticle. The underleaves are more uniformly 2-fid (except variably bisbifid in C. fissa and and C. peruviana). The oil-bodies are all coarsely segmented (except they are granular in C. peruviana), and are blue when fresh only in two species. The sexuality of species in the genus is autoicous, often paroicous; only C. suecica is dioicous.

SELECTED REFERENCES:

Bakalin, V. A. 2012. A small collection of hepatics from Oregon and California (western North America). Arctoa Vol. 21: 201--205.

Bakalin, V.A., Y. D. Maltseva, F. Müller, K. G. Klimova, Van Sinh Nguyen, Seung Se Choi and A. V. Troitsky. 2022.  Calypogeia (Calypogeiaceae, Marchantiophyta) in Pacific Asia: Updates from molecular revision with particular attention to the genus in North Indochina Plants  2022, 11, 983: 1--56.

Doyle, W. T. and R. E. Stotler. 2006. Contributions toward a bryoflora of California III. Keys and annotated species catalogue for liverworts and hornworts. Madroño, California Bot. Soc. 53: 89--197;

Stotler, R. E. and D. K. Crotz. 1983. On Mnium trichomanis Linnaeus (Hepatophyta). Taxon 32: 64--75.

Stotler, R. E. and B. Crandall-Stotler. 2017. A synopsis of the liverwort flora of North America north of Mexico. Ann, Missouri Bot. Gard. 102: 574--709.

1. Cells in fresh material with oil bodies distinctly bright ultramarine blue, shoot apices bright blue.

 2. Leaf apex usually entire or broadly angulate; leaves as wide as or often wider than long; leaf cells large, to 50 /um; underleaf lobes broadly triangular, parallel, sinus acute, narrow, lateral margins usually rounded and entire; underleaves typically imbricate, only slightly decurrent; a species of northwestern North America and disjunct to the northeastern United States (New England) and Eurasia      1. Calypogeia azurea, in part

 2. Leaf apex typically sharply 2-dentate; leaves often longer than wide; leaf cells smaller, to 40 /um; underleaf lobes mostly narrowly triangular, strongly divergent, sinus lunate-rounded, obtuse and broad, lateral margins nearly always with a blunt or acute tooth; underleaves typically remote, often distinctly decurrent; a species of southeastern North America and South America.   6. Calypogeia peruviana, in part

1. Cells in fresh and/or dried material with oil bodies colorless and pellucid or pale gray, shoot apices greenish to whitish or grayish green, or (in dried material) with a bluish-green tinge.

3. Underleaves entire, shallowly notched to emarginate (only 0.1 to 0.25 of length); base not or slightly decurrent; midline from base of shallow sinus or apex of orbicular underleaf to rhizoid-initial area in a series of usually (6-) 7--10 (--14) cells; lateral leaves often with tangentially elongate apical marginal cells.

 4. Leaf apex narrowly truncate, retuse, sometimes bluntly 2-dentate; leaves usually distinctly bordered with tangentially elongate apical marginal cells; leafy shoots small, 1--2 (--2.5) mm wide; underleaves somewhat distant, retuse to obscurely 2-lobed at the apex; rhizoid-initial zone transversely linear, indistinct, often sparsely rhizoidous; oil bodies in fresh material absent in median leaf cells, completely absent in underleaves     4. Calypogeia neesiana

 4. Leaf apex narrowly rounded; leaves indistinctly bordered, with tangentially elongate apical marginal cells discontinuous with isodiametric cells; leafy shoots larger, 2.4--3.2 mm wide; underleaves somewhat imbricate, rounded at the apex; rhizoid-initial zone suborbicular, distinct, densely rhizoidous; oil bodies in fresh material present in all cells of leaves and underleaves      2. Calypogeia integristipula.

  3. Underleaves consistently 2-lobed (0.50 or more of length); base decurrent or not; midline from base of sinus to rhizoid-initial area in a series of (1--)2--6 cells; lateral leaves mostly with cells isodiametric to oblong, lacking tangentially elongate apical marginal cells.

5. Mature plants small, usually less than 2 mm wide (often to 1 mm); leaf cells rather small, seldom 24--35 x 25--44 /um; cells with small but distinct trigones; plants only on organic substrates; plants never bluish green.

 6. lateral leaves obliquely ovate to triangular-ovate, underleaves slightly wider than stem, not or slightly decurrent, leaves and underleaves often remote, underleaves mostly lacking angulations on lateral margins, monoecious, mostly on moss and sphagnous peat                                                              7. Calypogeia sphagnicola

 6. lateral leaves ovate to suborbicular, underleaves often more than 2 x wider than stem, distinctly decurrent, leaves and underleaves contiguous to more usually imbricate, underleaves often angular or lobed on one or occasionally both lateral margins, dioecious, mostly on decaying logs                  8. Calypogeia suecica

5. Mature plants larger, usually more than 2 mm wide; leaf cells larger, (26-)30--48 x (26-) 34--70 /um; cells without distinct trigones; plants on organic substrates or not; plants bluish green or not.

 7. Plants (1.5--)2--2.5(--3) mm wide; lateral leaves typically longer than wide; leaf apices apiculate, acute or 2-dentate; underleaf lateral margins usually with an obtuse to subacute tooth or teeth; deeply divided to within 1--2(--3) cells of rhizoid initial area.

 8. Plants whitish green to slightly yellowish green, living shoot tips whitish green; lateral leaf apices rounded-acute, entire to bluntly apiculate by 1--3 cells, if slightly 2-dentate, the teeth juxtaposed and sinus narrow, variously V-shaped to broadly rounded-rectangular; underleaves 1.5--1.8 x stem width; underleaf lateral margin angulations obtuse to subacute, broad, mostly lacking teeth; cells from base of sinus to rhizoid initial area in a short row of 1--2(-- 3) cells; underleaf not or indistinctly decurrent                    5. Calypogeia neogaea

 8. Plants deep grayish green to dark bluish-green, living shoot tips bright ultramarine blue; lateral leaf apices obtuse, ending with two short, sharp widely separated teeth, the sinus broadly U-shaped (crescentic); underleaves wider, 1.8--2.5 x stem width; underleaf lateral margin angulations broadly to narrowly often sharply triangular, sometimes with additional short acute teeth; cells from base of sinus to rhizoid initial area in a slightly longer row of 2--3 cells; underleaf distinctly decurrent                                   6. Calypogeia peruviana

 7. Plants wider, 2.5--3.5(--4) mm wide; lateral leaves usually as wide as or wider than long; leaf apices rounded, typically entire; underleaf lateral margins mostly lacking a marginal tooth or angulation; cells from base of sinus to rhizoid initial area in a longer row of (3--)4--5(--6) cells.

9. Wet or dry plants usually greenish, whitish or grayish green at shoot apices; lateral leaf apices rounded, broadly obtuse to narrowly subacute; lateral leaf cells large 40--50 x (45--)55--70 /um; underleaves usually distant, seldom more than 1/3--2-lobed, never appearing 3-fid, cleft to (3--)-4--6 cells of rhizoid-initial area, lobes obtuse to broadly rounded, sinus often rounded; lateral margins smooth; rhizoid initial area transversely elongate-elliptic, base normally clearly decurrent; plants of wide distribution in the United States and Canada              3. Calypogeia muelleriana

9. Wet plants azure blue at shoot apices, dry plants deep grayish to dark green, somewhat bluish-gray at shoot apices; lateral leaf apices narrowly rounded, often bluntly acute-broadly subacute, lateral leaf cells smaller, 30--39 x 35--50 /um, underleaves mostly subimbricate to approximate, mostly 1/3--3/4, 2-lobed, often appearing 3-fid by the division of one lobe, cleft to 2--4(--5) cells of rhizoid-initial area, lobes broadly lanceolate-triangular, acute, subacute, to narrowly rounded; one lateral margin often bluntly angulate; sinus often acute to subacute; rhizoid initial area transversely oval to nearly round; base not or slightly decurrent; rare plants of the Pacific Northwest and disjunct to northeastern United States (New England)                     1. Calypogeia azurea, in part

1. Calypogeia azurea Stotler & Crotz, Taxon 32: 74. 1983

Plants translucent, usually dark, grayish blue-green to deep grayish to dark green, in older plants sometimes paler green to pale yellowish; when fresh, shoot apices turquoise-blue, when dry often bluish-green. Leafy shoots robust (1.8--)2.5--3.5 mm wide. Leaves varnished-nitid when dry, very broadly ovate: as wide as or more often wider than long, apices entire, rounded, often broadly and bluntly angulate-acute to broadly subacute, occasionally 2-lobed or 2-dentate in juvenile or underdeveloped leaves at the base of the shoot; midleaf cells 30--39 x 35--50(--65) /um, trigones indistinct, apical marginal cells isodiametric or nearly so, not forming a border of tangentially elongate cells. Oil-bodies present in all underleaf, stem and marsupial cells in fresh material, deep blue when fresh, essentially colorless when dry. Underleaves subimbricate, approximate, to subdistant, divided 1/3--3/4 of length to rhizoid initial area, often appearing 3-fid from the division of one lobe, lobes broadly triangular, narrowly rounded to narrowly obtuse, especially on one lobe, sinus acute to (narrowly) rounded, lateral margins entire, often with an obscure angulation or rounded lobe on one or both margins, midline from base of sinus to rhizoid-initial area in a series of 2--4 (--5) cells, rhizoid initial area not prominent [somewhat prominent, brown], transversely oval to nearly round, underleaf somewhat decurrent to a little below the rhizoid initial area, cuticle smooth. Specialized asexual reproduction by uni-or bi-celled gemmae infrequent.

Generally acidic substrates, including loamy or coarse, sandy soils, humus, thin peat on wet stones and rock, seldom on rotted bark, ends of logs, in damp, exposed or shaded upland ravines, stream banks, springs, seep edges, montane drainages; low to high elevations, 100--3000 m; Alta., B.C., N.B., N.W.T., N.S., P.E.I., Que., Yukon; Alaska, Calif., Conn., Idaho, Maine, Mont., Oreg., N.Y., Pa., Vt., Wash., Wyo.; Eurasia; Africa, Atlantic Islands.  

Calypogeia azurea is a subalpine species in moist, cool upland slopes in coniferous forests below timberline. Although scattered throughout the northern hemisphere, it is rare in Europe and in North America. V. A. Bakalin et al.  (2022) have restricted the distribution of the species in the Old World to Europe, excluding it from amphi-Pacific Asia. Most verifiable American reports are confined to the Pacific Northwest, in Alaska among the islands and bays along the eastern Pacific coast (H. Persson 1952). The species occurs in the middle and southern boreal forests of western North America, but is absent in the Far North. It is also reportedly frequent in Alaska (R. M. Schuster 1969). One specimen of C. azurea from eastern North America was accessible and verifiable (Vermont, R. M. Schuster 43801, F). It had the typical morphology of the species, but most importantly, the collector noted and described its blue oil-bodies; other collections verified by R. M. Schuster (1969) and presumably associated with blue oil-bodies display a disjunct occurrence of the species in northeastern North America. Schuster, in 1969, associated an ambiguous South Carolina specimen rather to C. peruviana, than C. azurea, hence excluding C. azurea from the southeastern United States and the potential overlap of the ranges of the two species.

In the eastern United States, R. M. Schuster’s concept of C. trichomanis excluded C. muelleriana, following K. Müller’s 1947 revision of the genus Calypogeia. Hermann Persson also accepted Müller’s definition of the two species when publishing collections of both C. muelleriana with hyaline and C. trichomanis with blue oil-bodies from Alaska and the Yukon (H. Persson 1952). In a footnote to this publication (1952), Persson stated he found a specimen of C. trichomanis from Quebec. Schuster’s distributions based on his own collections (where blue oil bodies were recorded as observed) included Nova Scotia, Quebec; Maine, New York, Vermont (R. M. Schuster 1969), the Maine and Vermont plants representing “typical material.”

The name Calypogeia azurea was established by R. M. Stotler and K Crotz in 1983 to dispose of and replace the name C. trichomanis sensu Müller (e.g. 1947) and modern authors such as R. M. Schuster (1969), since the latter name had contradictory lectotypes and original protologues. Plants named in North America as C. trichomanis usually refer to C. muelleriana and rarely, if ever, represent C. azurea (Stotler and Crandall-Stotler 2017) or, in the American South East, the species C. peruviana, which also has blue oil bodies. However, a brief review of herbarium specimens generally labelled C. trichomanis indicated such specimens should be considered as unidentified, as they represent nearly every species of the genus in North America.

The lateral leaves of C. azurea are distinctly wider than long, the distal (antical) leaf base somewhat auriculate, dilated and curving across the antical side of the stem, giving the overall impression of a heart-shape, with the apices narrowly and smoothly rounded, the underleaves broad, 1.5--2(--2.2) x wider than the stem, the lobes nearly acute, triangular to lanceolate and with rather frequent low marginal angulations, sometimes with a blunt tooth-like angulation above the middle making the underleaf appear trifid, the line of cells from the base of the sinus to the rhizoid initial area of (2--)3--5 cells, and they are not decurrent

The color of C. azurea when dry may be a deep, dark blue-green, while that of C. muelleriana, with its hyaline oil bodies, is pale green to light yellowish to whitish green. Two species, C. neesiana and C. integristipula with hardly bilobed underleaves, may have a flat, opaque grayish coloration when not a pale grayish green.

SELECTED REFERENCES

Bakalin, V. A., K. G. Klimova, and V.  S. Nguyan. 2020 A review of Calypogeia (Marchantiophyta) in the eastern Sino-Himalaya and Meta-Himalaya based mostly on types. PhytoKeys 153: 111--154.

Buczkowska, K., V. Bakalin, A. Baczkiecwicz, B. Aguero, P. Gonera, M. Ślipiko, M. Szczecińska and J. Sawicki. 2018. Does Calypogeia azurea (Calypogeiaceae, Marchantiophyta) occur outside Europe? Molecular and morphological evidence. PLoS One 13(10): e0204561. https://doi.org/10.1371/journal.pone.0204561.

Müller, K. 1947. Studien zur Aufklärung der europäischen Arten der Lebermoosgattung Calypogeia. Sv. Bot. Tidskr. 41: 411--30.

Persson, H. 1952. Critical or otherwise interesting bryophytes from Alaska-Yukon. Bryologist 55: 1--25.

Potemkin, A. D., E. A. Borovichev and E. G. Ginzburg. 2017. Calypogeia azurea (Calypogeiaceae, Marchantiophyta) in the Northwestern European Russia. Novosti Sist Nizsh Rast. 51: 263--273.

Stotler, R. E. and B. Crandall-Stotler. 2017. A synopsis of the liverwort flora of North America north of Mexico. Ann, Missouri Bot. Gard. 102: 574--709.

2. Calypogeia integristipula Stephani, Bull. Herb. Boissier, sér. 2, 8(9): 662. 1908

Calypogeia meylanii H. Buch; C. neesiana var. meylanii (H. Buch) R. M. Schuster

Plants translucent, pale to yellowish or grayish green. Leafy shoots robust, 2.5--3.2 mm wide. Leaves dull, matt when dry, varnished-nitid on margins, narrowly ovate, usually clearly longer than wide, apices entire, gradually narrowly rounded to narrowly obtuse; midleaf cells 33--43 x 36--50(--60) /um, trigones indistinct, apical marginal cells with an occasional, discontinuous border of tangentially elongate cells interrupted by nearly isodiametric ones. Oil-bodies present in all cells in fresh material, essentially colorless fresh or dry; oil-bodies present in all cells of living underleaves. Underleaves (sub)distant to typically imbricate, undivided, truncate or weakly emarginated, unlobed, when (sub)emarginated, the lobes broadly rounded, sinus absent to shallow, lateral margins entire, midline from apex of underleaf to rhizoid-initial area in a long series of 7--10(--14) cells; rhizoid initial area prominent, often brown, large, transversely oval to nearly round, densely rhizoidous, underleaf not decurrent, cuticle smooth. Specialized asexual reproduction by 1—2-celled gemmae frequent.

Inorganic clayey, sandy mineral soils but tolerant of purely organic substrates, wet humus, peat, rotted wood, damp to wet, deeply shaded places on inclined to vertical surfaces on subxeric or damp blocks of hard acid (sandstone) rock and stony ledges, pioneer on shaded sandstone walls, also in acidic wetland: mires, creek banks under willows, rotted stumps in marly basic fens, bogs, sphagnous swamps, Thuja woodlands, hummocks, edges of seeps, tarns and upland lakes, montane forests of Thuja and Pseudotsuga; 0--2540 m; Greenland; Alta., B.C., Nfld. and Labr. (Nfld.), Man., N. B., Nfld., N.S., N.W.T., Que., Ont., Sask., Yukon; Alaska, Calif., Colo., Idaho, Ill., Kans., Maine, Mass., Mich., Minn., Mont., N.Y., Okla., Oreg., Pa., Tenn., Utah, Wash., Wisc., W.Va., Wyo.; Eurasia; Atlantic Islands.

Calypogeia integristipula is a Holarctic species ranging north in North America to the southern boundary of the tundra, occurring throughout the Spruce-Fir zone, south in oceanic and most continental regions throughout the deciduous northern hardwoods and coniferous (Abies-Picea) forest Regions. It tends to occur in north temperate regions, ranging south to West Virginia in the east and ranging south in high elevations (2540 to 3212 m) in California in the west, and absent from mid continent.

Calypogeia integristipula has only been relatively recently (ca. 1948) separated from C. neesiana in the United States, hence earlier North American distribution records of C. neesiana are not reliable (R. M. Schuster 1969). The distributions above are reported relatively recently and conform mostly to Schuster’s concept of the species.

Unlike the other species in the genus with varnished-shining texture, C. integristipula is a nearly opaque, dull, deep grayish or glaucous green, except for a varnished-shining margin, but is not deep blue, as in C. azurea or C. peruviana. Calypogeia integristipula is a widespread species due to its tolerance of a diversity of acidic to (sub)basic and (sub)xeric mineral substrates, whereas C. neesiana is obligately acidic, typically over damp, shaded organic material. Calypogeia integristipula is often found over Sphagnum spp. with C. neesiana or C. sphagnicola. Both may be found on clay.

Other than the widely orbicular, entire underleaves and large size, the most important diagnostic character of the species is the occasional development of an interrupted leaf border of tangentially elongate apical marginal cells interrupted by isodiametric cells. Other distinctive species characters are the narrowly ovate lateral leaves distinctly longer than wide, the apices gradually narrowly rounded and typically entire.  The underleaves of C. integristipula are very broadly (1.5:1) transversely subreniform, ellipsoidal to orbicular, 1.7--2.5 x stem width, generally unlobed or shallowly and broadly emarginate, whereas the underleaves of C. neesiana are often (shortly) 2-fid. The rhizoid initial area in C. integristipula is prominent, large, transversely oval to nearly round, so large that the bordering cells on the margins appear decurrent, whereas in C. neesiana the rhizoid initial area is narrowly, transversely linear. The two species have separate continental distributions, C. integristipula frequent in the north and at high elevations, C. neesiana in the south at low elevations.

The widespread Calypogeia mulleriana which also has large lateral leaves (to 3 mm), has no distinctly elongate cells on its apical margin, the lateral leaves are usually wider than long, the underleaves are remote, notched and 2-fid by about 1/3 to 1/2 of the underleaf, the line of undivided cells short, only (3--)4--6(--9) cells with a narrow, strongly transversely elongate rhizoid initial area and  distinct decurrencies. The distribution of C. muelleriana is widespread throughout areas south of the reported range of C. integristipula.

3. Calypogeia muelleriana (Schiffner) Müller Frib., Beih.Bot. Centralbl. 10: 217. 1901

Kantius muellerianus Schiffner, Sitzungsber. Deutsch. Naturwiss.-Med. Vereins Böhmen "Lotos" Prag 48: 342. 1900, as Kantia muelleriana

Plants translucent, pale green to white- or yellowish green; growing occasionally abundantly in large mats. Leafy shoots robust, (2--)2.5--3.5(--4) mm wide. Leaves varnished-nitid when dry, broadly ovate, as wide as or wider than long (longer than wide in subsp. blomquistii), apices entire, broadly obtuse to narrowly rounded at apex to subacute; some shallowly emarginate apices atypical, rare on mature plants; midleaf cells large (45 –)55--70 x 40--50 /um, trigones indistinct, apical marginal cells mostly isodiametric or nearly so, not forming a border of tangentially elongate cells. Oil-bodies present in all cells in fresh material, essentially colorless fresh or dry. Underleaves mostly distant, sometimes approximate (rarely subimbricate), cleft to 1/3--1/2 their length to rhizoid initial area, lobes obtuse to broadly rounded-triangular, never appearing 3-fid, sinus acute, obtuse or rounded, lateral margins typically entire, occasionally with an obscure angulation on one margin, midline from base of sinus to rhizoid-initial area in a series of (3-) 4--6 (--7) cells, rhizoid initial area sometimes brown,  strongly transversely elongate-elliptical, sometimes nearly round; underleaves strongly decurrent, cuticle smooth. Specialized asexual reproduction by 1--2-celled gemmae, these often abundant.

Soil, rock, peat, rarely decaying wood; low to high elevations, 0--3200 m; Greenland, Canada, United States, Mexico, West Indies, Eurasia, Africa, Atlantic Islands.

Calypogeia muelleriana is a widespread and often abundant Holarctic boreal species occurring in subalpine areas between the Coniferous Forest north to the southern boundary of the Tundra and throughout the northern Deciduous Forest regions southward into non-tropical eastern North America and the western slopes of the Sierra Nevada south in California. The species appears to be less common or absent mid-continent in some representations. R. M. Schuster (1969) rejected Midwestern state reports that he did not personally see in herbaria, after extensive field work in that region.

This polymorphic species was first reported from North America in 1949 (R. M. Schuster 1949), mostly from European nomenclature applied to American material, confusion with C. neesiana, and the resolution of the now rejected name C. trichomanis, under which representative specimens with hyaline oil-bodies were previously placed (R. M. Stotler and K. Crotz 1983). The species is apparently the most widespread in the genus in the floral area, but given the difficulty in distinguishing this species from other common species, such as C. neogaea or C. integristipula, there is some uncertainty in the distribution both locally and in its total range. The rejected name C. trichomanis has often been applied to collections of C. muelleriana, but also to every other species in the genus, indicating an uncertainty of application of names among North American students.

R. E. Stotler and B. Crandell-Stotler (2017) have suggested that records of Calypogeia trichomanis in the North American literature be assigned to C. muelleriana, with the exception of material referable to C. azurea of the Pacific Northwest, or C. peruviana in the southeastern United States, both species with blue oil bodies in living material. Calypogeia muelleriana is universally reported as being translucent, nitid and a pale yellowish to whitish green color, with colorless oil-bodies. Equally robust plants with a bluish color may be C. azurea, or C. peruviana, and if a matt, slate-gray color, then C. integristipula.

Throughout its wide range and diverse ecological conditions, greater than other species in the genus, Calypogeia muelleriana often displays phenotypes that are impossible to identify or distinguish from the variability of other species, such as when plants are atypically narrow with reduced laminal cell size, with underleaves minute, angulate, the sinus cleft to 2 or 3 cells of rhizoid initial area, or very shallowly bilobed (emarginate) in large-leaved specimens. It is especially confused with C. integristipula, C. neogaea, and, in sphagnous situations C. sphagnicola fo. paludosa (Warnstorf) R. M. Schuster.

Typical C. muelleriana has margins of both lateral and underleaves edentate. This species, together with C. integristipula, and C. azurea, is large for the genus in shoot width (2.5--3.5(--4) mm wide); the lateral leaves are as wide as, or wider than long, a feature only characteristic of C. azurea which has lateral leaves even wider, and C. suecica, whose shoots are typically only to 1.8 mm wide. The apex of the lateral leaves has mostly isodiametric cells, are rounded-ovate and rarely and atypically subdentulate, not pointed, as in C. neogaea, but frequently with a small eminence of one to several cells. The lateral-leaf midcells are large, 40--50 x (45--)55--70 /um, like those of C. neogaea; the midcell size of C. azurea are somewhat smaller. The typically distinctly decurrent underleaves are more or less distant, rarely (sub)imbricate, the lobes typically broadly rounded-obtuse and lacking teeth or angulations on the lateral margins or these large and rounded. The rhizoid-initial area is strongly transverse, narrowly ellipsoidal to oval-oblong; those of C. integristipula are large, transversely oval to nearly round, as are those of C. azurea.

R. M. Schuster (1969) suspected that at least some of the prolific variability of this species was due to “much minor genetic diversity.” K. Buczkowska (2010) found that among 52 samples from Poland that resembled Calypogeia muelleriana, 21 belonged to a new taxon, as identified with isozyme markers. Based on chloroplast DNA sequences, this new taxon more closely resembles C. azurea than it does C. muelleriana, and this unnamed new species has also been identified in the U.S.A. (K. Buczkowska et al. 2013)

Mylia anomala (Hook.) Gray, often in sphagnous situations, resembles this species, having imbricate suborbicular leaves, but these are succubous with large to very large trigones in the leaf cells and the underleaves are subulate or very small and difficult to detect.

SELECTED REFERENCES

Buczkowska, K. 2010. Morphological differentiation of Calypogeia muelleriana (Jungermanniales, Hepaticae) in Poland. Biodiv. Res.Conserv. 17: 23–32. https:// doi.org/10.2478/v10119--010--0004--4

Schuster, R. M. 1949. The ecology and distribution of hepaticae in central and western New York. Amer. Midl. Naturalist, 42: 513--712.

Stotler, R. E. and D. K. Crotz. 1983. On Mnium trichomanis Linnaeus (Hepatophyta). Taxon 32: 64--75.

Stotler, R. E. and B. Crandall-Stotler. 2017. A synopsis of the liverwort flora of North America north of Mexico. Ann, Missouri Bot. Gard. 102: 574--709.

1.     Lateral leaves broadly ovate, wider than long, broadly and obtusely to narrowly rounded, sometimes shallowly emarginate; marginal cells smooth (the marginal cells with straight walls); median leaf cells comparatively short, 50 x 55--70 /um; underleaves usually transverse, distinctly wider than long, 2.5--2.7 x stem width, subrotundate to transversely oval, with short, broad, often obtuse-rounded lobes separated by a broadly U-shaped or broadly V-shaped sinus; divided to 1/3 length, leaf and underleaf margins not, or rarely obscurely crenulate, smooth, straight

…3a. Calypogeia subsp muelleriana

2.     Lateral leaves narrowly triangular-ovate, longer than wide, apices narrowly rounded and either bluntly acute or subapiculate and pointed; (some) marginal cells smooth, sometimes crenulate or crenulate-sinuate (concave on the edge); median leaf cells strongly elongated on mature leaves, 32--40(--42) /um wide x 72--85(--100) /um long, often twice as long as wide or more; underleaves longer than wide, 1.6 x stem width or less, orbicular to elongated to strongly elongated and ovate-lanceolate, some with lobes acute, parallel to connivent at their tips, separated by a narrow V-shaped sinus or, when divergent, the sinus wider; divided longer, to ½ their length; underleaf margins normally strongly crenulate-sinuate, (the marginal cells each concave medially along their outer edges)

    3b.  Calypogeia muelleriana subsp. blomquistii

3a. Calypogeia muelleriana subsp. muelleriana

Leaves of mature shoots usually nearly or quite as wide as long; apices bluntly to narrowly rounded, sometimes broadly 2-lobed, the marginal cells typically straight or bulging slightly outward; median leaf cells 50 x 55--70 /um, not twice as long as wide; underleaves usually to 2.7 x the width of the stem, distinctly wider than long, orbicular to transversely oval, the lobes short, broad, often obtuse with the sinus broadly U- or V-shaped, divided to 1/3 the length, on average 4--6 cells from sinus base to rhizoid initial area, leaf and underleaf margins not, or rarely obscurely crenulate, smooth, straight, typically lacking angulations on the margins or with one blunt angulation on one side in some leaves.

Weakly tolerant of deep shade or constant moisture, often over shaded (sandstone/metamorphic) rocks, inorganic and acid substrates such as loamy, clayey or silty, sometimes sandy mineral soils, wet (old logging) roadsides and associated ditches, moist soil (seep and stream) banks, (sandstone) rock surfaces in gorges, steep slopes, ravines, decaying logs and other wood, tightly adherent to needles and small woody debris in western coniferous woodlands, sometimes peat in swamps and (cranberry) bogs although rarely over and among Sphagnum, willow and birch thickets, in hardwood forests, ledges and slopes below snow fields; low to high elevations, 0—3200 m; Greenland; Alta., B.C., N.B., Nfld. and Labrador, N.S., Ont., Que., Sask., Yukon; Alaska, Calif., Colo., D.C., Fla., Ga., Kans., Idaho, Ill., Ind., Iowa, Ky., Maine, Md., Mass., Mich., Minn., Miss., Mo., Mont., N.J., N.Y., N.C., Ohio, Okla., Oreg., Pa.. S.C., Tenn., Vt., Va., W.Va., Wash., Wisc., Wyo.; Mexico; West Indies; Eurasia; Africa; Atlantic Islands.

The underleaves of the subsp. muelleriana are variously bilobed: when shallowly so they resemble those of C. integristipula, especially on the west coast of the United States, where they can be shallowly emarginate. The underleaves are transversely elliptic to oval, occasionally subrotundate, the lateral leaves broader at the base. The lateral leaf cells often rather thick-walled and collenchymatous. In C. integristipula the underleaves are emarginate to entire, round, almost circular, and the lateral leave longer than broad.

SELECTED REFERENCE

Doyle, W. T. and R. E. Stotler. 2006. Contributions toward a bryoflora of California III. Keys and annotated species catalogue for liverworts and hornworts. Madroño, Calif. Bot. Soc. 53: 89--197.

3b. Calypogeia muelleriana (Schiffner) Müller Frib. subsp. blomquistii R. M. Schuster, Hepat. Anthocerotae N. Amer. 2: 187. 1969  E

Leaves of mature shoots narrowly triangular-ovate, longer than wide, apices narrowly rounded and either bluntly acute or subapiculate and pointed; underleaves polymorphic on the same stem, some with lobes elongate and acute, drawn out, becoming strongly elongated; median leaf cells strongly elongated on mature leaves, 32--40(--42) /um wide x 72--85(--100) /um long, often twice as long as wide or more; lateral leaves and underleaves mostly distinctly much longer than wide, the lobes greatly elongate and narrow, narrowly-rounded, the margins, as in the lateral leaves, strongly crenulate-sinuate (the marginal cells each concave medially along their outer edges), with (3--)4--5 cells between sinus and rhizoid initial area; laterally lacking angulations.

Deeply shaded sandy, mineral, thin, flat pale green mats beneath overhangs, faces of shaded moist acid (sandstone/metamorphic) rock wall, sides of steep gorges and coves, beside creeks and cascades; 250--1000 m elevation; B.C., Yukon; Ark., Ga., Ill., Mass., Mo, N.C., S.C., Tenn., Wash.

Some specimens of the subsp. blomquistii  may be similar to Calypogeia azurea, especially in the underleaves, where C. azurea has erect, narrow to triangular lobes and lateral leaves wider than long (also a trait of the typical subspecies). The subsp. blomquistii may be distinguished from C. azurea which has blue oil-bodies when fresh, the lateral leaves wider than long, the smaller leaf cells not at all elongate in the leaf middle, the marginal cells of leaves and underleaves straight, not crenulate, the underleaves lacking decurrencies and the rounded-oval rhizoid initial area.

Subsp. blomquistii may be separated from Calypogeia neogaea, which has lateral leaves similarly pointed at the apex and deeply 2-fid underleaves, by the median cells of the lateral leaves less elongate, not twice as long as wide, by marginal cells of both lateral and underleaves straight, not crenulate, by the strongly transverse underleaves (not elongate), only 1-2 cells above the rhizoid initial area, and the margins with distinct angulations. 

The lateral leaves of subsp. blomquistii are often irregularly rounded, shallowly emarginate to broadly and bluntly apiculate, some lateral leaf marginal cells are also crenulate (depressed in the middle of the cell). In the typical subspecies, the underleaves are more transverse, 2.2--2.5(--2.75 x stem width, whereas those of subsp. blomquistii are more orbicular (as long as wide) and only around 1.6 x the stem width. 

On the west coast there occur specimens intermediate between the subspecies, with larger stems more typically subsp. muelleriana (broad, heart-shaped leaves, transversely large subrotundate underleaves), and smaller ones approaching subsp. blomquistii in character (narrowly ovate leaves, polymorphic underleaves suborbicular, only to 1.6 x stem width, slightly longer than wide with lobes acute (triangular), subparallel, subconvergent).

4. Calypogeia neesiana (C. Massalongo & Carestia) Müller Frib., in Loeske, Verh. Bot. Vereins Prov. Brandenburg 47: 320. 1905 [1906]

Kantius trichomanis (Linnaeus) Lindberg var. neesianus C. Massalongo & Carestia, Nuovo Giorn. Bot. Ital. 12: 351. 1880, as Kantia neesiana

Plants translucent, pale yellowish, whitish or grayish green, glaucous gray-green when dry. Leafy shoots small, 1--2(--2.5) mm wide. Leaves dull, matt, somewhat narrower than long to slightly wider than long, rarely broadly ovate-ellipsoidal, apices entire, narrowly truncate, frequently shallowly emarginate, less often rounded, never sharply 2-dentulate; midleaf cells 33--40 x 36--45(--55) /um, trigones indistinct, apical marginal cells with a distinct usually continuous border of tangentially elongate, slightly larger cells, adjacent non marginal cells essentially isodiametric. Oil-bodies absent in midleaf cells in fresh material, essentially colorless fresh or dry; oil-bodies all or nearly all absent in living underleaves. Underleaves approximate to more typically imbricate, undivided or weakly emarginated, unlobed, when emarginate the lobes broadly rounded, sinus absent to slightly emarginated to obscurely or shortly 2-fid, lateral margins entire, midline from apex of underleaf to rhizoid-initial area in a long series of 7--10(--14) cells, rhizoid initial area not prominent, not colored, transversely linear, underleaf base not decurrent, cuticle smooth. Specialized asexual reproduction by 1--2-celled gemmae frequent.

Acid, organic substrates, damp, shaded places, black humus, deeply rotted wood and plant litter, acid ledges, vertically cut and eroded peat, humus-covered vertically cut ditch sides and steep creek banks, often found with C. sphagnicola over Sphagnum marshes and Chamaecyparis swamps, wet cranberry bog holes, under Tsuga and mixed hardwoods on montane slopes near waterfalls, water between hummocks in seasonal sedge tundra bogs; low to high elevations, 100--1860 m elevation; Greenland; Alta., B.C., N.B., Nfld. and Labr. (Nfld.), N.W.T., N.S., Ont., Que., Yukon; Alaska, Calif., Colo., Conn., Fla., Ga., Idaho, Ind., Maine, Mass., Md., Mich., Minn., N.H., N. Mex., N.Y., N.C., Ohio, Oreg., S.C., Tenn., Vt., Va., Wash., W.Va., Wisc., Wyo.; w Europe, e Asia, Atlantic Islands (Azores).

The distributional reports for Calypogeia neesiana given above are relatively recent and reflect the removal (by ca. 1948) of C. integristipula from the species concept of C. neesiana, essentially the concept of R. M. Schuster (1969). Although C. integristipula occurs in a continuous east-west boreal continental band, C. neesiana appears to be absent in the mid-continental parts of North America, reflecting a gap between its longitudinal distribution in the west and east. Calypogeia integristipula is more common in the northern United States, but C. neesiana is sporadic in the north and is more frequent in the east, from the east coast of Hudson Bay to Quebec down to the Southern Appalachian highlands. In the south, C. neesiana grows in non-coniferous sites in the northern hardwoods, oak-hickory, and mixed mesophytic forests. The substrates are not as diverse as those of C. integristipula, hence this calciphobic species is more limited in its distribution, focused more on acid conditions and organic substrates than the mineral and (sub)basic soils and rocks typical of C. integristipula. Both may be found on clay.

Calypogeia neesiana may be a nearly opaque, dull, deep grayish or glaucous green, but not a saturated or deep blue, as in C. azurea or C. peruviana. The coloration is the same for C. integristipula, but that species also has varnished-shining marginal cells. Calypogeia neesiana is distinguished from all other species in the genus firstly, especially on smaller, or poorly developed plants, by the more distinct leaf border of tangentially elongate apical marginal cells, more continuous, especially in smaller plants, than in C. integristipula where such a border is discontinuous. The rhizoid initial area shape of C. neesiana is indistinct, often forming only a transversely linear line 2--3 cells high, often visible due to paucity of rhizoids, not the large, prominent, often brown, densely rhizoidous oval or nearly round rhizoid initial area in C. integristipula.

Often found in similar habitats, Calypogeia neesiana is a small plant with the shoot width similar to that of C. sphagnicola and C. suecica, both of which have thick-walled, isodiametric lateral leaf cells with trigones. The leaves and underleaves of C. neesiana can be likewise close to contiguous but the typically shallowly notched underleaf apex and smooth lateral margins of C. neesiana should separate it from them, as will the elongate apical-marginal lateral leaf cells. 

Depauperate specimens may resemble Calypogeia neogaea  in their bidentate leaf apices, the distant underleaves bilobed to a third of their length with only 4--5 cells in a line from the rhizoid initial area, and with somewhat angular lateral margins. These plants will be much smaller than  C. neogaea, slightly over 1 mm wide, with smaller leaf cells starting at 24 x 30 /um and with distinctive tangentially elongate marginal cells near the lateral leaf apex. These plants are often taken from rotted wood on the west coast.

5. Calypogeia neogaea (R. M. Schuster) Bakalin, Conserv. Biodivers. Kamchatka Coastal Waters, Proc. VII Int. Sci. Conf., Nov. 28–29, 2006: 9. 2007

Calypogeia fissa (Linnaeus) Raddi subsp. neogaea R. M. Schuster, Hepat. Anthocerotae N. Amer. 2: 169. 1969; C. shevockii Bakalin & Troizky

Plants translucent, pale whitish or grayish green. Leafy shoots (1.9--)2.2--2.9(--3) mm wide. Leaves varnished-nitid when dry, usually narrowly ovate, mostly longer than wide, apices normally rounded acute and sharply to bluntly apiculate, occasionally and atypically shortly bidenticulate on some leaves on isolated mature shoots; midleaf cells large, 35--48 x 45--60(--68) /um, trigones indistinct, apical marginal cells isodiametric or nearly so, not forming a border of tangentially elongate cells. Oil-bodies present in all cells in fresh material, essentially colorless fresh or dry. Underleaves consistently and uniformly quite distant, deeply divided 4/5--5/6 their length to rhizoid initial area, lobes usually strongly divergent, acute or subacute, more rarely obtuse, narrowly rounded, sometimes asymmetrically bidenticulate, sinus broadly rounded-rectangular to crescentic, occasionally V-shaped with a narrow sinus, lateral margins angular or mostly with 1--2 blunt to subacute angulations on one or both margins, sometimes smooth, sometimes with a sharp tooth above the middle, midline from base of sinus to rhizoid-initial area in a very short series of 1--2 cells, rhizoid initial area not prominent, not colored, narrowly elliptic or linear, not,  indistinctly, sometimes decurrent; cuticle smooth. Specialized asexual reproduction by 1--2-celled gemmae frequent.

Moist shaded mostly inorganic substrates, dry or moist sandy, clayey or silty alluvial mineral soil or as a pioneer on vertical sandstone/igneous rocks, hillsides, often in xeric sites in prairies, damp or moist loamy roadside ditches, stream banks, paths, gullies, ravines, alluvial soil of intermittent springs; seeps in Oak-Hickory hardwood and mixed mesophytic forests, and in the bark litter and duff, rarely rotten wood of conifers: Sequoia sempervirens, Pseudotsuga menziesii Notholithocarpus densiflorus forest  in the west; low to high elevations, 0--2895 m elevation; BC, N.W.T. Que.; Ala., Ark., Calif., Colo., Fla., Ga. Idaho, Ill., Ind., Ky., La., Maine, Mass., Md.; Mich., Miss., Mo., N.J., N.Y., N.C., Ohio, Oreg., Ohio; S.C.; Tex.., Vt. , Va.; Wash., W.Va. ; Wyo.; e Asia (Sakalin).

Calypogeia neogaea is largely North American in distribution. It was reported as sporadic and confined to the southern states, but common on the Coastal Plain and Piedmont (R. M. Schuster 1969).  W. S. Hong (1990) published reports for California, Oregon and Washington, W. T. Doyle and R. E. Stotler (2006) for California and Bakalin (2012) for California and Oregon.  N. A. Konstantinova et al. (2009) reported it from three locations in the Russian Far East.  Bakalin et al. (2022), however, stated that C. neogaea was probably endemic to North America, although molecular data was inconclusive, and in eastern Asia it is replaced by another taxon: C. kamchatica Bakalin, Troizk. & Maltseva.

R. M. Schuster (1969) effectively repudiated the occurrence of European Calypogeia fissa (Linnaeus) Raddi from North America. Both C. fissa and C. neogaea (both as subspecies) were considered to be Atlantic-oceanic in distribution, with both C. fissa and C. neogaea confined in North America to the Southeast and Central Atlantic states, occurring only sporadically northward into the New England states. All reports of C. fissa interior to these regions were to be considered “extremely” dubious. No report of C. neogaea outside of the regions specified, nor of C. fissa, were accepted by Schuster, and none from the west coast of North America, although Schuster did not appear to have examined specimens outside of the range he specified.

The morphological differences between Calypogeia fissa and C. neogaea in North America are solely based on the frequency of bidentate lateral leaf apices: typical in C. fissa throughout its European range, but “usually acute, only rarely slightly bidentulate” in C. neogaea (R. M. Schuster 1969), although the morphology of the lateral leaf apex in European C. fissa is extremely variable, as it is in C. neogaea. Technical characters requiring mature capsules involve the relative length to width measures of the capsule valves, and the presence or absence of nodular thickenings in the epidermal capsule cells. The spores are larger in C. fissa in Europe and the spores are smaller in C. neogaea of North America (R. M. Schuster 1969), and both characters require mature capsules, which are rare.

In Europe, J. A. Paton (1999) did not include North America in her global distribution of C. fissa. She found that in C. fissa in the British Isles that “no correlation between lateral leaves that are entire and underleaves with lateral lobes above the middle, which together characterize the N. American C. fissa subsp. neogaea R. M. Schuster.” K. Damsholt (2002) decided that C. fissa was “probably” replaced by C. fissa subsp. neogaea in North America after R. M. Schuster (1969).  V. A. Bakalin et al. 2022 determined that the two species as recognized here were distinct at the molecular level, leaving only the morphological details as crucial to separation in North America (and elsewhere). However, in the same study, the authors state that “Calypogeia fissa possesses an ecology similar to C. tosana and is restricted to Europe, while (the data are somewhat incomplete and may be questionable) C. neogaea is restricted to North America.”

R. E. Stotler and B. Crandall-Stotler (2017) also expressed uncertainty about North American reports of C. fissa and  C. neogaea, suggesting that C. fissa reports are “likely” C. neogaea. W. S. Hong (1990), reported that in the western United States and adjacent Canada, most specimens approached “subsp. fissa.” Its occurrence in B.C., N.W.T. were new. His records of subsp. neogaea, reported from Calif., Oreg. and Wash. were new as well. W. T. Doyle.and R. E. Stotler (2006) could not confirm C. fissa for California, following a concept requiring all or most lateral leaves to have distinctly or strongly bidentate apices, and specimens with only few such leaves were confirmed as C. neogaea for California. The present treatment corroborates this assessment.

Specimens may have some lateral leaf apices minutely bidentate, but never have most or all lateral leaves strongly bidentate, as in the excluded species Calypogeia fissa. Most early specimens named as C. fissa are C. neogaea. American plants with some bidentate leaves represent juvenile, or impoverished plants. The apices of the leaves of C. neogaea may be rounded and entire, rounded-acute and smooth on the same stem, and with a mostly single apiculation of one cell or often a bluntly acute hump of several cells. When some of the apices are bidentate, especially in leaves distal on the stem, the teeth are narrowly separated, not broadly so as in C. peruviana. This distinction may help differentiate early published reports of C. fissa from the southern U.S.A., esp. Florida, which may be C. peruviana instead. The underleaves are distant, sometimes minute, strongly transverse (wider than long), angled, sometimes strongly so, on the lateral margins and deeply bilobed to (1--)2--3 cells of rhizoid initial area.

The lateral leaves of C. neogaea are longer than broad (narrowly ovate) with a subacute to acute, sometimes bidentate apex, which separates the species from C. muelleriana and C. azurea, which have typically subcordate leaves, wider than long, with a more bluntly if narrowly rounded apex. The underleaves are distinct from all congeners in the underleaf lobes widely and the deepest lobed (midline from base of sinus to rhizoid-initial area in a very short series of 1--2 (--3) cells); they have rounded-acute, divergent lobes with lateral teeth or angulations high on the lateral margins. Examination of the youngest stems may best reveal the characters of C. neogaea.

Stem lateral leaves of C. neogaea from the section of a stem that is widest and most mature are recommended for identification of this species. To restrict one’s analysis to only this part of the stem is to ignore the earliest leaves at the stem base, and the youngest at the apex, where the demonstration of bidentition may be clearest, as well as the most representative underleaves with lateral margin angulations, especially above the middle. Note also should be made of these expressions on the reduced leaves on young branches and microphyllous leaves on gemmiparous stem extensions. Often the lateral leaves in these areas on the stem have long-decurrent leaf bases and leaf apices that are falcate-decurved. Variation in the lateral leaf apex includes nearly always some form of sharp or blunt apiculation, never as smooth as has C. muelleriana. There are often asymmetrical bidentate apices, with angulations

In C. muelleriana, with which C. neogaea is vexingly confused, the underleaves are only divided 1/3--1/2 their length, with a longer series of (3--)4--6(--7) cells, with their lobes and sinus obtuse-rounded. The underleaves of C. muelleriana are 2.2--2.5(--3) x wider than the stem, showing their mostly entire margins clearly, with strong decurrencies, whereas those of C. neogaea are usually smaller, narrower, usually only 1--1.8 x wider than the stem or sometimes to 2.5 x in robust specimens, but clearly displaying distinctive acute lobes and lateral marginal angulations with decurrencies none or slight. Underleaves of C. muelleriana are suborbicular, but in C. neogaea they are narrow and strongly transverse (wider than long), sometimes reduced to a mere, highly ornate fingernail-shaving.

A recently published new species of Calypogeia, C. shevockii Bakalin & Troizky, is here synonymized with C. neogaea. Study of the holotype (CAS) revealed more variation for the plant than that illustrated by the authors (V. A. Bakalin et al. 2022). It was found that overall, the range of variation of the holotype matched variation in C. neogaea in specimens examined over the range of that species in North America. The holotype displayed an unusual but not atypical degree of gemmiparous modifications of the stem apex as well as gemmiparous side-branches. The description of the species seemed to match the leaves from these modifications rather than those of the unmodified stem leaves, whose characters are usually selected in determination of species in the family. Characters displayed in the type can be compared with the detailed descriptions of variation in C. neogaea by R. M. Schuster (1969). The method of morphological comparison in descriptions of C. fissa from Europe and C. neogaea from Missouri in the paper involves too small a sample (single collections) to be representative of those two highly polymorphic species.

SELECTED REFERENCES

Damsholt, K. 2002. Illustrated Flora of Nordic Liverworts and Hornworts.

 Nordic Bryological Society. Lund University.

Damsholt, K. 2013. The Liverworts of Greenland. Nordic Bryological Society, Lund, Sweden.

Konstantinova, N. A., V. A. Bakalin, E. N. Andrejeva, A. G. Bezgodov, E. A. Borovichev,M. V. Dulin & Yu. S. Mamontov. 2009 [2010]. Checklist of liverworts (Marchantiophyta) of Russia. Arctoa 18: 1--64. [In English and Russian.]

Paton, J. A. 1999. The Liverwort Flora of the British Isles.  Harley Books, Totnes, Devon, U.K.

6. Calypogeia peruviana Nees & J. P. Montagne in Montagne, Ann. Sci. Nat., Bot., sér. l2, 9: 47. 1838

Plants translucent, usually dark blue-green, sometimes yellowish or light green to blue green, fresh shoot apices turquoise-blue, deep grayish green with a slightly bluish tinge when dry. Leafy shoots 2--2.5(--3.6) mm wide. Leaves varnished-nitid when dry, narrowly to more broadly ovate, often distinctly longer than wide, apices narrowed, usually slightly but sharply 2-dentate, the teeth short, ending in a uniseriate 1--2-celled tip, the teeth rather widely separated, apex occasionally entire; midleaf cells rather large, (26--)30--40(--45) x 50--65 /um, trigones indistinct, apical marginal cells isodiametric or nearly so, not forming a border of tangentially elongate cells. Oil-bodies present in all underleaf, stem and marsupial cells in fresh material, deep blue when fresh, essentially colorless when dry. Underleaves distant, divided 2/3--4/5x  their length to rhizoid initial area, lobes narrowly triangular, widely divergent, sinus broad, rounded to obtuse, lateral margins uniformly subangular or with 1--2 subacute to triangular angulations on one or both margins, sometimes with 1(--2) short, sharp teeth at or above the middle, midline from base of sinus to rhizoid-initial area in a series of 2--3 cells, rhizoid initial area not prominent, brown, broadly and narrowly ellipsoidal, underleaf variably slightly to distinctly decurrent, cuticle smooth. Specialized asexual reproduction by 1--2-celled gemmae frequent.

Deep shade of evergreen shrubs near running or standing water, damp sandstone rocks, wet humus, decaying logs, tree bases, moist, bare soil on creek banks, small streams in deep, shaded springy coves, soil-covered ledges in deep gorges with waterfalls, deep swamps and sporadically in hammock forests; low to moderate elevations, 0--762 m; Ala., Del., Fla., Ga., Ky., Md., Miss., N.C., S.C., Tenn., Va.; Mexico; West Indies; Central America; South America.

Calypogeia peruviana is a neotropical species wide-ranging mostly south of the floral area throughout South America, reaching the northernmost extent of its range in the southeastern United States in the eastern and southern edges of the Blue Ridge Mts., in the Escarpment area, and in lower elevations on the Gulf and Atlantic Coastal Plain. It is the only essentially South American species of the genus in North America.

As late as 1953, this species was unreported for North America (R. M. Schuster 1953). Some early herbarium specimens and collections with blue oil bodies identified but with the now rejected name Calypogeia trichomanis (Linnaeus) Corda from the southeastern states are most likely C. peruviana. This species is distinctive in the widely bidentulate lateral leaf apices, the teeth separated by a broad, crescentic sinus. The lateral leaves are narrowly ovate, longer than wide. The remote, decurrent underleaves have a broadly crescentic, rounded and obtuse sinus between triangular, widely divergent lobes. The lateral margins are generally sharply angulate, often with a large projection or tooth on the lateral margins. The underleaves of C. peruviana are only occasionally bis-2-fid (twice 2-fid: with a bilobed division on either side of a deeper middle sinus). In the typically bis-2-fid-underleaved representatives of this species from South America, all of the underleaves are bis-2-fid (M. H. Fulford 1968; illustrated by R. M. Schuster 1969). The undivided portion of the underleaf is short, of 2--3 cells.

Statements by R. M. Schuster (1969) that C. azurea co-occurs with C. peruviana actually refer to relatively large specimens of C. peruviana (mod. latifolia) from South Carolina with lateral leaves wider than long and under-leaves non- angulate with triangular lobes. These have, however, the typical, uniformly (not irregularly) symmetrically bidentulate apices with a broad, lunate sinus separating the teeth. The ranges of C. azurea and C. peruviana do not overlap. Calypogeia azurea occurs in northeastern North America, not south of New York State, while C. peruviana may be found in the southeastern United States from the Carolinas and east Tennessee to Florida and west to the state of Mississippi.

The other species often identified as C. trichomanis is C. muelleriana, a large, pale yellow-green plant, which has lateral leaves as wide as or wider than long, with blunt, entire, smooth apices. The underleaves have rounded-obtuse lobes with entire, non-angulate margins, the undivided portion longer (to 6 cells long).

Major differences between Calypogeia neogaea and C. peruviana, other than color, are noted in the key. Both species may be bidentuate at the lateral leaf apex. Calypogeia neogaea, whose teeth are approximate, but not regularly so. Calypogeia peruviana regularly has apical teeth that are widely spreading. Both species have underleaves transverse to the stem with widely divergent apical lobes. Those of C. peruviana seem generally larger (to 2.5 x the stem width) with a somewhat longer undivided area (2--3 cells) while those of C. neogaea are often to 1.8 x the stem, the undivided area shorter (0--)1--2(--3) cells. In Calipogeia neogaea the underleaves are strongly transverse (2:1), whereas in C. peruviana they are less so or not transverse (1:1). The ecology differs, with C. neogaea more often on subxeric inorganic substrates with sand or clay soil of roadside banks and ditches in oak-hickory forests, whereas C. peruviana grows on more organic substrates, such as tree bases/roots in evergreen forests and shaded swamps with perpetual running or standing moisture.

The size of the oil bodies of C. azurea and C. peruviana, as opposed to the size and number of their constituent segments (spherules or globules, helps to differentiate the two species in fresh material. In general appearance, the oil bodies of C. azurea look botryoidal (like grape bunches) whereas those of C. peruviana are more like raspberries: each individual segment spherical, protuberant and distinct---hence not granulose.  The oil bodies of C. azurea in aggregate are smaller (5--6 /um to 9--10 /um in various cells), whereas in C. peruviana they are larger (6 x 10--15 /um or 8 x 14--19 /um). The number of rounded oil body segments is less in C. azurea (2--4, and 5--8(9--10) segments. The number of segments is greater in C. peruviana (24-)35--50(--56) segments. The size of the segments themselves in C. azurea is 2--3 /um, whereas in C. peruviana they are minute (1--1.5 /um) in size. Some published illustrations of botryoidal oil bodies ascribed to C. peruviana are incorrect.

SELECTED REFERENCES

Fulford, M. H. 1968. Manual of the Leafy Hepaticae of Latin America. Part III. Memoirs of The New York Botanical Garden Vol. 11(3).

Schuster, R. M. 1953. Boreal Hepaticae: A Manual of the Liverworts of Minnesota and Adjacent Regions. Amer. Midl. Naturalist 49: 257--684.

7. Calypogeia sphagnicola (Arnell & J. Persson) Warnstorf & Loeske, Verh. Bot. Vereins Prov. Brandenburg 47: 320. 1905 [1906]

Kantius sphagnicola Arnell & J. Persson, Rev. Bryol. 29: 26. 1902; Calypogeia tenuis (Austin) A. Evans; C. trichomanis var. tenuis Austin; Kantius trichomanis var. tenuis (Austin) Underwood

Plants translucent, pale yellowish, whitish or brownish green. Leafy shoots small, (0.5--)1--1.8(--2.4) mm wide. Leaves varnished-nitid when dry, obliquely ovate to ovate-triangular, as wide as long or somewhat longer than wide, apices entire, more or less acute, sometimes  retuse, apiculate, sometimes falcate, sometimes somewhat bidenticulate; midleaf cells 25--35 x 26--38(--42) /um, somewhat collenchymatous, apical marginal cells isodiametric or nearly so, not forming a border of tangentially elongate cells. Oil-bodies present in all cells in fresh material, essentially colorless fresh or dry. Underleaves distant, rarely subimbricate, divided 3/5--3/4 x their length to the rhizoid-initial area, lobes acute, subacute, narrowly- to ovate-triangular, sinus acute to subacute, lateral margins typically somewhat angular with a small tooth or angulation on one side, rarely on both sides, midline from base of sinus to rhizoid-initial area in a series of 2--5 cells, rhizoid initial area not prominent, not colored, narrowly elliptic-semiannular, underleaf not or slightly decurrent; cuticle smooth. Specialized asexual reproduction by 1--2-celled gemmae common.

Strictly acid sites, hummock-forming Sphagnum, submerged in bog pools, moist peaty cliff crests and ledges above tree-line, usually in open raised valley or blanket bogs, tolerating periodically xeric conditions, creeping over and in flat patches appressed to the surface of dead or living; low to high elevations, 0--3100 m; Greenland; Alta., B.C., Nfld. and Labrador (Nfld.), N.W.T., N.S. , Ont. , Que., Yukon; Alaska, Calif., Conn., Idaho, Maine, Mass., Mich., Minn., N.H., N.J., N.Y. , N.C., Oreg., R.I., Vt., Va., Wash., W.Va., Wisc., Wyo.; South America (Tierra del Fuego); Eurasia; Atlantic Islands; Pacific Islands (New Zealand); Australia (Tasmania).

Over sphagnum mats, spruce or spruce-tamarack and cranberry bogs, rarely creek side soil banks, moist rocky slopes, coniferous forests; 100--1000 m elevation; Greenland; Alta., B.C. Ont.; Alaska, Calif., Conn., Iowa, Maine, Mich., Minn., N.J., N.Y., N.C., Oreg., Que., Va., Wash.

Calypogeia sphagnicola, except for the very different C. neesiana, is the only species typically or strictly reported as occurring in sphagnum bogs where it is often associated with dense tufts of Dicranum acutifolium (Lindberg & Arnell) C. Jensen, D. undulatum Bridel; D. bergeri Blandowi (A. W. Evans 1907; R. M. Schuster 1969: 65). It is also much smaller than other Calypogeia species with shoots only 1--1.8 mm wide, as compared with 1.6--3.5 mm for our other species. The very small laminal cells (those of the leaf tips mostly well under 30 /um) are diagnostic. It is not reported for California although Sphagnum bogs occur there from sea level to 160 m.

Asexual reproduction with gemmae in moist to subxeric situations almost invariably present, and gemmiparous shoots are sometimes present in enormous numbers, although usually absent in bog forms. Marsupia were found in western Greenland (R. M. Schuster 1969), but the species is infrequently fertile. In certain bog localities and in Greenland, plants may freely produce terminal, pseudochichotomous Frullania-type branches (as in Eocalypogeia, and species of Bazzania), otherwise branching is ventral-intercalary as are species in the remainder of the genus.

Calypogeia sphagnicola is a distinctive, usually tiny plant with small (33 x 31 /um) subisodiametrical lateral leaf cells, and the only species in the genus that has mostly widely-spaced (remote) to loosely imbricate, asymmetrical lateral leaves, and also remote underleaves. The lateral leaves are long-decurrent, distally falcate, appearing half-ovate (the distal half smaller than the proximal), strongly oblique, at an angle of (40--)45--60 ̊ to the stem (hence, not as widely spreading (to 90 ̊) as most species in the genus). Distinctive also is the smallness of the plants (ca. 1.5, rarely to 2 mm wide) and their typical growth over mostly Sphagnum moss in bogs. Calypogeia neesiana and C. integristipula are often found with C. sphagnicola over Sphagnum. Often specimens are single stems among Sphagnum plants and mixed with other taxa, requiring diligent search. The substrate appears to be more diverse than commonly given, as a fruiting (marsupiate) specimen with gemmiparous shoots has been reported from soil on an earth bank on an island off the coast of British Columbia.

The published descriptions of Calypogeia sphagnicola represent only a xeric extreme of the species. On the southern Appalachians, the fo. paludosa (Warnstorf) R. M. Schuster is distinctive by the much larger plant (over 2.2 mm wide, as in C. muelleriana) with thin-walled, barely collenchymatous median leaf cells, 40--52 x 55--85(--100) /um. This variant has (sub) distant and very decurrent lateral leaves with falcate distal portion, the base extending sometimes beyond the total length of the distal portion. Microphyllous branches appear to be numerous, etiolated, very long and delicate but wiry and filamentous with distant and reduced foliar structures, unlike those of other species of Calypogeia. The always-distant underleaves are generally longer than wide and are deeply 2-fid with acute lobes and lack decurrencies                                                                                                

The fo. bidenticulata R. M. Schuster is similar to fo. paludosa R. M. Schuster, but several or most lateral leaves are bidentulate, one tooth somewhat subulate, the underleaves also are seen to have marginal angulations and an occasional sharp unicellular tooth. Some extremely etiolated forms have 2-dentate lateral leaf apices and must not be confused with the much larger C. neogaea associated with mineral soils and forests, such as oak-hickory. A. Evans (1907) described Calypogeia tenuis fo. bidenticulata as having distant underleaves longer than wide, with a “strong tendency to be bidentate or bilobed,” as distinguished from C. fissa, which had sharp teeth on the lateral leaves, and the underleaves “considerably broader than long” (A. Evans 1907); both distinctions were removed in the illustration by R. M. Schuster (1969) showing sharply 2-dentate apices on some lateral leaves and transverse underleaves wider than long, making this form very similar to C. neogaea, including the size of the median cells.

Resemblance to the rare Eocalypogeia schusteriana is discussed under that species. Superficially, the most distinct characteristic of Calypogeia sphagnicola is the substrate: in acidic situations over species of Sphagnum. Eocalypogeia grows on calcareous mineral substrates.

Odontoschisma (Cephaloziaceae) species may resemble C. sphagnicola in the terminal clusters of yellowish gemmae and unlobed leaves, however, such plants are opaque, not pale and translucent, strongly concave, with rhizoids from the stems, the leaves are succubous with strongly trigonous cells, and underleaves none or small, to triangular to ovate-lanceolate. Species of Radula also have incubous lateral leaves, which are entire at the apex (except for gemmae formation) and display the scorpioid appearance of species of Calypogeia on the adaxial side. Radula has, however, no underleaves, the lateral leaves have a distinct abaxial lobule at the leaf base from which the rhizoids develop, and the species occur on mineral substrates. Incubous-leaved, depauperate Bazzania tricrenata (Wahlenberg) Lindbberg in Brotherus, which is also only 1.6--2 mm wide with large, orbicular underleaves, may resemble this species in the Arctic, but has reddish brown coloration, with apical teeth on lateral leaves, and generally grows on rock.

SELECTED REFERENCES

Arnell, S. 1956. I. Hepaticae. Illustrated Moss Flora of Fennoscandia. Lund, Sweden.

Evans, A. W. 1907. Notes on New England Hepaticae--5 (continued). Rhodora 9(100): 65--73.

8. Calypogeia suecica (Arnell & J. Persson) Müller Frib., Beih. Bot. Centralbl. 17: 224. 1904

Kantius suecicus Arnell & J. Persson, Rev. Bryol. 29: 29. 1902, as Kantia suecica

Plants translucent, pale, yellowish or whitish green or pale brown when dry. Leafy shoots small (0.8--)1.3--1.8(--2.5) mm wide. Leaves varnished-nitid when dry, broadly ovate to nearly orbicular, nearly as wide as long or longer, apices entire, variably broadly rounded to narrowly truncate, sometimes shallowly emarginated or bidentulate; midleaf cells 24--30(--35) x 26--35(--40) /um, collenchymatous, nearly isodiametric, apical marginal cells isodiametric or nearly so, not forming a border of tangentially elongate cells. Oil-bodies present in all cells in fresh material, essentially colorless fresh or dry. Underleaves subdistant or more usually distinctly imbricate, rather deeply divided 2/5--3/5 x their length to the rhizoid initial area, lobes mostly acute to obtuse, sinus acute to rounded-rectangular, lateral margins entire or often with a low, obtuse angulation on one or both margins, midline from base of sinus to rhizoid-initial area in a series of (2--)3--5(--6) cells, rhizoid initial area, brownish, broadly transversely oval-oblong, underleaf distinctly decurrent, cuticle smooth. Specialized asexual reproduction by gemmae rare; gemmae may be abundant sporadically in pioneer conditions.

Obligate lignicole, strictly acid, usually subxeric sites, often a pioneer species, shaded, moist, rotted, often peaty logs, crevices of rotting, decorticated coniferous or occasionally deciduous logs, coniferous tree bases in spruce-fir forests, very humid cove forests, gorges, valleys and ravines in deciduous or mixed woodland; low to high elevations, 0--3352 m;  Alta., B.C., N.B., Nfld. land Labr. (Nfld.), N.S., Ont., Que., Yukon; Alaska, Calif., Colo., Conn., Ga., Idaho., Maine, Mich., Minn., Mont., N.H., N.Y., N.C., Ohio, Oreg., Pa., S.C., Tenn., Vt., Va., Wash., Wis., Wyo.; Eurasia; Atlantic Islands.

Calypogeia suecica is the only species in the family in North America that is dioicous; although often with only androecia (as well as gemmae), it is also as often fertile with capsules. Calypogeia suecica and C. sphagnicola are unique in the family and similar to each other in their minute stems, mostly less than 2 mm wide. Both have collenchymatous laminal cells, the cells relatively small for the genus. The lateral leaves of C. suecica are characteristically strongly imbricate and stubby (mostly as broad as long with squared, truncate-retuse apices, the proximal bases only slightly decurrent), and spread from the stem at an angle of about 60 degrees, whereas C. sphagnicola has long-decurrent leaves more remote to quite distant on their stems, longer than broad with acute, rounded-acute apices and spread at an angle of 45 degrees. The relatively large imbricate underleaves of C. suecica are usually conspicuously wider than the stems: fully 2--2.5 x, often 3(--4) x the stem width, whereas in C. sphagnicola the leaves are remote and only slightly wider, usually up to only 1.8 x as wide as the stem. Underleaf marginal angulations of C. suecica may be smooth or as elaborate as in C. neogaea with high angular shoulders; occasional stems exhibit one or two 2-dentate lateral leaf apices, making it sometimes identified as C. fissa or C. neogaea of mineral soils, and which always have smaller and more distant underleaves. The branching is uniformly postical-intercalary, whereas that of C. sphagnicola often freely produces terminal, Frullania-type branches (as in Eocalypogeia).

Calypogeia suecica approaches C. neogaea in its apiculate, bidentulate often truncate lateral leaf apices, its sometimes distant (but typically imbricate) underleaves which may be deeply bilobed with acute-triangular lobes, and these angulate on the margins, but differs by the small stem size and small, collenchymatous lateral leaf cells, and the wide, decurrent underleaves often to 2--3 x the stem width.