Anthocerotae (Hornworts)

Abstract

A brief overview of the Anthocerotae, with reference to New Zealand species.

Keywords: Bryophyta, Anthocerotae, hornworts, Anthocerotales, Anthocerotaceae, Notothylaceae, Anthoceros, Phaeoceros, Megaceros, Dendroceros, Notothylas

Introduction

The class Anthocerotae differ from other bryophytes chiefly in possessing cells with large chloroplasts, each containing a single, large pyrenoid; the development of antheridia from hypodermal cells on the dorsal side of the gametophyte; archegonia almost completely embedded in the gametophyte; and a sporophyte possessing a meristematic region continually adding to the base of the capsule throughout the growing season (Smith 1955, p. 87).

The class is usually considered to comprise a single order, the Antherocerotales, in turn comprising only one family, the Anthocerotaceae. A number of authorites consider the genus Notothylas to belong in a separate family of its own, the Notothyaceae, and rather fewer additionally recognise a separate Notothylales order. However, recent DNA studies have shown that Notothylas is the sister genus to Phaeoceros, so such distinction is inappropriate.

Five to nine genera are recognised, including Anthoceros, Megaceros, Dendroceros, Phaeoceros (sometimes treated as a subgenus or partial synonym of Aspiromitus or Anthoceros), Folioceros, Notothylas and Nothoceros. These are widely distributed in temperate and tropical latitudes; all genera found in tropics and subtropics; most found on moist mineral soil of banks and cliffs, among grasses, and along streams, from sea level to alpine elevations.

Morphology

Spores

The spores adhere in tetrads until shed; may be multi- or unicellular when shed; are green in Megaceros, Dendroceros, but all others are yellow to black.

Gametophyte

Hornwort gametophytes are thallose, somewhat lobed or radially dissected, or sometimes exhibiting dichotomous branching. They are always dorsoventrally differentiated, possessing numerous smooth-walled rhizoids on the ventral surface which lacks both scales and mucilage hairs. Some species of Dendroceros are further differentiated laterally into a thick midrib with lateral wings a single cell in thickness.

Following germination there is scarcely any protonema; three main patterns occur:

1. short uniseriate germ tube that becomes two to four cells in length, apical cell develops (Anthoceros);
2. spore wall ruptures irregularly forming a multicellular mass from which the thallus develops (Notothylas);
3. chlorophyllose and multicellular when they are shed and initiate the apical cell directly develops from mass (Dendroceros).

The thallus is typically dark-green, succulent, brittle, dorsiventrally flattened, composed of thin-walled cells (parenchymatous); multistratose at least near the middle; attached to substratum by smooth rhizoids; each cell has a single disc-shaped chloroplast (except in Megaceros which has 12 per cell); the chloroplasts often have central pyrenoids and channeled thylakoids (both alga-like characters); ventral side of gametophyte with mucilage clefts that resemble stomata in some genera; lacking oil bodies; exhibits true dichomotomous branching (apical cell divides). The apical cell of most with four cutting faces, found in thallus notches, covered by mucilage which was secreted by epidermal cells (no mucilage hairs).

Plants of temperate plants often with mucilage-filled cavities formed by the breakdown of groups of cells, these cavities are often invaded by blue-green algae, Nostoc (through mucilage cleft); Nostoc is found in most thalli (fungal associations may also occur, endomycorrhizal), perhaps haustorial to Nostoc.

Asexual reproductive mechanisms include gemmae (Anthoceros produces gemmae at the thallus margin) and "natural division" when older parts of the plants decay up to dichotomies, leaving the younger portions to become separated and act as diaspores.

Sexual reproductive structures develop the same in all hornworts; sex organs are endogenous; in monoicous plants the antheridia develop and mature prior to the development of the archegonia.

Antheridia remain embedded in the upper layers of the thallus when mature, they are formed from superficial cells within the mucilage cavity; numerous antheridia often originate within a single antheridial chamber; secondary antheridia are developed from the basal cells of the primary antheridia; mature antheridia are spherical and have a short stalk; as they elongate they push through the roof of the cavity and expel the sperm; the antherida occur in scattered patches on the thicker portion of the thallus, often behind the growing point; thousands of sperm are produced per antheridium.

Archegonia are not discrete organs (no stalk), but are represented by neck canal cells and an egg surrounded by essentially undifferentiated cells of the thallus; surface cells above the neck cell become mucilage papillae (canal cells) which when disintegrate expose the neck canal; develop usually behind growing point; band-like thickenings in cells adjacent to archegonia and therefore to foot of sporophyte.

As the sporophyte develops, there are cell divisions of adjacent cells in the thallus, often called a thallus-calyptra (involucre-calyptra), because cells of the thallus are involved in the area where the venter would be.

Sporophyte

Hornwort sporophytes are characterised by a basal (or intercalary) meristem that continuously develops new sporangial tissue (indeterminate growth). However, the sporangium does not grow indefinitely. Instead, the sporophyte usually grows throughout the favorable season, shedding spores at the apex and differentiating new spores from the basal meristem. Sporophytes may reach lengths of 12 cm; first division of the zygote is by a longitudinal line (this is different from all other bryophytes); endothecium becomes the columella and the amphithecium produces the sporogenous layer and jacket; the sporogenous layer overarches the columella early in development.

The sporophyte is covered in a multistratose jacket with stomata (except in Dendroceros and Notothylas where they are absent and rudimentary in Megaceros); hypoepidermal cells with two chloroplasts per cell; outer layer sometimes with thickened transverse walls; sporogenous layer unistratose until meiosis.

The foot produces short haustorial projections that push among the cells of the thallus, increase absorptive capacity of foot.

The seta is an undefined zone (some say absent).

There is usually a cylindrical columella in the sporangium, which may have spiral and annular thickenings (Dendroceros), which are probably important in conduction.

Archesporial tissue gives rise to "elater" mother cells (small nuclei), and spore mother cells with large nuclei and which alternate in tiers.

Hornworts are said to possess pseudo-elaters; these are not true elaters, because they are not derived from same mother cell as spores. Pseudo-elaters are unicelluar and multicellular; variable in shape; some have no ornamentation, some have thickenings, some long, some short, possibly important in water conduction (Proskauer) as well as dispersal, may also serve as internal tapetum.

Sporophytes are photosynthetic; the columella and pseudo-elaters also serve a nutritional function. As in other bryophytes, the sporophyte remains permanently attached to the gametophyte.

Dispersal

The sporangium usually opens by one or two longitudinal slits. Initially the split does not extend to the apex of the sporangium, the jacket walls are often hygroscopic. As the apex of the sporangium matures and dries out, the slits gape open and expose the spores and pseudo-elaters; pseudo-elaters twist as they dry, in some, the jacket is hygroscopic; dehiscence continues downward as the sporangium matures and new spores are ready for dispersal.

Notothylas dehisces by decay of the jacket.

Phylogeny and Evolution

Affinities

Fossil Record

The earliest fossil evidence is the equivocal Late Cretaceous (Santonian) whole plant fossil Notothylacites filiformis, reported from Czechoslovakia (Krassilov & Schuster 1984). Somewhat younger, but more certainly assigned to the Anthocerotae, are latest Cretaceous (Maastrichian) spores. Note, however, that only one modern hornwort genus, Phaeoceros, exhibits spores with a homogeneous wall resembling those of most fossil spores, and that molecular phylogenetic analysis suggests Phaeoceros to be derived.

(After the Berkeley web site and Taylor 2002.)

Origins

Evolution

Systematics

This section does not attempt to be exhaustive at the species level, providing examples only, mostly (though not exclusively) drawn from the New Zealand flora.

Kingdom Plantae

Phylum (Division) Bryophyta

Class Anthocerotae

Distinguished from other bryophytes by cells with large chloroplasts, each chloroplast containing a pyrenoid; first division of the zygote by a longitudinal line; a development of antheridia from hypodermal cells on the dorsal side of a gametophyte; and a sporophyte whose growth is indeterminate owing to a meristematic region at the base of the capsule.

The class contains only one order.

Order Anthocerotales Schiffn. 1893

The order contains only a single family, the Anthocerotaceae. As noted above, separate recognition of the Notothylaceae as a distinct family is inappropriate. (Where it is recognised, Notothylaceae contains only the single genus, Notothylas.) Notothylas has not been recorded from New Zealand.

Family Anthocerotaceae Dum. 1829

Description: "Plants terrestrial or epiphytic, thallose, forming rosettes, or dichotomously branching. Thallus with internal cavities filled with mucilage or Nostoc. Ventral surface without scales, with rhizoids. Cells large and with one or few large chloroplasts. Dioicous or monoicous. Sporophyte arising from an involucre on the upper thallus surface. Capsule linear, cylindrical, opening by 1–2 longitudinal slits in the capsule wall, the slits progressively opening from the apex to the base. Capsule walls with or without stomata. Spores single or multicellular at maturity, with three flat faces and an outer spherical face, the faces granulose to papillose, rarely smooth. Elaters with helical thickenings or without, then irregular in shape (termed pseudoelaters)" (Glenny, unpublished manuscript).

Key to New Zealand Genera:

(Adapted from David Glenny, unpublished manuscript.)

Genus Anthoceros Linnaeus 1753 emend. Proskauer 1951?

Type: Anthoceros sp? Linnaeus 1753

Original Diagnosis: xxx

Description: xxx

Habit: xxx

Distribution: xxx

Anthoceros aneuraeformis Stephani 1893

Original Diagnosis: Dioica. Magna. Frons 4 cm longa linearis, repetito furcata, e basi simplici superne valde ampliata et flabellata; rami versus apicem frondis sensim sensimque latiores, 4 cellulas crassi, ramulis nascentibus quasi lobati; alveola mascula numerosa per frondis superficiem dispersa (omnia vacua erant.). Reliqua desunt.

Original Collection: Hab. Nova Zelandia, Auckland, leg. Helms.

Original Discussion: Distinctissima species, facile cognoscenda, crassitudine et ramificatione, Aneuris similis, ceterum insignis inflorescentia dioica, in genere rarissima.

Anthoceros muscoides Colenso 1884

Original Diagnosis:

Original Collection:

Description of jnr. syn. A. helmsii: Monoica? Dense caespitosa, 2 cm longa, margine profunde laciniata, laciniis late linearibus obtusis, margine varie angulatis, tenera, maxime cavernosa, praecipue in medio frondis, marginem versus magis tenuis, antis varie maximeque cristata, cristis lobatis, basi inflatis cavernosis superne acutis.

Androecia haud vidi. Involucra numerosa, magna, 6-7 mm longa, cylindrica, versus apicem angustata, cavernosa. Capsula longissima 5 cm longa, valde stomatifera. Sporae magnae, atrae, 43 m in diametro, echinatae. Pseudo-elateres concolores brevi-articulati.

Hab. Nova Zelandia, Greymouth, leg. Helms. Planta difficillime emollitura, spongiosa cum nulla alia commutanda.

Anthoceros? nostocoides Pearson 1923

Original Description (not in Latin - does that make the name invalid?): Sterile. Largish in size; olive green in color; densely stratose. Fronds bi-trifurcate, lobes erecto-patent (30°), linear, regular, slightly plano-convex, 3 to 4 cells thick at the middle, gradually thinning to margin which is one cell thick; cortical cells very small and indistinct, inner large and irregular in size, hyaline; lobulate; lobules few, 3-4; cuticle smooth; postical side with numerous narrow oval Nostoc colonies imbedded in the fronds.

Dimensions.- Fronds 1 to 2 inches long, 3 to 5 mm. wide, .2 to .3 mm. thick; Nostoc colonies .5 mm long x .25 mm. wide.

Habitat.- Pipiriki, North Island, New Zealand; coll. W.A. Setchell, 1904, no. 14. Type Herb. Univ. Calif., no. 213714.

Observations.- Although the plant was collected in considerable quantity I have not been able to find any trace of <male> or <female>, so am not able to say to which subgenus of Anthoceros the species belongs. [Which subgenera were recognised in 1923 - CC?] Mitten records only 4 species of Anthoceros from New Zealand, all very different from the above, and Stephani records 6 Megaceros and 3 Anthoceros, to none of which does this species agree according to his descriptions.

Genus Phaeoceros Proskauer 1951?

Type: Anthoceros laevis Linnaeus 1753

Original Diagnosis: xxx

Description: xxx

Habit: xxx

Distribution: xxx

Discussion: It seems Phaeoceros has sometimes been treated as a subgenus of Anthoceros since at least the late fifties, only a few years after Proskauer erected the name. I am uncertain of the name of the Jones publication (if anyone should track it down, I'd be grateful to learn of it) but I have a photocopied paper noting (p. 355):

Subgen. Phaeoceros (Proskauer, as genus) E. W. Jones, comb. nov.

Recent DNA studies by Chris Cargill have shown Phaeoceros, as presently recognised, to be polyphyletic.

Genus Dendroceros ?

Type: Anthoceros ? ?

Original Diagnosis: xxx

Description: xxx

Habit: xxx

Distribution: xxx

Discussion: Recent DNA studies by Chris Cargill have shown Dendroceros, as presently recognised, to be polyphyletic.

Genus Megaceros ?

Type: Anthoceros ? ?

Original Diagnosis: xxx

Description: xxx

Habit: xxx

Distribution: xxx

Megaceros "flagellaris"

The New Zealand taxon which goes by this name is unlikely to be that tropical species, based on DNA, but the name we should use is unclear, possibly M. gracilis (David Glenny, pers. comm.)

Megaceros longispirus

M. longispirus is not a synonym of M. pellucidus, as indicated in Ella Campbell's study.  M. pellucidus is a problem because the spores in the type are immature, so it can't be decided what that type represents (David Glenny, pers. comm.)

Megaceros novae-zelandiae Stephani 1916

Original Description: Planta monoica magna, valida, fusco-virens, terricola. Frons ad 4 cm. longa, irregulariter multiramosa, anguste ligulata, solida, plana, levis, ramis primariis longis similibus, breviter remoteque pinnulatis. Involucre solitaria, 5 mm. longa, cylindrica, levia. Capsula 3 cm. longa, tenuis. Sporae 27 m, pallidae, asperae. Elateres concolores, monospiri. Andraecia numerosa, aggregata, alveolis tetrandris. Hab. Nova Zelandia.

Megaceros pallens (Stephani 1892) Stephani 1916

Original Description: Monoica, flavicans vel dilute olivacea, in cortice putrescente arcte repens. Frondes 3-4 cm. longae, laeves, oblongae, inaequaliter lobatae, lobis rotundatis, ubique 5 cellulas crassae, laxe cavernosae, superficie itaque sub lente reticulata. Involucra oblongo-fusiformia, pariete basi 12 cellulas, apice 1 cell. crassa, cellulis irregulariter prominentibus quasi aspera. Capsula 4 cm. longa, robusta, flavo-rubescens, valvulis post dehiscentiam planis neque tortis, haud raro uno latere solum fissa. Elateres fibra laxe torta repleti, pallide flavescentes. Sporae 0.025 mm., dense verrucosae, flavescentes. Antherae in alveolis magnis geminatae.

[That's the end of the description, but he waffles onwards under the same heading, as follows:]

Species of Anthoceros are rather common all over Europe, and easily found in all stages of development; it is therefore scarcely necessary to state that young involucra are closed at the top, and later on ruptured by the protruding capsule, leaving an irregular lacerate opening, parts of which are torn away or remain adhering as scarious rudiments. The old authors have taken great care to describe these broken tissues as teeth or lips &c., and tried to find specific differences in what is naturally of quite accidental origin.

If a well-developed capsule of Anthoceros be taken out of the frond with the basal bulb adhering, and split open from top to bottom, spores and elaters in all stages of development will be found, ripe at the top, the youngest and least developed at the base; the walls of the capsule keep pace with the development of its contents, and the valves are firmly united at the base and still green. This lower part of the capsule has often been described as a pedicel, which certainly is not correct. This presumptive pedicel is called sometimes "long exserted" or "included," which of course means nothing more than the more or less advanced ripeness of the capsule, and can be of no diagnostic value.

Revised Description (Stephani 1916, pp. 954-5): Planta monoica, flavicans vel virens. Frons major, tenuis, subplana, cristulata, 25 mm. longa, 5 mm. lata, profunde lobata, lobis magnis, margine breviter denseque laceratis. Involucre solitaria, anguste cylindrica, 5 mm. longa, levia. Capsula 4 cm. longa. Sporae 27 m, pallidae, asperae. Elateres monospiri. Andraecia involucro approximata, dense aggregata, alveolis monandris. Hab. Nova Zelandia.

Genus Notothylas Sull. ex A. Gray 1846

Type: Anthoceros ? ?

Original Diagnosis: xxx

Notothylas is characterised by a very short sporophyte (only about 5 mm long it looked), yellow-brown spores, reduced pseudoelaters, and simultaneous spore maturation. As yet unpublished DNA sequencing studies by Chris Cargill shows it to be a sister genus to Phaeoceros.

Habit: xxx

Distribution: xxx

• sporophyte with columella surrounded by esporógeno weave of several rows of cells
• the intercalary meristem zone is active single during a time, the esporófito is short
• there are no oclusivas cells in estomas

Genus Nothoceros

Schuster also recognises Nothoceros, on the basis of its having a non-radiate thallus, and apparently there's one NZ species that fits that description (David Glenny, pers. comm.)

Conclusion

xxx

Further Information

xxx

References

Jones, Eustace W. 1958: An Annotated List of British Hepatics. [Journal name unknown] vol. 3, part 3, 16 July 1958, pp. 353-374.

Krassilov, V.A.; Schuster, R.M. 1984: Paleozoic and Mesozoic Fossils. In New manual of Bryology, R. M. Schuster, ed. Nichinan, Miyazaki, Japan: Hattori Botanical Laboratory, 1984, pp. 1172–1193.

Singh, D.K 1994. Distribution of family Notothylaceae and its phytogeographical significance. Adv. Pl. Sci. Res., 2:pp.28-43.

Singh, D.K. 2002: Notothylaceae of India and Nepal (A Morpho-Taxonomic Revision). Dehradun, Bishen Singh Mahendra Pal Singh, 271 pp.

Smith, Gilbert 1955: Cryptogamic Botany, volume II, 2nd edition. McGraw-Hill, 399 pp.