Belongs within: Monilophyta.
Contains: Osmundaceae, Gleicheniaceae, Matoniaceae, Hymenophyllaceae, Schizaeaceae, Marsileaceae, Salviniaceae, Polypodiales, Cyatheaceae, Dicksoniaceae.
The Leptosporangiatae include most familiar fern species. The clade is primarily characterised by distinctive sporangia (leptosporangia) of which the greater part develops from a single cell, as opposed to the multicellular-derived sporangia (eusporangia) of other ferns and fern-like plants. Known members of the Leptosporangiatae date back to the Early Permian, where they are represented by relatives of the royal ferns in the Osmundaceae (Schneider et al. 2004).
Representative of the Leptosporangiatae include the genus Lygodium, climbing ferns that grow high by means of twining rhachides (Allan 1961). The Loxomataceae are terrestrial ferns with a disjunct distribution in Central America and New Zealand, distinguished by sori with an elongating, hairy receptacle, and sporangia with an oblique annulus (Allan 1961).
When ferns don’t look like ferns
Published 2 September 2008
I suspect that I would hardly need to explain to anyone what a fern looks like—their cool, green, graceful appearance makes them a favourite of holders of foliage fetishes everywhere. What you possibly may not be aware with is that the classic fern is actually only part of the story. Odds are that the parent of the fern you next see growing in a pot or in a damp grove looked nothing like that fern, and if you took the spores of that fern and grew them, you may not recognise the product. Welcome to the world of alternating generations.
Alternation of generations is actually something that all land plants indulge in. A diploid sporophyte asexually produces haploid spores that grow into haploid gametophytes whose haploid gametes fuse to form the zygotes that grows into new sporophytes, as shown in the diagram above by Jeffrey Finkelstein. In seed plants, the gametophyte has been severely reduced and does not grow outside its parent—the female gametophyte remains contained within the parent flower or cone as the ovule, while the male gametophyte is only a few cells in size and forms the pollen grain. In ferns, the gametophyte grows as a separate (albeit really small—perhaps only about a centimetre across) individual with an undifferentiated thallus. Each gametophyte produces both male and female gametes at different places on the thallus, and male gametes require a layer of moisture across the surface to swim across to the female gametes and fertilise them. Cross-fertilisation occurs when multiple gametophytes grow in close proximity and joined by a common covering of moisture. The sporophyte then grows directly out of the parent gametophyte.
In the majority of fern species, the gametophyte is a small heart-shaped structure like in the diagram above. The meristem, the growing part of the plant, is restricted to the recessed point of the heart. In three fern families, though, the gametophyte is ribbon-like or filamentous with multiple marginal meristems and grows indeterminately. While gametophytes of other fern families tend to be short-lived affairs, the gametophytes of Hymenophyllaceae, Vittariaceae and Grammitidaceae can be much longer-lived. Dassler and Farrar (1997) recorded an individual gametophyte of the Hymenophyllaceae species Callistopteris baueriana still growing seven years after germination. What is more, some inderminately-growing gametophytes are able to reproduce asexually as well as sexually through the production of gemmae, side-buds that can detach and grow into new individuals (anyone who has owned a hen-and-chickens fern or a mother-of-millions plants may have seen gemmae growing along the edge of their leaves). For a very few species, this capacity for sexual reproduction has allowed them to bypass the sporophyte phase of the life-cycle entirely.
Currently, independent gametophytes (i.e. those that are able to establish populations without forming sporophytes) are known from a single species of Grammitidaceae, two Vittariaceae and nine Hymenophyllaceae (Lindsay 2003). Most of these species also produce sporophytes over part of the distribution, but the gametophytes are able to survive in areas that are seemingly not conducive to sporophyte production. Vittaria graminifolia, for instance, is known in Louisiana only as gametophytes, with the nearest sporophytes of the species over a thousand kilometres away in Mexico (Lindsay 2003). As yet, only three species are known that seemingly never produce sporophytes—Vittaria appalachiana, Hymenophyllum tayloriae and Trichomanes intricatum (Raine et al. 1991; Farrar 1992). Nevertheless, there are good reasons to suspect that the diversity of unrecognised independent gametophytes out there might be much higher. Fern gametophytes have been studied much less than sporophytes—not only are they small and difficult to find, but they have generally been regarded as decidedly low on taxonomically useful characters. Vittaria appalachiana, the first-known gametophyte-only species, was actually discovered sixty years before it was confirmed to be identifiably distinct from sporophyte-producing species of Vittaria. It does not escape notice that all three known gametophyte-only species come from the eastern United States, even though the families involved are found in tropical and subtropical habitats throughout the world. Things become particularly suspicious when you realise that a single person, Donald Farrar of Iowa State University, has been privy to the description of all three. More than likely, the apparent absence of gametophyte-only species from other parts of the world does not suggest that there is something unusual about the eastern United States, but simply that no-one has really looked anywhere else.
Like the relationship between asexually- and sexually-reproducing fungi, the taxonomic and ecological implications of the independent gametophyte may be significant. Rumsey et al. (1999) demonstrated that the Killarney fern (Trichomanes speciosum), previously regarded as extremely rare in the British Isles based on the distribution of the sporophyte, was actually fairly widespread and common as the gametophyte. The wide distribution of the eastern North American Trichomanes intricatum, including areas previously subject to glaciation and despite the apparent low dispersal potential of gametophytes reproducing by gemmae only, led Farrar (1992) to suggest that the “extinction” of the sporophyte form may have happened only recently. Has this species really forever lost the ability to produce sporophytes, or might a change of climate lead to the unfurling of a long-forgotten frond deep within the forests of New England?
Systematics of Leptosporangiatae
Synapomorphies (from Cantino et al. 2007): Leptosporangia present, originating from two cells, with sporangial stalk broad, capsule small with thin wall, annulus present, and 512 or less spores per sporangium; gametophytes with exposed antheridia and archegonia; less than 100 sperm per antheridium; first division of zygote more or less longitudinal; prone embryos with small foot; mesarch protoxylem; stem rhizomatous.
<==Leptosporangiatae (see below for synonymy)
|--+--Grammatopteris [Guiareaceae]SS04
| `--OsmundaceaePS01
`--+--+--+--GleicheniaceaeSP09
| | `--SzeaSS04
| `--+--MatoniaceaeSP09
| `--+--CheiropleuriaYM03 [CheiropleuriaceaeKTT04]
| | |--C. bicuspisYM03
| | `--C. integrifoliaSP09
| `--Dipteris [Dipteridaceae]PS01
| |--D. bifurcatumT-W89
| |--D. conjugataPS01
| `--D. horsfieldiiT-W89
`--+--HymenophyllaceaePS01
`--+--+--SchizaeaceaeSP09
| `--+--Stachypteris spicansSP09, C93
| `--Lygodium Swartz 1801SP09, A61 [incl. Ramondia Mirbel 1801M01; LygodiaceaeB06]
| |--L. articulatum Rich. 1832 [incl. L. gracilescens Col. 1896]A61
| |--L. circinatum [=Hydroglossum circinatum]BS-V28
| |--L. dichotomumT-W89
| |--L. flexuosum Swartz 1801B06 (see below for synonymy)
| |--L. japonicum (Thunberg) Swartz 1801B06 (see below for synonymy)
| |--L. lanceolatumSS04
| |--L. pubescensBS-V28
| |--L. reticulatumB78
| `--L. scandensBS-V28 (see below for synonymy)
`--+--+--MarsileaceaeSP09
| `--SalviniaceaeWP05
`--+--PolypodialesSP09
`--CyathealesRS12
|--+--+--CibotiumSP09
| | | |--C. barometz (Linnaeus) Smith 1842 [=Polypodium barometz Linnaeus 1753]I88
| | | `--C. schiedeiSP09
| | `--CyatheaceaeSP09
| `--+--DicksoniaceaePS01
| `--Metaxya rostrataSP09
`--+--Thyrsopteris [Thyrsopteridaceae]SP09
| `--T. elegansSP09
`--+--LoxomataceaeSS04
| |--Loxsomopteris anasilla Skog 1976SP09, C93
| `--+--Loxsomopsis pearceiSP09
| `--Loxoma Br. ex Cunn. 1837SP09, A61 [=LoxsomaA61]
| `--L. cunninghamii Br. ex Cunn. 1837A61 (see below for synonymy)
`--+--CulcitaSP09
| |--C. coniifoliaSP09
| `--C. stramineaH03
`--Plagiogyria [Plagiogyriaceae]WP05
|--P. communis Ching 1958I88
|--P. euphlebia (Kunze) Mett. 1858I88 (see below for synonymy)
|--P. japonicaWP05
|--P. pycnophylla [=Lomaria pycnophylla Kunze 1848]I88
`--P. semicordataJ87
Leptosporangiatae incertae sedis:
AdiantitesSS04
|--A. lindsayoidesSS04
`--A. obtususA38
Cynepteris [Cynepteridaceae]C93
`--C. lasiphora Ash 1969C93
Tempskya Corda 1845 [Tempskyaceae]C93
|--T. cretacea Hosius & von der Marck 1880C93
|--T. grandisC02
|--T. knowltoniC02
|--T. minorC02
|--T. rossicaC02
|--T. schimperi Corda 1845C93
|--T. superbaC02
|--T. wesselliiC02
|--T. wyomingensisC02
`--T. zolleriC02
Leptosporangiatae [Aspidiales, Filicales, Gleicheniidae, Hymenophyllidae, Osmundeae, Polypodieae, Schizaeales, Schizaeidae, Polypodiidae]
Loxoma cunninghamii Br. ex Cunn. 1837A61 [incl. Trichomanes coenopteroidesC06, Davallia dealbataC06]
Lygodium flexuosum Swartz 1801B06 [=Ophioglossum flexuosum Linnaeus 1753B06, Ramondia flexuosa (Linnaeus) Mirbel 1801M01]
Lygodium japonicum (Thunberg) Swartz 1801B06 [=Ophioglossum japonicum Thunberg 1784B06; incl. L. semibipinnatumB78]
Lygodium scandensBS-V28 [=Hydroglossum scandensBS-V28, Ophioglossum scandensBS-V28, Ramondia scandensM01; incl. L. microphyllumB78]
Plagiogyria euphlebia (Kunze) Mett. 1858I88 [=Lomaria euphlebia Kunze 1848I88; incl. L. articulataB78]
*Type species of generic name indicated
References
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[A61] Allan, H. H. 1961. Flora of New Zealand vol. 1. Indigenous Tracheophyta: Psilopsida, Lycopsida, Filicopsida, Gymnospermae, Dicotyledones. R. E. Owen, Government Printer: Wellington (New Zealand).
[B78] Bentham, G. 1878. Flora Australiensis: A description of the plants of the Australian Territory vol. 7. Roxburghiaceae to Filices. L. Reeve & Co.: London.
[B06] Biswas, A. 2006. Pteridophytes of Indian Botanic Garden, Howrah. Bulletin of the Botanical Survey of India 48: 175–188.
[BS-V28] Bory de Saint-Vincent, J. B. 1828. Voyage Autour du Monde, Exécuté par Ordre du Roi, Sur la Corvette de Sa Majesté, La Coquille, pendant les années 1822, 1823, 1824 et 1825. Botanique. Cryptogamie. Arthus Bertrand: Paris.
Cantino, P. D., J. A. Doyle, S. W. Graham, W. S. Judd, R. G. Olmstead, D. E. Soltis, P. S. Soltis & M. J. Donoghue. 2007. Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56 (3): E1–E44.
[C06] Cheeseman, T. F. 1906. Manual of the New Zealand Flora. John Mackay, Government Printer: Wellington.
[C93] Cleal, C. J. 1993. Pteridophyta. In: Benton, M. J. (ed.) The Fossil Record 2 pp. 779–794. Chapman & Hall: London.
[C02] Clifford, H. T. 2002. A new Devonian fern, Fanningopteris wyattii, from Queensland. Memoirs of the Queensland Museum 48: 71–77.
Dassler, C. L., & D. R. Farrar. 1997. Significance of form in fern gametophytes: clonal, gemmiferous gametophytes of Callistopteris baueriana (Hymenophyllaceae). International Journal of Plant Sciences 158 (5): 622–639.
Farrar, D. R. 1992. Trichomanes intricatum: the independent Trichomanes gametophyte in the eastern United States. American Fern Journal 82 (2): 68–74.
[H03] Heads, M. 2003. Ericaceae in Malesia: vicariance biogeography, terrane tectonics and ecology. Telopea 10 (1): 311–449.
[I88] Iwatsuki, K. 1988. An enumeration of the pteridophytes of Nepal. In: Ohba, H., & S. B. Malla (eds) The Himalayan Plants vol. 1. The University Museum, University of Tokyo, Bulletin 31: 231–339.
[J87] Judd, W. S. 1987. Floristic study of Morne La Visite and Pic Macaya National Parks, Haiti. Bulletin of the Florida State Museum—Biological Sciences 32 (1): 1–136.
[KTT04] Klavins, S. D., T. N. Taylor & E. L. Taylor. 2004. Matoniaceous ferns (Gleicheniales) from the Middle Triassic of Antactica. Journal of Paleontology 78 (1): 211–217.
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[M01] Mirbel, B. 1801. Mémoire sur le Ramondia, nouveau genre de fougère. Bulletin des Sciences, par la Societé Philomathique de Paris 2 (47): 179.
[PS01] Pryer, K. M., A. R. Smith, J. S. Hunt & J. Y. Dubuisson. 2001. rbcL data reveal two monophyletic groups of filmy ferns (Filicopsida: Hymenophyllaceae). American Journal of Botany 88 (6): 1118–1130.
Raine, C. A., D. R. Farrar & E. Sheffield. 1991. A new Hymenophyllum species in the Appalachians represented by independent gametophyte colonies. American Fern Journal 81 (4): 109–118.
[RS12] Rothfels, C. J., M. A. Sundue, L.-Y. Kuo, A. Larsson, M. Kato, E. Schuettpelz & K. M. Pryer. 2012. A revised family-level classification for eupolypod II ferns (Polypodiidae: Polypodiales). Taxon 61 (3): 515–533.
Rumsey, F. J., J. C. Vogel, S. J. Russell, J. A. Barrett & M. Gibby. 1999. Population structure and conservation biology of the endangered fern Trichomanes speciosum Willd. (Hymenophyllaceae) at its northern distributional limit. Biological Journal of the Linnean Society 66 (3): 333–344.
[SS04] Schneider, H., E. Schuettpelz, K. M. Pryer, R. Cranfill, S. Magallón & R. Lupia. 2004. Ferns diversified in the shadow of angiosperms. Nature 428: 553–557.
[SP09] Schuettpelz, E., & K. M. Pryer. 2009. Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proceedings of the National Academy of Sciences of the USA 106 (27): 11200–11205.
[T-W89] Tenison-Woods, J. E. 1889. On the vegetation of Malaysia. Proceedings of the Linnean Society of New South Wales, series 2, 4 (1): 9–106, pls 1–9.
[WP05] Wikström, N., & K. M. Pryer. 2005. Incongruence between primary sequence data and the distribution of a mitochondrial atp1 group II intron among ferns and horsetails. Molecular Phylogenetics and Evolution 36: 484–493.
[YM03] Yatabe, Y., & N. Murakami. 2003. Recognition of cryptic species in the Asplenium nidus complex using molecular data—a progress report. Telopea 10 (1): 487–496.