Revision of the fern genus Orthiopteris (Saccolomataceae) in Malesia and adjacent regions

Abstract A taxonomic revision of the Old-World representatives of the fern genus Orthiopteris is presented. We recognize eight species, one of which is newly described (Orthiopteris samoensis), and five varieties, of which two are newly described (Orthiopteris campylura var. insularis and Orthiopteris campylura var. laxa). Orthiopteris acuminata, Orthiopteris caudata, Orthiopteris minor and Orthiopteris kingii are all reduced to varieties of Orthiopteris campylura.

Th e question whether Orthiopteris is distinct from Saccoloma within the Saccolomataceae is also controversial, and requires further study (Smith et al. 2006;Christenhusz et al. 2011). Many authors have treated Orthiopteris as a synonym of Saccoloma (Tryon and Tryon 1982b;Kramer et al. 1990;Parris et al. 1992;Smith et al. 2006). Both genera share a similar rhizome anatomical structure, sorus shape and spore morphology. In transverse section the rhizome of Orthiopteris spp. and Saccoloma elegans Kaulf. shows two concentric, somewhat discontinuous, rings of vascular bundles. Both genera have pouch-shaped sori and tetrahedral-globose, with a plain exospore and perispore with low branching ridges. However, Orthiopteris fronds are bipinnate or more decompound, unlike the simple-pinnate fronds of the type species of Saccoloma, S. elegans (Kramer 1990). Using a single rbcL gene phylogeny, Wolf (1995) found Orthiopteris as here circumscribed in two widely diff erent clades. He reported Saccoloma moluccanum (based on a specimen from the Philippines, and therefore most likely corresponding with O. campylura var. campylura) in a clade with (American) Saccoloma elegans, and Orthiopteris kingii (based on a specimen from Indonesia) in a far more basal position. Since then there has not been any other phylogenetic study including representatives of both Orthiopteris and Saccoloma. Subsequent studies including only Saccoloma (Pryer et al. 2004;Schuettpelz and Pryer 2007;Rai and Graham 2010;Lehtonen et al. 2012) all place Saccoloma in a basal position, although with some uncertainty regarding the exact position (Lehtonen et al. 2012). We performed a reanalysis (not reported) of the rbcL marker of all accessions used in these studies, which placed all these in a clade with the Orthiopteris accession that Wolf (1995) placed in a basal position. A more densely sampled analysis is clearly needed to resolve the exact relationships between the two genera and their phylogenetic position.

Material and methods
Th is study was based entirely on herbarium specimens. In total, 240 specimens have been examined from K, L, MICH, MO, NY, SING and additional images or on-line images provided by BM, K, MICH, P, and the JSTOR Global Plants database (plants. jstor.org). Herbarium abbreviations follow Index Herbariorum (Th iers continuously updated). Sheets seen as digital image only are marked with "*". Data of all the studied specimens were entered into the BRAHMS database at L for storage and further analysis of geographic distribution. All studied specimens are listed in Appendix. We have selected lectotypes whenever necessary to resolve ambiguities in the application of a name. Most of the morphological characters were examined and measured with a stereo microscope or a compound microscope. In addition to light microscopy, scanning electron microscopy (using a Jeol JSM 7600F FEG-SEM) was used to study structure and ornamentation of the spores.

Morphology
Orthiopteris is often a large-sized fern; with a stout, erect rhizome and fronds often more than a meter long. Herbarium collections are often incomplete, and this makes an evaluation of the diff erentiating characters diffi cult. For the distinctions between the species, we have studied the following characters.

Rhizome
Due to lack of complete specimens, a thorough assessment of the variability of the rhizome morphology was impossible. From the available material, rhizomes can be assessed to be uniformly erect, and radially organized, and may form aerial trunks exceptionally to 1 m high. Characteristically, the vascular system shows two concentric cylinders of meristeles (well-illustrated in Bower 1918;1923). Th e morphology of the rhizome scales appears to show very little variation, and we have not found it useful for species distinction. In most of the species, rhizome scales are multistratose and pseudopeltate, tapering to a long narrow acumen from a rounded-cordate base, the margin usually being eroded and unistratose ( Figure 4).

Frond divisions
Division and venation of fronds are among the most confusing characters in Orthiopteris as the fronds are dissected to many levels, in many specimens reaching to quadripinnate. Th e gradual decrease in dissection from base to apex produces an almost perfectly fractal pattern, where the most basal pinnules are almost perfectly isomorphic with more apical pinnae ( Figure 1). Th is makes it diffi cult to judge this character in fragmentary specimens unless it is known exactly from which part of a frond the fragment is taken. In our species descriptions, we concentrate on the major (pinnae) and on the ultimate divisions (segments) (Figure 1).
We defi ne "ultimate segment" as the smallest distal unit with a branched venation around which lamina is incised completely, leaving no or very little lamina around the vein at its base. Margins are described as shallowly incised, crenate, dentate, or deeply lobed, with the degree of dissection quantifi ed, when necessary, by the distance from the base of the shallowest sinuses to nearest costule/vein ( Figure 2).

Sori
Th e most variable and important characters for distinguishing Orthiopteris species are found in the sori, the inner indusium and the outer indusium. Th e inner indusium is a thin membrane on the abaxial surface of the lamina. Th e outer indusium is continuous with the lamina on the adaxial surface. Each sorus thus forms a pouch-shaped structure that contains up to 30 sporangia, but mostly less, that are immersed within the indusium when young, but variously exserted when mature. We distinguish and classify several soral shape types as shown in Table 1 (see also Figure 3). In addition, we use the following descriptive terms: Outer indusium: (1) symmetric when it is not confl uent with the margin but is abruptly set-off from the lamina margin on two sides (Figure 3a, b, c, d...); (2) asymmetric when it is confl uent with the lamina margin on one side (Figure 3g,i,j...).
Inner indusium at apex: (1) obtuse-truncate without incision (Figure 3b, c, d,…), (2) extended into a lobe when it has a lobe 1/2-2/3 as wide as the entire sorus but shorter than 1/3 the length of the sorus (Figure 3g, h, i, j…), (3) extended into a narrow tongue, when it has a lobe less than ½ as wide as the entire sorus and longer than 1/3 the sorus length (Figure 3l, m, n, o…). To assess this character, it is necessary to examine more than one sorus because they can show some variations even on the same frond. In most species, the sori are in the same plane as the frond, but sori may also be curved towards the abaxial surface.

Sporangia and spores
Characters of the sporangia are deemed not important for species distinction. Sporangia are stalked with a spherical to hemispherical capsule and a vertical, interrupted annulus with 16-24 indurated cells, which are more or less equal to distinctly unequal in size ( Figure 5). Stalk and capsule are glabrous. All examined species have a more or less similar spore morphology resembling the American Saccoloma elegans (Tryon and Lugardon 1991: 269, fi g. 90). Spores are trilete, tetrahedral-globose with a smooth or fi nely wrinkled exospore closely overlain with a perispore ornamented with ridges ( Figure 6). Th e ridges strongly vary in width and density and in the degree to which they are sinuous and anastomosing. Description. Rhizome erect, stout, forming a trunk (2-)20-50(-100) cm high, in cross section showing two complete rings of vascular bundles, partly covered with scales, roots inserted on all sides of the rhizome especially in the older parts. Rhizome scales appressed at base, mostly basifi x, pseudopeltate to peltate, mostly narrow lanceolate with long attenuate tips, thick, stiff , brittle, dark brown. Fronds tufted, erect, monomorphic.
Ecology. Terrestrial, mostly in shaded moist habitats, river banks, moist slopes, ravines etc., in primary or disturbed forest, at 0-2000 m altitude.
Discussion. Orthiopteris campylura is the most variable species within the genus. It is widely distributed from Western Malesia to Papua New Guinea and the Pacifi c, existing as diff erent entities in each sub-geographical region, which in many cases have been recognized as individual species. However, we have regularly observed samples that were intermediate between the forms, and accordingly treat them here as varieties rather than as subspecies. Characters of the sori provide the best criteria to distinguish these varieties.
Th ere are no data that suggest that any of the varieties is distinguished by a diff erent ecology.
Discussion. Although in the shape of inner and outer indusium shape this species resembles Orthiopteris campylura var. kingii, the sori are not refl exed but usually fl at even when dried. Th e distribution center of this variety appears to be in the Philippines. Description. Sori not protruding from the margin on distinct lobes, not refl exed when dry, in one plane with lamina wings, 0.7-0.9 × 0.6-0.7 mm, asymmetric, funnelform, widest at mouth of sori; inner indusium bright-brown, fi rm, usually shorter but not shorter than 2/3 length of outer indusium, apex with c. 0.2 mm long lobe (< 1/3 length of sorus); outer indusium emarginate to undulate-truncate; sporangia 17-21 per sorus, capsule globose and rounded at apex, gradually narrowed toward base, indurated annulus cells 17-20, clearly unequal; spores in polar view 28-32 μm, in lateral view 25-28 μm.
Discussion. Th is variety is widespread in western Malesia. It is easily recognized when dry by its distinctly protruding and refl exed sori. Th e ultimate segments of this variety may be the widest among the varieties of Orthiopteris campylura, although many collections from the Moluccas have narrow segments. Th e abaxial surface is scaly, but the scales are very small and not easily observed. Description. Sori not protruding from the margin, not refl exed, in one plane with lamina wings, 0.8-1.0 × 0.5-0.6 mm, asymmetric, narrow obovate, widest just below mouth sori; inner indusium bright-brown, fi rm, usually shorter, sometimes equal to outer indusium, apex with 0.1-0.2 mm long lobe; outer indusium deeply emarginate, at one side strongly excurrent on lamina; sporangia 10-15 per sorus, capsule globose and rounded at apex, gradually narrowed toward base, indurated annulus cells 17-22, clearly unequal; spores not seen.

Distribution. Papua New Guinea (Bougainville), Solomon islands, Vanuatu (Erromango).
Etymology. Th e varietal epithet refers to the archipelagic distribution of this taxon. Discussion. Th is variety is quite widespread in the island archipelago stretching from Bougainville to the New Hebrides, but appears to be absent on the mainland of New Guinea. Description. Lamina not complete for measurement of size and shape, fi rm-herbaceous, yellowish-green, scales not found; ultimate segments 1.4-1.5 × 0.6-0.7 cm, sessile or very short-stalked, trapeziform, base asymmetric, cuneate, apex obtuse to acute, margin shallowly incised, distance from base of sinuses to costules 0.7-1.5 mm, lobes blunt; veins in lobes 3-15 forks, light to dark brown, not strongly contrasting with lamina, percurrent.
Distribution. Vanuatu (Aneityum), Fiji (Vanua Levu, Taveuni). Etymology. Th e varietal epithet refers to the general aspect of the fronds. Discussion. Th e specimens grouped here have been confused with Orthiopteris fi rma mainly because of the similarity in the lobed inner indusium, but diff er from that species in sorus shape and a less distinct cartilaginous border. Th e two available specimens examined here also show a considerable variation among themselves. More specimens or molecular evidence are needed to provide better support for the existence of this new variety. ( Description. Rhizome erect, rising at least 2 cm above ground, diameter unknown. Rhizome scales pseudopeltate, ca. 3.0 × 1.0 mm, lanceolate with long falcate acumen. Fronds 90-110 × 30-50 cm; stipes stout, 35-45 cm long, 0.4-0.5 cm across (at base), light brown; lamina deltoid, tripinnate to quadripinnate, ca. 70 × 30-50 cm, papyraceous, yellow-green when dry, glabrous or with few scattered scales; pinnae at 40-45° to rachis, largest at base, overlapping, stalk 2.0-2.5 cm, including stalk 25-35 × 10-15 cm, lanceolate, fi rst basiscopic pinnules of lowest pinnae enlarged; ultimate segments 1.0-2.0 × 0.5-0.7 cm, sessile or very short stalked, trapeziform, apex acute, margin with weak cartilaginous border; deeply incised to less than 0.2 mm from veins; lobes oblanceolate, veins in lobes unbranched or with 1 fork, light brown and not strongly contrasting with lamina, percurrent. Scales on rachis mostly present at base of segment, hair-like. Sori apical on small lobes, lateral on larger lobes, symmetric, not refl exed, slightly concave with lamina wings slightly recurved, 0.7-0.8 × 0.4-0.5 mm, wide obovate, widest just below mouth, not wider than the lamina below sorus; inner indusium brownish, fi rm, shorter than outer indusium, apex with c. 0.1 mm long lobe; outer indusium truncate-obtuse.
Discussion. Th is species is quite large and therefore often incompletely represented in collections. Rhizomes are usually missing and entire fronds are not preserved. Th e brightly colored, fi rm and large sori are very conspicuous on the dark green lamina. Th e majority of the specimens of Orthiopteris fi rma are from New Caledonia, except for the two specimens cited in the protologue and a single specimen from Fiji (Betche s.n.). All these represent records more than 100 years old for each respective location (collecting date is neither mentioned in literature nor indicated on specimen labels but collectors lived before 1913). For at least one of these specimens, a mistake in labelling is likely, as a similar specimen (MacGillivray s.n. B 200157509) is indeed labelled as originating from New Caledonia. All recent collections of O. fi rma are from New Caledonia, and therefore O. fi rma is best considered as an endemic for New Caledonia. Kuhn (1869) described Saccoloma moluccanum var. fi rma based on two specimens: Herus 85 (Aneityum, New Hebrides) and MacGillivray s.n. (Erromango, New Hebri- des, B200157508). Our study concludes that they belong to diff erent taxa. Herus 85 is O. campylura var. laxa, MacGillivray s.n. is this taxon, although probably with an erroneous location, and is here selected as the lectotype for Saccoloma moluccanum var. fi rmum to maintain nomenclatural stability. ( Description. Rhizome erect, rising at least 5 cm above ground, diameter 1.5-2 cm. Rhizome scales pseudopeltate-peltate, 1.5-3.0 × 0.5-1.3 mm, narrow lanceolate with long sinuose acumen, thick. Fronds 110-150 × 100-150 cm (length fairly equal with width); stipes slender, 30-50 cm long, 0.4-0.6 cm across (at base), dark brown; lamina rhomboid-deltoid, widest at 3-5 cm above the base, tripinnate to quadripinnate (lowest lobe of ultimate segments free or nearly so), 60-110 × 140-150 cm, papyraceous, thin, dull brown-yellowish green when dry, glabrous; pinnae at 45-50° to rachis, largest at the second from base, overlapping, stalk 3 cm, including stalk 30-50 × 10-15 cm, lanceolate, fi rst acrosopic, sometimes fi rst basiscopic pinnule of the lowest pinnae enlarged; ultimate segments 3-5 × 1.5-2.5 cm, 1-2 mm stalked, ovatetrapeziform, with strongly asymmetric base, lowest lobe almost completely separated, apex obtuse, margin with weak cartilaginous border; shallowly incised to 1.5-2.5 mm from veins; lobes rounded, veins in lobes 8-9 forks, dark brown, not contrasting with lamina, percurrent. Scales on rachis a few hair-like scales only on veins (few scales on an entire frond), hair-like. Sori lateral on lobes, symmetric, not refl exed, sometimes concave with lamina wings recurved, 0.8-1.1 × 0.5-1.0 mm, wide funnelformobovate, sometimes narrow funnelform, widest at mouth or just below mouth; inner indusium dull brown, papyraceous, thin but tough, with swollen joint at base with distinct dark line at the joint, 1/2 -2/3 as long as outer indusium, apex emarginate and irregularly eroded, not extending into a lobe; outer indusium truncate to obtuse; sporangia 10-17 per sorus, capsule globose and rounded at apex, gradually narrow edtoward base, indurated annulus cells 18-24, unequal in size; spores in polar view 30-38 μm, in lateral view 22-25 μm.
Ecology. Terrestrial in moist, shady, evergreen forest, on laterite soil derived from gneiss or in lowland dense disturbed forest with bamboo and Acanthaceae, border of the creek etc., at 350-1700 m altitude.
Discussion. Orthiopteris henriettae is the only representative of the genus in Madagascar, where it is not rare. It is clearly distinct from the Malay-Pacifi c species by its fronds having a papyraceous and thin texture, the ovate-trapeziform ultimate segments with shallowly crenate-dentate margin and usually swollen joints in the veins just below sori. Th e ultimate segments seem to be narrower in collections from higher altitudes. urn:lsid:ipni.org:names:77148375-1 Figs 2c, 3t, 3u, v, 4g, h, 6g, h Diagnosis. Diff ers from all other Orthiopteris species in relatively dense scales on lower surface of the lamina.

Orthiopteris tenuis
Distribution. Endemic to Fiji (Viti Levu, Vanua Levu, Ovalau). Ecology. Terrestrial, dense forest, bank along stream, at 0-1000 m altitude. Discussion. Th is species is highly variable in terms of frond dissection, and sorus shape. Plants from higher altitudes (above ca. 500 m) have larger fronds and furthermore diff er from the lowland plants in ultimate segments being deeply incised (distance of lamina from base of sinuses to costules less than 0.5 mm), and sori with almost equally long inner-and outer indusium. In contrast, the lowland plants have ultimate segments more shallowly incised (distance of lamina from base of sinuses to costules more than 0.5 mm), and sori with a large diff erence in length between inner and outer indusia. We could not separate the two forms because of the presence of intermediate specimens.  Description. Rhizome erect. Rhizome scales not seen. Fronds 120-160 × 40-50 cm; stipes stout, 40-50 cm long, 0.4-0.6 cm across (at base), dark brown; lamina deltoid, widest at base, tripinnate to quadripinnate, 100-120 × 40-50 cm, herbaceous, dark brownish green when dry, glabrous or with few scattered scales; pinnae at 30-35° to rachis, largest at base, overlapping, stalk 0.5 cm, including stalk 15-25 × 6-9 cm, lanceolate, fi rst basiscopic pinnules of lowest pinnae enlarged; ultimate segments 1.0-1.5 × 0.5 cm, sessile or very short stalked, trapezoid, apex acute, margin with weak cartilaginous border; almost completely dissected to less than 0.2 mm from veins; lobes narrowly oblong, veins in lobes unbranched or with 1 fork, dark brown and not contrasting with lamina, percurrent. Scales on rachis mostly at base of pinnae or pinnule, very few on veins, hair-like. Sori lateral or apical on lobes, symmetric, slightly refl exed, slightly concave with lamina wings slightly recurved, 1.0-1.2 × 0.6-0.7 mm, funnelform, widest at mouth, not wider than the sterile lamina below sorus; inner indusium dull brown, fi rm, 4/5-2/3 as long as outer indusium, apex truncate; outer indusium truncate; sporangia 7-12 per sorus, capsule globose and rounded at apex, gradually narrowed toward base, indurated annulus cells 16-20, ±equal; spores in polar view not studied, in lateral view .
Distribution. Papua New Guinea (Idenburg River). Ecology. Terrestrial in bottom of ravines, rain forest, at 1800 m altitude. Discussion. Th is species can be mistaken for Orthiopteris cicutarioides because the frond morphology is similar, with fronds very fi nely dissected in both species. However, O. trichophylla is more fi nely dissected with a single vein per lobe (similar to O. ferulacea), while O. cicutarioides has 2 or 3 one veins per lobe. Th e sori and indusia of O. trichophylla resemble those of O. campylura var. kingii, being funnelform and slightly refl exed, and the possibility cannot be excluded that O. trichophylla is locally derived from O. campylura var. kingii. Th e single specimen we examined (Brass 12239) diff ers slightly from the type (studied from scanned image of Brass 12027) by its shorter lobes. However, the sori and indusia are identical, and they were collected on the same day and at the same locality. Unlike in O. trichophylla, which may represent a similar case of a locally derived taxon, both specimens of O. cicutarioides look very productive with many ripe sporangia spreading over the mouth of the sorus. Brass noted that the species was very common and abundant at the collecting site (Idenburg river), but we have not seen any later collections than Brass's in 1939. Perhaps it is just abundant locally, and it may well be currently threatened.  (1828), for which the accepted name is now Tapeinidium moluccanum (Blume) C.Chr, Gard. Bull. Straits Settlem. 4: 399. (1929). For more details of this misapplication see De Joncheere (1984).