A revision of the Malesian genus Blumeodendron ( Euphorbiaceae )

The genus Blumeodendron (Euphorbiaceae) comprises nine species and is distributed from the Andaman Islands and Myanmar in the west through Malesia to the Bismarck Archipelago in the east. Two species are newly described, B. gesinus, with ridged fruits, and B. endocarpum, with a thickened endocarp around each seed. Three former synonyms, B. novoguineense (new name for Bennettia papuanum), B. philippinense and B. subrotundifolium, are reinstated as species. Two important characters were newly discovered, the presence of small lepidote hairs in all species and the indehiscent fruit of B. endocarpum


INTRODUCTION
Blumeodendron (Müll.Arg.)Kurz is a tree genus in the Euphor biaceae, which ranges from the Andaman Islands and Myanmar in the west through Malesia to the Bismarck Archipelago in the east.Blumeodendron belongs to the subfamily Acalyphoideae, tribe Pycnocomeae, subtribe Blumeodendrinae (Webster 1994, 2014, Radcliffe-Smith 2001) and is part of clade A1 of the core acalyphoids in the molecular Euphorbiaceae skeleton phylogeny of Wurdack et al. (2005).Clade A1 is sister to a clade combining Macaranga Thouars and Mallotus Lour.(including Trewia L.).The species are common in rain forests and are small to large (up to 65 m high) trees.Other typical characters are the absence of stipules, the presence of very small lepidote hairs (termed minute stellate hairs by Radcliffe-Smith 2001), small, unisexual flowers lacking petals, the staminate ones with many stamens and disc glands forming a ruminate pattern on a convex receptacle, the fruits large, woody and probably indehiscent or late dehiscent (partly after Merrill 1920, Airy Shaw 1975).
During the last 150 years the genus was studied by various researchers, but most revisions are already quite dated, the only 21st century revision was for Thailand (Chayamarit 2005(Chayamarit , 2007)).The genus Blumeodendron was established by Müller in 1866 as a subgenus of Mallotus.In 1874 Kurz raised Blumeodendron to genus level when he studied B. tokbrai (Blume) Kurz.The description of this species was followed by several others (e.g., Merrill 1920).In 1975 Airy Shaw reduced the then known twelve species to six species after a revision of the Bornean Euphorbiaceae.After Airy Shaw's revision most species appeared to be present on Borneo and only two were widespread outside Borneo, B. kurzii (Hook.f.) J.J. Sm. and B. tokbrai.A revision of Blumeodendron, covering its complete distribution, has not yet been made.Since the last revisions much more material has been accumulated, which will allow for new insights into the variability of the various species and which will perhaps alter species boundaries.
The variation within Blumeodendron is very high, especially in the former circumscription of the two widespread species.It is typically a genus where it takes time to become familiar with the species before a sensible delimitation can be made.As a result, the species circumscriptions have changed dramatically.The definition of the widespread B. kurzii and B. tokbrai is much more restricted as B. borneense Pax & K.Hoffm.(with B. con color Gage as synonym), B. novoguineense Ottens & Welzen and B. subrotundifolium (Elmer) Merr.(with the seemingly distinct B. calophyllum Airy Shaw as synonym) are regarded as distinct species.Thailand now contains three instead of two species (www.nationaalherbarium.nl/thaieuph).Also, two species were not recognized before, B. gesinus Ottens, with reddish leaves and fruits and distinct rims on the fruits, and B. endocarpum Ottens & Welzen, with a thick endocarp around each seed instead around all seeds.Characters used for species recognition are indumentum, leaf aestivation, thickness and colour of dried leaves, inflorescence length and fruit type.The revision will be part of the ongoing revision of the Euphor biaceae for the international Flora Malesiana Project (www.nationaalherbarium.nl/euphorbs).
The aims of this study are to revise the genus, to capture the species variability, show the distributions and to create an identification key.

Nodes
In a number of Blumeodendron species the leaves are on the nodes of several successive short internodes, which can be extremely short and individually indistinguishable in the species with 'whorled' leaves.The short nodes alternate with much longer, leafless internodes.The nodes of the species B. borneense, B. bullatum Airy Shaw, B. endocarpum and B. kurzii are much thickened; those of the other species are less thickened.Leaves of B. bullatum and B. endocarpum are alternate to subopposite and the node is thickened at the side of the leaf attachment.The nodes of B. kurzii are very distinctly thickened, almost globular in shape, and carry whorls of more than three leaves.The leaves of B. borneense are alternate in semi-whorls, with globular or one-sided thickenings of the nodes, respectively.The thickened nodes at the side of the leaf attachment of B. borneense resemble most closely those of B. endocarpum, less those of B. bullatum.The other species have alternate to subopposite (to three whorled) leaves and less thickened nodes.

Indumentum
All species, except the hairy B. bullatum, appear to be glabrous, but high magnification shows that they all possess very small lepidote hairs (called minute stellate hairs by Radcliffe-Smith 2001).In many descriptions these were overlooked.Young parts of the plant are totally covered with these small, yellow to orange lepidote hairs and, as a result, may even have an orange glow.Probably, the lepidote hairs have a secretory function as some specimen labels indicate stickiness and young parts may look lacquered when dry (or seem to have a layer of glue after dehydrating with boiling water).The hairs disappear with age, but on buds, fruits and in the axils of adult leaves the hairs are more resistant, though on the bark they become obscured by the formation of secondary bark, lenticels and often by fungal infections (probably due to the sweet secretion).

Leaf morphology
-Stipules are absent.Quite often stipules are very early caducous in Euphorbiaceae, but then small scars remain, and neither these, nor the presence of stipules near young leaves, were observed.
-The petioles are bipulvinate and mostly transversely grooved when dry.
-The leaves are generally elliptic to somewhat ovate or obovate.The colour of the dry leaves varies with the species and is often quite typical.-The large variation in dimensions of the leaf blade, most extreme in B. kurzii and the closely similar B. subrotundi folium, and the little variation between the species complicates the identification of the species.

Extrafloral nectaries
All species have two round (indistinct) extrafloral nectaries near the base of the leaf on the upper surface and usually also additional ones between the secondary nerves along the midrib and the margin.The number of nectaries along the midrib and margin is variable (up to 20(-40)) and not typical for a species.
The nectaries occur on both surfaces, but in different numbers.
The basal ones are generally larger than those along the midrib and margin and are sometimes visible to the naked eye.

Inflorescences
All the inflorescences resemble racemes but are thyrses (reduced cymes racemosely distributed along the inflorescence rachis).Bracts are generally absent or early caducous.

Flowers
The pedicel has a distinct abscission zone and flowerless inflorescences are often the result.In B. novoguineense and B. tokbrai the abscission zone can be halfway the pedicel giving an almost ladder-like appearance after flower drop.The buds are globose.The staminate flowers have 3-4 sepals, the pistillate flowers (3 -)4-5 sepals; they lack petals.
Very typical for the staminate flowers are the disc glands which provide a ruminate appearance on the dome-shaped receptacle.The many stamens arise among the glands.The amount of stamens varies per species.The anthers are basifixed, 2-thecate, and open latrorse via lengthwise slits.A pistillode is absent.
The pistillate flowers have a circular, somewhat lobed, broad disc.The ovary is 2-3-locular with a single ovule per locule and on top 2-3 non-divided, recurved stigmas that are papillate above.

Fruits and seeds
The fruits show some key characters for identification.They are woody and globular to ovoid.Young fruits are often covered with the small lepidote hairs; on older fruits lepidote hairs are sometimes still visible.The upper part of the pedicel is thickened.Differences between the species can be found in the thickness of the wall, the thickness of the endocarp and the presence of ridges.
The wall of B. endocarpum is ovoid and dented in the middle of the upper margin (Fig. 3f), while the other species have very globular to ovoid fruits.Blumeodendron endocarpum differs in various ways from the other species; it has a thick endocarp surrounding every individual seed, while the endocarp encloses all seeds together in the other species (Fig. 3f).Another difference is that the exocarp of B. endocarpum separates from the meso-and endocarp during drying (Fig. 3f), while the layers remain stuck together in all the other species.Finally, there is a difference in the manner of dehiscing.The fruits of all species dehisce tardily loculicidally, while the fruits of B. endocarpum do not seem to open and probably the seed will germinate after the woody endocarp decayed.
The seeds are typical, more or less bean-shaped, though the shape varies somewhat per species, and are attached in the middle (in a dent) to (less typical) more subapical.
It is unknown how the diaspores are dispersed.The fruits are woody and large, thus bird dispersal is ruled out.The seeds are covered by a thin, mainly yellow sarcotesta, which could imply that larger animals, like monkeys, might consume the seeds and disperse them.Considering the broad distributions of some of the species, then dispersal by means of water/sea is also a possibility, as the fruits generally dehisce very late, are buoyant, and relatively thick-walled.Habitat & Ecology -In mixed dipterocarp lowland forest, secondary forest, alluvial forest, mossy forest, primary upper montane forest, often along water and on very wet (but not inundated) soil; soil on (sandy) clay, igneous derived sandy clay.Altitude: 25-700 m.Flowering: January; fruiting: February-May, July, September, October, December.
Notes -1.Quite typical for B. borneense are the light coloured twigs, of which the upper ones are flattened or triangular, the leaves that dry light green, especially the lower surface, the almost fascicled flowers (one specimen in bud seen), and the thin-walled fruits (wall 2 mm at most).Blumeodendron borneense is mainly known from Borneo.In Borneo a group of specimens, B. tokbrai, dries dark green and resemble B. bor neense, but the leaves are alternate to (sub)opposite and seldom in whorls of 3 (end of branches), the flowers are along rachises and the fruits are very thick-walled (c. 5 mm).
2. The type of B. concolor, Curtis KD 1368 (K) from the Malay Peninsula, strongly resembles B. borneense, as the leaves are of the same size, elliptic and also dry green, the flowers are in fascicles.However, the leaves are alternate.Another example of a specimen with leaves alternate (but close together) or in pseudo-whorls is a cultivated specimen from Borneo in the Bogor Botanical Garden, Gravendeel, de Wilde & Hovenkamp 521 (Kebun Raya IX.C.144).As the leaves in Bornean B. born eense can also be in pseudo-whorls B. concolor is regarded as a synonym of B. borneense.
3. Specimens from Sarawak, including the type, and Brunei have a tendency to show ovate leaves, those of Sabah and Kalimantan are elliptic.Distribution -Borneo (Sarawak; only known from the type).
Note -Airy Shaw (1965) was not certain if this species belonged to Blumeodendron, but the absence of stipules, the ruminate staminate disc glands and the presence of orange lepidote hairs on the buds are all indicative of only Blumeodendron.Resembling B. subrotundifolium in short inflorescences and alternate to subopposite leaves, differing in leaves chartaceous (to coriaceous), drying greenish brown, very short pistillate pedicels and most of all, a thick endocarp around every seed, not around the seeds together.-Type: BW (Kalkman) 6282 (holo L), [Indonesia, Papua,] Div.W. New Guinea, Beriat, c. 12 km S of Teminaboean.
Notes -1.Gesinus is the first name of the first author's husband.The name is a personal name and not a latinisation, therefore ICN art.60C.4 applies (http://www.iapt-taxon.org/nomen/main.php?page= art60), the name should not be changed into gesinum.1 cm e 2. This new species was generally confused with B. tokbrai, because of the long inflorescences.Very typical are the rims on the fruits and their orangish colour when dry.The same colour can be found on the lower surface of the dried leaves.
3. The variation in inflorescence lengths seems to be large, varying between short (bud) to long (flowers), but inflorescences with buds are not yet fully grown and will largely extend during maturation of the flowers.

5.
Blumeodendron kurzii (Hook.f.) J.J.Sm.-Fig.5; Map 4 Blumeodendron kurzii (Hook.f.) J.J. Sm. (1910)  Trees, to 35 m high, bole to 30 m high, dbh to 60 cm; sometimes slightly fluted at base, flutes c. 1.5 m high, out 50 cm to sometimes a short buttress; flowering branches 4 -22 mm diam, round to sometimes triangular in section below the nodes, internodes up to 18 cm long; terminal bud surrounded by round or triangular axillary buds.Outer bark dark brown to brown-grey to greyish (black), smooth to cracked in irregular pieces to (powdery) scaly, soft to hard, 0.5 -6 mm thick; inner bark beefy red outside to (pale) reddish to brown inside, 3-6 mm thick, sap absent to clear; sapwood white, yellow, reddish or brown; heartwood yellowish red to pinkish brown (to rays brown).Leaves always in whorls of 3 -5 per node, young ones yellow-green to light green; petiole 1.3 -12 cm long, diam of Habitat & Ecology -Ranging from primary and evergreen forest to logged over and secondary forest (with bamboo); soil: often rich, varying from igneous derived sandy soil to sandy clay to loamy soil to limestone; bedrock once reported as basalt.Altitude leaves are used by the Dusun in N Borneo as rain shelter and to repair leaks in roofs.The seeds are eaten in the Philippines.
Note -Typical are the brown drying leaves present in pseudo-whorls: leaves in a whorl but originating at slightly different levels.widened nodes at end of short nodes, alternate to subopposite to in pseudo-whorls of 3; petiole 1-4.1 cm long, diam of thinnest part 0.8 -1.2 mm, round, basal pulvinus 1.3 -2 mm diam, fast fading orange lepidote hairs; blade (ovate to) elliptic, 5.3-17.5 by 2.5 -9 cm, length/width ratio 1.5 -2.6, pergamentaceous to coriaceous, symmetric, glabrous, base (broadly) cuneate, margin recurved, apex acuminate, tip rounded, extrafloral nectaries on both surfaces along midrib, 2 to many, along margin several, both surfaces smooth, mid to dark green when fresh, dull and lighter beneath, drying brownish green, slightly darker brown underneath; venation slightly raised on both sides, marginal vein indistinct, secondary nerves pinnate, 5-8 pairs, sometimes very parallel, at c. 52° angle with midrib, tertiary nerves more or less scalariform, perpendicular to midrib, higher order nerves indistinct, reticulate.Inflorescences axillary, mostly single, staminate rachises up to 9.5 cm long, 1-1.3 mm diam, pistillate ones up to 3 cm long in flower, up to 9 cm when in fruit, 1-1.5 mm diam, thickening during fruit set to c. Fruits capsular, flattened obovoid, angular (perhaps not ripe yet) with often slightly raised suture, 2-2.9 cm wide by 2-2.9 cm high; pedicel c. 3 mm long, abscission zone subbasally; wall 1-1.8 mm thick, brown when dry, surface somewhat rugose; endocarp enclosing all seeds; stigma mostly persistent.Seeds bean-like to flattened at one side, c. 1.9 by 1.3 by 1 cm, attached in middle, black.Distribution -New Guinea.
Wood -Sapwood not defined from heartwood, white to strawcoloured, close grained, medium hard to hard, medium heavy to heavy.Pores few, small, visible to naked eye, short radial chains.2. This species closely resemblances B. tokbrai, but differs in the size and form of the fruits, smaller (2 -2.9 by 2 -2.9 cm vs 2.3 -4.8 by 2.3 -4.1 cm) and often angular and with slightly thickened sutures (vs round, without thickened sutures), the thickness of the fruit wall is thinner (1-1.8 mm vs 4 -7 mm) and the presence of broader sepals in the pistillate (1.4-2 mm vs 0.5 -1.1 mm) and staminate flowers (2.5 -3.5   Note -Distinctive for this species are the alternate, coriaceous leaves and the very short inflorescences.The short inflorescences are reminiscent of B. kurzii (leaves in whorls) and alternate leaves are found in various species, but all with longer inflorescences except for B. borneense from the Malay Peninsula, but the latter form has light green dried leaves instead of brown dry leaves.(Elmer) Merr.-Fig.8; Map 6
2. Blumeodendron calophyllum is added here as a synonym of B. subrotundifolium.Most specimens can easily be divided over both species as they look spectacularly different.Small, coriaceous leaves with slender petioles and more axillary smaller fruits are present in typical B. subrotundifolium, while much larger, very coriaceous (not bendable) leaves with thick petioles and cauliflorous large fruits are found in B. calophyllum.However, quite a number of specimens bridge the gap between both typical forms (see Table 1).Both forms are generally high trees with (very) coriaceous leaves on relatively long petioles, which are dry dark shiny brown above and dull brown underneath.Leaf sizes also vary strongly in B. kurzii, a species with which B. subrotundifolium was often confused.
They are variable in length, while the lengths are very typical for the species (pistillate inflorescences are always shorter than staminate ones).Almost fascicle-like inflorescences of less than 2 cm length, are found in B. borneense, B. bullatum, B. kurzii and B. philippinense.Longer inflorescences, staminate ones up to 4.5 cm, pistillate ones up to 2.5 cm, are present in B. endocarpum and B. subrotundifolium.The longest inflorescences are present in B. gesinus, B. novo guineense and B. tokbrai (staminate ones up to 20 cm, pistillate ones up to 10 cm).The basal internodes of the longer inflorescences are longer than the more terminal internodes as can be seen in B. tokbrai.Pistillate flowers are single per node, staminate flowers are generally in small groups, with one flower open and the others generally present as buds.
The number of inflorescences per node also varies.Pistillate inflorescences are single except B. kurzii with c. 4 inflorescences per node.Staminate inflorescences are single (B.bullatum), paired (B.endocarpum, B. gesinus and B. subrotundifolium) or vary between 3 and 4 (B.tokbrai and B. philippinense) to 8 inflorescences per node in B. kurzii.The latter probably as a result of having mostly four whorled leaves and multiple inflorescences per leaf.