Tetrameranthus (Annonaceae) revisited including a new species

Abstract The taxonomic revision of the infrequently collected genus Tetrameranthus by Westra (1985) is updated. A new species is described from French Guiana and Amapá, Brazil, increasing the number of species in this genus to seven.


Introduction
An as-yet unknown species of the rare genus Tetrameranthus has been collected a few times in French Guiana and also once in neighboring Amapá, Brazil. Th e material was too incomplete to justify publication. Recently a new collection from French Guiana came in bearing ripe fruits and also reported to have a white fl ower. Th is made us decide now to formally publish this new species. We then also decided to update the revision of the genus Tetrameranthus (Westra, 1985), with the inclusion of T. globuliferus published later (Westra, 1988), adding the present new species as well. Some, mostly color, photographs of this seldom collected genus serve as an illustration.

Taxonomic history
Th e Annonaceae form a large pantropical family, the largest family in the order Magnoliales, currently with (about) 129 genera and >2000 species (Stevens 2001 onwards). In the Neotropics the family is represented by 40 genera and c. 900 species . Annonaceae are woody plants, mostly trees and shrubs; lianas are mainly found in the Old World, only few lianas occur in the New World. Th e family is very distinctive and generally easy to recognize by, among others, simple leaves placed in two rows and without stipules, fl owers with perianth members in 3-merous whorls, many tightly packed stamens, and a varying number of free carpels that remain free or become fused in fruit.
Th e Neotropical genus Tetrameranthus was described by Fries (1939) with the only species T. duckei R.E.Fr., It is aberrant by, among others, the unusual leaf disposition in a spiral instead of in two rows, the presence of four bracts placed in a whorl under the articulation of the fl ower stalk, and, above all, the perianth consisting of 4 sepals and 2 whorls of 4 petals each. Th e position of this peculiar genus is discussed by Fries in that paper, placing Tetrameranthus in an isolated position within the Annonaceae.
Over fi fteen years later Fries added a second species, T. macrocarpus R.E.Fr., from Southeastern Colombia (Fries 1957). In his large survey of the whole family Fries even more emphasized the isolated position in placing it as the only member in a tribe Tetramerantheae in subfamily Annonoideae (that also included Uvarieae and Unoneae) (Fries, 1959).
Four more species were added in later years, viz. T. laomae D.R.Simpson from Eastern Peru (Simpson 1975), T. pachycarpus Westra from the environs of Iquitos, Peru, T. umbellatus Westra from northern Amazonian Peru, and T. globuliferus Westra from Yasuní National Park, Ecuador (Westra 1985(Westra , 1988. Gradually more material was collected, particularly around Manaus (T. duckei), and near Iquitos (T. pachycarpus). Outside these areas of concentration mainly collections from scattered localities have come in spanning a range from Andean Amazonia and the Pacifi c coast of Colombia (Chocó: one collection) in the West to French Guiana and adjacent Amapá, Brazil, in the East -including now the newly described Tetrameranthus guianensis in this paper. With the notable exception of the locally common T. duckei, Tetrameranthus as a whole still must be regarded as a rather rare genus.
Based on recent molecular data it was shown that Tetrameranthus belongs to an early branching lineage within Annonaceae (Richardson et al., 2004;Couvreur et al., 2011;Chatrou et al. in press). It is classifi ed in the subfamily Ambavioideae Chatrou, Pirie, Erkens and Couvreur (Chatrou et al. in press). Within this subfamily the South American genus Tetrameranthus is part of a highly supported clade together with the Southeast Asian genus Mezzettia and the African genera Ambavia and Cleistopholis. Recent analyses show Tetrameranthus in a fully resolved clade as sister to the other three above mentioned genera (Surveswaran et al. 2010;Chatrou et al. in press).
Th e generic name is composed of the Ancient Greek word elements "tetra" (four), "meros" (part), and "anthos" (fl ower), referring to the four-parted fl owers.

Vegetative part
Tetrameranthus is a genus of shrubs to (large) trees. As for all Annonaceae, the leaves are simple, entire, pinnately veined, symmetrical, and lack stipules, generally of moderate to fairly large size (greatest length ±30 cm). In contrast to the rest of Annonaceae, where the leaves are in two alternate rows almost without excep tion (Fries 1959: p. 8), in all species of Tetrameranthus the leaves are spirally arranged. Another uncharacteristic feature of this genus is the apical disposition of the leaves, generally found 10 cm from the apex of the branches, the ones below that are shed.
Th is rosette-like appearance of leaf disposition is suggestive of a number of other plant families such as Sapotaceae, but not of Annonaceae. Th is could explain in part why Tetrameranthus might seem rare, i.e., simply because many botanists do not identify it as Annonaceae.
lnflorescences Infl orescences in Tetrameranthus are truly axillary. As for the structure of the infl orescence in Annonaceae in general, the reader is referred to publications by Fries (1919Fries ( , 1959. Tetrameranthus conforms to Fries's type 1 (1959: p. 13) in that it has a primary fl ower stalk which carries bracts below the articulation, but no bracts above it. Seen more closely, the infl orescence structure is somewhat unusual within Annonaceae. Single-fl owered infl orescences, as most commonly seen in Tetrameranthus, appear as an articulate stalk bearing the fl ower. Th e articulation in all but one species is at some distance above the base (the leaf axil; see e.g. Figures 3A, 3E). Th e only exception is in T. laomae where the articulation is found at the base (see Figure 2E). Immediately below the articulation there are (mostly) 4 bracts in a whorl. Th e bracts are shed before or (shortly) after fl owering. In T. duckei a fl ower is sometimes seen originating from the axil of one the bracts, thus creating a 2-fl owered infl orescence ( Figure 2A). Th e pedicel of that lateral, or second-order, fl ower has an articulation at the base and lacks bracts. In T. umbellatus all four bracts have the potential to develop a similar axillary fl ower, thus resulting in an umbel-like infl orescence ( Figure  2G). Pedicels of lateral fl owers being bractless, infl orescences of Tetrameranthus are static: they cannot expand by reiterative growth processes as is characteristic for the rhipidium in most Annonaceae. Th e infl orescence of Tetrameranthus is best circumscribed as a botryoid (Weberling and Hoppe 1996: p. 32-33), albeit mostly reduced to a single fl ower.
For these reasons the basal part of the fi rst-order fl ower stalk up to the articulation and including the whorl of bracts is referred to as peduncle, while the part above the articulation is termed pedicel. Th e stalks of second-order fl owers, then, are termed pedicels in their entirety.

Flowers
As in most Annonaceae, the perianth consists of one whorl of sepals and two whorls of petals ( Figure 1A). Th e whorls are 4-merous in at least fi ve of the seven species, although incidentally a single deviating fl ower might occur, e.g. a 3-merous fl ower on one specimen of T. laomae, and a 5-merous fl ower on the type collection of T. pachycarpus. Such phenomena are not unusual throughout fl owering plants in general, and have been observed in other Annonaceae genera (Couvreur 2009). T. globuliferus appears exceptional by having 6-merous whorls as far as seen, but this may need confi rmation from more collections yet to be made. No good fl ower has been collected in T. guianensis so far, but see under the notes with that species. It should be stressed that in all other genera where deviations from trimery occur, this is an autapomorphy for individual species. In Tetrameranthus, however, this is synapomorphic for the genus (see also Saunders 2010).
Th e sepals are small in relation to the petals. Th ey are free or connate just at the base. Th e aestivation is imbricate, only observable in very young buds as the sepals soon spread. Th e sepals drop after fl owering.
Th e petals vary from rather fl eshy (e.g. T. duckei, Figure 2C) to rather thin (T. laomae, T. umbellatus, Figure 2F), those of the outer whorl being somewhat larger or broader than those of the inner whorl. Th e photographs also show curved petals in T. duckei in the living condition, while in T. umbellatus (and possibly also in T. laomae) the petals appear rather fl at at least before anthesis. Th e petals are adorned with a callus or callus-like tissue at the base on the inner side: this is an area of varying size, depending upon the species, which is devoid of indument. In T. duckei the callus appears as a protruding hump ( Figure  2C), particularly on the inner petals where it is even larger than on the outer petals. In the other species the callus is smaller in relation to the size of the whole petal than in T. duckei.
Th e convex torus bears mostly numerous stamens and a mostly rather small number of free carpels in the center. Th e stamens have a short fi lamental part, a thick connective capped by a massive, more or less conical or fl at shield, and an extrorse to latrorse anther. Th e carpels contain two (exceptionally three), lateral, superposed ovules, and have on top a sessile stigma which varies from trilobed to an irregularly lobed disc.
Curculionidae beetles have been observed as pollinators in T. duckei (Webber 1981;Gottsberger 1999). Th ere are no reports known to us so far for other Tetrameranthus species.

Fruit
Depending on the species, the number of free monocarps varies from 1-15. Th e ellipsoid to oblongoid monocarps are fl eshly, indehiscent, and two-seeded or, due to abortion of one ovule, one-seeded (rarely three seeds develop) ( Figure 1C-G). Th e seeds are laterally attached, with the lowest one near the base, and are ascending, thus resulting in the characteristic oblique constriction seen in monocarps with >1 seed on herbarium specimens. In fresh fruits the constriction is less obvious, and in very thick-walled monocarps of some of the species (e.g. T. guianensis, T. pachycarpus) it becomes practically indistin-guishable. In herbarium material the fruit wall is smooth in most species, but becomes shriveled in T. globuliferus (Westra 1988: pp 269, 278, Fig. 21) and T. guianensis.
Th e seeds are quite large in relation to the fruit body; they are slightly com pressed dorsiventrally, and possess ruminations in the shape of fairly numerous lamellae protruding from the seed coat into the interior almost to the middle.

Indument
Th e indument of Tetrameranthus consists of stellate hairs with 2-10 rays, varying with the species. In addition to stellate hairs, simple hairs are present in varying densities, also depending upon the species. Most genera of Neotropical Annonaceae have simple hairs, or have stellate hairs beside simple hairs in a small percentage of the species only (e.g. Annona including Rollinia). Th e notable exception (apart from Tetrameranthus) is Duguetia: in this genus most species even have scales, rather than stellate hairs (Maas et al. 2003).
Indument in Tetrameranthus is found especially on young vegetative parts and infl orescences. Some of it persists on the primary vein of the leaves, and to a lesser extent on the secondary veins, mainly on the lower side; it is also seen on petioles and branchlets in the leafy zone. In T. umbellatus stellate hairs are also found diff usely spread over the leaf surface, especially on the abaxial side. In T. laomae, too, scattered stellate hairs may be spotted on the lower leaf surface.
Floral parts, with the exception of stamens and the callus area on petals mentioned earlier, are usually covered with a dense indument of stellate hairs. Carpels, when enlarging into monocarps, quickly become glabrous.
Th e trichome length on vegetative parts (except in a very young stage, and persisting near axils) does not exceed 0.1-0.2 mm in T. laomae and T. umbellatus: these two species thereby are easily distinguished from the other ones, where considerably longer (to 0.5 mm, or even more) and stiff er trichomes are found, next to simple hairs of the same size. Trichomes on infl orescences and fl ower parts may reach a somewhat larger average size than those on vegetative parts (this we did not investigate in detail). Type. Tetrameranthus duckei R.E.Fr. Description. Trees or shrubs. Leafy twigs and most fl oral parts sparsely to densely covered with stellate to simple hairs to glabrous. Leaves spirally arranged, often concen-trated towards the end of the branches, primary vein impressed to slightly raised on the upper side. Infl orescences axillary, 1-fl owered to several-fl owered and umbel-like, bracts up to 4 below the articulation. Flowers bisexual, 4-merous or less often 5-6-merous, white to yellow or cream; sepals 4(-6), imbricate, free or basally connate; petals 8(-12), free, subequal, imbricate, much longer than the sepals, often with a callus at the inner base; stamens numerous, connective shield discoid, either fl at, cushion-shaped, or with a conical prolongation; carpels c. 5-30, ovules 1-2(-3), lateral, stigma sessile, more or less lobed. Fruit apocarpous; monocarps 1-15, free, sessile or sometimes narrowed into a short and thick stipe-like base, indehiscent, sometimes constricted, wall rather thick (1-7 mm) and fl eshy. Seeds 1-2(-3) per monocarp, lower one near the base, upper one(s) lateral.

Genus
Distribution. Seven species in the Amazon regions of Venezuela, Colombia, Brazil, Peru, and Ecuador, but also in the Colombian state of Chocó and in French Guiana and neighboring Amapá, Brazil. Description. Shrub or tree, 3-12 m tall, 4-8 cm diam., young twigs and petioles densely to rather densely covered with brown, stellate hairs >0.5 mm long, becoming glabrous. Leaves: petioles 10-40 mm long, 1.5-4 mm diam.; lamina narrowly elliptic to narrowly obovate, 10-25 by 3-10 cm (index 2.7-4), chartaceous to coriaceous, dull or slightly shiny brown or greenish brown above, dull brown or greenish brown below in sicco, rather densely covered with stellate hairs on primary vein, otherwise glabrous above, rather densely to sparsely covered with stellate hairs on primary vein and secondary veins, otherwise mostly glabrous below, the stellate hairs similar to those on branchlets, base acute, apex acuminate (acumen 5-25 mm long), primary vein impressed above, secondary veins 8-12 on either side of primary vein, impressed above, loop-forming, shortest distance between loops and margin 1.5-5 mm, or not loop-forming in basal part, tertiary veins slightly raised, fl at, or indistinct above, percurrent to reticulate. Infl orescences 1(-2)-fl owered, peduncles 5-15 mm long, c. 1.5 mm diam., fruiting peduncles to c. 3 mm diam., bracts 4, narrowly triangular, 3-6 mm long, soon falling after fl owering, pedicels 10-25 mm long, c. 1.5 mm diam., fruiting pedicels to c. 40 mm long, 3 mm diam., peduncles and pedicels densely covered with stellate hairs, becoming glabrous. Flowers green, turning yellow in vivo; sepals elliptic to obovate, free, 5-7 mm long, outer side densely covered with stellate hairs; outer petals ovate, 20-25 by 9-12 mm, inner base with fl eshy and longitudinally grooved callus 5-6 mm long and extending across the whole width, inner petals narrowly ovate to ovate, 15-22 by 6-9 mm, with similar callus to c. 8 mm long, outer side of petals densely covered with stellate hairs, the callus on the inner side glabrous; stamens 2-2.5 mm long, connective shield conical or acuminate, 1-1.5 mm long, more or less curved toward the center. Monocarps 1-6, green or shiny green, turning green-yellow in vivo, brown to dark brown in sicco, ellipsoid or oblongoid to narrowly so, 25-65 by c. 20(-25) mm, with (2-seeded forms) or without oblique constriction, apex a thick obtuse beak 2.5-10 mm long.  Note. In a previous paper (Westra, 1985) there was some doubt about the identity of the collection Lleras et al. P17302. It should be regarded as no more than an extreme form of T. duckei, with pedicels to c. 40 mm long and outer petals to c. 15 mm wide. Description. Medium-sized tree, >10 cm diam., young twigs and petioles densely covered with pale brown, stellate hairs >0.5 mm long. Leaves: petioles 4-8 mm long, 4-6 mm diam., lamina narrowly obovate, 27-37 by 9-15 cm (index 2.8-2.9), chartaceous, shiny green above in vivo, greenish brown above, pale greenish brown to brown below in sicco, rather densely covered with stellate hairs >0.5 mm long on primary vein, to rather sparsely so on smaller veins on both sides, base acute to attenuate, to obtuse or rounded at the extreme base, apex acute to acuminate (acumen to c. 10 mm long), primary vein fl at to slightly raised above, secondary veins 20-25 on either side of primary vein, fl at to impressed above, loop-forming, shortest distance between loops and margin 1.5-3 mm, or not loop-forming, tertiary veins fl at to raised above, percurrent to more or less reticulate. Infl orescences 1-fl owered; peduncles 3-5 mm long, 3-4 mm diam., fruiting peduncle c. 5 mm diam., bracts [4?] narrowly oblong or narrowly triangular, 4-5 mm long, falling after fl owering, pedicels {18-30} mm long, {4-6} mm diam., densely covered with brownish, stellate hairs; fl owers with perianth in 6-merous whorls, cream with the inner petals yellow at the inner base in vivo; sepals broadly ovate-triangular, connate at the very base, {6-11} by {5-10} mm; outer petals elliptic to ovate, {30-45} mm long, {10-25} mm wide, with small callus at the inner base; inner petals {30-40} mm long, {5-10} mm wide, more or less narrowed toward the base, with larger callus, outer side of petals densely covered with stellate hairs, the callus on the inner side glabrous; stamens {2-2.5} mm long, connective shield fl at, cushion-shaped. Monocarps 2-7, globose or almost, green in vivo, brown in sicco, c. 40 mm diam., wall strongly shriveled in sicco. Seeds 1-2 per monocarp, 25-30 by 15-20 mm.

Key to the species of Tetrameranthus
Distribution. Ecuador (Orellana). Only known so far from Parque Nacional Yasuní.
Habitat and ecology. In rain forest on terra fi rme. At elevations of 200-400 m. Note. Th e description of the fl ower was largely made from a very recent photograph of a freshly collected twig of Pérez & Santillán 4404 (QCA). Measurements between { } were made on two fl owers preserved in alcohol kept in QCA and were kindly supplied to us by Álvaro J. Pérez C.
Á. J. Pérez also reports to us a clustered occurrence of T. globuliferus: he found few individuals all close to the one that he collected, but did not spot any more around the trails of the Yasuní Scientifi c Station. Th e species has been listed as near-threatened on the IUCN red list (Muriel and Pitman 2003). In an important paper on global conservation signifi cance of Yasuní National Park T. globuliferus is documented as one of fi ve species (and one of only two woody species) not found anywhere else in the world (Bass et al. 2010 ; young twigs and petioles densely covered with brownish, stellate and simple hairs >0.5 mm long. Leaves: petioles 5-10 mm long, 3-4 mm diam., more or less thickened toward the base; lamina narrowly obovate to obovate-elliptic, 14-26 by 5-10 cm (index 2.4-2.9), chartaceous, shiny green above in vivo, dark brown above and pale brown below in sicco, rather densely covered mainly on large veins to rather sparsely covered with stellate hairs >0.5 mm long or glabrous elsewhere above, densely covered with stellate hairs on large veins, rather densely to sparsely so or almost glabrous elsewhere below, base acute to attenuate, apex abruptly acuminate (acumen 2-12 mm long), primary vein impressed above, secondary veins 14-19 on either side of primary vein, impressed above, loop-forming, shortest distance between loops and margin 1-3 mm, or not loop-forming, tertiary veins impressed above, percurrent to reticulate. Infl orescences 1-fl owered, only seen in postfl oral and fruiting stages, peduncles c. 10 mm long, c. 3 mm diam., fruiting peduncles to c. 5 mm diam., pedicels c. 20 mm long, c. 3 mm diam., fruiting pedicels to c. 5 mm diam., peduncles and pedicels densely covered with brownish, stellate and simple hairs; sepals not seen; petals whitish (fi de collectore) in vivo, estimated to be c. 35 by 40 mm; stamens not seen. Monocarps 7-15, ellipsoid to fusiform, yellowish green to yellowish orange in vivo, pale brown in sicco, 35-60 by 20-30 mm, apex obtuse, rounded, or bluntly pointed, with or without weak oblique constriction, wall shriveled in sicco. Notes. Tetrameranthus guianensis is the fi rst species of the genus reported from the Guianas. It is distinct from other species of Tetrameranthus by a dense cover of coarse stellate and simple hairs on all vegetative parts. Like the Ecuadorian T. globuliferus, it has shriveled fruit walls in dry condition.
As no complete fl owers were available in herbarium material, description of fl oral characters is based in part on fi eld observations of a single living fl ower at distance. Th e collector, D. Sabatier, has informed us that an attempt to collect that fl ower which was high up in a large tree and out of reach had failed. Sabatier (pers. comm.) notices 5 scars per whorl on the receptacle (compare Figure 3A) implying that we have a 5-merous fl ower here! Th is defi nitely requires confi rmation from further collections, though.
Two sterile collections, namely Mori et al. 23521, 23674, also from French Guiana, seem to come quite near this species, diff ering mainly in the leaf shape (obovateelliptic, rather than narrowly obovate), and the less dense and more coarse indument of stellate hairs of comparable size. It concerns trees of 8 m, 10 cm diam., and 15 m, 12 cm diam., respectively, from non-fl ooded moist forest. More material, and more complete in particular, is needed here.
Distribution. Colombia (Vaupés). Only known from the type collection. Habitat and ecology. Not recorded. Note. Th is single collection of Tetrameranthus macrocarpus seems to come quite near some forms of the variable T. duckei. It is distinct from the latter primarily by the larger fruit. Moreover, it is reported to be a tall tree (without more precise indication of size), whereas reports for T. duckei indicate a medium-sized tree to about 12 m tall so far. Nevertheless one might wonder if T. macrocarpus is merely an extreme form of T. duckei, but more extensive collecting in the western Amazon region is needed before this question could be answered. Description. Tree, 4-26 m tall, young twigs and petioles densely to rather densely covered with brown, stellate hairs >0.5 mm long, becoming glabrous. Leaves: petioles 20-30 mm long, 2-4 mm diam., slightly thickened toward the base, lamina elliptic, narrowly elliptic or narrowly obovate, 17-22 by 5-10 cm (index 2.1-3.4), coriaceous, brown in sicco, glabrous except for primary vein above, rather densely to sparsely covered with stellate hairs on large veins and otherwise sparsely covered with stellate hairs to glabrous below, base acute to attenuate, apex obtuse, acute, or acuminate (acumen 1-5 (rarely more) mm long), primary vein impressed to almost fl at above, secondary veins 10-15 on either side of primary vein, not loop-forming, or less often loopforming, shortest distance between loops and margin 2-3 mm, tertiary veins fl at and inconspicuous above, percurrent to more or less reticulate. Infl orescences 1-fl owered; peduncles 4-5 mm long, 1-2 mm diam., fruiting peduncles to c. 5 mm diam., bracts 2(-more?), narrowly triangular to linear-triangular, 3-5 mm long, outer side densely covered with stellate hairs, falling at or after fl owering, pedicels 10-15 mm long, 1.5-2 mm diam., fruiting pedicels to c. 25 mm long, 3-4 mm diam., peduncles and pedicels densely to rather densely covered with stellate hairs, becoming glabrous; fl owers yellow in vivo; sepals broadly elliptic, 3-4 mm long, connate at the very base, outer side densely covered with stellate hairs; outer petals narrowly elliptic to oblong, to c. 35 by 16 mm, outer side densely to rather densely covered with stellate hairs, the inner base glabrous, to c. 3 mm long, inner petals narrowly elliptic to oblong, somewhat smaller than outer petals and with slightly larger glabrous inner base; stamens c. 2 mm long, connective shield more or less conical and curved toward the center. Monocarps 1-3, yellow in vivo, brown in sicco, ellipsoid, 2-seeded forms to c. 70 by 40 mm, without or with inconspicuous, oblique constriction, apex rounded. Seeds 1-2 per monocarp, 30-40 by 20-28 mm.

Tetrameranthus pachycarpus
Distribution. Peru (Loreto), fairly common in the region around Iquitos, not known elsewhere so far.
Habitat  , young twigs and petioles densely to rather densely covered with stellate hairs <0.2 mm long, becoming glabrous. Leaves: petioles 5-25 mm long, 1.5-3 mm diam., lamina narrowly obovate or narrowly elliptic-obovate, 15-30 by 4-9 cm (index 2.4-4.7), chartaceous, greenish brown to brown above, pale greenish brown to brown below in sicco, sparsely covered with stellate hairs to glabrous above, rather densely to sparsely covered with stellate hairs on primary vein and sparsely covered to glabrous otherwise below, base acute to attenuate, decurrent along the petiole, apex acute to (abruptly) acuminate (acumen 5-10 mm long), primary vein fl at to slightly impressed above, secondary veins 13-20 on either side of primary vein, slightly impressed to raised above, loop-forming, shortest distance between loops and margin 0.5-2 mm, tertiary veins fl at to raised above, percurrent to more or less reticulate. Infl orescences up to 5-fl owered, umbel-like; peduncles 5-25 mm long, c. 1.5 mm diam., densely to rather densely covered with stellate hairs, becoming glabrous in age, fruiting peduncles to c. 3 mm diam., bracts 4, oblong, 4-5 mm long, outer side densely covered with stellate hairs, falling before fl owering, pedicels 25-70 preparing the distribution maps. We also want to thank Álvaro J. Pérez Castañeda who made some measurements on a fl ower preserved in alcohol in QCA, thus enabling to make the description of T. globuliferus more complete.