Revision of the Neotropical genus Sapranthus ( Annonaceae )

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INTRODUCTION
The genus Sapranthus was described and illustrated by Seemann in 1866, his generic name based upon the characteristic fetid odour of the flowers, which he had experienced in the field in Nicaragua.A second species was assigned to the genus by Fries (1900), followed by two additional species by Standley (1922), all transfers from other New World genera.At the time of the last revision, Fries (1930Fries ( , 1931) ) recognized seven species based on only 23 collections.Fries (1948) subsequently described one more species, and thus enumerated eight species in the 'Die natürlichen Pflanzenfamilien' synthesis of the family Annonaceae (1959), while inexplicably omitting yet another new species described during the intervening years by Standley & Steyermark (1943).More recently, two additional species of Sapranthus have been described with green flowers: S. viridiflorus from Mesoamerica (Schatz 1998), and S. isae from Colombia (Vélez-Arango & Cogollo-Pacheco 2007).Based on the examination of over 520 exsiccatae, the current work recognizes 8 species of Sapranthus, including two new species.

Habit
Species of Sapranthus are shrubs to small trees 1 to 15 m tall.The main trunk is relatively slender in species for which diameter has been recorded, varying from 3 -30 cm diam, rarely to 60 cm diam in S. palanga.

Leaves
Leaves are simple, entire, petiolate, and estipulate, and arranged alternately in a single plane along lateral branches (distichous), and are usually deciduous.Petioles are shallowly canaliculate, and vary from 2 -16 mm long.The shape of the lamina is elliptic to obovate, sometimes narrowly so.The texture of the lamina is membranous, the surface dull to shiny and usually smooth, but rarely weakly to strongly verruculose in S. microcarpus.The lamina varies in length from 5-34 cm.The base of the lamina is attenuate to acute to obtuse, sometimes asymmetric or rarely subcordate in S. palanga.The apex of the lamina is generally acute to acuminate, the acumen to 20 mm long.The primary vein is usually distinctly impressed above.The venation is eucamptodromous to weakly brochidodromous with 5 -14 secondary veins per side, with S. microcarpus exhibiting an unusually low number of secondary veins (5 -8), as well as uniquely having pocket domatia in the axils of the secondary veins with the primary vein below; the tertiary venation is distinctly percurrent or less often reticulate in S. microcarpus.The indument on young branches, petioles and lamina is composed of simple, appressed or erect hairs, or in S. isae reported to be mixed with stellate hairs (Vélez-Arango & Cogollo-Pacheco 2007).Most species of Sapranthus have leaves that are rather densely covered with both appressed and erect whitish hairs below; several species are distinguished by their indument: S. hirsutus by its long, whitish to golden brown hairs on the stems, petioles, and especially the primary vein below; and S. palanga by its stiff, short, erect hairs (hispid-strigose) rendering the lower surface of the lamina somewhat rough.

Inflorescences
Inflorescences are terminal rhipidia, usually appearing leaf-opposed by the overtopping of the renewal shoot, usually bearing a solitary flower (or rarely 2 flowers); flowers are occasionally borne on older wood or the main trunk in S. isae, S. violaceus, and S. viridiflorus, and in two species the rhipidia bear multiple flowers: a single flower at a time on a perennial short shoot just back from the leaves (ramiflory) (S. chiapensis), or a cluster of flowers at condensed perennial flowering nodes mostly on the main trunk from ground level on up (trunciflory) as well as on old lateral branches (ramiflory) (S. palanga).The pedicel (here measured as the entire stalk both below and above the articulation, i.e., including the peduncle) usually bears a single foliaceous ('leafy') bract 3 to 35 mm long at the articulation near the base of the pedicel to about midway to the flower, rarely with two bracts reported in S. isae.Pedicels vary in length from 5 to 40 mm (lengthening in fruit to 80 mm), with shorter pedicels exhibited by S. chiapensis (7-10 mm) and S. isae (5-8 mm).

Flowers
Flowers are pendant, with 3 free sepals and 6 free petals in 2 equal to subequal whorls, the aestivation imbricate.The torus is convex and densely covered with erect hairs.Sepals exhibit evident venation, and vary in length from 4 -22 mm, with especially long sepals present in S. hirsutus (15 -22 mm) and S. violaceus (6 -18 mm).Petals are usually membranous with evident venation, or rarely fleshy coriaceous and lacking evident venation (S. viridiflorus) at anthesis, albeit exhibiting venation in bud and throughout much of development.Petals are dark purple brown or maroon or sometimes reddish or rarely green (S. isae and S. viridiflorus) with purple tint at the base, and usually bear a corrugated, yellow, white or rarely black (S.isae) food body at the base of the inner petals where they narrow to a short geniculate claw; in S. viridiflorus, the food body is rudimentary (perhaps vestigial?)and present as a small, triangular, white patch.Stamens are numerous, with a very short filament and a discoid connective apex.Carpels are free, generally numerous (only 1-6 in S. viridiflorus), the stigma is sessile or with a very short style, spherical to napiform to flattened ellipsoid, attached to the ovary obliquely.Ovules (3 -23) are lateral in usually two rows, or rarely in a single row (S.microcarpus).

Fruits
Fruits are apocarpous, a cluster of 1-25 indehiscent berry-like monocarps, usually short-stipitate but sessile in S. campechianus and S. isae.The monocarps are usually ellipsoid to oblongoid to obovoid and mostly much larger than 20 mm diam, with two alternating rows of seeds, sometimes interdigitated and therefore giving the appearance of a single row; in S. microcarpus, with a single row of seeds, the monocarps are less than 20 mm diam and greatly resemble those of Desmopsis.The monocarps are green or yellow, sometimes maturing orange or red.Seeds vary in number from 1 to 19, and are usually spherical wedge-shaped; in S. isae the seeds are flattened ellipsoid to spherical wedge-shaped, and in S. microcarpus they resemble those of Desmopsis and are either subspherical to ellipsoid if the monocarp has only a single seed, or discoid and hemispherical when the monocarp has two or more seeds.Seeds are smooth, or rarely pitted and slightly grooved (S. isae), with the endosperm ruminations lamellate in four parts to peg-shaped.

THE PHYLOGENETIC POSITION OF SAPRANTHUS WITHIN ANNONACEAE
Sapranthus has been placed in tribe Miliuseae of subfamily Malmeoideae (Chatrou et al. 2012).Recent plastid phylogenies of tribe Miliuseae (Chaowasku et al. 2014, Ortiz-Rodriguez et al. 2016) have recovered Sapranthus in a clade of Meso american taxa sister to Tridimeris, the two of them in turn sister to the Desmopsis alliance including Desmopsis (Schatz et al. 2018), Stenanona (Schatz & Maas 2010), and several undescribed and unplaced taxa.This Mesoamerican clade of Miliuseae, which has been formally described as subtribe Sapranthinae (Ortiz-Rodriguez et al. 2016), is nested in a larger clade of Asian genera, and most closely related to an undescribed genus from Thailand and Meiogyne.Sapranthus can be distinguished from Tridimeris (Schatz 1987) principally by its 3-merous flowers vs the 2-merous flowers of Tridimeris.

Distinguishing characteristics of Sapranthus within Mesoamerican Miliuseae subtribe Sapranthinae
Sapranthus can be distinguished from the other Mesoamerican genera with which it has been traditionally allied (Desmopsis, Stenanona, and Tridimeris) by its membranous petals with visible venation (clearly evident during development of the flowers of S. viridiflorus albeit lacking at anthesis), the three petals of the inner whorl possessing a fleshy, white to yellow (to reportedly black) 'food body' at their base (rudimentary in S. viridiflorus and resembling the white patch at the base of the inner petals of Tridimeris chiapensis M.A. Escobar & Ortíz.-Rodr.).The food body serves as an attractant/food reward to visiting Coleoptera (Carabidae, Dermestidae, Tenebrionidae) that effect pollination (Schatz 1987, Olesen 1992).Studies of wood anatomy in four species of Sapranthus representing both sections of the genus (Ter Welle & Van Rooden 1982) demonstrate that Sapranthus can be separated from either Desmopsis or Stenanona respectively on the basis of fewer aprotracheal parenchyma bands per millimeter (8.6-11.1 vs 10.9-13.8 or 12.0-15.2),shorter vessel members (222 -336 μm vs 360 -423 μm or 321-400 μm), and less tall rays (834 -1548 μm vs 2070 -3426 μm or 1911-3195 μm).Pollen of Sapranthus is flattened ellipsoid in shape with two large sulci, i.e., disulcate, with smooth exine, whereas pollen of Desmopsis is boat-shaped with two more or less obscure sulci and a verrucate exine, and that of Stenanona is spherical and appears inaperturate also with a verrucate exine (Schatz 1987, Waha & Hesse 1988, Waha & Morawetz 1988).Fries (1930) divided Sapranthus into two sections (sect.Sapranthus and sect.Microsapranthus R.E.Fr.) based on flower size, the conspicuousness of petal venation, and the number of carpels and ovules.With the additional material now available, a distinct division of the genus into two groups is indeed clear, but is based on none of the above characters.Instead, the verruculose leaves with domatia, and bright orange, small, oblongoid to ellipsoid-oblongoid monocarps with discoid or hemispherical seeds in a single row of S. microcarpus (similar to those of Desmopsis) clearly set it apart from the rest of the genus, and it is thus retained as the sole member of sect.Microsapranthus.All other Sapranthus species lack verruculose leaves with domatia, and possess dull-coloured green to yellowish green (sometimes maturing orange or red), larger, ellipsoid-oblongoid to obovoid monocarps with spherical wedge-shaped or flattened ellipsoid seeds in two alternating and sometimes interdigitating rows, a morphology that suggests dispersal by mammals.At Santa Rosa in Guanacaste, Costa Rica, the seeming absence of a contemporary disperser of the fruit of S. palanga has led to the inclusion of Sapranthus in a guild of plant species perhaps formerly dispersed by a now extinct Pleistocene megafauna (Janzen & Martin 1982, Janzen 1983).Tree or shrub 2 -10 m tall, 3 -30 cm diam; young twigs and petiole densely covered with erect and appressed, white hairs to c. 0.5 mm long.Leaves: petiole 2-9 mm long, 1-2 mm diam; lamina elliptic to obovate to narrowly so, 6 -21 by 3 -9 cm, rather densely covered with erect and appressed hairs, becoming sparsely so to glabrous above, densely covered with erect and appressed, white hairs below, base acute to obtuse, apex acute to acuminate (acumen 5 -15 mm long), venation weakly brochidodromous, primary vein slightly impressed above, secondary veins 8-12 on either side of primary vein, slightly raised to flat above, tertiary veins slightly raised to flat above, more or less percurrent.Inflorescence and flower indument: pedicels and outer side of bracts, sepals, and petals densely to rather densely covered with appressed and erect, white hairs.Uses -'Make a hedge around the house; to fasten the palm leaves on the roof of a house; fire wood' (Wallnöfer 9652, Guatemala).

Sapranthus
Note -Fries (1930) included S. campechianus in his sect.Microsapranthus along with S. microcarpus because of its relatively smaller flowers with fewer carpels.However, with relatively larger monocarps and wedge-shaped seeds in two rows, and lacking verruculose leaves with domatia, S. campechianus is clearly more closely related to all other Sapranthus species than it is to S. microcarpus, and is therefore assigned herein to sect.Sapranthus.Within sect.Sapranthus, S. campechianus is dis tinguished by its small sepals (4-8 mm long), membranous, red petals and smooth, sessile monocarps.Notes -Standley annotated the only two known collections of this species, both collected by Matuda, as Sapranthus chiapensis sp.nov.However, the name was never published, and we here adopt his epithet for this narrow Mexican endemic.With respect to leaf indument and floral characters, this distinctive   Tree 5 -15 m tall, diam not recorded; young twigs and petiole densely covered with erect and appressed, golden brownish hairs (hirsute) c. 2 mm long.Leaves: petiole 3-7 mm long, 1-3 mm diam; lamina narrowly elliptic to narrowly obovate, 8-27 by 3 -9 cm, rather densely to sparsely covered with erect, golden brown hairs (hirsute) above, densely so below, base acute to obtuse, apex acute to acuminate (acumen 5 -10 mm long), venation weakly brochidodromous, primary vein impressed above, secondary veins 9 -13 on either side of primary vein, slightly raised above, tertiary veins slightly raised above, percurrent to reticulate.Inflorescence and flower indument: pedicels and outer side of bracts, sepals, and petals densely to rather densely covered with erect and appressed, white hairs, and longer golden brown hairs above the veins on outer side of sepals and petals.Other specimens examined.Honduras, Comayagua, Barranca Trincheras, 1050 m, Allen 6202 (DS, F, GH); Barranca Trincheras, 3 km from Montañuela, 1200 m, Molina R. 13657 (F, LL, NY, US 2 sheets); 6 km after Siguatepeque, 3 km from Montañuela, near Canal 5 (radio station, 1100 m, Van Rooden 850 (COL, F, K, MO, NY, P, S, U, W, WIS, WU 2 sheets).nicaragua,Zelaya, Reserva Bosawas, Falda oeste del Cerro Salaya, entre el Campamento Los Monos y la cima, Grijalva et al. 5948 (MO).

Sapranthus chiapensis
Note -Van Rooden used the epithet 'hirsutus' for this taxon in a paper on wood anatomy (Ter Welle & Van Rooden 1982: 17), but never validly published the name.We here adopt his epithet for this rare species known from two localities in Honduras and Nicaragua.Sapranthus hirsutus is clearly most closely related to the widespread Pacific dry forest species S. violaceus, from which the new species differs most markedly by its dense hirsute indument, which covers not only the lamina, but also bracts, sepals, and petals.In addition, its sepals are distinctly larger (15 -22 by 12 -16 mm) than those of S. violaceus (6 -18 by 5 -12 mm), and in fact, are the largest in the genus.Tree 6 -10 m tall, deciduous, diam not recorded; young twigs and petiole densely covered with yellow simple and stellate hairs.Leaves: petiole 8-10 long, 1-1.5 mm diam; lamina elliptic, 6.5 -20 by 3.5 -9 cm, with yellow simple and stellate hairs on both sides, base attenuate to acute to obtuse, apex acuminate, venation brochidodromous, primary vein impressed and covered with yellow hairs above, secondary veins 10 -14 on either side of primary vein, impressed above, tertiary veins percurrent.
Notes -Despite possessing typical flowers with evident petal venation, S. microcarpus differs markedly from all other Sapranthus species, and is here retained as the sole member of an emended sect.Microsapranthus, with S. campechianus reassigned to sect.Sapranthus, as discussed above.Sapranthus microcarpus is distinguished by its weakly to strongly verruculose leaves with domatia present on the lower side of the lamina in the axils of the secondary veins with the primary vein, and its brightly orange-coloured monocarps with mostly discoid seeds arranged in a single row, all characters unique within Sapranthus.Tree or shrub 3 -12 m tall, 6 -60 cm diam; young twigs and petiole densely covered with erect and appressed, white hairs to c. 1 mm long.Leaves: petiole 4 -16 mm long, 1-4 mm diam; lamina obovate to elliptic, the first leaves of a shoot sometimes orbicular, 8 -34 by 4 -18 cm, densely covered with erect and appressed, stiff, white hairs to c. 1 mm long, soon subglabrous above, except for the primary vein, densely (at last rather densely) so below and therefore somewhat rough (hispid-strigose), base obtuse, sometimes subcordate, rarely acute, apex acute to shortly acuminate (acumen to c. 10 mm long), venation eucamptodromous, primary vein slightly impressed above, secondary veins 8 -13 on either side of primary vein, slightly raised above, tertiary veins slightly raised above, percurrent.Inflorescence and flower indument: pedicels and outer side of bracts and sepals densely covered with white erect and appressed, curly hairs, outer side of petals densely to sparsely so mainly along the longitudinal veins.
Note -Sapranthus palanga is unique among Sapranthus species in possessing a hispid-strigose indument that renders the lower surface of the leaves somewhat rough.Although other Sapranthus species occasionally bear flowers on older wood (S. chiapensis), S. palanga is remarkable for its high degree of trunciflory, bearing flowers primarily along the main trunk from ground level on up, as well as occasionally on older leafless horizontal branches (ramiflory), but never among the leaves.
Habitat & Ecology -In low, dry semideciduous forest.At elevations of 0 -1200 m.Flowering: all year through, but particularly May and June; fruiting: all year through.
Although Safford (1911) first signalled the correct generic placement of Dunal's (1817) Unona violacea by providing new combinations for both it and Asimina foetida in Sapranthus, Fries (1930: 11) was reluctant to recognize Unona violacea Dunal despite his statement that 'the plant is certainly a Sapranthus species'.Under his discussion of S. foetidus, Fries (1930) cites the pedicel in the Dunal illustration (Dunal 1817: t. 25, f. 4) as being too long for S. foetidus (and, therefore, why did it not correspond to his newly described species S. longepidunculatus?), and his having not examined a type specimen of Unona violacea, as justifications for not treating the Dunal species.
Ironically, however, Dunal based his description of Unona violacea, as well as those of Annona purpurea Sessé & Moc.ex Dunal and Unona penduliflora [= Cymbopetalum penduliflorum (Dunal) Baill.], the three Annonaceae he described from the Sessé and Mociño Expedition to New Spain, solely on the drawings made during the expedition, which were brought to Montpellier by Mociño after he fled from Spain in 1813.They serve as the types for these three species (McVaugh 1980, 1982, 1998, Murray 1993).Unona violacea is represented by three of the Sessé & Mociño drawings: one, a less polished field sketch (Torner Collection 1814 (Fig. 3a)) and two other nearly identical more finished drawings, one of which has been numbered Torner Collection 1791 (Fig. 3b), the other of which has been left unnumbered.These latter two drawings served as the model upon which the artist Node-Veran based his engraving for Dunal's Monograph, Plate 25 (Fig. 3c).The field sketch (Torner Collection 1814) has written on it in ink (the handwriting perhaps that of Mociño, 'Ubaria purpurea N', the 'b' presumably a linguistic transformation of a Spanish 'v', and hence indicating a new species and preliminary assignment to the genus Uvaria.The more finished drawing (Torner Collection 1791) has written in pencil below the drawing 'Uvaria?purpurea', the handwriting perhaps Dunal's.The nearly identical unnumbered drawing lacks any annotation.With the exception of failing to include the secondary cross venation in the petals and completing the three leaves cut off at their margins on the original drawing, Node-Veran accurately copied the drawing in preparation for the engraver.By the time the Monograph appeared in 1817, Dunal had rejected placement of the species in Uvaria, describing it instead as a Unona, with the epithet 'violacea' instead of 'purpurea'.
Insofar as the expedition drawings of S. violaceus are not part of the Icones Florae Mexicanae (a numbered series of species collected in western Mexico during the early part of the expedition), it is not possible to determine the exact provenance of the plants from which the drawings were made.In all likelihood they were encountered relatively late in the expedition during the travels of Mociño and the artist Cerda from Mexico to Costa Rica and back, during the period 1795 -1799 (McVaugh 1977 and pers. comm.).
The five species brought together here in synonymy under S. violaceus have previously been distinguished on the basis of petal size and shape, and pedicel length, all of which vary greatly and continuously, both within an individual, and throughout the broad geographical range extending from Nicaragua north to Sinaloa, Mexico.For example, although Standley & Steyermark (1943) described the petals of S. megistanthus from Guatemala as 170 -190 mm long, supposedly 'twice as long as any other member of the genus', two different flowers from the type collection with petals measuring 130 and 139 mm were seemingly ignored, one of which overlaps with petals 132 mm long exhibited by a collection from Nicaragua (Schatz & Stevens 587).Similarly, Fries (1930) described the petals of S. borealis from Sinaloa, Mexico, as 25 -33 mm long despite one flower on the type collection with petals 44 mm long.He later annotated another Sinaloa collection (Ortega 6695) with petals to 55 mm long as S. borealis 'petala longa', which falls within the range of variation in petal length exhibited in Nicaragua.Pedicel length is also highly variable, exhibiting nearly as much variation in a single collection (12 -33 mm long for Schatz & Stevens 586 from Nicaragua) as the total variation of 6 -43 mm manifest throughout the total distribution range, thus easily encompassing the 28 -35 mm long pedicels of the type of S. longipedunculatus (Langlassé 128bis) from Guerrero, Mexico.Tree or rarely shrub 3 -12 m tall, 10 -25 cm diam; young twigs and petiole densely covered with erect and appressed, white hairs to c. 0.5 mm long, soon glabrous.Leaves: petiole 4 -10 mm long, 1-2 mm diam; lamina elliptic to obovate, 8 -29 by 3 -13 cm, sparsely covered with erect and appressed, white hairs to c. 0.5 mm long above, densely to rather densely so below, base acute to obtuse, or somewhat truncate, apex acuminate (acumen 10-20 mm long) to acute, venation weakly brochidodromous, primary vein impressed above, secondary veins 10-12 on either side of primary vein, slightly raised above, tertiary veins slightly raised above, more or less percurrent.