Research Article |
Corresponding author: Kenneth J. Wurdack ( wurdackk@si.edu ) Academic editor: Alexander Sennikov
© 2019 Kenneth J. Wurdack, Charles E. Zartman.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Wurdack KJ, Zartman CE (2019) Insights on the systematics and morphology of Humiriaceae (Malpighiales): androecial and extrafloral nectary variation, two new combinations, and a new Sacoglottis from Guyana. PhytoKeys 124: 87-121. https://doi.org/10.3897/phytokeys.124.34679
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Humiriaceae have had little recent comparative morphological study except for their distinctive fruits. We surveyed the diversity of stamen structures in the family with consideration of dehiscence patterns and the evolutionary transitions between tetra- and disporangiate anthers. Novel interpretations of floral morphology support new combinations (Duckesia liesneri K.Wurdack & C.E.Zartman, comb. nov. and Vantanea spiritu-sancti K.Wurdack & C.E.Zartman, comb. nov.) for two species formerly in Humiriastrum. We investigated all eleven species of Sacoglottis for diagnostic features that may contribute to better species delimitations, and describe Sacoglottis perryi K.Wurdack & C.E.Zartman, sp. nov. as an endemic of the Pakaraima Mountains in western Guyana. Finally, our survey across Humiriaceae for extrafloral nectaries (EFNs) revealed their presence on leaves of all extant species as adaxial basilaminar and/or abaxial embedded glands, in addition to the frequent occurrence of marginal glandular setae. The significance of inter-generic variation in gland position and anther morphology within the family are discussed.
anthers, Duckesia, extrafloral nectaries, floral morphology, glands, Humiriastrum, Vantanea
Humiriaceae
contains approximately 65 species of extant trees and shrubs characterized by small white to greenish-cream (rarely red to pink) flowers and with a center of taxonomic richness in the Rio Negro Basin, the largest tributary of the Amazon River. The family is notable for its rich fossil record of distinctive, woody endocarps, and for its unusual biogeography as a nearly wholly neotropical family except for one species in tropical West Africa. The most comprehensive synoptic revision of the family or any of its eight constituent genera was published in 1961 by noted authority José Cuatrecasas. In that visionary work, Cuatrecasas radically restructured Humiriaceae with 24 new taxa, 33 new combinations, and the segregation of four new genera of which three (Duckesia [Ducke] Cuatr., Hylocarpa [Ducke] Cuatr., and Endopleura [Huber] Cuatr.) were monotypic Amazonian endemics. The genera as defined by
Although Humiriaceae is clearly monophyletic and placed in Malpighiales, its relationships within the order (
Glandular tissues on leaves, sepals, floral disc, and/or anthers have been reported for Humiriaceae (
Sacoglottis, the systematics focus of this study, is distinguished among the eight genera in having the lowest stamen number (10). Morphological and molecular evidence indicates a nested phylogenetic placement for Sacoglottis within the family (
We herein describe this new species of Sacoglottis and present comparisons of its vegetative and reproductive characters in relation to the often poorly known other species in the genus. We surveyed stamen structures from exemplars of all genera to provide more detailed information on features of systematics and evolutionary interest, especially relating to anther morphology and interpretation of sporangial reductions. As a result of this objective we also present new combinations based on novel interpretations of previously overlooked floral structure for two taxa. Finally, on noting the frequent occurrence of EFNs on Humiriaceae but little mention of them in the literature, we conducted a comprehensive EFN survey of all species to document their occurrence and any qualitative generic-level distinctions.
Scanning electron microscopy (SEM) of untreated or rehydrated-ethanol transitioned then critical point dried (CPD) herbarium fragments was conducted with a Zeiss EVO MA15 (Carl Zeiss SMT, Inc., Peabody, Massachusetts) SEM at 5–10 kV after sputter coating with 10 nm of C + Au/Pd using a Leica EM ACE600 (Leica Microsystems GmbH, Wetzlar, Germany). Light microscopy (LM) was with an Olympus DSX100 (Olympus Corp., Tokyo, Japan) and extended focus imaging (EFI) for higher magnifications, or with a Zeiss Universal Compound Microscope. Androecial diversity of the family was broadly surveyed at US and then examined in detail with SEM and/or LM for representatives for each genus, including: Duckesia liesneri comb. nov., Henderson 933 (US); D. verrucosa (Ducke) Cuatrec., Ducke 2108 (US); Ducke [MG-16325] (US). Endopleura uchi (Huber) Cuatrec., Baker 58 (US), Assunção 605 (US). Humiria balsamifera var. imbaimadaiensis Cuatrec., Wurdack 4814 (US); H. crassifolia Mart., Cowan & Soderstrom 2145 (US). Humiriastrum cuspidatum (Benth.) Cuatrec., Cid et al. 4264 (US), Ducke 243 (US); H. dentatum (Casar.) Cuatrec., Hatschbach 56145 (US); H. diguense (Cuatrec.) Cuatrec., Quizhpe et al. 612 (US); H. glaziovii (Urb.) Cuatrec., Landrum 4262 (US). Hylocarpa heterocarpa (Ducke) Cuatrec., Ducke [JBRJ-30137] (US). Sacoglottis gabonensis, Gentry & Pilz 32860 (US); S. guianensis Benth., Carvalho et al. 4346 (US); S. maguirei Cuatrec., Maguire et al. 30693 (NY, US); S. perryi sp. nov., Redden 7264 (US), Tripp 2984 (US). Schistostemon macrophyllus (Benth.) Cuatrec., Maas et al. 6577 (NY); S. oblongifolius (Benth.) Cuatrec., Maas et al. 6804 (US). Vantanea bahiensis Cuatrec., Belém & Magalhães 748 (US); V. compacta (Schnizl.) Cuatrec., Hatschbach 21265 (NY); V. depleta McPherson, Hammel & Trainer 12954 (MO), McPherson & Stockwell 10892 (US); V. micrantha Ducke, Ducke [JBRJ-30135] (US); V. peruviana J.F. Macbr., Rimachi 4577 (US); V. spiritu-sancti comb. nov., Silva et al. 1436 (US). Stamen vasculature was examined after clearing with aqueous 5% (w/v) sodium hydroxide, followed by saturated chloral hydrate. For floral anatomy of Vantanea spiritu-sancti, buds were cleared of tannins with Stockwell’s bleach, paraffin-embedded, sectioned at 10 μm, and stained with toluidine blue O. Stamen structure descriptions follow the work of Endress (e.g.,
Character states in Tables
Representative leaves from nearly all Humiriaceae species and varieties were surveyed with LM for the presence of foliar glands and leaf margin features. Type collections were utilized where possible to avoid identification uncertainty, and multiple specimens were studied, especially for taxa with glands characterized as scarce or potentially absent. In some cases, distinguishing between plant structures and leaf damage, which creates circular depressions with marginal scarring, was difficult. We employed additional search criteria of expected location and positional patterns, although the laminar glands of some species are clearly sparse and erratically distributed.
The flowers of Duckesia verrucosa have (22–)25 stamens of two types, including five fertile antepetalous that each alternate with a group of 4–5 sterile on less stout filaments of varying lengths. One stamen per sterile group is usually as long or longer (clearly the medial antesepalous stamen when five per group) than the fertile stamens and the rest shorter. The filaments are subulate, complanate, basally very short-connate, proximally short-papillose, and distally smoother (especially so on the fertile stamens). Abnormally short filaments (1/3–1/2 of the normal length) lacking anthers rarely substitute for sterile stamens; these are likely the occasional staminodes reported by
Stamen structure of Humiriaceae. A Duckesia verrucosa tetrasporangiate anther, dorsal B Duckesia verrucosa tetrasporangiate anther, lateral C Duckesia liesneri tetrasporangiate anther, lateral D Endopleura uchi disporangiate anther, lateral E Endopleura uchi tetrasporangiate anther, lateral F Duckesia verrucosa sterile anther, lateral G Humiriastrum cuspidatum disporangiate anther, lateral H Humiriastrum cuspidatum androecium, dorsal I Endopleura uchi tetrasporangiate anther, lateral J Humiriastrum dentatum disporangiate anther, lateral K Humiriastrum dentatum disporangiate anther, ventral L Humiriastrum diguense disporangiate anther, lateral M Humiria balsamifera var. imbaimadaiensis stamen cluster with 2 of 3 types, dorsal. f = filament attachment location. Sources: A, B, F Ducke 2108 C Henderson 933 D, E, I Assunção 605 G, H Cid et al. 4264 J, K Hatschbach 56145 L Quizhpe et al. 612 M Wurdack 4814 (all US.)
The flowers of Endopleura have 20–22 stamens (to 30, fide
The flowers of Humiria have 20 stamens of three types, including five long antesepalous, 10 short and adjacent to antesepalous, and five antepetalous of intermediate length. Two (
The flowers of Humiriastrum (Urb.) Cuatrec. have 20 stamens of two types, including 10 long antesepalous and antepetalous, and 10 short that are adjacent to the long (Fig.
The flowers of Hylocarpa (examined with LM from a single, young bud and additional fragments) have 20 stamens of two types, including 12 fertile and the rest sterile (30 stamens with 5–15 fertile according to
The flowers of Sacoglottis have 10 stamens of two types, including five long antesepalous and five short antepetalous. The filaments are subulate, complanate, basally connate to form an androecial tube, and smooth; each contains a vascular bundle that continues into the connective protrusion for nearly its entire length and distally usually bears short stubby branches. In bud, the filaments are straight and longer than the anthers. The filament width and length of connation (1/10–2/3 of total length) vary between species and can be diagnostic (see Table
The flowers of Schistostemon (Urb.) Cuatr. have 20 stamens of three types, including five long trifurcate antesepalous, 10 short and adjacent to the antesepalous, and five of medium length antepetalous, and have 30 anthers (Fig.
Stamen structure of Humiriaceae. A Sacoglottis perryi stamen cluster of 2 types, ventral B Sacoglottis perryi stamen cluster of 2 types, dorsal C Sacoglottis perryi short-stamen anther with open stomium and pollen D Sacoglottis guianensis androecium with interstaminal staminodes (st), dorsal E Schistostemon macrophyllus stamen cluster of 3 types, ventral F Schistostemon macrophyllus stamen cluster of 3 types, dorsal G Schistostemon oblongifolius trifurcate filament tip, dorsal. Sources: A–C Tripp 2984 D Carvalho et al. 4396 E, F Maas et al. 6577 G Maas et al. 6804 (all US).
The flowers of Vantanea vary in stamen number across the species, ranging from 15–28 in V. depleta to >200 in V. maculicarpa Sabatier & J. Engel (fide
Stamen structure and anatomy of Humiriaceae. A Vantanea compacta anther, lateral B Vantanea compacta anther, dorsal C Vantanea depleta anther, lateral D Vantanea spiritu-sancti anther, lateral E Schistostemon oblongifolius clearing of androecium with 3 stamen types, ventral F Vantanea spiritu-sancti longitudinal section of ovary with 2 superposed ovules per locule; lower left ovule partial G Hylocarpa heterocarpa anthers (left to right): disporangiate dorsal, ventral; sterile, dorsal. Sources: A, B Hatschbach 21265 C Hammel & Trainer 12954 D, F Silva et al. 1436 E Maas et al. 6804 G Ducke [JBRJ-30137] (all US).
Foliar glands were found to be present on 64/65 accepted species and 22 infraspecific taxa of Humiriaceae (85 taxa examined, 100% presence; Appendix 1, Fig.
In Sacoglottis the paired adaxial glands usually occur near the base of the leaf blade (Fig.
The leaf margins are either untoothed and entire (Humiria, Vantanea), or have glandular setae at regular intervals associated with teeth of varying degrees of prominence (remaining taxa). The non-entire margins are variously described herein (Appendix 1) and in the literature as crenate(-serrate), crenulate(-serrate), or serrate; they are rarely subentire and nearly smooth with little evidence of setae. This terminology reflects a continuum among species in the height and curvature of their small teeth. Most species have asymmetric teeth that are shallow and rounded (crenate), and more rarely have pointed projections with strongly concave distal flanks (serrate). Humiriastrum melanocarpum with leaves described as having “the margin slightly crenate with small glands” (
Extrafloral nectary and leaf margin diversity of Humiriaceae. A Vantanea depleta laminar glands, abaxial B Duckesia liesneri basilaminar glands, adaxial C Schistostemon oblongifolius basilaminar glands, adaxial D Humiriastrum ottohuberi laminar glands, abaxial E Duckesia verrucosa robust seta at margin F Sacoglottis guianensis basilaminar glands, adaxial G Humiria fruticosa shoot tip with marginal glands exposed on expanding new leaf H Humiria fruticosa marginal gland I Hylocarpa heterocarpa laminar gland, abaxial J Humiria balsamifera var. minarum dense row of marginal glands, abaxial K Duckesia verrucosa laminar gland, abaxial L Schistostemon retusus darkened scar from deciduous seta M Schistostemon retusus intact seta at margin. g = gland, s = seta scar. Sources: A Mori & Kallunki 4889 B Liesner 22589 C Maas et al. 6804 D Maguire 34912 E, K Ducke 2108 F Jansen-Jacobs et al. 1898 G, H Steyermark 103255 I Ducke [JBRJ-30137] J Mexia 5815 L Redden 3372 M Cuatrecasas 7203 (all US).
Micromorphology of Sacoglottis perryi. A Marginal glandular seta B basilaminar gland, adaxial C laminar gland near margin, abaxial D sepal tip, inner side with terminal gland E paired glandular stipules and petiole scar F pollen inside sporangium G stigma with ephemeral lobes intact and showing secretion H stigma lobes shredded showing thin walls I gynoecium with diagnostic hirsute ovary J glandular disc with erose margin. Sources: A–C Gillespie 2810 D–J Tripp 2984 (all US).
Humiriastrum liesneri Cuatrec., Phytologia 71: 165. 1991. Type: VENEZUELA. Amazonas, Depto. Rio Negro: Cerro Aracamuni, summit, Proa camp, 1400 m, 28 Oct 1987, R. Liesner & G. Carnevali 22589 (holotype: US-3111383; isotypes: MO-3641994, NY-00329209, US-3118837, VEN-277523).
When
Characters | Duckesia verrucosa | Duckesia liesneri | Endopleura uchi |
---|---|---|---|
Habit | Tree, 12–30 m (27–67 cm dbh) | Shrub to small tree, 2–4 m | Tree, (12)20–40 m (30–70 dbh) |
Leaves | Petiole to 1 mm long; blade 5.5–7.5 ×1.7–2.3 cm, lanceolate, subcoriaceous; teeth setae robust, to 0.2 mm long, sometimes retained at maturity; abaxial glands sparse, 0–3 per leaf, 2/3 exmedial distance | Petiole to 2 mm long; blade 3.5–4.5 × 2.2–2.7 cm, elliptic to obovate, coriaceous; teeth setae delicate, to 0.3 mm long, rapidly deciduous; abaxial glands absent | Petiole 10–30 mm long; blade 17–28 × 5.5–6.5 cm, oblong to narrowly elliptic, subcoriaceous; teeth setae delicate, to 0.5 mm long, rapidly deciduous; abaxial glands in row near margin |
Inflorescence | Axillary, small, to 1.5 cm long; bracts persistent | Axillary and subterminal, to 2.5 cm long; bracts deciduous | Axillary, to 6.5 cm long; bracts persistent |
Flower | Calyx glabrous with minutely hispid margin; petals glabrous | Calyx hispid; petals coarsely hirsute | Calyx centrally coarsely hirsute, margin minutely hispid; petals coarsely hirsute |
Androecium | Filaments papillose, very short-connate; anthers 5 tetrasporangiate and 15+ sterile | Filaments smooth, connate up to 1/3 length; anthers 20 tetrasporangiate | Filaments minutely papillose, very short-connate; anthers 10 tetrasporangiate and 10+ disporangiate |
Gynoecium | Pistil longer than ovary | Pistil shorter than ovary | Pistil as long as ovary |
Fruit | Ovoid; endocarp corrugated, 13+-radiate with densely packed woody ribs; resinous cavities small; valves conspicuous | Unknown | Ellipsoid; endocarp star-shaped, 10-radiate with 5 divided woody ribs; resinous cavities absent; valves inconspicuous |
Distribution & ecology | Brazil (Amazonas especially near Manaus, Pará); 50–125 m elevation, terra firme | Venezuela (Amazonas on Cerro Aracamuni and Sierra de Unturán); 1150–1400 m elevation, upland cloud or semi-open tepui forest | Bolivia (Pando), Brazil (Amapá, Amazonas, Pará, Rhondônia) Guyana, Suriname, Venezuela; 50–620 m elevation, terra firme |
Macromorphology of Sacoglottis perryi. A Dried fruit with central seed embedded in woody endocarp, longitudinal split along carpel wall (dissected by Cuatrecasas) B dried fruit with 2 central seeds and endocarp lacunae, transverse section C fresh fruit with fleshy yellow-green exocarp and liquid in endocarp lacunae, transverse section D young inflorescence with bracts intact (b) or fallen leaving bract scars (bs) E mature bud with marginal sepal gland (small red dot in center) F partly open flower with intact anthers G post-anthetic flower H freshly cut trunk I type in life just before pressing. Sources: A Gillespie 2810 B Tripp 2984 C, E–I Redden 7264 D Hoffman 1600 (all US).
Humiriastrum spiritu-sancti Cuatrec., Ciencia, Mexico 23(4): 137. 1964. Type: BRAZIL. Espírito Santo, Mun. de Santa Tereza: Lombardia, 25 Jan 1954, G. Dalcolmo s.n. (holotype: RB-86212; isotype: US-2827596).
Humiriastrum spiritu-sancti was poorly known until recent ample collections allowed a fuller characterization.
Illustration of Sacoglottis perryi. A Habit B bud C bud with petals removed D open flower, axial E open flower, lateral F gynoecium G stamen cluster of 2 types, ventral H floral diagram I post-anthetic flower J young fruit K, L fruit M fruit with 2 central seeds and endocarp lacunae, transverse section. Source: A–M from specimens and life photos of Redden 7264 (US).
Differs from Sacoglottis guianensis in smaller elliptic leaves, smaller short-pedunculate inflorescences with deciduous bracts, glandular sepals, hirsute ovaries, and subglobose fruits.
GUYANA. Cuyuni-Mazaruni Region: Below 1st escarpment (of four) of Kamakusa Mt., Powis Creek (2nd) Camp, gallery forest, 5°48'26.7"N, 60°14'6.9"W, 662 m, 20 May 2012 [fl], K. Redden 7264 (holotype: BRG, isotypes: K, NY, US-3694797). Note: type tree of 10 cm dbh was cut down (Fig.
Habit usually small tree, 6–8 m, 10–12 cm dbh (to 14 m, 50 cm dbh), trunks lacking buttresses; bark rough, scaly, inner bark coarsely fibrous, dark brown; wood reddish-brown, diffuse porous, growth rings distinct and delimited by a fibrous zone, vessels narrow, mostly solitary, tyloses present, axial parenchyma scanty paratracheal, rays conspicuous (wood described from a 4 cm diam. trunk section); lateral leafy twigs 2–3 mm diam., puberulous, trichomes to 0.1 mm long. Stipules ca. 0.6 × 0.3 (at base) mm, narrowly triangular (rarely with smaller secondary lobes), thickened, glandular, rapidly deciduous. Leaves alternate, distichous on lateral branches, simple; petioles 6–10 (long) × 1 (wide) × 0.8 (high) mm mid-petiole, subterete (dorsiventrally slightly flattened), proximally slightly pulvinate, distally expanded to 2× wider with narrow wing extending from margins of lamina along shoulders of petiole, sparsely puberulous; blades 4.4–10.8 × 1.7–4.6 cm, length:width ratio 2.19–2.59:1 (mean = 2.37, SD = 0.256, n = 100 from 10 mature leaves × 10 collections), oblong to ovate, base angle obtuse, base obtuse to rounded, apex angle acute, apex shape acuminate with drip tip 0.5–1.5 cm long, tip ending in minute apiculate glandular tooth at distal apex of midvein; subcoriaceous, abaxially sparsely puberulous, adaxially glabrous; basilaminar glands (0–1)2, usually symmetric as pair, along adaxial margin of leaf base, 0.2–0.5 × 0.1–0.2 mm, widely to narrowly elliptic; abaxial laminar glands sparse, up to 4 per side, 0.2–0.7 mm from edge, 0.1 mm wide, nearly circular, slightly sunken; margin shallowly crenate, darkened glandular spots in sinuses, 0.2–0.3 mm diam., when young these spots bearing deciduous glandular setae, 0.3 × 0.1 mm; dark green above and light green below in life; venation pinnate, brochidodromous; secondaries 8–9 pairs, excurrent attachment; intersecondaries frequent. Inflorescences axillary, small (shorter than leaves), <20 flowers, 3–4 orders of branching, peduncle to 1 mm long, rachis 5–10(20) mm long, internal internodes successively shorter in higher order branches, to 2.5 mm long on secondary branches, terminal branches (pedicels) subsessile to 0.5 mm long; bracts 1.8 × 1–1.5 mm, obtuse to rounded, margin entire, sparsely puberulous, rapidly deciduous leaving joint scars. Flowers bisexual, actinomorphic, mature buds 4–4.5 × 1.5–2 mm; calyx cupular, sepals 5, equal, free to base of ovary (when observed from inside), connate at base of receptacle for 1–1.5 mm, imbricate, free portion widely rounded to minutely retuse, 1 × 1.5 mm, sparsely short puberulent (trichomes shorter than elsewhere on plant) inside and out, margin finely ciliate, hyaline, usually with single gland ca. 0.1 mm diam. at minutely retuse apex, in life sepals green and gland red; petals 5, free, 4–4.5 × 1 mm, oblong-lanceolate, tip acute, thick with narrow hyaline entire margin, glabrous, aestivation quincuncial, greenish-white in life and reflexed at anthesis; stamens 10, glabrous, stiffly erect in bud and at anthesis, dimorphic, alternating in 2 lengths; 5 antesepalous longer, filaments 3.5–3.6 mm long; 5 antepetalous shorter, filaments 3 mm long; filaments of both lengths subulate, complanate, basally connate to 1.5 mm and tips free, 0.3–0.5 mm wide at start of free portion × <0.1 mm thick, in life greenish-white; anthers slightly dimorphic and differing in length of connective apex due to tight packing in bud which prevents full development of shorter anthers, antesepalous 0.8–0.9 × 0.5 mm, antepetalous 0.6–0.7 × 0.5 mm, dorsifixed; connective thickened, apical tip acute, base V-shaped and forcing pollen sacs to slightly diverge distally; pollen sacs 2 per anther (disporangiate), ca. 0.3 mm long, in proximal half of anther, stomium narrowly elliptic, covered by valve with a thin dorsal hinge and opening with a ventral lip, yellow-orange in life; ovary 1–1.2 × 1.2–1.3 mm, subglobose, densely hirsute with long trichomes to 0.5 mm; disc 0.5–0.6 mm high, thin, cupular, margin erose with rounded irregular lobes to 0.1 mm high; style 2–2.5 × 0.3 mm, single, columnar, with distinct discontinuity and slightly thinner for distal 1/3, glabrous; stigma minutely 5 lobate-capitate. Infructescence: 1–2 fruits maturing per inflorescence; fruit stalk 5–8 × 1 (diam.) mm, consisting of pedicel and 1–2 inflorescence nodes; petals and anthers caducous, sepals and filaments persistent, filaments forming protective palisade-like sheath around young developing fruit, stigmas and distal thinner part of style senescing rapidly. Fruit drupaceous, 33–35 × 23–30 mm (nearly mature, but ultimate size unknown), length:width ratio 1.07–1.44:1 (mean = 1.23, SD = 0.107, n = 19 from 9 collections, excluding McDowell 2993), sub-globose to ellipsoid, tip short apiculate, glabrescent but sparse trichomes remaining at apex, surface smooth when fresh, when dry sometimes slightly dimpled due to underlying endocarp, exocarp 0.5–1 mm thick; endocarp woody, obscurely bullate on surface due to underlying lacunae, with 3 slight longitudinal furrows, brown, interior with numerous lacunae; lacunae 1.5–5 × 1–4 mm, asymmetric ellipsoidal, greatly varying in size and exact shape within a fruit, in life filled with watery light brown fluid that dries to form thin dark brown, glassy, resinous layer; walls between lacunae <0.05 mm (translucent)–0.5 mm, grading thicker at vertices between multiple lacunae, distinctly thickened around seeds (locule cavity wall) and along the indistinct carpel sutures; locule snug around seed. Seeds 1–3 per fruit, 15 (long) × 5–6 (deep; parallel to embryo) × 4–5 (wide; perpendicular to embryo) mm, oblong, (sub)circular in transverse section, proximal end rounded, distal (hilar) end attenuate; coat thin, papery, brown; endosperm copious, fleshy, oily.
The specific epithet commemorates Claudius Perry (1977–2011;
Sacoglottis perryi is apparently confined to the Pakaraima Mountains of Guyana, and most localities are along mid-elevation (500–800 m) primary and secondary creeks in the headwaters of the Mazaruni River basin. It should be expected in other upland areas of the Mazaruni watershed including in adjacent Venezuela and perhaps Brazil. The tree typically grows in gallery forests at the edge of those waterways, or in forest patches in the white-sand savanna/forest mosaics of the region. Flowering occurs in May–June, with the fruits slowly developing over the course of a year. The timing of fruit ripening, likely in the fall, and features of the ripe fruit are unclear. The Kamakusa collections with the largest fruits on any specimens were hard and green when fresh (Fig.
GUYANA. Cuyuni-Mazaruni Region: Imbaimadai, Partang River along riverbank past first rapids NE of base camp, 05°42'10.5"N, 60°16'50.1"W, 873 m, 2 Dec 2002 [fr], Forbes 325 (US); Maipuri Falls, Karowrieng River, 05°41'N, 60°14'W, 570–600 m, 20 Dec 1989 [fr], Gillespie 2810 (US); Imbaimadai Creek, 1 km W of Imbaimadai, 05°42'N, 60°18'W, 500 m, 16 May 1992 [fl, fr], Hoffman 1600 (NY, US); basecamp 8.6 km NE [of] Imbaimadai on Partang River tributary, 0.75 km E, 05°46'N, 60°15'W, 625 m, 20 May 1992 [fl, fr], Hoffman 1745 (MO, NY, US); basecamp 8.6 km NE Imbaimadai on Partang River tributary, 1.25 km E, 05°46'36"N, 60°15'49"W, 600 m, 20 May 1992 [fl], Hoffman 1755 (MO, NY, US); Mt. Aymatoi (sandstone), 05°55'N, 61°W, 1150 m, 16 Oct 1981 [fr], Maas et al. 5753 (MO, US); Imbaimadai Savannas, Upper Mazaruni River, 24 Oct 1951 [fr], Maguire & Fanshawe 32250 (MO, NY); Sagaraimadai Savanna, Upper Mazaruni River, 16 Nov. 1951 [fr], Maguire & Fanshawe 32619 (MO, NY); from Utshe River to Great Falls on Kamarang River, 4–5 km SE of Utshe camp, 05°43'N, 61°07'W, 850–975 m, 26 May 1990 [fl], McDowell 2920 (MO, NY, US); 7 km N of Paruima Village, after descent from south face of Mt. Waleliwatipu, 05°54'N, 61°02'W, 980–1060 m, 30 May 1990 [fl, fr], McDowell 2993 (MO, NY, US-2 sheets); to plateau [at] S end of Haiamatipu, 05°28'N, 60°32'W, 610–914 m, 20 Jun 1991 [fl], McDowell 4734 (NY, US); Imbaimadai Creek, W of Imbaimadai, 05°42'N, 60°18'W, 503 m, 22 Jun 1986 [fr], Pipoly 7990 (MO, NY, US); Vicinity of Chinoweing Village, 5°32'N, 60°07'W, 650–670 m, 21 Feb 1987 [fr], Pipoly 10484 (NY-2 sheets, US); Imbaimadai, Karowrieng River, towards waterfall 2.32 mi E of Base Camp 1, bordering Karowrieng Creek, 5°40'42.4"N, 60°14'30.8"W, 575 m, 22 Jan 2004 [fr], Redden 1489 (US); Mazaruni River, just above ABC Falls, trail/track 2.03 mi SW of Base Camp 6 heading E, 6°4'25.2"N, 60°39'14.3"W, 605 m, 19 Feb 2004 [young fr], Redden 2008 (US); Kako River, top of waterfall, 05°28'50.8"N, 60°50'49.3"W, 687 m, 15 May 2009 [fl, fr], Redden 6582 (US); below 1st escarpment (of four) of Kamakusa Mt., Powis (2nd) Camp and vicinity, along creek bank at camp 5°48'34.6"N, 60°14'21.5"W, 651 m, 21 May 2012 [fl, fr], Tripp 2984 (US); Kako River, gallery forest near rapids, 05°30'27"N, 60°50'30.3"W, 505 m, 10 May 2009 [fl], Wurdack 4911 (US); below 1st escarpment (of four) of Kamakusa Mt., Powis (2nd) Camp and vicinity, along creek bank at camp 5°48'34.6"N, 60°14'21.5"W, 651 m, 13 Jun 2012 [young fr], Wurdack 5898 (US).
The 11 species of Sacoglottis are compared in Table
The biogeography of Sacoglottis includes disjunctions with clear long-distance dispersal to Africa for S. gabonensis and to Isla del Coco far off the Pacific coast of Costa Rica for endemic S. holdridgei Cuatrec., and there is direct evidence of contemporary and fossil sea drift (
The significance of inflorescence structure variation in Sacoglottis has not been previously emphasized, although it is implicit in details of the descriptions and key of
Schistostemon, presently containing nine species, was formerly a subgenus or section of Sacoglottis and elevated to a genus principally based on differences in androecial structure with a doubling of stamen number to 20, an increase to 30 anthers, and three stamen types instead of two (
Comparison of select diagnostic features among all 11 species of Sacoglottis.
Characters | amazonica | ceratocarpa | cydonioides | gabonensis | guianensis | holdridgei | maguirei | mattogrossensis | ovicarpa | perryi | trichogyna |
---|---|---|---|---|---|---|---|---|---|---|---|
Inflorescence structure, peduncle/pedicel lengths | Short pedunculate, 5–6 / 0.3–1 mm | Very short pedunculate, <1 / < 0.5 mm | Long pedunculate, 20–40 / 0.5–2 mm | Long pedunculate, 10–30 / <0.5 mm | Pedunculate, (2)5–35 / 0.3–3 mm | Short pedunculate, few flowered, 1–4 / 0.2–1 mm | Pedunculate, 7–15 / 1–4 mm | Long pedunculate, 15–40 / 1.5–4.5 mm | Short pedunculate, 1–2 / < 0.5 mm | Very short pedunculate, to < 1 / < 0.5 mm | Pedunculate, clustered, 3(–6) / 0.1–0.5 mm |
Bracts | Deciduous; triangular, carinate | Deciduous; shape unseen | Persistent; acute | Deciduous; triangular, carinate | Persistent; acute | Deciduous; rounded | Persistent; short, rounded | Persistent; acute | Deciduous; acute, carinate | Deciduous; obtuse to rounded | Deciduous; rounded |
Sepal features | Multiple tooth-like marginal glands per sepal; margin short ciliate | No glands; sparsely short puberulent | No glands; glabrous, margin ciliate | No glands; sparsely hirsute, margin ciliate | No glands; glabrous, margin ciliate | No glands; glabrous, margin short ciliate | No glands; hispidulous | No glands; glabrous | 0–1 apical gland per sepal; sparsely short puberulent, margin short ciliate | 1 apical gland per sepal; sparsely short puberulent, margin ciliate | No glands; glabrous to sparsely pubescent |
Petal vestiture | Glabrous | Glabrous | Hispidulous, fide Cuatrec. | Hirsute (subsericeous, fide Cuatrec) | Glabrous to puberulous | Glabrous | Hispidulous. | Glabrous | Glabrous | Glabrous | Glabrous |
Filament connation (relative length) | Connate 1/3 | Long connate 2/3 | Connate 1/2 | Short connate <1/5 (barely beyond sepals) | Connate 1/3 | Connate 1/2 | Connate 1/2 | Connate 1/4 | Connate 1/2 | Connate 1/3 | Very short connate ca. 1/10 |
Ovary vestiture | Glabrous | Glabrous | Glabrous | Glabrous | Glabrous | Glabrous | Glabrous | Glabrous | Glabrous | Hirsute | Hirsute |
Fruit shape; average length:width ratio | Ellipsoid; 1.4:1 | Subfusiform, elongate; ca. 2.35:1 | Globose; 1.02:1 | Subglobose; 1.17:1 | Ellipsoid-oblong; 1.6:1 | Ellipsoid; 1.3:1 | Subglobose; ca. 1.1:1 (very young fruit only) | Globose; 0.92:1 | Ellipsoid; ca. 1.2:1 (partly dissected fruit) | Subglobose to ellipsoid; 1.23:1 | Ellipsoid, large; 1.43:1 |
Exocarp thickness | 1.5 mm | 1 mm | 1–2 mm | 1 mm | 1–2 mm | 1–2.5 mm | Unknown | (0.8)1.5–2 mm | Thick, to 5 mm | 0.5–1 mm | Thick, 3–6 mm |
Distribution | Brazil (Amazonas, Pará), Venezuela (Delta Amacuro), Trinidad | Columbia (Vaupes), Brazil (Amazonas), Venezuela (Amazonas) | Brazil, Guyana, Surinam, Venezuela | Sierra Leone to Angola | Brazil, French Guiana, Guyana Surinam, Venezuela, | Costa Rica (Isla del Coco) | Venezuela (Amazonas: Cerro Yapacana) | Brazil (Bahia, Pará) | Colombia (Valle del Cauca) | Guyana (Cuyuni-Mazaruni: Pakaraima Mtns.) | Nicaragua, Costa Rica, Panama |
Humiriaceae
share stamens partly connate, filaments subulate and complanate, and anthers that are dorsifixed, versatile, caducous, lacking stomata, and possessing connective protrusions. Most of these shared androecial features are broadly distributed, even in combination, across the rosids (
Vantanea has long been considered the most ancestral genus of Humiriaceae based on androecial structure (
Disporangiate-dithecal anthers are often correlated with specialized floral biology, which can be enabled by restrictive anther openings such as valves (
We documented EFNs in all species of Humiriaceae, and found distributional and morphological differences. Some of these differences appear informative at the generic level, including the marginal glands of Humiria, entire eglandular margins of Vantanea, and the exceptionally large laminar glands of Hylocarpa. Our EFN survey, although mostly qualitative in nature, also reveals that their species-level taxonomic value is limited due to high variation in abundance and position, and low intra-specific morphological variation. The EFN ubiquity indicates that they are phylogenetically conserved (i.e., plesiomorphic) for the family, and is a conclusion that differs greatly from character reconstructions that could be hypothesized under the prior understanding of their taxonomic distribution in only three species. This conclusion is also important when considering EFN evolution in the broader context of Malpighiales where they have been documented in 13/39 families (
We thank Alice Tangerini for the botanical illustration, Stanley Yankowski for the floral anatomy, Marcelo Pace for the description of gross wood structure, Ana S. S. de Holanda for sharing further observations on pollination biology, Peter Endress for stamen perspectives, Paul Berry and Domingos Cardoso for constructive comments, the NMNH Scanning Electron Microscopy Lab, and MO, NY, and US for relevant collections. For fieldwork, we thank the other members of the 2012 Kamakusa Expedition including Aleks Radosavljevic, Karen Redden, Erin Tripp, and the Amerindian team led by James Ralph. That expedition was supported by the National Geographic Society / Waitt Grants Program (Redden, PI), and the Biological Diversity of the Guiana Shield Program (BDG) of the Smithsonian Institution.
Qualitative survey of Humiriaceae for extrafloral nectaries and leaf margin features. For abaxial glands not near margins, relative exmedial distances (midvein to margin) are indicated where patterns are apparent.
Taxon | Abaxial glands | Basilaminar (adaxial) glands | Leaf margin features | Representative voucher(s) |
---|---|---|---|---|
Duckesia | ||||
D. liesneri (Cuatrec.) K. Wurdack & C.E. Zartman | Absent | 1–2 pairs at margin | Crenate, setae present | Liesner & Carnevali 22589 (US, holotype) |
D. verrucosa (Ducke) Cuatrec. | Sparse, 0–3 per leaf, 2/3 exmedial distance | Absent | Crenate, setae present, large | Ducke 2106 (US) |
Endopleura | ||||
E. uchi (Huber) Cuatrec. | Row near margin | Absent | Crenate, setae long and scars large | Assunção 605 (US) |
Humiria | ||||
H. balsamifera var. coriacea Cuatrec. | Marginal, along proximal third | Absent | Entire | Cardona 1823 (US, holotype) |
H. balsamifera var. floribunda (Mart.) Cuatrec. | Marginal, along entire length | Absent | Entire | Maguire & Politi 27974 (US) |
H. balsamifera var. guaiquinimana Cuatrec. | Marginal, along proximal third | Absent | Entire | Cardona 1112 (US, holotype) |
H. balsamifera var. guianensis (Benth.) Cuatrec. | Marginal, along entire length | Absent | Entire | Schomburgk 270 (US, isotype) |
H. balsamifera var. iluana Cuatrec. | Marginal, along proximal half | Absent | Entire | Maguire 33388 (US, holotype) |
H. balsamifera var. imbaimadaiensis Cuatrec. | Marginal, along proximal half | Absent | Entire | Maguire & Fanshawe 32158 (US, holotype) |
H. balsamifera var. laurina (Urb.) Cuatrec. | Marginal, along entire length | Absent | Entire | Schomburgk 560 (US, isotype) |
H. balsamifera var. minarum Cuatrec. | Marginal, along entire length | Absent | Entire | Mexia 5815 (US, holotype) |
H. balsamifera var. parvifolia (A. Juss.) Cuatrec. | Marginal, along proximal half | Absent | Entire | St. Hilaire (US, isotype fragment) |
H. balsamifera var. pilosa (Steyerm.) Cuatrec. | Marginal, along entire length | Absent | Entire | Steyermark 60289 (NY, isotype) |
H. balsamifera var. savannarum (Gleason) Cuatrec. | Marginal, along entire length or proximal half | Absent | Entire | Tate 330 (NY, type); J. Wurdack & Monachino 41380 (US) |
H. balsamifera var. stenocarpa Cuatrec. | Marginal, along entire length | Absent | Entire | Maguire & Maguire 40105 (US, holotype) |
H. balsamifera var. subsessilis (Urb.) Cuatrec. | Marginal, dense along entire length | Absent | Entire | Spruce 2454 (US, isotype) |
H. crassifolia Mart. | Marginal, sparse, denser at base and apex | Absent | Entire | Huber & Fernandez 11331 (US) |
H. fruticosa Cuatrec. | Marginal, 2–4 per side near base | Absent | Entire | Maguire et al. 36580 (US, holotype) |
H. wurdackii Cuatrec. | Marginal, along entire length, widely spaced; absent on very narrow forms | Absent | Entire | J. Wurdack & Adderley 42760 (US, holotype); Huber 4842 (US), narrow-leaved |
Humiriastrum | ||||
H. columbianum (Cuatrec.) Cuatrec. | Sparse abaxial; absent on type, save for a few erratic structures that could be damage. | Absent | Serrate, setae long | Lamb 141 (US, holotype); best gland evidence is on Gentry & Stein 46898 (US); Romero Castañeda 4942 (US) |
H. cuspidatum (Benth.) Cuatrec. | Small, sparse, near margin | 1 pair, elliptic | Crenate, setae long and thin | J. Wurdack & Monachino 40881 (US) |
H. cuspidatum var. glabriflorum (Ducke) Cuatrec. | Small, sparse, near margin | 1 pair at margin (sometimes a single gland) | Serrate, setae scars | Ducke [JBRJ-23436] (US, isotype) |
H. cuspidatum var. subhirtellum Cuatrec. | Small, sparse, near margin | 0–1 pair | Serrate, setae present | Fróes 25463 (US) |
H. dentatum (Casar.) Cuatrec. | Small, sparse, near margin | 1 pair at margin, nearly abaxial | Serrate, setae present | Hatschbach 4294 (US) |
H. diguense (Cuatrec.) Cuatrec. | Along secondary vein loops toward margin | 1–3 pairs at margin, nearly abaxial | Crenate, setae scars | Cuatrecasas 14956 (US, isotype) |
H. diguense var. anchicayanum (Cuatrec.) Cuatrec. | Along secondary vein loops toward margin | 1 pair at margin, nearly abaxial | Crenate, setae scars | Cuatrecasas 14418 (US, isotype) |
H. diguense subsp. costaricense Cuatrec. | Along secondary vein loops toward margin, relatively sparse | 1 pair | Crenate, setae relatively stout, clearly terminating veins | Allen 5812 (US, holotype) |
H. excelsum (Ducke) Cuatrec. | Near secondary vein loops toward margin, relatively sparse | 1 pair at margin | Crenate, setae present | Museu Goeldi 9672 (US) |
H. glaziovii (Urb.) Cuatrec. | Absent | 1 pair at margin, nearly abaxial | Serrate, setae present | Pabst 4726 (US) |
H. glaziovii var. angustifolium Cuatrec. | Absent | 1 pair at margin, nearly abaxial | Crenate, setae scars | Glaziou 16724 (US, holotype) |
H. mapiriense Cuatrec. | Sparse, toward margin | 0–2 pairs | Crenate, setae scars | Buchtien 1518 (US, isotype) |
H. melanocarpum (Cuatrec.) Cuatrec. | Very rare on few leaves, scattered, hard to distinguish from potential leaf damage | Absent | Crenate, with setae | Cuatrecasas 19909 (US); best gland evidence is on Prance 28055 (US) |
H. mussunungense Cuatrec. | Absent | 0–1 pair at margin, nearly abaxial | Crenate, setae present | Folli 1393 (US, holotype) |
H. obovatum (Benth.) Cuatrec. | Sparse, scattered | 0–1 pair at margin, nearly abaxial | Subentire, setae scars sparse, hirsute | Schomburgk 1359 (US) |
H. ottohuberi Cuatrec. | Row near margin | 1–3 pairs, oval | Obscurely crenate, setae present | Steyermark & Bunting 102442 (US, holotype) |
H. piraparanense Cuatrec. | Tiny, sparse, near margin | 1–2 pairs | Crenate, setae scars | Schultes & Cabrera 15922 (US, holotype); glands better developed on García-Barriga 14287 (US) |
H. procerum (Little) Cuatrec. | Towards margin along loops between secondary veins | 1(–2) pairs at margin | Crenate, setae scars | Little & Dixon 21148 (US) |
H. subcrenatum (Benth.) Cuatrec. | Absent | 1 pair at margin | Crenate, setae scars | Martin s.n. (US, type fragment) |
H. villosum (Fróes) Cuatrec. | Tiny, sparse, in row near margin | 1 pair at margin, small | Serrate, setae scars | Humbert & Schultes 27363 (US) |
Hylocarpa | ||||
H. heterocarpa (Ducke) Cuatrec. | Large, erratic, near secondary or intersecondary veins, 1/2–2/3 exmedial distance | Absent | Subentire, setae scars | Ducke [JBRJ-30137] (US, isotype |
Sacoglottis | ||||
S. amazonica Mart. | Small, near margin | 1 pair | Obscurely crenate, setae scars | J. Wurdack 293 (US) |
S. ceratocarpa Ducke | Relatively large, near margin | 1 pair, large, narrowly elliptic, at margin of leaf base extension | Subentire, setae present | Fróes 21192 (US) |
S. cydonioides Cuatrec. | Tiny, near margin | 1 pair, elliptic, sometimes large | Serrate, tooth tips with darkened spots (setae scars?) | B.W. [Surinam Forestry Dept.] 4720 (US) |
S. gabonensis (Baill.) Urb. | Absent | 1(–2) pairs at margin | Crenate, setae present | McPherson 13714 (US) |
S. guianensis Benth. | Small, row near margin | 0–1 pair at margin | Shallowly crenate; setae present, more persistent than is typical | Schomburgk 574 (NY, syntype) |
S. guianensis var. hispidula Cuatrec. | Tiny, near margin | Absent | Serrulate, setae scars | Krukoff 6653 (US, holotype) |
S. guianensis var. maior Ducke | Small, row near margin | Absent | Crenate; setae more persistent than is typical | Ducke [JBRJ- 23818 (US, isotype) |
S. holdridgei Cuatrec. | Small, row near margin | 1(–2) pairs | Shallowly crenate, setae scars | Holdridge 5164 (US, isotype) |
S. maguirei Cuatrec. | Sparse (0–2), tiny, near leaf apex margin, most leaves lacking | Absent | Shallowly crenate, setae scars | Maguire et al. 30693 (US, holotype) |
S. mattogrossensis var. subintegra (Ducke) Cuatrec. | Small, sparse, near margin | Absent | Subentire, setae scars obscure | Ducke [JBRJ-23820] (US, isotype) |
S. ovicarpa Cuatrec. | Absent | 1 pair | Subentire, setae scars | Cuatrecasas 17226 (US) |
S. perryi K. Wurdack & C.E. Zartman | Tiny, near margin | 1 pair, relatively small, obscure | Shallowly crenate, setae present | McDowell 2920 (US) |
S. trichogyna Cuatrec. | Absent | 1 pair | Shallowly crenate, setae scars | Holdridge 5216 (US, isotype) |
Schistostemon | ||||
S. auyantepuiensis Cuatrec. | Tiny, with reticulate veins near margin | 1 pair, large elliptic | Very obscurely crenate, setae scars | Davidse & Huber 22804 (US) |
S. densiflorus (Urb.) Cuatrec. | Small, row near margin | 0–1 pair | Obscurely crenate, setae present | Schomburgk 543 (US isotype) |
S. dichotomus (Urb.) Cuatrec. | Small, row near margin | 1 pair | Crenate, setae scars | Sabatier 989 (US) |
S. fernandezii Cuatrec. | Near margin | 1 pair, oval | Obscurely crenate, small setae present | Fernandez 2276 (US, holotype) |
S. macrophyllus (Benth.) Cuatrec. | Row near margin, widely spaced | 1 pair, elliptic | Shallow teeth, setae scars | Ducke 1744 (US) |
S. oblongifolius (Benth.) Cuatrec. | Near margin | 1–2 pairs | Small, shallow teeth, setae scars | Maas et al. 6804 (US) |
S. reticulatus (Ducke) Cuatrec. | Near margin | 1–2 pairs at base, up to 3 per side near apex | Obscurely crenate | Ducke [JBRJ- 23819] (US, isotype), Klug 1564 (US) |
S. reticulatus var. froesii Cuatrec. | Near margin | 1 pair at base, no glands at apex | Subentire, setae scars sparse | Fróes 21370 (US, isotype) |
S. retusus (Ducke) Cuatrec. | Near margin, relatively regular all the way to tip | 1 pair, large | Subentire, setae scars sparse | Cuatrecasas 7203 (US) |
S. sylvaticus Sabatier | Row near margin | 1–2 pairs at base | Very obscurely crenate, setae scars | Loubry 1074 (US) |
Vantanea | ||||
V. bahiaensis Cuatrec. | Tiny, near secondary or intersecondary veins | 1 pair | Entire | Belém & Magalhães 748 (US); Carvalho & Gatti 484 (NY, holotype) |
V. barbourii Standl. | Near secondary or intersecondary veins | 1 pair | Entire | Hartshorn 2139 (US) |
V. celativenia (Standl.) Cuatrec. | Row 1/3 exmedial distance | 1 pair, often others near base | Entire | Krukoff 7182 (US, isotype) |
V. compacta (Schnizl.) Cuatrec. | Tiny, near intersecondary veins near margin | 0–4 pairs per side | Entire | Hatschbach 21265 (US) |
V. deniseae W.A. Rodrigues | Near secondary or intersecondary veins | Absent | Entire | Freitas et al. 860 (US) |
V. depleta McPherson | Near secondary veins, row half exmedial distance | 1 pair | Entire | McPherson & Stockwell 10892 (US, isotype) |
V. guianensis Poir. | Scattered | Absent | Entire | Maguire et al. 56006 (US) |
V. macrocarpa Ducke | Scattered | Absent | Entire | Ducke 2230 (US) |
V. magdalenensis Cuatrec. |
Tiny, near secondary and intersecondary veins | 1 pair | Entire | Lamb 133 (US, holotype) |
V. micrantha Ducke | Scattered | Absent | Entire | Ducke 751 (US) |
V. minor Benth. | Large, sparse, proximal half near primary vein | Absent | Entire | Liesner 23974 (US) |
V. morii Cuatrec. | Absent | 2(–4) pairs | Entire | Mori & Benton 13181 (US, holotype) |
V. obovata Benth. | Near secondary or intersecondary veins | 1–2 pairs | Entire | Anderson et al. 36781 (US) |
V. occidentalis Cuatrec. |
Large, near intersecondary veins, row 1/3 exmedial distance | Absent | Entire | Patiño 12 (US) |
V. ovicarpa Sabatier | Tiny, close to secondary veins | 0–1 pair, rarely others near base | Entire | Granville 10792 (US) |
V. paraensis Ducke | Near secondary or intersecondary veins | 1 pair, often others along secondary near base | Entire | Ducke [JBRJ-23430] (US) |
V. parviflora Lam. | Along loops of secondary veins, near margin | Row of 2–4(5) pairs, usually close to mid-vein | Entire | Prance et al. 17770 (US) |
V. parviflora var. puberulifolia Cuatrec. | Along loops of secondary veins, near margin, usually surrounded by vein | 2 (1–3) pairs, closer to midvein | Entire | Ducke [JBRJ-23428] (US, holotype) |
V. peruviana J.F. Macbr. | Large, row, mostly near intersecondary veins, 1/4–1/3 exmedial distance | Absent | Entire | Rimachi 4577 (US) |
V. spichigeri A.H. Gentry | Row, 1/5 way to margin, often near secondary veins | 1–2 pairs | Entire | Abadie s.n. 12-9-74 (US), Spichiger et al. 1743 (NY, isotype) |
V. spiritu-sancti (Cuatrec.) K. Wurdack & C.E. Zartman | Sparse, small along secondary or intersecondary veins, half exmedial distance | 1–2 (type); 5–7 pairs along proximal edge | Entire | Dolcolmo [JBRJ-86212] (US, isotype fragment); Silva et al. 1436 (US), more abundant |
V. tuberculata Ducke | Along secondary veins, half exmedial distance | Absent | Entire | Ducke [JBRJ-30134] (US, isotype) |