Vigna (Lasiospron)

Delgado-Salinas, Alfonso, Lavin, Matt, Snak, Cristiane & Lewis, Gwilym P., 2022, Systematics of Vigna subgenus Lasiospron (Leguminosae: Papilionoideae: Phaseolinae), Systematic Botany (Basel, Switzerland) 47 (1), pp. 97-124 : 99-107

VIGNA SUBG. LASIOSPRON (Benth.) Marechal, Mascherpa & Stainier , Taxon 27: 201 (1978).

TYPE: Vigna lasiocarpa (Benth.) Verdc. , designated by Verdcourt (1970: 539).

Phaseolus section Strophostyles sensu Bentham , pro parte, Comm. Leg. Gen.: 74 (1837); Hassler in Candollea 1: 462 (1923), non Elliot; Piper in Contr. U.S. Natl. Herb. 22: 677 (1926).

Phaseolus section Strophostyles emend. Benth. , in Martius, Flora Brasiliensis 15(1): 187 (1859).

Vigna section Lasiospron (Benth.) Verdc., Kew Bulletin 24: 539 (1970).

Perennials or occasionally annuals, scrambling or climbing (sinistrorsely) vines up to 5 m or more long, with foliage and reproductive parts covered with yellow hairs, these often over 1 mm long, some individuals also conspicuously invested with minute glandular hairs. Stems herbaceous, hollow, angulate (sturdy), older ones lignescent, frequently developing adventitious roots, stems and roots reported to have nodules. Leaves entire or seldom lobed, rarely with sinuous margins, membranaceous to chartaceous, oblong to ovate or widely ovate, sometimes rhombic or linear-lanceolate, usually obtuse or acute or even acuminate at apex, with 3 basal or supra-basal nerves (one prominent and central, and one to either side), lateral leaflets asymmetrical, lateral vein on the broader side diverging ca. 30, venation brochidodromus; stipules extended at the base or point of insertion, scarcely to distinctly and unequally bilobed or very distinctly spurred (sometimes adnate to the stem), membranaceous to chartaceous, triangular to lanceolate, 6–10-veined, not reflexed, persistent; stipels oblong to triangular, often trapezoidal, shorter than petiolules, glanduliferous due to glandular hairs; petioles mostly shorter than terminal leaflets, petioles and rachis bifacial, adaxially canaliculate, drying angled. Inflorescences few-flowered pseudoracemes, the flowers clustered at the apex, 2 flowers per node, the nodes adhering laterally to the rachis, swollen, with few to ca. 10 vestured glanduliferous orifices, these sparsely scattered or distributed in rows; primary and secondary bracts caducous, bracteoles mostly persistent at anthesis, as long or twice as long as the calyx tube, bracts and bracteoles lanceolate and at base geniculate, often spurred; pedicels shorter than calyx tube, longer and twisting in fruit, covered with straight, retrorse hairs; calyx campanulate, calyx-teeth generally short and subequal or forming two lips, the upper lobe broad and emarginate or the sinus as deep as the other three lower lobes, the lower lobe (two laterals and one central tooth) mostly equalling the tube length. Flowers predominately orange yellow or greenish yellow, glabrous; standard petal asymmetric, deeply emarginate or bilobed at apex, two parallel callosities on the centre of lamina at the point of folding, with two thick, fleshy auricles at the margins above the claw, the portion of the lamina immediately above the claw covered with micro-papillae; wing petals longer than keel, right wing (flower’ s right-side seen from the front) positioned clearly as a landing platform for visiting insects, the left wing (flower’ s left side) distally clasping around the left-side wall of the keel; keel distinctly beaked, loosely coiled to ca. 270 or through ca. 360, twisted to the right side of the flower, the keel wider at region of connation with wings; stamens 10, diadelphous, the single free stamen with a broad or cup-shaped appendage on the basal portion; pollen grains triporate, with coarsely reticulate exine, interstitium granular; ovary with a basal nectary disc less than 1 mm long, lobed distally; ovules few to many, style tenuous to variously thickened, with a short, curled or spreading pollen brush, twisted at the apex, thus placing the stigma sideways and mostly extended beyond the stigma and projected into a horn-like or hook-like appendage, stigma small, elliptic or transversely ovate, introrse [= opening inwards and a term usually referring to anthers] or terminal, sparsely ciliate. Fruit inverted by a post-pollination twisting of the pedicel, patent (diverging from the axis at ca. 90), or held erect (parallel to rachis), often placed on one side of the rachis (secund), straight to slightly falcate, subcylindrical or flattened, valves membranaceous or coriaceous, turning dark brown or black at maturity, covered with bristly, yellow, straight hairs, elastically dehiscent. Seeds asymmetrical, broader than long (D-shaped), compressed to subglobose (surrounded in fruit by a membranaceous whitish layer), hilum oblong, as long as seed width, covered by an epihilum and this often by a short epi-groove, with a distinctly raised rim-aril, and often with a conspicuous white membranaceous aril towards the lens. Seedlings with hypogeal germination. Chromosome number: 2 n = 20 or 22.

Etymology — Bentham (1837) possibly named this group of plants Lasiospron to emphasize the hairiness of their pods: Lasio (hairy); spron (beak).

Taxonomic History —The taxonomy of this group of plants began with Bentham (1837), who published five new species in his taxonomic treatment of the genus Phaseolus . In Phaseolus section Strophostyles (Elliott) Benth., Bentham described Phaseolus schottii , P. longifolius , and P. ovatus , and an unnamed variety under the last. In addition, P. hirsutus and P. lasiocarpus were described under a newly proposed Phaseolus section Lasiospron Benth. Bentham classified P. pilosus Kunth (1823) under Phaseolus section Leptospron Benth. In his treatment of the genus in Flora Brasiliensis, Bentham (1859) synonymized P. schottii under P. longifolius , P. hirsutus under P. lasiocarpus , and recircumscribed P. campestris Benth. (1837) . All these were included within P. section Strophostyles and not within Bentham’ s P. section Lasiospron . Chodat and Hassler (1904) and later Hassler (1923), in his treatment of the genus for South America, reduced all published taxa classified under P. section Strophostyles to two species, Phaseolus schottii with four varieties (and six formas) and P. pilosus with two varieties. Piper (1926) recognized only four species in this group, P. hirsutus , P. campestris , P. schottii , and P. pilosus . Verdcourt (1970), as part of a taxonomic study of subtribe Phaseolinae for the Flora of Tropical East Africa, which involved delimiting the genus Phaseolus , transferred this group of species into the reinstated section under Vigna Savi and recognized only three species, V. lasiocarpa , V. juruana , and V. longifolia . Marechal et al. (1978) raised V. section Lasiospron to the subgenus rank under Vigna and followed Verdcourt’ s species classification. Lackey (1983) preferred the placement of V. subg. Lasiospron under V. subg. Vigna and followed again Verdcourt in recognizing only three species.

In sum, taxonomic misconception and uncertainties likely result, in part, from the similar morphologies of the six V. subg. Lasiospron species, which are all adapted to thrive in riparian and wetland habitats. In addition, ambiguities occur in original species descriptions, such as Hassler’ s (1923) description of P. schottii var. campestris , which combines diagnostic traits of more than one species (see Notes under Vigna juruana ). Imprecise label information of critical herbarium specimens causing taxonomic uncertainty is exemplified by Vigna trichocarpa (see Notes under this species). Original and type specimens have been lost, as in the case of the holotype of V. juruana . We thereby provide a modern taxonomic synthesis of Vigna subg. Lasiospron , a group that has puzzled taxonomists for almost 200 yr.

Morphological, Ecological, and Karyological Traits ( Figs. 5–6 ) —Habit. All species of Vigna subg. Lasiospron are vines, mostly herbaceous and rarely woody and then mostly with age and at the base of the stem, which climb mainly on trees at forest edges particularly along riparian corridors. Stems. Mainly herbaceous, hollow or with a spongy pith, angulate (sturdy), becoming lignescent with age. Floating stems of Vigna lasiocarpa have been reported carrying nitrogen fixing nodules on adventitious roots and on stems, but vascularly attached to the bases of adventitious roots ( James et al. 2001). Vegetative multiplication by stems occurs in plants of Vigna lasiocarpa ( Pott and Pott 2000) . Climbing direction in Vigna longifolia has been noted in the field label of the herbarium specimen Ahumada et al. 3373 (K), which records the direction of twining from left to right (sinistrorsum), when in other species it is from right to left. Leaves. The leaflets display a wide variation in size and shape even within the same species. They range in form from narrowly linear to broadly ovate, sometimes even with lobes at the base. In addition to showing different shapes, Vigna lasiocarpa leaflets have undulate margins. Due to this variation, leaflet shape and size are not reliable characters for species separation. Stipules and stipels. The stipules are moderately appendaged or distinctly produced below their point of insertion. The upper portion is generally lanceolate or widely triangular, and always conspicuously veined. The lower portion or appendage can be a single spur or bilobed ( Fig. 5A–B ). The texture varies from membranaceous to somewhat chartaceous and brittle. Stipules tend to be loosely fixed to stems, although often, as in V. lasiocarpa , they are closely adnate to the stem. Stipels are mostly ovate, although trapezoidal forms also occur. They tend to be covered with minute glandular hairs forming a nectariferous area. Inflorescence and node ’ s extrafloral nectary. The inflorescences of Vigna subg. Lasiospron are pseudoracemes, where all secondary branches have been completely reduced and transformed into cushion-like glanduliferous nodes that generally carry two flowers each. These nodes are attached laterally to the inflorescence rachis and have few to ca. 10 vestured secretory orifices or extrafloral nectaries ( Marazzi et al. 2019). These orifices are distributed sparsely or in close rows ( Fig. 5C–F ). In Vigna subg. Lasiospron species the shape of these nodes varies, as does the placement of the secretory orifices. The nodes in Vigna juruana are spatuliform, and the orifices are distributed in a scalariform pattern, with transverse separations, whereas in Vigna lasiocarpa , the nodes are elliptical and voluminous, and the orifices are displayed in two rows. In other species of the subgenus, they are subspherical or obpyriform, with the orifices distributed in a sparse-alternate pattern, and no transverse separations are visible.

Although notably different in shape and orifice distribution, the nectaries present in Vigna subg. Lasiospron may have a similar vascular supply to that found in Vigna unguiculata (L.) Walp. ( Kuo and Pate 1985). These extrafloral nectaries in V. lasiocarpa have been reported to be active during the day even when the plants are fruiting ( Lewis and Owen 1989) and are often visited by bees of the genus Trigona (da Silva et al. 2384) and by other Hymenoptera ( Hoc et al. 1993) . In Argentina, Hoc et al. (1993) registered wasps and ants actively sucking nectar from the inflorescence nodes. Ants were observed patrolling the plant displaying deterrent behaviour against other visitors to the plant. Flower. Flower colour varies from yellow to greenish yellow ( Fig. 5D ). The standard petal is deeply emarginate or bilobed at its apex and is sometimes not fully extended because the standard bends backwards in anthesis, leaving a portion of the margins joined to form a hood. On the internal face of the standard petal, two parallel thickenings or appendages, and two prominent, thick fleshy auricles, are located above a short petal claw. The concavity or furrow produced by the backward bending of the standard at anthesis, enclosed by the parallel thickenings and auricles, is papillate. This protected region directs the bee’ s mouth parts to the nectary, which is located at the base of the gynoecium.

Wing petals are adnate to the keel by their claws, and by their positioning upon the keel lateral pocket. Wing sculpturing occurs mainly on the right-side wing (as observed from the front of the flower). The sculpturing is in a lamellate pattern in the upper basal and upper central regions of the petal, and the upper basal margins of the petal are incurved. The auricles in the upper basal region are thick and fleshy, and in V. juruana a line of four to five hairs or cilia are present. These interlock with the basal auricles of the standard. The right-side wing petal extends distally and rotates to form a landing platform, whereas the left-side wing is held vertically and distally embraces the keel, thus blocking entry to the nectary by unwanted flower visitors.

Keel petals are united to each other for almost their whole length and form a tubular structure that encloses the androecium and gynoecium. The keel is curved at its mid-length position and there held erect between the wings; distally it is curved and rotated towards the right side of the flower. The two keel petal claws are strongly adnate to the staminal tube, whereas their lateral basal walls have a concave pocket and fold which attaches them to the wing petals, thus forming a lever mechanism of the four united petals when a pollinator lands on them. A semi-circular opening of the keel apex exposes the protruding stigma which is adjusted for nototribic or pleurotribic pollination.

The androecium is diadelphous and comprises nine stamens partially united to form a staminal sheath or tube, and one free vexillary stamen. The vexillary stamen filament has a conspicuous appendage just above its base. The appendage upper surface is verrucate. Verrucate surfaces are also present on adjacent margins of the staminal tube, constituting a shield that protects the ovary, as a visiting insect’ s proboscis searches for the basal fenestrae that lead to the nectary cavity. Stamen filaments are cylindrical with vascular traces running internally. The walls of the filaments have spirally coiled, free, elongate epidermal cells ( Fig. 6A–B ). These stretchy interweaved walls may provide the filament with some degree of elasticity that may play a role in promoting pollen transfer to the stylar pollen brush. Anthers are uniform, oblong in shape, basifixed to almost dorsifixed, and of longitudinal dehiscence.

Pollen grains are characterized by being triporate and with a wide reticulum, as seen in other species of Vigna ( Marechal et al. 1978) . Their shape is suboblate to oblate, with a semi-angular to angular outline as viewed from the polar region ( Fig. 6D–F ). Pores comprise a globular to granulate operculum membrane. Pollen studies have described the interstitium as granular (non-orientated to orientated, and without a foot layer; Horvat and Stainier 1980; Ferguson and Skvarla 1983). However, the interstitium has been reported for Vigna lasiocarpa as columellar ( Di Stilio 1994).

The gynoecium comprises a sessile, non-stipitate, straight ovary, with a lobed basal nectary disc confined within the base of the staminal tube. The length of the style is highly variable and ranges from around 1.5 cm in V. juruana to 5–6 mm in V. lasiocarpa . The style is thread-like or tenuous for about one-third of its length, then thickened uniformly for the next third, and narrows once again for the final third. A pollen brush is confined to the upper part of the style and is made up of curly ( Fig. 6H ) or straight hairs ( Fig. 6I ). The style-tip may be curved inwards to very different degrees, placing the stigma in a subterminal position ( Fig. 6G ), except in V. juruana where it is in an apical position ( Fig. 6I ). The stigma bears a whorl of non-receptive, short hairs ( Drewes and Gamba 2011). In mature flowers of Vigna lasiocarpa the stigma surface produces a copious exudate and is located at the opening of the keel.

Pollination Studies —Flowers of Vigna longifolia and V. diffusa are effectively pollinated by bees of the genus Megachile , and V. diffusa by Apis mellifera , Bombus morio , and Xylocopa brasilianorum ( Hoc et al. 1993; Souza et al. 2017, initially reported as V. longifolia but later determined to be V. diffusa ). Pollen transference is nototribic, placing the pollen in an area between the head and thorax of the bee, or pleurotribic and sternotribic, in the case of the deposition of the pollen of V. diffusa in the entire metasoma, where the pollen brush slides from the dorsal to the ventral region in Megachile spp. ( Hoc et al. 1993; Souza et al. 2017). Label data of da Silva et al. 2384 (in herb.) mentioned that large bees ( Fig. 6E ) are struck by the stigma on the side of their bodies (pleurotribic) while visiting the flowers of V. lasiocarpa .

Fruit and Seeds —The pods in Vigna subg. Lasiospron are usually laterally flattened, with chartaceous, thin valves ( Fig. 5G ). However, in Vigna lasiocarpa and V. longifolia the pods are nearly cylindrical, with their valve walls thicker than those of the rest of the species in the subgenus. Pod valves are covered with golden-yellow appressed hairs which turn black on drying. Pods are usually elastically dehiscent ( Fig. 5H ) along both sutures and the pedicels rotate and twist as the fruit matures, presenting it in either an ascending or pendent position. In an ascending position the abaxial suture faces the inflorescence axis, whereas in the pendent position the abaxial suture faces upwards. Seed orientation in the pod is mostly with its long axis parallel to the suture, although in V. lasiocarpa it tends to be somewhat oblique. Funicles in nearly all species are short, except in V. trichocarpa where they are approximately 1 mm.

Seeds vary in size and shape and are sometimes almost isodiametric to oblong-elliptic. Although more generally flattened to some extent, in V. lasiocarpa and V. longifolia seeds tend to be subglobose. In these two species, a white hippocrepiform aril develops at the edge of the hilum ( Fig. 5I ); the other four species have variable or no aril development ( Table 1 ). Arils are found also in some species of Old World Vigna such as in wild plants of Vigna aconitifolia (Jacq.) Marechal ( Takahashi et al. 2016) . A comparison of some morphological characters of the species of V. subg. Lasiospron is presented in Table 1 .

Seed Dispersal —Marsh deer, waterfowl, and cattle have been seen eating the foliage and seeds of Vigna species in the Brazilian Pantanal ( Pott and Pott 1994, 2000). Waterfowl species that breed in North America and winter in Central and South America and the Antilles, which migrate across the Atlantic to Africa, are potentially able to disperse seeds over long distances ( Somenzari et al. 2018). Species with a seed aril could be dispersed by birds and vertebrates. The widest ranging New World species, Vigna lasiocarpa and V. longifolia , have seed arils that are consistently well developed. In contrast, the least widely ranging species, Vigna schottii , has seed arils that are variably developed. However, the three amphi-Atlantic species, Vigna trichocarpa , V. juruana , and V. diffusa , have seed with little or no aril development ( Table 1 ), suggesting the development of cartilaginous arils is not required for long distance trans-oceanic dispersal.

Chromosome Numbers —Chromosome counts of three Vigna subg. Lasiospron species have been reported ( Marechal 1969; Senff et al. 1992, 1995; Mercado-Ruaro and Delgado-Salinas 1996; Schifino-Wittmann 2000). Vigna diffusa (as V. longifolia ) and V. longifolia have 22 somatic chromosomes, with counts of 2 n = 22, whereas V. lasiocarpa is a dysploidy species, with a chromosome count of 2 n = 20. These counts conform with the overall pattern found in Vigna ( Goldblatt and Johnson 1979; Costa et al. 2019), which is a base chromosome number of n = 11 being most common, and base number of n = 10, 12, and others uncommon.

Synapomorphies of Vigna Subg. Lasiospron —In a mature flower, the distal portion of the keel twists to the right-hand side of the corolla, often into a complete coil. Pedicels, which are shorter than the calyx tube, twist following pollination to render the adaxial suture of the fruit upside down (resupinate). Fruits are pendent or ascending and their valves turn brown or black at maturity.

Figures

FIG. 5. Photographic images of reproductive structures of Vigna subg. Lasiospron. A. Stipules peltate or medifixed of Vigna trichocarpa (Snak 1066). B. Stipules with a bilobed spur of Vigna diffusa (Snak 269). C. Vigna lasiocarpa floral buds, notice the long bracts and bracteoles and the arrow pointing to extrafloral nectaries (Vibrans 8246). D. Vigna diffusa flower (Snak 269). E. Xylocopa brasilianorum pollinating V. diffusa (Snak 501). F. Pods of Vigna lasiocarpa, with rotated pedicels (Vibrans 8246). G. Flattened pods of Vigna trichocarpa (S~ ao-Mateus s.n.). H. Nearly cylindrical, dehiscent pods of Vigna lasiocarpa (Vibrans 8246). I. Seed aril of Vigna lasiocarpa (Vibrans 8246). Photographs taken by Wallace M. B. S~ ao-Mateus, Cristiane Snak, and Heike Vibrans.

FIG. 6. SEM images of reproductive structures of Vigna subg. Lasiospron. A. Vigna diffusa, dorsifixed anther with pollen grains. B. detail of filament showing helically orientated, intertwining arrays of cell walls. C. Vigna schottii, detail of filament showing cell walls helically orientated. D. Vigna diffusa, triporate pollen grains, equatorial and polar view. E. Vigna lasiocarpa, pollen grain, equatorial view. F. Vigna lasiocarpa, pollen grain, polar view. G. Vigna longifolia, stigma with wet stigmatic membrane and hooked style-tip (arrow). H. Vigna juruana, pollen brush of style comprising curly hairs. I. Vigna schottii, truncate stigma with fringed hairs and secretion containing pollen grains. Specimens: (A, B, D) Vigna diffusa (Cordeiro 616); (H) Vigna juruana (Henkel 5321); (E) Vigna lasiocarpa (Jansen-Jacobs 5019); (G) Vigna longifolia (Vibrans 8246); (F) Vigna longifolia (Kew Slide Collection 279); (C, I) Vigna schottii (Zardini 8650). Scale bars on images A–I. SEM photos by Hannah Banks. Image G, by H. Vibrans.