Digitaria clarkiae Sánchez-Ken, 2017

Sánchez-Ken, J. Gabriel, 2017, Digitaria clarkiae (Paniceae, Panicoideae, Poaceae), a new species with a paniculate synflorescence, and the first record of D. costaricensis from México, Phytotaxa 321 (1), pp. 125-138 : 126-131

Digitaria clarkiae Sánchez-Ken , sp. nov. ( Figs. 1 , 2 )

Type:— MÉXICO. Puebla, Mpio. Tilapa, 2 km del entronque con la carretera Cuautla-Izúcar por la carretera a Atlapanala, aprox. 5 km W de Izúcar, [18º35’ N, 98º33’ W], 320 m, 4 September 1995, L. Aragón 362 (holotype MEXU!, isotype MEXU!).

Annuals or apparently short-lived perennials. Culms 35–75 cm tall, erect, ascending; internodes shorter or longer than the leaf-sheaths, 3–5.5 cm long, branching towards the base or in the middle, glabrous; nodes brown, the lower ones shortly hirsute becoming glabrous towards the synflorescence; sheaths shorter or longer than the internodes, the lower ones hirsute becoming nearly glabrous towards the synflorescence, sometimes only papillose-hirsute at the base or sparsely pilose on the sides at the summit; collar narrow, yellowish; ligules 0.6–2.5 mm long, membranous, glabrous, the edges sometimes separating like auricles, apex erose; blades 6–12(–15) × 3–7(–9) mm, the lower ones much shorter, lanceolate, membranous, both surfaces hirtellous becoming glabrescent or distally sparsely puberulent, midvein thickened, margins scabrellous, base slightly narrowed, apex acute; synflorescence 13–20(–25) cm long, terminal and commonly axillary, paniculate, open, diffuse, base commonly enclosed in the uppermost sheath, not breaking up at maturity; branches 9–12 per synflorescence, 7–15 cm long, alternate, distributed along an axis, spikelets at the base paired, sometimes in threes or rarely solitary (when one is reduced or absent with only the pedicel remaining, which apparently becomes a sterile branch), rachis capillary, pulvini sometimes at the base and also on each pair of spikelets; pedicels 7–24(–37) mm long, capillary, scabrellous; spikelets 2.7–3.2 × 0.6–0.8 mm, elliptic to slightly lanceolate, all similar; glumes heteromorphic, separated from the florets by a rachilla ca. 0.1 mm long; first glume 0.1–0.2 mm long, ovate, membranous, glabrous, veinless; second glume 2.1–3.1 mm long, 3-veined, scarcely to densely pilose between the veins and along margins, the hairs up to 0.5 mm long, white to sometimes purplish, apex acute, usually exceeding the apex of the fertile lemma; sterile lemma 2.4–3.1 mm long, 7-veined, the veins unequally spaced, the three central veins widely spaced, the four lateral veins closer to the margins, spaces between the central veins glabrous, spaces between the marginal the veins scarcely to densely pilose, the hairs up to 0.8 mm long, white to purplish, apex acute; sterile palea 0.3–0.7 mm long, hyaline, abaxially papillose; fertile lemma 2.4–2.7 × 0.7–0.8 mm, 3-veined, lanceolate to elliptic, cartilaginous, pale green to yellowish, softly papillose, glabrous, margins membranous, apex acute; fertile palea as long as and similar to the fertile lemma, glabrous, 2-veined; lodicules 2, minute, fleshy; stamens 3, anthers 0.2–0.3 mm long; caryopses 1.65–1.7 × ca. 0.7 mm, ovate, slightly flattened, white, hilum 1/2–1/3 as long as the embryo, oblong, embryo 1/3 as long as the caryopsis.

Distribution and Habitat: —The new species is endemic to México, known only from the states of Guerrero, Morelos and Puebla ( Fig. 5 ), where it grows in tropical deciduous forests at elevations of 320 to 1500 m.

Phenology: —Flowering September and October. The synflorescences of the specimens Aragón 450 and 366 have several apical spikelets that are abnormally long. These spikelets are up to 5.5 mm in length (normal length 2.7–3.2 mm), bear two masculine florets and the anthers seem to dehisce before they are exposed from the bracts. Parasites might cause the formation of masculine florets. Wipff & Hatch (1994) also noted that anthers dehisced before they were exposed from the bracts in D. arenicola and D. cognata . It will be necessary to study anther dehiscence on living plants to better understand this observed abnormality in the development of the spikelets.

Etymology: —The specific epithet, clarkiae , honors Professor Lynn G. Clark at Iowa State University, who has made an extensive contribution to understanding of Poaceae systematics, and who was my major professor during my graduate studies.

Micromorphology: —The lemma epidermis of D. clarkiae is composed of long cells with lobed parietal walls, and with papillae on the distal end. The long cells are longitudinally arranged with the papillae not coinciding horizontally nor longitudinally ( Figs. 2B , 4C ). Macrohairs of the second glume and sterile lemma are elongated, with smooth walls and an acute apex. The epidermis of the first glume has swollen long cells with sinuous walls intermixed with dumbbell-shaped silica bodies, these almost shaped like an X ( Fig. 2A ) and without indumentum. Lodicules of the fertile floret are rhomboid, truncate, short, fleshy, glabrous, and appear wrinkly, probably due to dehydration ( Fig. 2 ).

Overall, lemma epidermis morphology of D. clarkiae is similar to that of most species of the genus; however, the papillae in D. clarkiae are not longitudinally or horizontally aligned like in D. arenicola , D. cognata , D. patens and D.

pubiflora ( Fig. 4 : C, F, I, L, O). The lengths of the long cells, and the separation and sizes of the papillae ( Fig. 4 : C, F,

I, L, O), vary among these species.

Photosynthetic Pathway: —The C 4 photosynthetic pathway of D. clarkiae was confirmed by hand sections of leaf blades ( Fig. 3 ). The leaves have the Kranz Mestome Sheath anatomy, subtype NADP-dependent malic enzyme

(NADP-ME), where the vascular bundles have one bundle sheath with cells with centripetal chloroplasts ( Webster

1981, Vega et al. 2009, Rao & Dixon 2016) and with one or two chlorenchyma cells in the mesophyll between vascular bundles.

Additional Specimens Examined: — MÉXICO. Guerrero: Mpio. Zitlala, Coacoyul , [17º49’ N, 99º06’ W], 1100 m, 8 September 1994, U. González Q. 788 ( MEXU) ; Mpio. Tepecoacuilco de Trujano, 2 km al N de Mezcala , [17º56’ N, 99º36’W], 1500 m, October 1981, G. Campos 271 ( MEXU). Morelos: Mpio. Tepalcingo, Ixtlilco el Grande, 1 km, [18º32’N, 98º50’W], 980 m, 28 September 1993, O. López A. 62 ( MEXU). Puebla: Mpio. Albino Zertuche, paraje La Cañada Grande, aprox. 8 km al SW de Tulcingo de Valle a 5 km del entronque con la carretera Tulcingo-Atlapa por la terracería a Acaxtlahuacán, [17º59’N, 98º29’W], 1400 m, 7 September 1995, L. Aragón 422 ( MEXU) ; Mpio. Chiautla, Cerro Pelón, Km 17 brecha Colucan-Chiautla , [18º28’N, 98º28’W], 1300 m, 27 September 1985, I. Núñez et al. 248 ( MEXU) ; Mpio. Chinantla, barranca La Puerta, 16 km al SW de Tehuitzingo, carretera a Axutla , [18º13’N, 98º20’W], 960 m, 6 September 1995, L. Aragón 400 ( MEXU) ; Mpio. Petlalcingo, 16 km al SE de Acatlán, carretera a Huajuapan de León , [18º09’N, 97º58’W], 1370 m, 7 September 1995, L. Aragón 452 ( MEXU) ; Mpio. Teotlalco, Mina de Almadre , 20 km S de Axochiapan sobre la carretera Axochiapan-Jolalpan , aprox. 2 km de Tlaucingo, [18º22’N, 98º49’W], 960 m, 5 September 1995, L. Aragón 366 ( MEXU) ; Mpio. Xayacatlán de Bravo, a la orilla del río, 2 km al W de Xayacatlán de Bravo, carretera Acatlán-Totoltepec , [18º14’N, 97º59’W], 1250 m, 7 September 1995, L. Aragón 450 ( MEXU) .

Related Species: —The combination of morphological characters of D. clarkiae is unique and does not align with any existing section of Digitaria . As such, sectional classification of the new species must await molecular study. Based on some morphological characters, the closest section might be Pennatae sensu Clayton & Renvoize (1986), characterized by having pedicelled spikelets often in groups, with pedicels shortly pilose and primary branches radiating stiffly. This section includes the American species with paniculate synflorescences ( D. arenicola , D. cognata and D. pubiflora ) that are often deciduous, like the “tumbleweeds” of the Australian species also classified in sect. Pennatae (i.e., D. divaricatissima ( Brown 1810: 192) Hughes (1923: 314) and D. coenicola ( Mueller 1855: 45) Hughes (1923: 313)) . The other morphologically close section is Trichachne sensu Clayton & Renvoize (1986) , whose species have paired spikelets with an elongated rachilla between the glumes and the florets (e.g., D. patens ). Recently, the circumscription of this section was tested in a phylogenetic study based on ITS and morphological data ( Lo Medico et al. 2017). In that study, the species of sect. Trichophorae were embedded in a clade with species of sect. Trichachne . Accordingly, Lo Medico et al. (2017) emended the circumscription of the latter section to include perennial plants with knotty or spreading rhizomes, and abundant long whitish, purplish to ochraceous hairs on the second glume and sterile lemma.

The paniculate, open and diffuse synflorescence of D. clarkiae suggests the new species is near subg. Leptoloma sensu Henrard (1950) (or the corresponding sect. Pennatae of Clayton & Renvoize 1986). Indeed, all specimens of the new species were previously misidentified as either D. cognata or D. pubiflora , which have similar synflorescence morphologies. These two species were included in subg. Leptoloma by Chase (1906), circumscribed it to include all known American and Australian species with paniculate synflorescences. However, Henrard (1950) divided subg. Leptoloma , leaving the American species within it and placing the Australian species in the sect. Pennatae of the typical subgenus. According to Henrard (1950), subg. Leptoloma is characterized by having genuine, effuse, and divaricate panicles, without verticillate primary branches with solitary spikelets. However, the American species do not fit entirely this circumscription because some specimens have verticillate to subverticillate primary branches of the synflorescence and paired spikelets that sometimes, by reduction of one spikelet, appear solitary. Based on these observations, D. arenicola , D. cognata and D. pubiflora should have been placed in sect. Pennatae, not in subg. Leptoloma , as treated by Henrard (1950).

Clayton & Renvoize (1986) simplified the subdivisional classification of Digitaria by suggesting a new infrageneric classification of the genus, with only sections recognized. All American, Australian and Indian species with paniculate synflorescences and secondary branches bearing long axes were placed in sect. Pennatae, returning to Chase´s (1906) concept of subg. Leptoloma . Wipff & Hatch (1994) studied the American species and recognized sect. Pennatae in the sense of Clayton & Renvoize (1986); they stated that the species have long pedicelled spikelets, primary branches of the synflorescence spreading, synflorescence usually disarticulating as a unit at maturity, and a perennial habit. Following the interpretation of Wipff & Hatch (1994), the Australian species would be part of sect. Pennatae, and the Indian species D. tomentosa (J. Koenig ex Rottler 1803: 220) Henrard (1934: 100) would be placed elsewhere in the genus.

Of the three American species of sect. Pennatae, it was assumed only D. cognata and D. pubiflora occurred in México ( Dávila et al. 2006, Herrera & Cortés 2010). However, Sánchez-Ken (2012) confirmed the presence of D. pubiflora and D. arenicola of sect. Pennatae in México. Digitaria arenicola , which was thought to be restricted to the Texas coast ( Wipff & Hatch 1994, Wipff 2003), is now also known from the state of Tamaulipas, México, about 130 km south of the border of Mexico and Texas ( Sánchez-Ken 2012). Digitaria pubiflora is distributed from Arizona to central Texas and south to central México (Guanajuato, Jalisco and Veracruz), whereas D. cognata is restricted to the United States ( Wipff & Hatch 1994, Sánchez-Ken 2012). Digitaria clarkiae has a restricted distribution in south central México, known only from the states of Guerrero, Morelos and Puebla ( Fig. 5 ).

Digitaria clarkiae shares with the American species of sect. Pennatae the paniculate synflorescence with primary branches spreading, secondary branches with long axes, long pedicels, as well as the rare presence of sterile branches. Wipff & Hatch (1994) mentioned sterile branches at the base of the synflorescence of the American species of sect. Pennatae; these branches are indeed pedicels on which the spikelets are aborted. In some specimens of D. clarkiae , some spikelets similarly are aborted and appear to be sterile branches, but are actually pedicels. Even though these characters are shared, other diagnostic characters prevent the inclusion of the new species in sect. Pennatae. These other diagnostic characters of sect. Pennatae are the sterile lemma veins equally spaced and pilose, the papery and longer first glume and the absence of an elongated rachilla between the glumes and the florets. In D. clarkiae , the branches of the synflorescence are alternate and never verticillate or subverticillate, the synflorescence does not disarticulate at maturity, the habit is annual or short-lived perennial without a knotty base, the spikelets are paired or rarely solitary, with the second glume 3-veined, the sterile lemma central vein spaces unequal and glabrous, the first glume minute and membranous and an elongated rachilla between the glumes and florets present ( Table 1, Fig. 4A ).

The synflorescences of most species of Digitaria have a peduncle, a shortened or elongated axis and primary branches. These primary branches may be spaced along an elongated axis, verticillate, or may arise along a shortened axis, having a digitate arrangement. On each primary branch, the spikelets are either solitary, paired, or in groups of three or more. When the spikelets are solitary by reduction or abortion of spikelets, they may be sessile, forming a spicate primary branch (sect. Solitaria ), or pedicelled, forming a paniculate primary branch. In the latter case (i.e. species with spikelets paired or in groups of three or more) the spikelets belong to secondary branches. These secondary branches may have a very short axis, like most species with paired spikelets (e.g., D. ciliaris ( Retzius 1786: 16) Koeler (1802: 27) in sect. Digitaria ) or like D. michoacanensis Sánchez-Ken (2012: 129) in sect. Ischaemum , which has spikelets in groups of three or more arising on a short axis. However, there are also species with secondary branches with one, two, or more spikelets in which the axis is elongated, such as species in sections Pennatae and Ischaemum sensu Clayton & Renvoize (1986) , as well as D. clarkiae . The elongated axes and long pedicels that bear two (paired) or more spikelets makes the synflorescences appear as a “true panicle”, as interpreted by Henrard (1950) and McVaugh (1983). Following this interpretation, almost all species of the genus Digitaria , except those from sect. Solitaria , have “true panicles”.

The presence of an elongated rachilla between the glumes and florets in D. clarkiae suggests it may be related to sect. Trichachne . Section Trichachne is characterized by having perennial species with knotty rhizomes, paired and lanceolate spikelets, and an elongated rachilla between the glumes and the florets. The latter character is called the stipe of the fertile floret by Clayton & Renvoize (1986) and Lo Medico et al. (2017). The synflorescences in species of sect. Trichachne are paniculate with loose primary branches that are usually rebranched and verticillate at the base, or sometimes subdigitate to digitate ( Stapf 1898), and the secondary branches have a short axis. Many authors (e.g., Henrard 1950, Clayton & Renvoize 1986) refer to the primary branches as racemose, although, as explained above, the spikelets, which are either solitary or in groups, arise from a shortened or elongated axis along the primary branch forming a paniculate synflorescence.

Digitaria clarkiae has elliptical spikelets more similar to those of species sect. Pennatae than in sect. Trichachne , whose species have lanceolate spikelets ( Fig. 3 ). However, the presence of an elongated rachilla between the glumes and the florets, and the unequally spaced veins of the sterile lemma, link D. clarkiae to sect. Trichachne , although the species of this section are perennial with knotty bases and the secondary branches have a short axis. The American species of sect. Pennatae lack a short rachilla between the glumes and the florets, and the veins of the sterile lemma are equally spaced ( Fig. 4 : A, D, G, J, M).

Given the complexity of the classification of Digitaria , the lack of a comprehensive phylogeny on which to base a classification, and the fact that the new species does not clearly fit any of the known sections, the new species is best classified as incertae sedis in the genus.

Figures

FIGURE 1. Digitaria clarkiae. A. Plant. B. Ligular area. C. Synflorescence branching pattern. D. Spikelet frontal view showing first glume and sterile lemma. E. Spikelet showing second glume. F. Sterile palea. G. Fertile floret. From the type (L. Aragón 362, MEXU).

FIGURE 2. Micromorphology of Digitaria clarkiae. A. First glume. B. Fertile lemma. C. Lodicules of fertile floret. From the type (L. Aragón 362, MEXU).

FIGURE 3. Hand section of leaf blade of Digitaria clarkiae. From the type (L. Aragón 362, MEXU).

FIGURE 4. Spikelet morphology of Digitaria clarkiae and species of sections Pennatae and Trichachne. Incertae sedis: Digitaria clarkiae (A-C). A. Spikelet adaxial view. B. Spikelet abaxial view. C. Fertile lemma. Sect. Trichachne: D. patens (D-F). D. Spikelet adaxial view. E. Spikelet abaxial view.F. Fertile lemma. Sect. Pennatae: D. pubiflora (G-I). G. Spikelet adaxial view.H. Spikelet abaxial view. I. Fertile lemma. D. cognata (J-L). J. Spikelet adaxial view. K. Spikelet abaxial view. L. Fertile lemma. D. arenicola (M-O). M. Spikelet adaxial view. N. Spikelet abaxial view. O. Fertile lemma.

FIGURE 5. Distribution of Digitaria clarkiae (solid black rhomboids) in Guerrero, Morelos and Puebla, and of D. costaricensis in Veracruz (solid black circle).