Greenwoodiella deserticola Salazar, Hernández-López & J. Sharma, 2016

Salazar, Gerardo A., Hernández-López, Tania J., Sharma, Jyotsna, Jiménez-Machorro, Rolando, Cabrera, Lidia I. & Treviño-Carreón, Jacinto, 2016, Greenwoodiella, a New Genus of Spiranthinae (Orchidaceae) from North and Central America and the Greater Antilles, with a New Species from the Chihuahuan Desert, Systematic Botany (Basel, Switzerland) 41 (4), pp. 823-838 : 831-834

Greenwoodiella deserticola Salazar, Hernández-López & J. Sharma , sp. nov. — TYPE: MEXICO. Tamaulipas: municipio Miquihuana, Sierra de Miquihuana, 6 km al NW de la Colonia Agrícola La Peña, camino a Las Cabañas, lado este del camino, bosque de Pinus nelsonii ,

2,227 m elev., 3 May 2013, Hernández-López & Treviño-Carreón 166 (holotype: MEXU!).

Terrestrial, acaulescent herb 23–47 cm in height including the inflorescence. Roots 2–4 per shoot, tuberous, subspherical to cylindrical-fusiform, dull yellow, glabrous to sparsely pubescent, 10–65 mm long, 6–15 mm in diameter, united to the clump of roots of the previous shoot by a terete, whitish rhizome to ca. 30 mm long, 1.2– 2.4 mm in diameter. Leaves usually 1 per shoot, less commonly 2 but then the second (uppermost) leaf distinctly smaller than the first one; deciduous, withered at flowering time, distinctly petiolate, in fresh condition fleshy, lustrous, petiole green suffused with purple, blade deep green and rugose (because of the slightly prominent veins) on the upper surface, grayish with purple suffusion and smooth on the underside, margins translucent; petiole channeled, 20–30 mm long, 2– 2.5 mm wide; blade ovate to elliptic, acute or shortly acuminate, base broadly rounded, 32–44 mm long, 26–33 mm wide. Inflorescence erect; scape terete, olive green to greenish red, glabrous below, sparsely glandular-pubescent above (trichomes short, septate, translucent with yellowish apical cell), partially covered by 5–10 tubular, strict, glabrous bracts, these green or green suffused with red (often distinctly reddish in dried condition), ovate, acuminate, 4.2–10. 5 mm long; raceme laxly few-flowered (2–15 in the specimens examined), most flowers directed more or less toward the same side (but not strictly secund), 3–15 cm long. Floral bracts ascending, glabrous, green with reddish tip, lanceolate, acuminate, 6–7. 5 mm long. Flowers resupinate, shortly tubular-campanulate, slightly descending, opening in succession until several of them are open simultaneously; dorsal sepal deep green on the proximal 2/3, becoming paler towards the apex, sometimes suffused with red; lateral sepals pale green near the base, turning paler toward the apex, sometimes suffused with red; petals brownish, labellum white with a large yellow area covering most of the proximal two thirds. Ovary ascending, fusiform, obliquely arching at apex, slightly twisted, green to greenish red, sparsely glandular-pubescent (trichomes shortly clavate, with the translucent apical cell prominent), 4–8 mm long, 1.2– 2.1 mm in diameter. Sepals slightly inflated at base, free; dorsal sepal erect, externally pubescent as the ovary on the proximal half, slightly concave-channeled, oblong-elliptic, obtuse, the very apex slightly incurved, three-veined, 3.5–6. 5 mm long, 2– 2.8 mm wide; lateral sepals erect, slightly incurved, externally pubescent as the ovary near the base, oblong-triangular, slightly oblique, obtuse, three-veined, 3.5–6. 8 mm long, 1.8– 2.2 mm wide. Petals erect, slightly concave-channeled, adhered for most of their length to the dorsal sepal, spathulatefalcate, rounded, sometimes shortly apiculate, one-veined, 4–6 mm long, 1– 1.6 mm wide. Labellum erect with the distal third slightly deflexed, shortly clawed, shortly and broadly pandurate, with 7 main veins, 5.0–6. 3 mm total length, claw ca. 0.5 mm long, 1.5 mm wide; hypochile more or less quadrate, ca. 3.5 mm long and 4.1 mm wide, with a broad sinus on each lateral margin and a rounded, retrorse lobule at each side of the base, these ending in a slightly raised, papillose thickening (nectar gland), blade with a prominently papillose, transverse ridge slightly below the middle, the papillae diminishing in size towards the claw, the surface above the transverse ridge smooth; epichile semiorbicular, ca. 2.5 mm long, 3.5 mm wide, deeply emarginate, conduplicate at apex in natural position, papillose throughout, margins crenulate. Column shortly clavate, straight, ventrally pubescent, 2.8– 3.5 mm long, column foot conspicuous, ca. 1 mm long; rostellum abbreviated, upon removal of the pollinarium consisting of a narrow, transverse flap with a triangular central tooth and two smaller lateral teeth. Anther ovate, acute, brownish, with fleshy connective; pollinarium ca. 0.4 mm long, consisting of two deeply cleft, oblong pollinia united to a massive, oblong-ovate viscidium. Capsule ellipsoid, 12 mm long, ca. 4 mm in diameter. Figures 1 , 5 .

Etymology — The specific epithet, deserticola , refers to the distribution of this species on the eastern margin of the Chihuahuan Desert.

Distribution and Habitat — This species is known only from two locations, one in the area of Miquihuana, Sierra Madre Oriental, Tamaulipas, and another in the Chisos Mountains, Big Bend National Park, southern Texas. However, there are extensive areas with potentially suitable habitat between these two localities, and it is likely that further exploration will reveal its presence in the intervening ranges in Coahuila and Nuevo León. It lives in sandy loam soil covered with leaf litter in areas with xerophilous scrub dominated by rosette-leaved plants such as Dasylirion miquihuanense Bogler and Agave gentryi B. Ullrich , with patches of Quercus sp. and Pinus nelsonii Shaw , and in oak-juniper-pinyon woodland, at 2,100 –2,300 m elevation. It has often been found occurring in the shade of large plants of Agave and Dasilyrion. Considering its very limited known distribution in Big Bend National Park, the U. S. National Park Service is drafting a Conservation Plan for the newly discovered species. While the remoteness of the known locations might minimize the threats of trampling and collection in both the U. S. A. and Mexico, official conservation planning is a prudent step to safeguard the species for which additional locations are currently unknown.

Phenology — Flowering recorded in the field from March to May, and in cultivation in January and March. Mature dehiscing fruits that had already dispersed the seeds were observed in the field in mid-July ( Fig. 1J ).

Remarks — Greenwoodiella deserticola is distinguishable from its relatives at once by the proportionately short flowers, labellum with a large yellow blotch on the hypochile, five green veins on the epichile, proportionately short and broad labellum about as long as wide and provided with a fleshy, transverse ridge below the middle, and deeply emarginate epichile ( Figs. 1 , 5 ).

Additional Specimens Examined — MEXICO. Tamaulipas: municipio Miquihuana, Sierra de Miquihuana , 4.5 km al NW de la Colonia Agrícola La Peña , camino a Las Cabañas , matorral rosetófilo de Dasylirion miquihuanense , 2,122 m elevation, collected 18 Jan. 2013, pressed in cultivation 8 March 2013, Hernández-López & Treviño-Carreón 151 ( MEXU) ; same locality, 23 March 2013, Hernández-López & Treviño-Carreón 152 ( MEXU) ; same locality, 3 May 2013, Hernández-López & Treviño-Carreón 163 ( MEXU) . U.S.A. Texas: Big Bend National Park , east-facing slope, 2,100 –2,200 m elev., collected 17 Aug. 2013, pressed in cultivation 29 Jan. 2015, Sharma JS 0001 ( AMES) .

Greenwoodiella micrantha (Lex.) Salazar & R. Jiménez , comb. nov. Neottia micrantha Lex. , Nov. Veg. Descr. 2: 5. 1825. Spiranthes llaveana Lindl. ex Benth., Pl. Hartw. 72. 1839, non auct., replacement name for Neottia micrantha Lex. — Schiedeella llaveana (Lindl. ex Benth.) Schltr., Beih. Bot. Centralbl. 37(2, Heft 3): 380–381. 1920.—TYPE: [Mexico. Michoacán:] “Habitat versus Sancta Maria et Jesus, prope Vallisoletum, floretque aprili”, Lexarza s.n. (not located). NEOTYPE (here designated): MEXICO. Michoacán: municipio Morelia, km 19 S of Santa María [del Guido] on road to Jesús del Monte, 2,020 m elev., 22 March 1987, Greenwood & Soto 1318 (AMO!; isoneotype: MEXU!). Figure 6 .

Schiedeella romeroana Szlach., Rhodora 95: 2. 1993.—TYPE: MEXICO. Oaxaca: km 6.3 from Ixtlán, on brecha N from km 5.8 on Natividad road, elev. 2,100–2,400 m, pine-oak- Arbutus forest, in shade, in bud, flower and unripe capsule, very few spikes seen, 18 March 1984, Greenwood 1185 (holotype AMO!; isotypes AMO!, MEXU!).

Distribution and Habitat — Endemic to Mexico. This auto-pollinating variety has been recorded in the Transverse Volcanic Belt (Michoacán) and the Sierra Madre Oriental (northern Oaxaca). Terrestrial, in leaf mold in Pinus - and Pinus-Quercus forest, often with other broadleaved trees such as Arbutus , Styrax , Carpinus , Symplocos , and Ternstroemia . From 2,000 to 2,400 m elevation.

Phenology — Flowering from late February to early April. Well-developed fruits were observed in late March and April.

Remarks — For nearly two centuries, the identity of Neottia micrantha Lex. remained obscure. Lexarza’ s (in de la Llave and Lexarza 1825) treatment of the orchids of (mostly) the surroundings of Morelia, then Valladolid, Vallisoletum, was the first comprehensive inventory of this family for any region of Mexico, and it is outstanding because of its detailed descriptions and specified locality data. Most of the 50 orchid species proposed by Lexarza have been recognized and accepted in subsequent works (e.g. Williams 1951; McVaugh 1985; Soto 1988; Espejo and López-Ferrari 1997, 1998; Hágsater et al. 2005; Soto et al. 2007), although some remain difficult to identify because, with the exception of Alamania punicea Lex. , Lexarza’ s specimens have not been located ( Espejo et al. 1993). Nevertheless, a careful read of the protologue of N. micrantha and its comparison with modern records of all the terrestrial orchids occurring in the region of Morelia — one of the floristically best-known areas of Mexico — demonstrates that it closely matches the plants subsequently described both as Schiedeella garayana ( González 1993) and S. romeroana ( Szlachetko 1993) . This species is relatively common and widespread in south/central Mexico, although its inconspicuous leaves, inflorescences and flowers are easily overlooked ( Fig. 2A–H, J, K ).

The specimen we selected as the neotype of Neottia micrantha (Greenwood & Soto 1318) comes from the type locality indicated by Lexarza , on the road between Santa María del Guido and Jesús del Monte in what today are the outskirts of the city of Morelia. It is significant that, in a handwritten note relative to this collection, Greenwood noted the existence of variation in column morphology, with populations with and without a rostellum (E. W. Greenwood, in litt., AMO!): “[This plant] is distributed in many parts of southern and central Mexico, and sometimes is abundant. Most interesting is that it commonly auto-pollinates, but there are plants with perfect flowers, others somewhat modified, and others completely lacking a rostellum; however, it is not cleistogamous” (free translation by G.A.S.). Greenwood also prepared detailed line drawings of fresh flowers from his specimen, reproduced here as Fig. 6 , which clearly show the column lacking a rostellum and with pollinium fragments stuck to the stigmatic surface. Oddly, Szlachetko (1992b; Szlachetko et al. 2005) misidentified specimen Greenwood & Soto 1318 as Schiedeella amesiana , failing to associate it with Neottia micrantha in spite of both coming from the same place. Neither Szlachetko (1992b) nor Szlachetko et al. (2005) provided any information on the type of N. micrantha , which suggests that they did not see the protologue and that may explain why they did not relate the modern specimen (Greenwood & Soto 1318) with N. micrantha .

A careful comparison of Greenwood and Soto’ s Morelia specimen with another specimen collected by Greenwood in northern Oaxaca (Greenwood 1185), which is the holotype of Schiedeella romeroana , demonstrates that they are indistinguishable in all respects, including the erostellate column ( Figs. 2C , 6I–J ). This conclusion is further supported by our phylogenetic analysis, as the accession from the type locality of S. romeroana analyzed (Salazar et al. 6118, labelled “ Greenwoodiella micrantha mic . ” in the phylogenetic trees of Figs. 3 and 4 ) is mixed with samples of cross-pollinating G. micrantha var. garayana from Guerrero (Salazar et al. 7420), Michoacán (Salazar et al. 9225), and Morelos (Soto & Jiménez-Machorro 10691). The cross-pollinating, rostellate populations, represented by the plant described by González (1993) as Schiedeella garayana , are treated here as G. micrantha var. garayana (see later).

As noted earlier, the name Schiedeella llaveana has long been misapplied to the distinctive species for which the first validly published name is Spiranthes transversalis A. Rich. & Galeotti (i.e. Schiedeella transversalis ). Bentham (1839 -1857: 72), quoting a manuscript of Lindley, proposed Spiranthes llaveana as a new name for Lexarza’ s Neottia micrantha . In fact, nearly simultaneously Lindley (1840: 458) published Neottia micrantha for a different species, a genuine member of Neottia Guett. from China. It is difficult to understand how this clear-cut fact escaped the attention of most subsequent authors, in spite of McVaugh’ s (1985: 342) conclusive clarification of the issue:

“By a strict interpretation of the International Code of Botanical Nomenclature, Spiranthes llaveana Lindl. was illegitimate when published, Lindley having based the name entirely on Neottia micrantha Lex. , without including any word of description (Pl. Hartw. 72. Mar 1840). At that time he should not have provided a new epithet, but should have transferred Neottia micrantha to Spiranthes , assuming that he believed his plant to belong to the same species as that of Lexarza . Later the same year (Gen. & Sp. Orch. Pl. 474. Sep 1840), Lindley referred to the name published earlier in Plantae Hartwegianae, provided a description based on Hartweg’ s plant, and queried the earlier identification of this plant, Spiranthes llaveana , with Neottia micrantha Lex. Those who now wish to use the epithet llaveana argue that Lindley really meant in March 1840 what he wrote in September 1840, and thus never thought that the specimen he studied belonged to the same species as Neottia micrantha .”

Some authors have considered Neottia micrantha Lex. as a synonym of Schiedeella transversalis (as S. llaveana ; e.g. Williams 1951; McVaugh 1985; Szlachetko 1992b; Szlachetko et al. 2005). However, S. transversalis , as other genuine members of Schiedeella s. s., has a narrowly elliptic leaf blade with attenuate base ( Fig. 7D–F ), it is leafless at flowering time ( Fig. 7G ), and the epichile of its labellum is not distinctly expanded nor crenulate ( Fig. 7H ), all which conflicts with Lexarza’ s description of N. micrantha .

Additional Specimens Examined — MEXICO. Oaxaca: municipio Capulalpam de Méndez, 0.5 km por la brecha que parte 4.3 km al E de Ixtlán de Juárez hacia La Natividad. 2,140 m elev., 25 March 2000, Salazar et al. 6118 ( MEXU) ; municipio San Juan Tepeuxila, camino Tepeuxila- Tlacolula , 2,048 m elev., collected 10 July 2004, pressed in cultivation 2 March 2005, Salazar et al. 6653 ( MEXU) .

Figures

FIG. 1. Greenwoodiella deserticola A. Group of three plants during the phase of vegetative growth in the shade of Dasylirion miquihuanense at the Sierra de Miquihuana, Tamaulipas, Mexico (Hernández-López & Treviño-Carreón 166). B. Front view of an inflorescence of one of the same plants. C. Side view of inflorescence of another plant growing nearby. D. Flower from side (Tamaulipas, Mexico, Hernández-López & Treviño-Carreón 151). E. Same flower from front. F. Two plants in bud and early flowering (marked with arrowheads) growing near Agave sp. at Big Bend National Park, Texas (Sharma JS0001). G. Plant from the Texas population removed from soil. H. Plant from same population starting blooming in situ. I. Close-up of flower. J. Dehiscing, empty capsules. Photographers: A–C: Tania Hernández-López; D–E: Gerardo A. Salazar; F–G: Jyotsna Sharma; H–I: Ron Coleman; J: Joe Sirotnak.

FIG. 5. Greenwoodiella deserticola. A. Flowering plant. B. Inflorescence. C. Floral bract. D. Flower, oblique view. E. Flower, front view. F. Flower, side view. G. Flower from side with sepals and petals excised to show the labellum partially clasping the column. H. Dorsal sepal. I. Petal. J. Lateral sepal. K. Labellum. L. Column, side view. M. Column, ventral view. N. Ventral view of column apex after removal of the pollinarium showing the rostellum remnant. O. Pollinarium, side view. P. Pollinarium, ventral view. Q. Pollinarium, dorsal view. Drawn with camera lucida by Rolando Jiménez-Machorro from Hernández-López & Treviño-Carreón 151.

FIG. 6. Floral analysis of the neotype of Neottia micrantha (Greenwood & Soto 1318), basionym of Greenwoodiella micrantha var. micrantha. A. Flower, oblique view. B. Flower, side view. C. Flower, front view. D. Flower viewed from above. E. Flower viewed from below. F. Labellum and column in natural position from above. G. Labellum and column in natural position from side. H. Labellum, spread out. I. Column from side. J. Column from below showing fragments of pollinia on the margins of the stigma. K. Rostellum from above. L–N. Pollinarium removed from an unopened flower bud (at anthesis the fusion of the pollinia bases to the stigma precludes removal of a complete pollinarium). L. Pollinarium from below. M. Pollinarium from side. N. Pollinarium from above. Drawn with camera lucida by E. W. Greenwood. Courtesy of Herbario AMO.

FIG. 2. A–C. Greenwoodiella micrantha var. micrantha (Mexico, Oaxaca, Salazar et al. 6653). A. Inflorescence from side. B. Close-up of flower. C. Ventral view of column apex showing the absence of rostellum and the “melting” of the pollinium bases in contact with the stigmatic fluid, which results in autopollination. D–K. Greenwoodiella micrantha var. garayana (Mexico, Guerrero, Salazar et al. 7420). D. Small group of plants in situ. E. Plant removed from soil showing the leaf upper surface. F. Same as previous showing the leaf underside. G. Leaf upper surface showing the leathery, rough texture. H. Leaf underside showing the characteristic grayish-green coloration and purplish petiole and central vein. I. Roots of two shoots from consecutive growth seasons joined by a slender rhizome. J. Inflorescence from side. K. Inflorescence from front. L–P. Greenwoodiella wercklei (Mexico, Puebla, Pérez-Bravo 100). L. Flowering plant in situ. M. Leaf upper surface. N. Leaf underside. O. Inflorescence from side. P. Inflorescence from front. Photographer: Gerardo A. Salazar.

FIG. 3. Strict consensus trees from maximum parsimony analyses of the separate datasets. A. Plastid matK-trnK and trnL-trnF DNA sequences. B. Nuclear ITS region. Numbers below branches indicate bootstrap percentages.

FIG. 4. Phylogenetic relationships in Spiranthinae inferred by maximum parsimony (A) and maximum likelihood (B) analyses of combined plastid (matK-trnK, trnL-trnF) and nuclear (ITS) DNA sequences. Numbers below branches indicate bootstrap percentages. Numbers within filled circles mark clades discussed in the text. Gray shading indicates the position of Schiedeella transversalis, type species of the genus Schiedeella.

FIG. 7. A–C. Morphology of Mesadenus polyanthus (Mexico City, Salazar 7370). A. Clump of three plants in situ growing on basaltic rock in a xerophilous scrub just after flowering (note the brownish, drying scapes). B. Portion of inflorescence. C. Close-up of flowers. D–H. Morphology of Schiedeella transversalis (D–F: Mexico, Chiapas, Salazar s.n.; G–H: Mexico, Oaxaca, García-Mendoza et al. 8489). D. Two plants growing on a moist roadside bank. E. Leaf upper side. F. Leaf underside. G. Flowering plants. H. Close-up of flowers. Photographer: Gerardo A. Salazar.