Desmopsis terriflora G.E.Schatz, T.Wendt, Ortiz-Rodr. & Martinez-Velarde, 2023

Martinez-Velarde, Maria Fernanda, Rodrigues-Vaz, Carlos, Soule, Vincent, Nge, Francis J., Schatz, George E., Couvreur, Thomas L. P. & Ortiz-Rodriguez, Andres Ernesto, 2023, Desmopsis terriflora, an extraordinary new species of Annonaceae with flagelliflory, PhytoKeys 227, pp. 181-198 : 181

Desmopsis terriflora G.E.Schatz, T.Wendt, Ortiz-Rodr. & Martinez-Velarde sp. nov.

Figs 1 , 2 , 3 , 4 , 5 , 6

Type.

Mexico. Veracruz, Municipio Uxpanapa, Ejido Progreso Chapultepec , 17°13'58.9"N, 94°18'20.5"W, 105 m, 26 Abril, 2022 (fl,yfr), Ma. F. M. Velarde 72 (holotype MEXU; isotypes: MO, P) .

Diagnosis.

Desmopsis terriflora is similar to Stenanona flagelliflora since both species have flowers and inflorescences growing exclusively on flagella. Desmopsis terriflora differs from it by the combination of larger-sized individuals, flowers with rigid petals, food bodies at the base of the inner petals, fused sepals, a greater number of carpels and ovules per carpel, by its monocarps with a hard and woody testa, and its flagella up to 15 meters in length (Table 2 ).

Trees, 7-10 m tall, 12-45 cm DBH, bark dark green, verrucose in vivo, dark brown when dry, young branches and terminal shoots golden sericeous. Leaves membranaceous, alternate, distichous, broadly elliptic to oblong-elliptic, 17-31 cm long,4-10 cm wide, base obtuse to rounded, apex acute to acuminate, young leaves golden sericeous on both sides, mature leaves glabrous above and below, venation brochidodromus, 13-18 secondary veins per side, barely elevated to impressed above, raised below, the midrib impressed above but slightly canaliculate toward the base (sometimes with erect to appressed pale brown hairs), raised below and sparsely covered by golden brown hairs, petiole swollen, canaliculate, 5-8 mm long, sparsely covered by golden brown hairs. Inflorescences flagelliflorous, 5-20 woody flagella per trunk, glabrous, shoots emerging from the main trunk from near the base to 2 to 3 m high, then buried in the leaf litter just below the surface (subterranean), to 15 m long, branching; leaves and roots absent, apical parts of flagella greenish and thin, becoming progressively dark and woody toward the base, bearing perennial rhipidia at leafless nodes: the rhipidia terminal but lateral at each node because the flagellum keeps growing by a renewal shoot. Flower bearing part of the generally inflorescence erect, protruding above the leaf litter; Flowers 1 or 2 per inflorescence, flowering pedicels 8-30 mm long, densely covered by golden brown hairs, borne in the axil of a minute, clasping, ovate bract, and bearing a second minute, clasping ovate bract ca. midway, each bract 2 mm long, 2 mm wide, apex acute, outer surface densely covered by golden brown hairs, sepals 3 (rarely 4), valvate, connate at the base, triangular, 3-10 mm long,3-4 mm wide, apex obtuse, outer surface sparsely covered by minute golden brown hairs, glabrous on the inner surface, petals 6 (rarely 8), free, subequal, in two whorls, thick and stiff, pinkish-red, outer petals oblong-lanceolate 13-16 mm long,4-5 mm wide, apex obtuse to acute, outer surface sparsely covered by minute golden brown hairs, essentially glabrous on inner surface, margin ciliate, inner petals oblong-lanceolate, 17-20 mm long, 4-6 mm wide, apex acute, outer surface sparsely covered by minute golden brown hairs, essentially glabrous on inner surface, food bodies (an abrupt thickening) in the basal adaxial side, often with white striations below the food bodies, stamens ca. 30, 1.5-1.7 mm long, the filament 0.3 mm long, thecae 1-1.3 mm long, the anther connective 0.1 mm thick, either expanded discoid or prolonged into a deltoid ligulate appendage bent toward the gynoecium, carpels 6-9, stigmata globose, capitate to napiform, ca. 1 mm in diameter, covered by minute golden brown hairs, ovaries 1.2-1.6 mm long, densely covered by minute golden brown hairs, 1-2 ovules per carpel, lateral. Fruits apocarpous, consisting of 4-8, subsessile, globose monocarps, 1-2 cm in diameter, apex apiculate, base rounded, the longitudinal suture visible (ribbed), stipe up to 1 mm long, exocarp dark reddish to brown, ligneous when mature, endocarp yellow, coconut-scented at maturity. Seeds 1-(2) per monocarp, ellipsoid or rarely discoid, surface slightly rugose, endosperm ruminate (spiniform)1-1.5 cm long,1-1.7 cm wide.

Distribution.

Desmopsis terriflora is only known to date from the Uxpanapa region (Veracruz state) in southern Mexico (Fig. 2 ).

Habitat and ecology.

The species occurs in lowland tropical rainforests (100-200 m elevation) on karstic rock formations and on shallow soils, mainly occurring along ravines and river banks, protected from the wind and sun. It forms part of the middle stratum along with species of Amphitecna ( Bignoniaceae ), Dialium ( Fabaceae ), Mortoniodendron ( Malvaceae ) and Terminalia ( Combretaceae ). At the type locality, most individuals were found along a shallow river, and the flagella were all directed downstream and the woody fruits usually float on the water.

Phenology.

Flowering from April to May; fruiting between May and September.

Etymology.

The specific epithet " Desmopsis terriflora " refers to its flowers emerging from the ground.

Phylogenetic relationships.

Desmopsis terriflora is phylogenetically related to Stenanona migueliana , S. morenoi , S. stenopetala , and S. zoque (Fig. 3 ), from which the new species is distinguished by its glabrous leaves (versus sparsely to densely pubescent), flagelliflorous habit (versus trunciflorous), the red color of its flowers (versus pink, yellow and white), the basal fusion of its sepals (versus totally free sepals), and by the reduced number of ovules (1 to 2) per carpel (versus several (5 to 10) ovules per carpel) ( Ortiz-Rodriguez et al. 2018; Moreno-Méndez and Ortiz-Rodriguez 2020).

Additional specimens examined.

Mexico, Veracruz, Municipio Minatitlán, Lomas al S. de Poblado 11, ca. 27 km al E de La Laguna, 17°13'45"N, 94°18'30"W, 370 m, 1 April 1981 (fl), T. Wendt, A. Villalobos C. and I. Navarrete 3125 (CHAPA). loc. cit., 14 April 1984 (fl, yng fr), Schatz & Wendt 985 (MO); type locality, abril 2014 (fl, fr), Andres E. Ortiz-Rodriguez 783, 784 (MEXU) .

Figures

Figure 1. Desmopsis terriflora G. E. Schatz, T. Wendt, Ortiz-Rodr. & Martinez-Velarde A multiple flagella emerging from the base of the main trunk B flagella lying on the rocky ground C, D lateral inflorescences on the flagellum E flower in anthesis F monocarps G male flower releasing pollen H female flower.

Figure 2. Geographic distribution of Desmopsis terriflora Schatz, T. Wendt, Ortiz-Rodr. & Martinez-Velarde A currently known localities for the species B tropical rainforest at Poblado 11 in Uxpanapa, Veracruz, Mexico.

Figure 3. Maximum likelihood tree (RaxML) of the Neotropical clade of Miliuseae (subtribe Sapranthinae) based on 323 Annonaceae wide exons and with emphasis on the species of Stenanona Standl. and Desmopsis Saff. Darker circles indicate strongly supported clades (bootstrap values greater than 90 and Posterior Probabilities greater than 9.0). The shaded clade includes the new species. * = flagelliflorous species. In the photo, a flower of Desmopsis terriflora emerging from the ground is shown.

Figure 4. Scanning electron microscopy (SEM) images of pollen grains A Desmopsis terriflora G. E. Schatz, T. Wendt, Ortiz-Rodr. & Martinez-Velarde, pollen grain without externally visible aperture (s) B exine sculpturing weakly rugulate to fossulate (- perforate) ornamentation C Desmopsis trunciflora (Schltdl. & Cham.) G. E. Schatz, pollen grain showing one (another one at the opposite side likely to be also present) aperture exine area D exine sculpturing weakly rugulate to fossulate (- perforate) ornamentation E Stenanona tuberculata G. E. Schatz & Maas, pollen grain without externally visible aperture (s) F exine sculpturing verrucate ornamentation.

Figure 5. Timing of phenological events and visitor activity during sexually functional phases of Desmopsis terriflora flowers. The pistillate phase occurs between 1400 hours and 1800 - 1900 hours of the day, during this phase the floral visitors (light green: flies, blue: ants) are attracted by the strong banana-like odor in the flowers. The pistillate phase is succeeded by a long interim period of 11 - 12 h, during which the flowers were not sexually functional, neither floral scent dissipated, nor floral visitors observed. The staminate phase occurs between 1200 - 1300 hours of the second day, during which there is an obvious increase in floral scent and visitors are again attracted. Note that the beetles (dark green) are only present in the staminate phase.

Figure 6. Scanning electron microscopy (SEM) pictures and stereoscopic images of the potential pollinators of Desmopsis terriflora flowers A, B unidentified beetles C, D unidentified ants E unidentified beetle F unidentified fly.