Tacinga gladispina J.G.Freitas & E.M.Almeida, 2021

Freitas, Juliana Gomes, Alves, Lania Isis Ferreira, Zappi, Daniela Cristina, Almeida, Erton Mendonça De, Peraza-Flores, Lizandro N., Amaral, Daniel Oliveira Jordão Do, Araújo, Daniel Bruno Pereira & Batista, Fabiane Rabelo Da Costa, 2021, Novelties in Cactaceae from Eastern Brazil: Adding two new species and one new nothospecies to Tacinga (Opuntioideae), Phytotaxa 490 (3), pp. 239-252 : 246-250

Tacinga gladispina J.G.Freitas & E.M.Almeida , sp. nov. ( Figs. 2 , 4D–F , 5C , 6B , 7F–G ).

Type:— BRAZIL. Bahia: Morro do Chapéu. Próximo à Lagoa das Velhas, 924 m a.s.l., 11º29′512″S, 41º19′547″W, 10 December 2016, fl., fr., Almeida 1829 (holotype EAN23540!) .

Diagnosis:— Tacinga gladispina is similar to Tacinga inamoena differing by its lateral shoots in the basal stemsegments (vs. usually apical or marginal in distal stem-segments), stem-segments spines sword-shaped (vs. unarmed), flower pericarpel short and small (vs. oblong), flower segments 0.7–1.5 cm (vs. 1.5–2.5 cm), flower internal segments obovate (vs. oblong to spatulate), and fruit pulp whitish and fibrous (vs. orange and fleshy, almost liquid and without fibers).

Description:— Terrestrial erect shrub, 40–60 cm tall, forming dense mats of plants originated from seeds or fallen stem-segments and fruits (from areole shooting); roots fibrous, much branched and superficial; stem-segments oblong, 9–15 × 6–8 × 0.5–1.3 cm, erect, flat, spiny, podaria slightly raised, green, shoots 1–2, apical or marginal; areoles circular, up to 2 mm in diameter, disposed in 6–10 clockwise spirals, 60–130 per stem-segment (slightly denser in the apex of stem-segments), hairs whitish, woolly, located in the center of areoles, glochids brownish, arranged in a crown shape around areoles’ hairs; spines 1(–3) per areole, 1.0– 1.5 cm long, rigidly acicular, sometimes with a flat base, directed towards the apex or diagonal to stem-segment, whitish tipped brownish, absent in young stem-segments. Leaves subulate, 0.2–0.3 × 0.1 cm, fleshy, light green, early deciduous. Flowers solitary, 2.5–3.3 × 1.5–2.5 cm, apical or marginal in the distal stem-segments; pericarpel obovate, 1.6–1.8 cm in diameter, ca. 2 cm high, slightly depressed, forming a tube in the apex; flower bracts subtending each areole, subulate, fleshy, reddish, early deciduous; flower areoles disposed in 3–4 clockwise spirals; perianth triseriate, 18–24 tepals, tube relatively short, external segments 0.7–1 cm long, cymbiform, fleshy, red with orange margins, internal segments 1.0– 1.5 cm long, obovate, reflexed, petaloid, apex acuminate with a terminal hair, orange; stamens numerous, included, 1.0– 1.5 cm long, orangish yellow, surrounding the stigma lobes; anthers white; stigma 6–lobed, yellowish, lobes slightly exserted in relation to stamens. Fruits solitary, immediately deciduous after ripening, depressed-globose, 2.5–2.6 × 2.5–2.7 cm, funiculus slightly depressed, 0.8–1.5 cm in diameter, 0.4–0.6 cm deep, pericarp orangish green, spineless, areoles with glochids and hairs, mesocarp yellowish green, pulp whitish with cream fibers. Seeds pyriform, 58–66 per fruit, two different kinds, small atrophied seeds up to 0.3 cm in diameter, without embryo, large developed seeds up to 0.5 cm in diameter, integument bony, perisperm whitish, woolly, mesosperm rigid, cream, endosperm membranaceous, brownish, embryo half-moon-shaped, white translucent, occupying half of the seed cavity.

Etymology:— The specific epithet combines Latin gladius “sword” and spina “spine”, in reference to the spines shape and their position in the areoles (erect, mostly solitary spines sited centrally in the areoles, giving the impression of a sword).

Phenology:— In its natural habitat, Tacinga gladispina flowers between November and December. In cultivation, flowering has been observed in December and May. Each flower remains open for two hours early in the morning (07:00 to 09:00 hr, GMT-3) and late afternoon (16:00 to 18:00 hr). Fruits are observed immediately after anthesis and reach complete maturity after two months. They fall out of stem-segments immediately after ripening.

Distribution and habitat:— Tacinga gladispina is known from a single population of approximately 500 individuals inhabiting an area of ca. 32,000 m 2 at 900 m of elevation in the municipality of Morro do Chapéu, Bahia, Brazil ( Fig. 5B ). These plants usually grow associated to shrubs (i.e. Jatropha sp. , Syagrus sp. , and several species of Fabaceae and Myrtaceae ) and herbs [i.e. Neoglaziovia variegata Mez (1894: 427) , Cenchrus sp. ] of caatinga vegetation growing in sandy soils at 900 m of elevation (see Fig. 2A ).

Conservation status:— According to the IUCN (2019) criteria, Tacinga gladispina should be considered vulnerable to extinction (VU-B1a e VU-D1) due to its restricted geographic distribution (EOO = 4 km 2 and AOO <0.1 km 2), its presence in less than 5 different localities, its small population size (<1,000 reproductive individuals), and a distribution in areas of strong human disturbance (close to a roadway and private properties of intense agricultural activities).

Cytogenetic notes:— Tacinga gladispina has a 2CDNA = 3.71 pg, a karyotype 2 n = 44, mostly of relatively symmetric metacentric chromosomes (40M and 4SM) with a size ranging from 2.10 to 3.55 μm, and five CMA + chromosomes. Two metacentric chromosomes have interstitial CMA + bands in their short arms. Three other metacentric chromosomes have terminal CMA + bands, one band in each of two homologous chromosomes and one in another chromosome ( Fig. 6B ).

It was first thought that Tacinga gladispina (2n = 44) was a hybrid between T. werneri (2n = 66) and T. inamoena (2n = 44). However, the most parsimonious hybrid karyotype count between T. werneri and T. inamoena would be 2n = 55 and only a meiotic nondisjunction (producing unbalanced gametes) would explain a hybrid karyotype of 2n = 44. Thus, we discarded a hybrid hypothesis of T. gladispina in favor of the most parsimonious explanation for the origin of its karyotype number (it originated from a 2n = 44 ancestral species).

Tacinga × flammea J.G.Freitas & E.M.Almeida, nothosp. nov. ( Tacinga inamoena × Tacinga werneri ). ( Figures 3 , 4G–I , 5D , 6C , 7C–D ).

Type:— BRAZIL. Minas Gerais: Pedra Azul , 720 m a.s.l., 16º00′44.8″S, 41º15′59.3″W, 17 December 2016, fr., Almeida 1980 (holotype EAN23542!) .

Diagnosis:— Tacinga × flammea resembles Tacinga werneri from wich differs in having stem-segments with spines up to 3.5 cm (vs. up to 2.0 cm) long, orange flowers with numerous reflexed segments (vs. red with slightly erect to expanded segments), and orange-yellow fruits (vs. whitish green). It is also similar to T. inamoena from which differs by long spined stem-segments (vs. unarmed) and oblong fruits with translucent pulp (vs. globose, with orangish yellow pulp).

Description:— Terrestrial or saxicolous erect shrub, 40–50 cm tall, forming dense mats of plants originated from seeds or fallen stem-segments and fruits (from areole shooting); roots fibrous, much branched and superficial; stemsegments oblong, 8–12 × 4–6 × 0.5–1.3 cm, erect, flat, spiny, without podaria, dark green, shoots 1–4, apical or marginal; areoles circular, 1–2 mm in diameter, disposed in 5–8 clockwise spirals, 75–112 per stem-segment (denser towards apex), hairs whitish, woolly, located in the center of areoles, glochids brownish, arranged in a crown shape around areoles’ hairs; spines 1–3 per areole, 1.0– 3.5 cm long, rigidly acicular, golden (young) to whitish tipped brownish (aged). Leaves spatulate, 0.3–0.5 × 0.1–0.2 cm, fleshy, brownish, early deciduous. Flowers solitary, 3.5– 4.0 × 1.5–2.5 cm, apical or marginal in the distal stem-segments; pericarpel oblong, 1.6–2.0 cm in diameter, 2.0– 2.8 cm high, slightly depressed, forming a tube in the apex; flower bracts subtending each areole, subulate, fleshy, green, early deciduous; flower areoles disposed in 4–5 clockwise spirals, hairs present; perianth tetraseriate, 36–48 tepals, tube relatively short; external segments 1.0– 1.5 cm long, cymbiform, fleshy, red, internal segments 1.6–2.0 cm long, oblong, reflexed, petaloid, apex acuminate with a terminal hair, orange basally and gradually changing to red outwardly; stamens numerous, included, 1.0– 1.5 cm long, yellow-orange, surrounding the stigma lobes; anthers yellowish; stigma 6–lobed, yellowish, lobes exserted in relation to stamens. Fruits solitary, oblong, 2.5–3.2 × 1.5–2.0 cm, deciduous immediately after ripening, funiculus depressed, 1.0– 1.6 cm in diameter, 0.9–1.2 cm deep, pericarp reddish orange, spineless, areoles with glochids and hairs, mesocarp yellowish green, pulp translucent with magenta fibers. Seeds pyriform, 38–66 per fruit, two different kinds, small atrophied seeds up to 0.2 cm in diameter, without embryo, large developed seeds up to 0.3 cm in diameter, tegument bony, perisperm whitish, woolly, mesosperm rigid, cream, endosperm membranaceous, brown, embryo J-shaped, white translucent, occupying all the seed cavity.

Etymology:— The specific epithet is from the Latin flammeus “flaming, flame-colored”, in reference to the gradual outward color change (from orange to red) of the perianth segments, that gives it the appearance of a flaming torch.

Phenology:— In its natural habitat, Tacinga × flammea flowers in December. Under cultivation, flowering has been observed in December and May. Each flower only remains open for approximately one hour early in the morning (08:00 to 09:00 hr, GMT-3) and late afternoon (16:30 to 17:30 hr). Fruits are observed immediately after anthesis and complete maturation after three months. They fall out from stem-segments immediately after ripening.

Distribution and habitat:— Tacinga × flammea is known from a single population of approximately 20 individuals inhabiting an area of ca. 2,000 m 2 in the municipality of Pedra Azul, Minas Gerais, Brazil ( Fig. 5D ). These plants grow at full sun exposure on rocky outcrops (between rocks or at rock edges) in elevations of ca. 720 m. This species usually grows associated to several subshrubs (i.e. Borreria sp. ) and grasses ( Poaceae ) in caatinga vegetation ( Fig. 3B ). Taylor & Zappi (2002) mentioned plants of probable hybrid origin (involving T. inamoena and T. werneri ) near Pedra Azul (Minas Gerais, Brazil) and Morro do Chapéu (Bahia, Brazil). They referred these plants to either Platyopuntia inamoena ( Schumann 1890: 306) F. Ritter (1979:32) f. spinigera Ritter (1979:32) or T. × quipa. The plants from Pedra Azul probably represent T. × flammea. The plants from Morro do Chapéu are in fact one of the new species here described, T. gladispina .

Conservation status:— According to the IUCN (2019) criteria, Tacinga × flammea should be considered critically endangered (CR-B1a) due to its restricted geographic distribution (a single locality with an AOO less than 0.1 km 2 and an EOO of 4 km 2), its small population size (less than 50 individuals), and inhabiting an area with severe fragmentation. Furthermore, stochastic events (i.e. natural or human-induced fires) can drive this species to extinction due to these three characteristics.

Taxonomic and cytogenetics comments:— Tacinga × flammea is characterized by a shrubby erect habit, forming dense mats, probably with little genetic variation (vegetative reproduction: sprouting of fallen stem-segments); stemsegments thick; spines long, whitish tipped brownish, directed towards the stem-segments apex or at an angle of 90º from stem-segment, mostly solitary (rarely up to three) in the areole ( Fig. 4I ); flowers pericarpel long, perianth tetraseriate (twice the flower segments if compared to T. inamoena ), internal segments reflexed at the apex, color changing outwards from orange to red (bringing to mind a firing torch); fruits oblong, funiculus strongly depressed, wide, green (young) to greenish orange (mature), pulp translucent, and seeds small.

Tacinga × flammea is here proposed as hybrid between T. inamoena and T. werneri . It is similar to T. inamoena due to its shrubby habit (mats with many individuals); stem-segments oblong, thick, dark green; and, flowers orange, emerging from the apex or margins of distal stem-segments. It differs from this species by its stem-segments armed and spines long (vs. unarmed); and, fruits oblong, funiculus deeply depressed, and pulp translucent (vs. globose, funiculus slightly depressed, and pulp yellowish). T. × flammea is also similar to T. werneri due to its stem-segments oblong, dark green, armed, spines whitish, pericarpel and fruits oblong. It differs from the latter due to its stem-segment spines long and thick, directed toward the apex (vs. short and thin, pointing downward), perianth internal segments reflexed (vs. erect), flowers changing outwardly from orange to red (vs. completely red), tetraseriate (vs. triseriate), fruit epicarp reddish orange (vs. whitish) with no color distinction around areoles (vs. dark green ring around areoles), seeds 38–66 per fruit, up to 0.3 cm in diameter (vs. 26–30 seeds, up to 0.4 cm in diameter).

Tacinga × flammea has a 2CDNA = 4.50 pg, a karyotype 2 n = 55, mostly of relatively symmetric metacentric chromosomes (49M and 6SM), a chromosome size ranging from 1.45 to 2.71 μm, and three chromosomes with CMA + bands. Two homologous metacentric chromosomes have terminal CMA + bands on their short arms. One of the submetacentric chromosomes has only one interstitial CMA + band on its short arm ( Fig. 6C ). T. × flammea has a CMA + band number and pattern halfway between T. inamoena (2 n = 44, two terminal CMA + bands) and T. werneri (2 n = 66, two terminal and two interstitial CMA + bands), see Alves et al. (2019) for more information.

We believe that Tacinga inamoena and T. werneri are the putative parental species of T. × flammea. The latter has intermediary morphological characteristics of parental species. It also has sympatric geographic distribution with both parents ( Taylor & Zappi 2004, 2018, Hunt et al. 2006) and an intermediary karyotype (2 n = 55, T. × flammea; n = 22, T. inamoena ; n = 33, T. werneri ).

Figures

FIGURE 2. Tacinga gladispina. A. Habit, plant in habitat; B. Stem-segment with flower bud and immature fruits; C. Flower, frontal view; D. Flowers, lateral view; E. Mature fruit, showing funiculus; F. Mature fruit, longitudinal section to show pulp color and seeds.

FIGURE 3. Tacinga × flammea. A. Habit, cultivated plant; B. Habit, plant in habitat; C. Flower bud, lateral view; D. Flower, lateral view; E. Flower, frontal view; F. Fruit, lateral view; G. Fruit, longitudinal section to show pulp color and seeds.

FIGURE 4. Seeds and areoles of the three new taxa of Tacinga. A–C. Tacinga armata, A. Lateral view of seed; B. Longitudinal section of seed, showing the embryo shape and position; C. Areole; D–F. Tacinga gladispina, D. Lateral view of seed, E. Longitudinal section of seed, showing the embryo shape and position, F. Areole; G–I. Tacinga × flammea, G. Lateral view of seed, H. Longitudinal section of seed, showing the embryo shape and position, I. Areole. Drawn by Juliana Freitas.

FIGURE 5. Distribution maps of new taxa.A. Brazil outline map highlighting the states of Bahia (BA), Minas Gerais (MG), Paraíba (PB) and Pernambuco (PE); B–D. Distribution of new taxa in elevation maps of BA, MG, PE and PB; B. T. armata in PE and PB, red filled circles; C. T. gladispina in BA, red filled star; D. T. × flammea in MG, red filled triangle.

FIGURE 6. Mitotic metaphases of the three new taxa of Tacinga after the CMA/DAPI fluorescent dying. A. Tacinga armata (2n = 66 = 2SM + 42M); B. Tacinga gladispina (2n = 44 = 4SM + 40M); C. Tacinga × flammea (2n = 55 = 6SM + 49M). Yellow arrows indicate chromosomes with terminal or interstitial CMA+ bands. Insets highlight the pairs of chromosomes with CMA+ bands.

FIGURE 7. All known species of Tacinga. A. T. armata; B. T. braunii; C–D. T. × flammea; E. T. funalis; F–G. T. gladispina; H–I. T. inamoena; J. T. lilae; K–L. T. palmadora; M. T. × quipa; N–O. T. saxatilis; P–Q. T. subcylindrica; R. T. werneri.