Opuntia delafuentiana Martínez-González, Luna-Vega, Gallegos-Vázquez & García-Sandoval, 2015

Martínez-González, César Ramiro, Luna-Vega, Isolda, Gallegos-Vázquez, Clemente & García-Sandoval, Ricardo, 2015, Opuntia delafuentiana (Cactaceae: Opuntioideae), a new xoconostle from central Mexico, Phytotaxa 231 (3), pp. 230-244 : 233-240

Opuntia delafuentiana Martínez-González, Luna-Vega, Gallegos-Vázquez & García-Sandoval , sp. nov.

Type:— MEXICO. Hidalgo: Villa Tezontepec Municipality, Villa de Tezontepec , 19 ° 53 ‘0.7’’ N, 98 ° 48’ 46’’ W, 2329 m, Martínez-González 4 (Holotype, MEXU!; Isotypes, ARIZ, MO and CHAPA). Figs. 1 to 4 .

Diagnosis:— The new species is similar to the sympatric ones Opuntia joconostle , O. matudae , O. leiascheinvariana and O. oligacantha , but differs in having the following characteristics: length and diameter of the pericarpel and fruit (that is smaller than in the other species), reniform to lenticular small seeds and the maturation stage of the fruit that occurs in January of the year following the blooming. The color of the styles is always white and the walls of the fruit are always whitish. The mature cladodes are obovate, the areoles are arranged in 10 to 12 series, epidermis pubescent, spines arranged around the cladode, setoses, porrect and reflexes, white with yellowish apices; pericarpel obovate; style always white, stigma lobes 8 generally papilose, green; small fruits ellipsoid to obovate, yellowish with green-whitish tones, with thick walls, acidic, edible; funicles semi-dry, tasteless; mature fruit persistent, observed on cladodes for 5−6 months or more.

Etymology:— The species epithet is dedicated to the former chancellor of the Universidad Nacional Autónoma de México, Dr. Juan Ramón de la Fuente Ramírez for his commitment and devotion to the UNAM: “we will give way to a new, brighter cycle in the life of the University”.

Vernacular name:— Known locally as “xoconostle de cerro blanco” for the whitish color of the interior walls of the fruit.

Description (macromorphology):— Bushy habit, 1.13 m in height ( Fig. 1A ). Trunk undefined (inconspicuous, little apparent), 25 cm in diameter. Epidermis pubescent, unicellular and conical ( Fig. 3E ). Cladodes obovate, 30 × 18 cm, about 2.1 cm thick, grayish-green, covered with a thin layer of wax ( Fig. 1B ). Areoles arranged in 10−12 series, 2.5 cm separation between series, 2.2 cm separation between areoles, semicircular (0.3−0.4 × 0.3 to 0.4 cm), trichomes short, blackish. Glochids yellow, short, arranged on the top of the areole ( Fig. 3D ). 1−6 spines arranged around the cladode, setoses, porrect and reflexes, the central ones erect, unequal, 0.5−3 cm long, white with yellowish apices. Young cladodes medium green, with prominent tubercles, areoles with short trichomes, pink, setose hairs white, subulate leaves, erect, reddish with uncinate apex ( Fig. 1C ). Flower buds acute, perianth segments brown, apex acuminate, pericarpels obovate, elevated tubercles, areoles with short trichomes, pink, brown glochids, some bordered with brown bristles ( Fig. 2A and 2B ). Yellow flowers ( Fig. 2C ), 5−7 cm long, pericarpel obovate of ca. 2.9 × 2.1 cm, areoles arranged in 7 series, 0.3 cm distant from each other, basal scale thick, outer perianth segments deltoid, apex mucronate, reddish, with the medium groove green, inner segments obovate, apex emarginate, yellow, stamens ⅓ the length of the perianth, filaments yellowish, anthers white, style cuneiform, about 1.9 cm long, white, stigma lobes 8 generally papillose, about 0.3 cm long, green, with medium groove grayish ( Fig. 2D ). Fruits ellipsoids and obovate ( Fig. 2E ), 5.8 cm long, yellowish-with green whitish zones, floral scar slightly sunken (0.7 cm), striate, small areolas, semicircular, arranged in 4−6 series, 0.8 cm distant from each other and 0.9 cm between series, spines absent, glochids yellowish-brown, walls thick, whitish, acidic, funicles whitish, semi-dry and tasteless ( Fig. 2F ). Seeds reniform to lenticular, white with gray tones, about 0.3 cm diameter, irregular lateral aryl, lateral micropylar region, deep, inclusive funicle and micropyle, doted testa ( Fig. 4C ).

Description (micromorphology): —Spines with lignified epidermal cells, long and wide in the apical part, 109.08 μm and 29.54 μm respectively ( Fig. 3B ), middle part of the spine with epidermal cells of 92.02 μm long and 10.76 μm wide, continuous epidermal cells without fissures between the cells and rough texture ( Fig. 3C ). Glochides with barbellate epidermal cells with elevated apices ( Fig. 3D ). Epidermis pubescent, unicellular and conical papillae, isodiametric epidermal cells with smooth texture anticlinal walls ( Fig. 3E ) and paracytic stomata of 16.96 μm wide and 37.13 μm long ( Fig. 3F ). Pollen grain polyhedral, 103.86 μm diameter, 7353.64 μm 2 of area, 15.91 μm of distance between each distal opening (pores), with a diameter of 17.86 μm ( Fig. 4A ), 14–16 pores with width walls of 1.61 μm and glabrous. Seed lenticular to reniform with irregular lateral aril, micropylar-hilum region lateral, inclusive funicle and micropyle and dotted testa ( Fig. 4E ).

Morphological comparison ( Table 2):— The larger values in the length of the lignified epidermal cells of the apical part of the spine were recorded in O. delafuentiana (109.08 μm), O. oligacantha (101.90 μm), O. matudae (97.60 μm), while the smallest value in O. joconostle (94.62 μm). Concerning the width of the lignified epidermal cells of the apical part of the spine, larger values were recorded in O. delafuentiana (29.54 μm), which comes from wild populations, followed by O. joconostle (24.00 μm), O. matudae (22.00 μm) and oligacantha (21.04 μm), found in the wild and sunny orchards in the state of Hidalgo. The correlation of the two previous characters shows that the area of the apical portion of the spine of O. delafuentiana is significantly different to the other species, having the largest value (2544.5 μm 2), because they are setose long spines with a size up to 3 cm.

Concerning the interspecific variability of the size of the lignified epidermal cells (medium part of the spine), the length of the middle part in O. delafuentiana shows significant differences with respect to the other species studied, registering a value of 92.02 μm, a greater value than that observed in O. oligacantha and O. joconostle (87.19 and 88.58 μm, respectively), lower than the one presented by O. matudae (105.01 μm). We found the largest value of the width of the middle part of the spine in O. matudae . This variability was also highlighted by Martínez-González et al. (2014).

Phylogenetic results:— The alignment for Cactaceae (modified from Hernández-Hernández et al. 2011) included

203 taxa and 2659 characters, 564 characters are parsimony informative. The parsimony analysis of the matrix found 42

trees of 2123 steps (CI=0.5066, HI=0.4934, RI=0.8615, RC=0.5446). The strict consensus recovers O. delafuentiana within the Opuntioideae clade, with a bootstrap frequency of 98%; maximum likelihood analysis of the same matrix recover the new species in the Opuntioideae clade as well, with bootstrap frequency of 94% (results not shown).

The alignment for Opuntia s.s. included fifty-two species ( O. delafuentiana was sampled with three specimens) and 1955 characters, 108 characters are parsimony informative. The parsimony analysis of the alignment found 374 trees of 205 steps (CI=0.7033, HI=0.2967, RI=0.9075, RC=0.7880). The strict consensus recovers specimens of O. delafuentiana as a monophyletic group with a bootstrap frequency of 87%, but no clear affinities can be recognized because of the lack of resolution in the consensus, probably resulting from the lack of parsimony informative characters. Maximum likelihood analysis of the same alignment recovers the same monophyletic clade with the specimens of O. delafuentiana with 98% of bootstrap frequency ( Fig. 6 ), as a sister group with O. leiascheinvariana , another Mexican xoconostle (Martínez-González et al. 2014), in the Rhizomatosa clade sensu Majure et al. (2012). Bayesian MC3 chain ran for 750 thousand generations, until standard deviation between the chains was stabilized at 0.01. Estimated sample size for the parameters was 332 or above for all the parameters. After discarding 25% of the trees, the majority rule consensus recovered specimens of the new species in a monophyletic group with a posterior probability of 1.0, and in the Rhizomatosa clade next with O. leiaschenvariana ( Fig. 6 ).

Distribution and phenology: —The existence of Opuntia species in Mexico producing xoconostles is more widespread than previously thought. Nowadays we can recognize 11 species. There is only one reference locality for O. delafuentiana , wild species and distributed in the municipality of Villa Tezontepec, Hidalgo, Mexico. It blooms in March–April and fruits occur from January to March the year following their blooming. The fruits persist for 5−6 months in the cladodes, where they can be consumed by cattle or by wild animals when they fall off of the cladodes. The wild populations of O. delafuentiana help prevent soil erosion and are used as a refuge for several species of birds, reptiles and small mammals.

Conservation status: —According to the IUCN Red List of Threatened Species criteria, O. delafuentiana may be assessed in some of the categories for threatened species, mainly because of its very restricted distribution range, similar to the narrow endemic distributional pattern described by Hernández et al. (2010) for the cacti in the Chihuahuan Desert, and its extensive use in human activities observed in the field by the first author. The species is cultivated in the Botanical Garden of the Instituto de Biología, Universidad Nacional Autónoma de México, in the “Colección Nacional de Especies Silvestres de Nopales Mexicanos: National Collection of wild Mexican Nopales” in walkway OP-7 with the registration number CM4.

The Mexican list of threatened and endangered species (NOM 059; SEMARNAT 2010) includes only three Opuntia species, i.e. O. arenaria Engelmann (1856: 301) , O. bravoana Baxter (1933: 149) and O. excelsa Sánchez-Mejorada (1972: 68) , all of them tunas. It is necessary to include many other species of Opuntia , mainly those that are endemic to the central part of Mexico, including many species of xoconostles.

Figures

FIGURE 1. —A. Bushy habit, 1.13 m height. Native plant from Villa de Tezontepec Municipality, Hidalgo, Mexico. —B. Obovate cladodes, spines present on the areoles. —C. Young cladode, prominent tubers, areoles with short trichomes, pinkish, setose hairs, white, leaves subulate, erect, reddish and with an uncinate apex. Reference specimen: C. Martínez-González 4 (MEXU).

FIGURE 2. —A y B. Acute floral bud, segments of the perianth brown, acuminate apex, reddish, obovate pericarpel, prominent tubers, areoles with short trichomes, pinkish, brown glochides and some areoles with brown bristles. —C. Flower in anthesis, superior view, interior segments yellow, obovate with an emarginate apex. —D. Longitudinal cut of the flower, yellowish filaments and white anthers, white style, green lobes of the stigma. —E. Elliptic to obovate fruits, yellowish with green-whitish tones, 4–6 series of areoles, spines absent, glochides brown-yellowish. —F. Longitudinal cut of the fruit, 5.8 cm long, wide walls, green whitish and acids, funicles whitish, semidry and insipid. Reference specimen: C. Martínez-González 4 (MEXU).

FIGURE 3. —A.Areole with short trichomes, glochides, base of a triangular central spine and four radial spines (x25). —B.Apical part of a spine, short epidermic cells (x125). —C. Middle part of a spine, continuous epidermic cells without fissures between the cells and with rugose texture (x110). —D. Glochides with prominent apexes of the epidermic cells (x250). —E. Pubescent epidermis, epidermic cells with smooth anticlinal walls (x400). —F. Paracytic stomata (x500). Reference specimen: C. Martinez-González 4 (MEXU).

FIGURE 4. —A. Polyhedric pollen grain, 14–16 pores (x800). —B. Zoom of a pollen grain: reticle, foramens and part of two pores, with wide and glabrate walls (x2500). —C. Lenticular seed, irregular lateral aril, wider in the inferior left side (x25). —D. Basal view of the seed, lateral hilo-micropilar region, deep, micropile and funicle included, testa punteate (x30). —E. Lateral aril cells (x90). Reference specimen: C. Martínez-González 4 (MEXU).

FIGURE 6. Maximum clade credibility tree for the Opuntia s.s., including O. delafuentiana. Character support values along branches for maximum likelihood and parsimony non-parametric bootstrap respectively.Bold branches correspond with Bayesian posterior probabilities of 0.95 or above. Clade names follows Majure et al. (2012).