Stenanona zoque Ortiz-Rodr. & H.Gómez, 2018

Ortiz-Rodriguez, Andres Ernesto, Gómez-Domínguez, Héctor, Jiménez, Josefa Anahí Espinosa-, Ruiz-Sanchez, Eduardo, Ornelas, Juan Francisco & Brewer, Steven, 2018, Living on the rocks: a new species of Stenanona (Annonaceae) from karst limestone forests of southern Mexico, Phytotaxa 383 (3), pp. 293-300 : 294-298

Stenanona zoque Ortiz-Rodr. & H.Gómez , sp. nov. ( Fig. 1 )

Type:— MEXICO. Chiapas: Ejido Veinte Casas, Municipio Ocozocoautla , sendero que lleva a la antena de monitoreo de incendios, 16º 58’ 45.8’’ N, 93º 32’ 59.9’’ W ; 1127 m., 07 May 2016, Gomez-Dominguez 3615 (holotype: HEM; isotypes: MEXU, MO, XAL) .

Stenanona zoque is similar to Stenanona migueliana Ortiz-Rodriguez & Schatz (in Ortiz-Rodriguez et al. 2014: 38) and Stenanona stenopetala (Donn. Sm.) Schatz (in Maas et al. 1994: 465), but it can be distinguished from these two species by the combination of large floral pedicels, yellow petals with evident venation in vivo and slightly involute margins, small triangular sepals and biseriate ovules ( Fig. 2 ; Table 1).

Trees 5–12 m tall, young twigs and petioles covered with erect to appressed golden brown hairs. Lamina oblong to elliptic, 14–21 × 5–8 cm, punctate, with minute lens-like warts, shiny and glabrous above, below sparsely covered with erect to appressed golden brown hairs, more dense on primary and secondary veins, base obtuse to rounded, often asymmetrical, apex acuminate, primary vein slightly raised above and prominent below, secondary veins 8–15 on each side of primary vein; petiole densely covered with golden brown hairs, canaliculate, 4–9 mm long. Inflorescences produced among leaves, on leafless portions of branches or the main trunk (cauliflorous), a condensed rhipidium bearing one flower at a time, frequently two or three times branched when near the base of the trunk, pendent; peduncle 2–13 mm long or up to 10 cm when elongate near the base of the trunk; pedicels and abaxial surfaces of bracts, sepals and petals densely covered with erect to appressed, golden brown hairs. Flowers strongly fragrant of ripe banana at anthesis; pedicels 20–45 mm long, each borne in the axis of a minute triangular bract 0.6–2.5 mm long; sepals 3, free, triangular, 2.0–2.5 × 2.5–3.0 mm, apex acute; petals 6, free, slightly involute, in 2 subequal whorls, yellow, narrowly triangular to linear, apex acute to acuminate, slightly curved at the tip, with longitudinal venation evident in vivo, outer petals 17–47 × 2–7 mm, inner petals 20–48 × 3–7 mm; stamens numerous, c. 80, 1.5–2.0 mm long, apical part of connective compressed, ellipsoid to angulate, glabrous, projecting towards the gynoecium; carpels 6–10, 2–3 mm long, without a style, ovary and stigma densely covered with golden brown hairs; stigma capitate, 0.3–0.5 mm long, ovules 6–9, biseriate. Fruits not seen.

Habitat and ecology:— Stenanona zoque is known only from the type locality in El Ocote Biosphere Reserve in northwestern Chiapas, Mexico. The species inhabits rainforests on outcrops of sedimentary rocks, mainly composed of karst limestone (calcium carbonate), where large cliffs, caves and chasms (sinkholes) characterize the landscape (Müllerried 1957; CONANP/ SEMARNAT 2001); soils are shallow and alkaline with good drainage and high organic matter content (CONANP/ SEMARNAT 2001). Nevertheless, Stenanona zoque only inhabits sites with steep slopes and, when present it is represented by several individuals separated from each other by a few meters. Probably due to the characteristics of the soil and steep topography, some individuals of S. zoque have bent trunks leaving some of them semi-prostrate.

Flowers of S. zoque , as has been reported for most species of the Desmopsis - Stenanona clade with yellow flowers ( Schatz 1987, Schatz et al. 2018), release a sweet ripe banana odour at anthesis. Unfortunately, we did not observe floral visitors. Some individuals of S. zoque show considerable elongation of their floral peduncles, similar to that of some species of Monoon Miquel (1865: 15) and Polyalthia Blume (1830: 68) . This has been called idiocladanthy ( Mildbraed 1922, Schatz & Wendt 2004; Fig. 1 ). Little is known about the origin and evolution of peduncle elongation in Annonaceae ; in some species it becomes so long that it is considered flagelliflory ( Maas et al. 2003). However, in some species of Annonaceae with flagelliflory, the flagella represent elongated peduncles (internodal elongations of a single inflorescence, with extreme development of a sympodial rachis; Maas et al. 2003), whereas in others, like Stenanona flagelliflora Schatz & Wendt (2004: 30–36) , the flagella are modified branches with all leaves poorly developed or reduced to bracts and successive lateral shoots ending in inflorescences ( Schatz & Wendt 2004, Maas et al. 2003), so these structures are not homologous.

Phenology:— Flowering April–May; fruiting individuals not observed.

Etymology:— Honouring the Zoque indigenous culture of the karst forests of southern Mexico.

Phylogenetic relationships and morphological differentiation:— Phylogenetic relationships of the new species are based on Ortiz-Rodriguez et al. (2018, Fig. 2 ). Stenanona zoque (labelled Desmopsis sp. nov. Chiapas in Ortiz-Rodriguez et al. 2018) is part of subclade A, composed of Desmopsis and Stenanona species distributed mostly towards northern Mesoamerica (from Honduras to Mexico; Fig. 2 ). Within subclade A, S. zoque is related to S. migueliana and S. stenopetala , which are cauliflorous and share long-pedicellate flowers with inner and outer petals equal to subequal, linear to linear-triangular in shape ( Fig. 2 ). However, S. zoque can be distinguished from the other two species by the flower colour, petal margin shape, petal venation, sepal length and ovule arrangement ( Figs. 1 , 2 ; Table 1).

Other species also closely related to S. zoque are Desmopsis schippii Standley (1932: 130–131) and D. uxpanapensis Schatz (in Schatz et al. 2018:83) ( Fig. 2 ). Like S. zoque , both species of Desmopsis have yellow flowers with linear to linear-triangular petals. However, in both species of Desmopsis the petals lack the longitudinal venation evident in vivo. Furthermore, both species of Desmopsis have flowers with 1–3 ovules per carpel arranged in one series ( Table 1).

Conservation status:— We assessed the conservation status by calculating the extent of occurrence (EOO) and the area of occupancy (AOO) using the GeoCAT tool ( Bachman et al. 2011). The above is part of criterion B of the IUCN red list, which is the most often-used criterion in the evaluation of the conservation status of plant species using geographic distribution data ( Dauby et al. 2017). We take the precautionary approach in tentatively determining that S. zoque is critically endangered, CR B1ab (iii). Its estimated area of occupancy (AOO) is 8,000 km ² and extent of occurrence (EOO) is 0 km². Despite the small number (two) of known georeferenced locations and therefore likely underestimation of the EOO due to incomplete sampling, actual EOO and AOO for this species are likely restricted given the rarity of intact habitats remaining in this landscape.

Additional notes:— Based on precipitation patterns and species endemism, Wendt (1989) suggested that the karst areas of southern Mexico and northern Central America have served as refugia for tropical forest species at different times and places, from the Miocene to the Pleistocene. The existence of refugia in limestone areas probably favoured persistence of several plant clades but also promoted disjunction between populations and influenced speciation events ( Carstens & Knowles 2007). It seems that temporal fluctuations in the magnitude of isolation among karst refugia determined the floristic composition of each and the level of morphological and genetic differentiation between disjunct species or populations ( Wendt 1989, Faille et al. 2015, Xie et al. 2017).

The Mexican species of Stenanona , unlike most species of Desmopsis and Central American species of Stenanona , predominately inhabit areas with alkaline soils. Some Mexican species of Stenanona show spectacular morphological characteristics such as flagelliflory in Stenanona flagelliflora or stolons in Stenanona humilis (Miranda) Schatz (in Maas et al. 1994: 465), S. monticola Maas & Schatz (in Schatz & Maas 2010: 217) and S. wendtii Schatz & Maas (2010: 221–223) that clearly distinguish them from their congeners. The four species mentioned above appear to form a strongly supported clade ( Fig. 2 ). In addition, the morphological differences between sister species are evident, and although sympatric in some regions their morphological characteristics make distinction easy ( Schatz & Maas 2010). Other karst forest species, such as S. migueliana , S. stenopetala , D. uxpanapensis and S. zoque , do not exhibit different morphological characteristics compared to those species of Desmopsis or Stenanona that inhabit other types of forests. In addition, all these allopatric species ( Fig. 3 ) appear to form a strongly supported clade ( Fig. 2 ) with subtle morphological differences among them ( Table 1).

It is thus probable that some divergence events favoured evolution of clear morphological differentiation between pairs of sister species prior to those events related to the current disjunction between populations or pairs of sister species. In the latter, there has been little further morphological differentiation between pairs of sister species, a hypothesis previously proposed by Wendt (1989). This is in agreement with the fact that deep divergences (13–6 million years ago; Ortiz-Rodriguez et al. 2018) are related to the origin of the main Desmopsis - Stenanona clades, and radiation within each of them occurred only in the last five million years.

Additional specimens examined:— MEXICO. Chiapas: Ejido Veinte Casas, Municipio Ocozocoautla, sendero que lleva a la antena de monitoreo de incendios, 16º 58’ 45.8’’ N, 93º 32’ 59.9’’ W, 1127 m, 07 May 2016, Gómez-Domínguez 3730–3734 (XAL).

Figures

FIGURE 1. Stenanona zoque. A. Habit. B. Abaxial leaf surface. C. Longitudinal section of flower showing carpels and stamens. D. Inflorescence (rhipidium) with elongate, branched peduncle (sympodial rachis) with several simultaneous long-pedicellate flowers. E. Inflorescence (rhipidium) with a short peduncle and one long-pedicellate mature flower and one floral bud. Drawn by Christian Valencia Celiz from the type.

FIGURE 2. Phylogenetic relationships and morphological differentiation of Stenanona zoque.A. From top to bottom, flowers of Stenanona migueliana, Stenanona stenopetala and Stenanona zoque. B. The Bayesian tree based analysis of seven plastid regions (psbA-trnH, trnL-F, rps16-trnQ introns/spacers and matK, ndhF, rbcL and ycf1 exons) and nuclear ribosomal ITS (modified from Ortiz-Rodriguez et al. 2018). In the phylogenetic tree Stenanona zoque (in red) is placed in subclade A of the Desmopsis-Stenanona clade.

FIGURE 3. Distribution of Stenanona zoque (yellow dots), Stenanona migueliana (green triangles) and Stenanona stenopetala (blue squares) based on georeferenced localities available at the Global Biodiversity Information Facility.