Research Article |
Corresponding author: Andres Ernesto Ortiz-Rodriguez ( ortizrodriguez.ae@gmail.com ) Academic editor: Thomas L.P. Couvreur
© 2016 Andres Ernesto Ortiz-Rodriguez, Marcos Alberto Escobar-Castellanos, Miguel Angel Pérez-Farrera.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ortiz-Rodriguez AE, Escobar-Castellanos MA, Pérez-Farrera MA (2016) Phylogenetic analyses and morphological characteristics support the description of a second species of Tridimeris (Annonaceae). PhytoKeys 74: 79-96. https://doi.org/10.3897/phytokeys.74.10371
|
Based on phylogenetic and morphological evidence, Tridimeris chiapensis Escobar-Castellanos & Ortiz-Rodr., sp. n. (Annonaceae), a new species from the karst forest of southern Mexico, is described and illustrated. The new species differs from Tridimeris hahniana, the only described species in the genus, in that the latter has flowers with sepals densely tomentose outside, one (rarely two) carpel(s) per flower and fruits densely covered with golden-brown hairs, while Tridimeris chiapensis has flowers with glabrous sepals outside, two to five carpels per flower and glabrous fruits. Furthermore, a shallow triangular white patch at the base of the inner petals is found in T. chiapensis, a morphological character shared with the sister genus Sapranthus but absent in T. hahniana. Geographically, both species occur allopatrically. With just one known locality and seven individuals of Tridimeris chiapensis recorded in one sampling hectare, and based on application of the criteria established by the IUCN, we conclude tentatively that the species is critically endangered.
Dimery, Neotropical, Miliuseae, tropical rainforest
Annonaceae is a plant family composed of about 110 genera and 2,500 species of trees and lianas (
Tridimeris is a monotypic and poorly studied genus. Baillon (1869) described its only species, Tridimeris hahniana Baill., based on exemplars from Veracruz, Mexico (
During a floristic study in southern Mexico, several individuals of an unusual species of Annonaceae were collected. The general characteristics of its flowers, notably dimery, suggested that it probably was a species related to the genus Tridimeris; however, its fruit characteristics did not fit with those of Tridimeris hahniana. To elucidate this, we performed molecular phylogenetic analyses including one sample of the putative new species and studied its morphological characteristics in detail to corroborate its identity at the genus level and to determine whether the collections from Chiapas represent a second species of Tridimeris for the Mexican flora.
DNA extraction was performed using a CTAB (acetyl trimethyl ammonium bromide) method (
Phylogenetic relationships among taxa were estimated using Bayesian inference (BI), maximum likelihood (ML), and parsimony methods. Analyses of six cpDNA regions were conducted separately (for regions with information available for the new species) and in combination.
For BI, three partitioning strategies were used: (1) data matrix divided into six partitions based on DNA region identity, (2) six plastid markers concatenated and analyzed without partitioning, and (3) 2-partitioned, distinguishing coding (matK, ndhF, rbcL and ycf1) and non-coding (psbA-trnH and trnL-F) regions. jModelTest ver. 3.06 (
For the ML analysis, the dataset was divided based on Bayes factor results (see above and results). Phylogenetic reconstruction was performed using RAxML ver. 8.2.4 (
The most parsimonious trees were obtained using the ratchet strategy (
We examined the specimens of Tridimeris hahniana deposited at
We assessed the conservation status by calculating the extent of occurrence (EOO) and the area of occupancy (AOO) using the GeoCAT tool (
Each individual cpDNA region provided a relatively good resolution within Sapranthinae clade, with most branches resolved in the four separate trees (Suppl. material 1–4). Analyses of the matK, rbcL and ycf1 coding regions showed that Sapranthinae is composed of two main subclades, the Desmopsis-Stenanona clade and the Sapranthus-Tridimeris clade, while the analysis of trnL-F spacer showed very low resolution recovering only the Sapranthus-Tridimeris clade (Suppl. material
The concatenated 32-accession dataset contained 6419 aligned positions, of which 746 were variable and 208 were parsimony informative. For the Bayesian analyses, the substitution model was GTR+G for matK, trnL-F, psbA-trnH and unpartitioned datasets, GTR+G+I for rbcL, ndhF and coding datasets and HKY+G for non-coding dataset.
The six partitioned strategy considerably improved the mean −lnL values in the Bayesian analyses (mean −lnL non-partitioned = –15754.57; mean –lnL 2-partitioned= –15725.73; mean –lnL 6-partitioned = –15722.11). Bayes factor comparison indicated that the analyses using six partitions provided a better explanation of the data than unpartitioned and 2-partitioned analyses. For the ML analyses the likelihood score of the optimal ML tree, was ln L = –15572.87. The parsimony analysis of the combined regions resulted in 20 most parsimonious trees of 1030 steps with a Consistence Index of 0.79 and a Retention Index of 0.60. The subsequent presentation of the results is restricted to the 50% majority rule consensus tree derived from Bayesian analyses using six partitions.
The partitioned BI, ML and parsimony analyses resulted in similar tree topologies. The 50% majority-rule consensus BI tree resulting is shown in Fig.
The 50% majority-rule consensus tree from the Bayesian analysis of six cpDNA markers. Numbers on branches of the major clades indicate Bayesian posterior probabilities (PP), maximum likelihood (MLBS) and parsimony (MPBS) bootstrap values in that order. In red, the position of Tridimeris chiapensis Escobar-Castellanos & Ortiz-Rodr.
Morphologically, Tridimeris chiapensis has a set of morphological characters that clearly distinguish it from T. hahniana (Fig.
Tridimeris chiapensis Escobar-Castellanos & Ortiz-Rodr. A Dimerous flower B Large and fleshy fruits C Flower showing the pollen release and a triangular white patch at the base of the inner petals D Five carpels surrounded by numerous stamens E Leafy branches. Photographs by Marcos Escobar-Castellanos.
Comparison of diagnostic morphological characters of Tridimeris chiapensis and Tridimeris hahniana.
Characters | Tridimeris chiapensis | Tridimeris hahniana |
---|---|---|
Pedicel | Glabrous | Golden tomentose |
Sepals | Glabrous outside | Densely tomentose outside |
Inner petals | Thick and fleshy | Flat and thin |
Carpels | 2–5 | 1 (occasionally 2) |
Monocarps | Glabrous | Golden brown tomentellous |
Distribution | Mexico (Chiapas) | Mexico (Puebla, San Luís Potisí and Veracruz) |
The phylogenetic analyses showed that Tridimeris chiapensis and T. hahniana form a strongly supported monophyletic group (Fig.
Tridimeris chiapensis clearly differs from T. hahniana by its number of carpels per flowers, fruit surface, glabrous pedicels and sepals, and by the presence of a triangular white patch near the base of inner petals (Fig.
Ecologically T. chiapensis inhabits wet forests on karstic topography around 1000 m elevation, while T. hahniana occurs in lowland wet forests (200–900 m) or even in cloud forests in the northern portion of its distribution (
Mexico. Chiapas, Municipio de Berriozábal, Zona Sujeta a Protección Ecológica “La Pera”, Campamento “Trepatroncos” carretera Berriozábal-Joaquín Miguel Gutiérrez, km. 12 desvío a Montebello, 1081 m, 16°52'20.3"N, 93°19'32.5"W, 11 August 2016 (fl) Escobar-Castellanos M. A. 0689 (holotype
Tridimeris chiapensis is phylogenetically related to Tridimeris hahniana with which it shares axillary and dimerous flowers and large and fleshy fruits. However, Tridimeris chiapensis differs in having flowers with glabrous sepals, a triangular white patch near the base of inner petals and 2-5 carpels per flower and glabrous fruits (Fig.
Tree 3–9 m tall and 3–14 cm DBH; young branches slightly pubescent, trichomes appressed and golden-brown in color, glabrescent with age. Leaves membranaceous to chartaceous, alternate, phyllotaxy distichous, 11–20 cm long to 3.5–8 wide, narrowly elliptic to obovate, the apex acute to acuminate, the base acute to obtuse, sometimes asymmetrical; upper surface glabrous, the lower side glabrescent; venation brochidodromus, 6–9 veins per side, pocket domatia in the axils of the main veins; the midrid impressed above and slightly canaliculate toward the base (sometimes with erect to appressed light-brown hairs), lateral veins barely elevated above; the midrib and lateral veins prominently elevated below and with sparsely light-brown hairs, lateral veins decurrent at midrid insertion ; petiole swollen, 0.5–1 cm long, canaliculate, with sparsely light-brown hairs. Inflorescences always one-flowered, axillary, sometimes arising on leafless part of branches (ramiflory), the pedicel glabrous, 1–1.7 cm long, bearing 2–3 minute, densely golden tomentose and broadly ovate basal bracts. Sepals 2, connate, to 2 mm long × 4–5 mm wide, decurrent along the pedicel, broadly ovate, rounded at apex, glabrous inside and outside, the margins ciliate. Petals 4, in two subequal whorls, 8–14 mm long × 3–5 mm wide, lanceolate to triangular, green to yellowish green, glabrous inside and outside, the margins ciliate, acute at apex, the base truncate and cusped around the stamens; the outer petals, more or less thin, with faint venation, reflexed at anthesis; the inner petals thicker and fleshier and not reflexed with a shallow, more or less triangular white patch near the base. Stamens, c.a. 40, 1–1.5 mm long, extrorse, filament very short, apical part of connective expanded over the thecae, shield-shaped, ellipsoid to angulate, glabrous. Carpels, 2–5 per flower, to 2.5 mm long; the stigma more or less globose and essentially glabrous; style absent; the ovaries ellipsoid and more or less curved, like a small banana with sparsely light-brown hairs; the ovules, 12–18, lateral, in two rows. Monocarps, 1-4 per fruit, large and fleshy, 8–11 cm long × 3–5 cm wide, ellipsoid, the apex and base rounded, glabrous, shortly stipitate, stipes to 7 mm long; young monocarps green, yellow to light brown when ripe with a peach-like sweet odor; seeds lunate to wedge-shaped, 1.3–2.2 cm long with lamellate ruminations.
The type locality of Tridimeris chiapensis is locally named as “La Pera” and “Pozo Turipache” or “El Pozo” and it lies within the ecological state reserve La Pera, which is mostly covered by tropical rainforest. Thin soils, rough limestone outcrops, caves, crevices, sinkholes and almost no surface water that form a typical karst landscape can be observed around El Pozo (
Tridimeris chiapensis forms part of the understory vegetation and it is associated with Mortoniodendron ocotense Ishiki & T. Wendt, M. vestitum Lundell, Trichilia moschata Sw., Neea tenuis Standl., Pseudolmedia glabrata (Liebm.) C.C. Berg, Quararibea funebris (La Llave) Vischer, Quercus lancifolia Schltdl. & Cham. and Heliocarpus appendiculatus Turcz. (
The species was found in full bloom in August and bearing fruits in March and May.
The specific epithet is in honor of the Mexican state of Chiapas where the species was found.
Tridimeris chiapensis is known only from the type locality at the ecological state reserve La Pera. According to the criteria established by the IUCN, it is possible to tentatively determine that the species is Critically Endangered [CR B1ab (iii)]. The Area of occupancy (AOO) of T. chiapensis is 0.314 km² and the Extent of occurrence (EOO) is 1.519 km², suggesting a very restricted overall distribution. Although the only known population of the species is located within a protected natural area, only 7 individuals of Tridimeris chiapensis in one hectare of sampling were recorded (
MEXICO. Chiapas, Municipio de Berriozábal: Zona Sujeta a Protección Ecológica “La Pera”, Campamento “Trepatroncos” carretera Berriozábal-Joaquín Miguel Gutiérrez, km. 12 desvío a Montebello, 1081 m, 16°52'20.3"N, 93°19'32.5"W, May 2014 (fr) Escobar-Castellanos M. A. 0599 (
We extend our sincere gratitude to Antonio Arreola, owner of Campamento Trepatroncos where the type species was collected, and Christopher Davidson and Sharon Christoph for partially financing visits to the type locality through the project “Floristic diversity and evolutionary ecology of endangered species in protected natural areas from Chiapas, México”. We thank Yuyini Licona, Juan Francisco Ornelas, Eduardo Ruiz and Francisco Lorea for helpful comments on previous versions of the manuscript. We especially thank Andrew Vovides (Laboratorio de Biología Evolutiva de Cycadales) for his careful revision that considerably improved the writing of this paper; and Thomas Couvreur, George Schatz, Lars Chatrou, Roy Erkens and one anonymous reviewer for their valuable criticisms and suggestions. The first author thanks CONACyT (Consejo Nacional de Ciencia y Tecnología, México) for the support of his doctoral scholarship number 262563. This work constitutes partial fulfillment of AEOR’s doctorate in Biodiversity and Systematics at the Instituto de Ecología, AC. This research was partially supported by a competitive grant (155686) from the Consejo Nacional de Ciencia y Tecnología, México (CONACyT) and research funds from the Instituto de Ecología A.C. (INECOL; 20030/10563) awarded to Juan Francisco Ornelas.
Voucher specimens for the accessions cited in this study. The information is presented in the following order: Taxon; GenBank accessions: rbcL; matK; ndhF; trnLF; psbA-trnH; ycf1; Voucher information (herbaria in parentheses). Long dash (—) = sequence not available.
Alphonsea elliptica Hook.f. & Thomson; AY318966; AY518807; JQ690401; AY319078; JQ690402; KJ418378; Van Balgooy 5141 (L); Gardner & Sidisunthorn ST 2214, Indonesia. Asian undescribed GenusA; —; KC857607; KC857608; KC857606; —; JX544757; Chaowasku 108(L) Thailand. Dendrokingstonia gardneri Chaowasku; KJ418381; KJ418391; KJ418385; KJ418406; KJ418399; KJ418378; Gardner & Sidisunthorn ST 2214 (L) Thailand. Desmopsis lanceolata Lundell; KU727378; KU727296; —; KU727414; KU727337; KY026102; Rubén Martínez Camilo 2370, (
Figure S1. The 50% majority-rule consensus tree from the Bayesian analysis of rbcL coding region
Data type: JPEG image
Explanation note: Numbers on branches of the major clades indicate Bayesian posterior probabilities (PP), maximum likelihood (MLBS) and parsimony (MPBS) bootstrap values in that order.
Figure S2. The 50% majority-rule consensus tree from the Bayesian analysis of matK coding region
Data type: JPEG image
Explanation note: Numbers on branches of the major clades indicate Bayesian posterior probabilities (PP), maximum likelihood (MLBS) and parsimony (MPBS) bootstrap values in that order.
Figure S3. The 50% majority-rule consensus tree from the Bayesian analysis of ycf1 coding region
Data type: JPEG image
Explanation note: Numbers on branches of the major clades indicate Bayesian posterior probabilities (PP), maximum likelihood (MLBS) and parsimony (MPBS) bootstrap values in that order.
Figure S4. The 50% majority-rule consensus tree from the Bayesian analysis of trnLF spacer
Data type: JPEG image
Explanation note: Numbers on branches of the major clades indicate Bayesian posterior probabilities (PP), maximum likelihood (MLBS) and parsimony (MPBS) bootstrap values in that order.