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Research Article
Taxonomic and floristic novelties for Echeveria (Crassulaceae) in Central Michoacan, Mexico
expand article infoIgnacio García-Ruiz, Dagoberto Valentín-Martínez§, Pablo Carrillo-Reyes|, Mihai Costea
‡ Instituto Politécnico Nacional, Jiquilpan, Mexico
§ Escuela de Biología de la Universidad Michoacana, Morelia, Mexico
| Universidad de Guadalajara, Guadalajara, Mexico
¶ Wilfrid Laurier University, Waterloo, Canada
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Abstract

A new species, Echeveria coruana, is described and illustrated from the malpaís near San Andrés Corú, Michoacan, Mexico. The species belongs to series Gibbiflorae and the new taxon was compared with E. purhepecha and E. patriotica, with whom it shares the closest morphological affinities. Additionally, E. yalmanantlaensis an endangered species from Sierra of Manantlán Biosphere Reserve, State of Colima, was also discovered near San Andrés Corú and is reported for the first time from the State of Michoacan. The conservation status of both species was (re)evaluated according to the criteria of the International Union for Conservation of Nature.

Keywords

Conservation, Echeveria , malpaís, morphology, ser. Gibbiflorae, ser. Valvatae, taxonomy

Introduction

Echeveria DC. comprises ca. 140 species of which the majority (95%) have evolved in Mexico where the genus is characterized by a high degree of endemism (Uhl 1992, Thiede 1995, Meyrán and López-Chavez 2003, Pérez-Calix and Franco 2004, Vázquez et al. 2013). Among the infrageneric groups of this genus, ser. Gibbiflorae (Baker) Berger (sensu Walther 1972) is the third most diverse, being surpassed only by ser. Racemosae and ser. Nudae (Pilbeam 2008). It is noteworthy mentioning that the majority of new Echeveria species discovered in the last decade belong to ser. Gibbiflorae (García and Pérez-Calix 2007, Jimeno-Sevilla and Carrillo-Reyes 2010, Reyes and González 2010, Reyes et al. 2011a, 2011b, García and Costea 2014, Nieves-Hernández et al. 2014, Jimeno-Sevilla et al. 2015), which suggests an incomplete knowledge of the species diversity in this group.

The village of San Andrés Corú is located at ca. 12 km NE of the National Park Barranca del Cupatitzio, on the eastern side of the city of Uruapan, in the State of Michoacan (19°27.982'N, 101°56.644'W). This area is a part of the Trans-Mexican Volcanic Belt and has a particularly rich flora and vegetation consisting of a mixture of pine-oak and tropical deciduous forest elements (Rzedowski 1978). During the last years, systematic botanical explorations have been conducted to produce a floristic inventory of the malpaís surrounding San Andrés Corú. The malpaís (“badlands”) is a landform that consists of relict yet recognizable lava fields that exhibit various degrees of erosion and vegetation succession stages depending on their age (Neuendorf et al. 2005). In some of the field trips undertaken NW and W–SW of the village, an unknown Echeveria belonging to ser. Gibbiflorae was discovered. Also, growing in the same type of ecosystem, at ca. 6 km SE of San Andrés Corú, E. yalmanantlanensis A. Vázquez & Cházaro, an endangered species of ser. Valvatae Moran previously known only from one population in the State of Colima (Vázquez et al. 2013), was also discovered. Thus, the first objective of this article is to describe the new species, which we named E. coruana, and to explore its morphological affinities with other species of ser. Gibbiflorae. The second aim is to report E. yalmanantlanensis as a new species for Michoacan.

Materials and methods

In addition to herbarium specimens, flowers and leaves of E. coruana and E. yalmanantlanensis were fixed in FAA (Ruzin 1999) for morphological studies. Several living plants of both species were collected with soil and cultivated in Jiquilpan, Michoacán for further study. We examined the basic morphology of both fresh and fixed flowers under a Nikon SMZ1500 stereomicroscope equipped with a PaxCam Arc digital camera and Pax-it 7.8 software (MIS Inc., Villa Park, Illinois). For scanning electron microscopy (SEM), we used hexamethydisilazane (HMDS) as an alternative for critical dry point (Wright et al. 2011). Fixed flowers were dehydrated using a series of ethanol steps (70%, 80%, 95% and 100%; each step 10 minutes), immersed for 10 minutes in 1:1 ethanol: HMDS, and passed through three changes, each of 30 minutes in 100% HMDS. Samples were air dried and coated with 20 nm gold using an Emitech K 550 sputter coater. Micromorphological examination, measurements and pictures were taken at 10 kV using a Hitachi SU1510 variable pressure scanning electron microscope. Because only E. coruana is described, micromorphological data for pollen and seeds are presented only for this species. Additional images than those provided in the article have been uploaded in Phytoimages (Nickrent et al. 2006 onwards).

Results

The new species, E. coruana belongs to ser. Gibbiflorae, which as summarized by Kimnach (2003), includes glabrous plants, acaulescent or with monopodial stems; leaves are medium-sized to large, commonly narrowed basally into a pseudo-petiole; inflorescences are paniculiform; bracts are similar to the leaves but smaller; pedicels may reach 10 mm in length; calyx has unequal sepals; corolla is large, up to ca. 13 mm long, pentagonal-conical in bud, cylindrical-urceolate to campanulate at anthesis, ± glaucous, often with carinate petals exhibiting a basal cavity on the inner side; nectaries are large, fleshy; styles whitish to dark-red or nearly black. Echeveria coruana possesses a distinctive characteristic encountered only in four other species of ser. GibbifloraeE. dactylifera E. Walther (Walter 1972), E. novogaliciana J. Reyes, Brachet & O. González (Reyes et al. 2011), E. marianae I. García & Costea (García and Costea 2014), and E. rulfiana Jimeno-Sevilla, Santana Mich. & P. Carrillo (Jimeno-Sevilla et al. 2015): the presence of corolla appendages at the base of antipetalous staminal filaments. However, it markedly differs from these species in having smaller leaf rosettes, a different leaf morphology, shorter inflorescences, cincini with fewer flowers, and shorter pedicels. Among all these species, E. coruana has the shortest and most inconspicuous appendages. A detailed comparison of E. dactylifera, E. novogaliciana and E. marianae was provided by García and Costea (2014), and E. coruana can be easily contrasted with these species using the data included in Table 1. The most recently described species with corolla appendages, E. rulfiana, differs from E. coruana in its evidently caulescent habit and canaliculated leaves (Jimeno-Sevilla et al. 2015). Here we compared E. coruana with two other species, E. patriotica I. García & Pérez-Calix and E. purhepecha I. García, which appear morphologically closer even if they do not possess corolla appendages (Table 1).

Table 1.

Comparative morphology of Echeveria coruana with E. patriotica (García and Pérez-Calix 2007) and E. purhepecha (García 2011); “—“ indicates data not available for comparison.

Character Echeveria coruana sp. nov. E. patriotica E. purhepecha
Caudex Acaulescent or inconspicuous Evident Evident
Length × diameter (cm) 3–8 × 1–1.3 20 × 1–2.5 8–11× 1.2
Rosette
Diameter (cm) 10–15 10–35 8–10
Position of leaves in rosette Spreading Spreading Ascendant
Leaves
Color Light-green to dark green in the median part and apex Green to reddish in the older leaves Dark-green
Shape Linear-oblanceolate to spathulate; apex acuminate, short mucronate Oblong-obovate to spathulate; apex rounded, short mucronate Oblong obovate; apex rounded, mucronate
Length (cm) 8–16 6–18 2–6.5
Width (cm) 2–2.5 3.5–11 1–2.5
Inflorescence
Number of main axes 1–4 1–7 2–3
Length (cm) 28–65 20–100 15–30
Diameter at the base (cm) 0.3–0.5 1 0.3-0.6
Number of flowers/ cincinus 1–4(5) 1–8 1–7
Bracts
Shape Oblong-lanceolate Oblong-lanceolate Oblong-obovate
Length (cm) 0.8–7.2 1.1–12 0.8–3
Width (cm) 0.6–3 0.6–4 0.3–1.3
Pedicel
Length (cm) (1.3) 1.6–2.2 0.7–1 0.3–1.3
Corolla shape at anthesis Cylindrical-urceolate Cylindrical-urceolate Cylindrical-urceolate to campanulate
Length (mm) 15–20 18–20 10–12
Width (mm) 7–9 10–14 ca. 8
Sepals (calyx) Spreading to ± reflexed at anthesis Spreading at anthesis Addressed at anthesis
Shape Triangular-lanceolate Triangular-lanceolate Oblong-elliptic to lanceolate
Length x width (mm) 6–9 × 3–4 9–14 × 3-6 4–9 × 2.5–3.5
Petals
Shape Lanceolate Lanceolate Oblong-lanceolate
Length × width (mm) 15–21 × 4–6.5 18–20 × 5-7.5 10–11 × 4
(External) color Whitish-yellow at the base, light-yellow to orange in the median part and orange-reddish at the tips White to cream white at the base, orange-reddish in the median part and scarlet-red at the tips Scarlet-red or coral from the base to the tip
Appendages (1)2 per antipetalous staminal filament; conical or dome-like, 0.2–0.3 mm long Absent Absent
Nectaries
Length × width (mm) 1.8–2.2 × 0.8–1 3 × 1 1.2 × 0.5
Color White-yellowish Purple-red Pale yellow
Follicles 5–6 mm long, erect to somewhat spreading 12–18 mm long, erect ca. 5 mm long, erect
Flowering Nov–Jan Oct–Jan Sep–Nov
Geographical distribution Michoacan, Mpio. Ziracuaretiro: Malpaís de San Andrés Corú Jalisco, Mpio. Mazamitla Michoacan, Mpio. Nuevo Parangaricutiro
Vegetation type Mixture of oak-pine and tropical deciduous forest Oak and oak-pine forest Oak-pine forest

Echeveria coruana I.García, D.Valentín & Costea, sp. nov.

Figures 1, 2

Diagnosis

Echeveria coruana morphologically resembles most E. patriotica and E. purhepecha, with which it shares a similar flower morphology, but differs from both in having acaulescent or inconspicuous stems, acuminate leaves, and corolla appendages at the base of antipetalous stamen filaments. It differs from E. patriotica in having smaller leaf rosettes, 10–15 cm in diameter, smaller inflorescences, 28–65 cm long, longer pedicels, (1.3) 1.6–2.2 mm and a narrower corolla, 7–9 mm in diameter. It can be distinguished from E. purhepecha by the larger rosettes with spreading linear-oblanceolate to spathulate leaves, 8–16 cm long, and the larger corolla, 15–20 mm long, light-yellow to orange in the median part and orange-reddish at the tips of corolla lobes.

Type

MÉXICO. Michoacán: Municipio de Ziracuaretiro, lado noroeste de San Andrés Corú; 19°28.116'N, 101°57.410'W; 1730 m; bosque de encino-pino alterado con huertas de aguacate; 27 Nov 2015; I. García & M. García 9138 (holotype: CIMI!, isotypes: DAO!, ENCB!, IEB!, MEXU!, MICH!, WLU!).

Description

Perennial herb, glabrous, acaulescent or with an inconspicuous caudex, 3–8 cm long and 1–1.3 cm in diameter; rosette lax, 10–15 cm in diameter with 15–18 leaves; leaves fleshy, light-green to dark green in the median part and apex, leaf blade linear oblanceolate to spathulate, 8–16 × 2–2.5 cm, 0.5–1 cm thick at the base, margin entire, occasionally with a thin, red-colored line, apex acuminate, short mucronate, base narrowed to form a pseudo-petiole, 2–3 cm long, corrugated ventrally; inflorescence paniculiform thyrse, 1–3 per rosette, 28–65 cm long and 0.3–0.5 cm wide at the base, with 1–4 secondary axes (cincinni), each with 1–4(5) flowers; bracts spiralled, adpressed, green to yellowish-red, oblanceolate to oblong-lanceolate, 0.8–7.2 × 0.6–3 cm, 1.2–1.5 mm thick in the median part and 7–8.5 mm at the base, base auriculate, soon caducous; pedicels (1.3–) 1.6–2.2 mm long and 2–3 mm thick; calyx gamosepalous, star-shaped, the tube 1–1.5 mm long, lobes green, unequal, 6–9 × 3–4 mm, spreading to somewhat reflexed at anthesis, triangular-lanceolate; corolla pentagonal-conical in bud, cylindrical-urceolate at anthesis, petals 15–21 × 4–6.5 mm, fused for 1–1.5 mm at the base, lanceolate, carenate, tips mucronate, erect to slightly deflexed, color whitish-yellow at the base, light-yellow to orange in the median part and orange-reddish at the tips; nectaries reniform, 1.8–2.2 × 0.8–1 mm, white-yellowish; stamens 10, 5 antipetalous, 9–16 mm long (including the anthers), with a pair of conical or dome-like appendages at the base, 0.2–0.3 mm long; episepalous stamens 5, 10–16 mm long (including anthers); pollen polymorphic, most abundant type is 3-colpate, oblate to oblate-spheroidal in equatorial view and triangular or round in polar view, 30–34 × 17–20 mm, less common grains are 3-colpate, prolate, 34–38 × 18–20 mm or 4-colpate, rectangular or spherical, 28–31 × 17–20 mm; in all pollen grains tectum is imperforate, scabrate; pollen grains eventually agglutinate into large masses; ovary with 5 apocarpous carpels, 9–11 × 0.3–0.4 mm; styles (including the stigmas) 4–5 mm long, red-purplish; follicles 5–6 mm long, erect to somewhat spreading; seeds numerous, oblong to obovate, light to dark-brown, reticulate, 0.5–0.65 × 0.2–0.25 mm; reticulum size 15–30 mm.

Figure 1. 

Habitat and general morphology of Echeveria coruana. A Habitat B Leaf rosette of type specimen C Developing plant (in cultivation) D–F Inflorescence D General view E Developing cincinus F Terminal cincinni G–H Flowers of type specimen viewed in the field from different angles I–J Flowers from type specimen fixed in FAAI Dissected flower (removed corolla) to show stamen bases and nectaries. J Conical appendages at the base of antipetalous staminal filaments (indicated with black arrows). Scale bars 1 mm.

Figure 2. 

Scanning electron microscopy of E. coruana, pollen and seed (García & García 9138). A–C Heteromorphic pollen grains; arrows indicate a few 3-colpate, prolate pollen grains B 4-colpate (left, upper) and 3-colpate pollen (right, down) grains C 3-colpate, prolate pollen grain D–E Seed morphology.

Discussion

A detailed comparison of E. coruana with E. patriotica and E. purhepecha is presented in Table 1. If these three species are related from an evolutionary point of view, the corolla appendages have evolved at least two times in ser. Gibbiflorae. The antipetalous stamen appendages of E. coruana are considerably smaller and less complex than those of E. novogaliciana, E. marianae, E. dactylifera and E. rulfiana, the other species of ser. Gibbiflorae that are known to possess them (García and Costea 2014, Jimeno-Sevilla et al. 2015). García and Costea (2014) indicated that these appendages do not have a secretory function and their role may be to protect the nectar accumulated at the base of petals from pollinators lacking a specialized feeding apparatus. In E. coruana, the appendages are too small to cover the corolla cavities in which nectar accumulates. Alternatively, if E. coruana is evolutionarily related to these latter four species, the reduction of antipetalous corolla appendages in E. coruana likely indicates the loss of this hypothetical nectar defense function. Corolla appendages at the base of stamens have also evolved in Pachyphytum (Walther 1972, Thiede and Eggli 2007), a genus that forms a sister clade to the remaining “Echeveria group” (Carrillo-Reyes et al. 2009). A molecular study for ser. Gibbiflorae with more extensive sampling that of Carrillo and et al. (2009) is necessary to understand the evolutionary relationships among the numerous members of this group (Walther 1972), including the several recently described species.

Ecology

The new species grows in the understory of mixed pine-oak and tropical deciduous forest on volcanic basaltic rocky outcrops or small ledges. However, it has also been observed growing epiphytically on Quercus sp. The tree layer is dominated by Quercus magnoliifolia Née, Ficus membranacea C. Wright, Juglans major (Torr.) Heller, Photinia microcarpa Standl., Bursera ariensis (H.B.K.) Mc. Vaugh & Rzed., and Clusia salvinii Donn.; the most common shrubs are Bursera bipinnata (Sessé & Moc. ex DC.) Engl., Montanoa bipinnatifida (Kunth) C. Koch, Montanoa frutescens (Mairet) ex DC. and Rhus terebinthifolia Schltdl. & Cham. The herbaceous understory vegetation includes among others: Arenaria lanuginosa (Michx.) Rohrb, Bonplandia geminiflora Cav., Tripogandra amplexicaulis (Klotzsch ex C.B. Clarke) Woodson, Phaseolus acutifolius var. latifolius G.F. Freeman, and Dryopteris maxonii Underw. & C. Chr.

Phenology

November to January.

Etymology

The specific epithet derives from San Andrés Corú, the nearest village to the malpaís where the species was discovered. “Corú” in the local Purhépecha language means “a place where the quails sing”.

Conservation status

Echeveria coruana is currently known only from three populations located at ca. 1–2 km from one another in the malpaís of San Andrés Corú. Although it is relatively common in the studied sites, it is threatened because of the increasing demand and exploitation of volcanic rocks in the area. Furthermore, the recent establishment of avocado orchards at elevations of 1670–1750 m has led to significant habitat loss in the area, and this practice is likely to continue in the future. Although it was not possible to use GeoCAT (Bachman et al. 2011) to calculate the extent of occurrence because of the reduced number of localities from which the species is known, we determined the area of occupancy, which was 8 square km (based on 2 km cells). Therefore, using the IUCN (2012) criteria B2 biii, we preliminarily categorize this species as Critically Endangered (CR). More research in the field will be carried out in the future to determine the best strategy to mitigate the above mentioned threats.

Additional specimens examined

México. Michoacán: Municipio de Ziracuaretiro, Malpaís de San Andrés Corú, bosque de encino-pino, 1676 m, 1 Dec 2012, D. Valentín 502 (CIMI!, EBUM!); Malpaís de San Andrés Corú, lado oeste-suroeste de San Andrés Corú, 1660 m, 29 Apr 2015, I. García, D. Valentín and A. Fuentes 9078 (CIMI!).

Echeveria yalmanantlanensis new for the flora of Michoacán

The exploration of the malpaís located at ca. 6 km SE of San Andrés Corú also led to an important floristic discovery: a new record of E. yalmanantlanensis (Fig. 3). This species has been considered in danger of extinction and endemic to the Cerro Grande Massif, which is situated in eastern Sierra of Manantlán Biosphere Reserve, Municipality of Comala, State of Colima, where it is known from one single population (Vázquez et al. 2013). More than a decade of concerted explorations conducted by multiple botanists to find additional populations at the type locality, the adjacent volcanic areas, Sierra de Manantlán Central, and Nevado de Colima, have been unsuccessful (reviewed by Vázquez et al. 2013). Under these circumstances, it was totally unexpected to discover it in Michoacan at about 210 km from the type locality. This finding suggests a disjunct distribution of E. yalmanantlanensis, which although rare may also be present at other localities in Central Michoacan.

Figure 3. 

Echeveria yalmanantlensis in the new habitat from Michoacan. A General habitat view of young epiphytic plants B–D Leaf rosettes and developing plants E Inflorescence.

Habitat and phenology of E. yalmanantlanensis. In Michoacan, E. yalmanantlanensis grows on volcanic rocks and occasionally as epiphyte in shady habitats that maintain sufficient humidity even during the dry season (Fig. 3). The vegetation at the new locality is very similar to that of E. coruana (see above), consisting of a mixture of pine-oak and tropical deciduous species. The vegetation at the type locality in Sierra of Manantlán includes some elements of tropical deciduous forest at 1500 m above the sea level; however, the companion species indicated by Vázquez-García et al. (2013)Jatropha bartlettii Wilbur, Bursera macvaughiana Cuevas & Rzed., and Agave attenuata Salm-Dyck. — have not been observed at the new site in Michoacan. Furthermore, at the original site, oak-pine forest vegetation elements were absent. The substrate at the original site in Colima State is calcareous, while in Michoacan it is volcanic. Also the epiphytic habitat observed in Michoacan (Fig. 3) was not reported from the type locality. The phenology is also somewhat different between the two sites: it extends to December at the new locality in Michoacan, while in Sierra of Manantlán plants were noted to flower from the end of July to the beginning of October. Only the climate is more or less similar at both sites, as it belongs to the type (A)C(w)(i´)(w2) (García 1988), semi-warm, sub-humid, with an annual average temperature between 18° and 22°C and characteristics intermediate between warm and temperate climates.

Conservation status of E. yalmanantlanensis.Vázquez-García et al. (2013) proposed the inclusion of E. yalmanantlanensis in the Mexican Endangered Species Act as an endangered species (Norma Oficial Mexicana, NOM-ECOL-059-2010). In Michoacan, only three populations with very few mature individuals (4–10) were found. An evaluation of the conservation status based on the geographical distribution using GeoCAT (Bachman et al. 2011) revealed that the extent of occurrence and area of occupancy (based on 2 km cells) in Michoacan are 62.01 km2 and 8 km2, respectively. Including the population from Colima and using the IUCN (2012) criteria, we provisionally propose an endangered status (EN) for this species. Like in the case of E. coruana, the habitat of E. yalmanantlanensis is threatened by the development of avocado plantations and exploitation of volcanic rock.

Specimens examined. MEXICO. Colima: Municipio de Comala (originally cited as Jalisco-Colima because of the proximity to the border between the two states), camino a Campo Cuatro, Cerro Grande, on a rock of a limestone slope, 1550 m, 26 Sep 2011, J. Antonio Vázquez-García, M. Cházaro B. & J. Padilla-Lepe 9175 (holotype: IBUG!; isotype: NY!). Municipios Comala border, camino de Campo Cuatro a La Añilera, Cerro Grande, tropical dry forest, on a rock of a limestone slope, 1500 m, 18 Jul 2004, Vázquez-García & Contreras 7830a, 7830b (IBUG!). Michoacán: Municipio de Ziracuaretiro, Malpaís de San Andrés Corú, Bosque de Encino, epífita sobre Quercus sp., 1513 m, 22 Dec 2012, D. Valentín 537 (CIMI, EBUM!); Malpaís de San Andrés Corú, bosque mixto con encinos, sobre rocosidades, 1510 m, 29 Apr 2015, I. García & D. Valentín 9077 (CIMI!); 15 Sep 2015, I. García & D. Valentín 9077 (CIMI!, WLU!).

Acknowledgements

We would like to thank the managers/directors of the CIMI, EBUM and IEB herbaria for providing access to collections, and to David Jimeno Sevilla for reviewing the manuscript. We are also grateful to Jesús Contreras León for his help during the field trips, to Patricia Silva Sáenz for her constructive comments, and to Fidel Carrillo for providing the initial information about the location of E. coruana. Last but not least, the first author is grateful to COFAA and EDI, and in particular SIP projects 20141105 and 20150493 of the Instituto Politécnico Nacional, Mexico for supporting this research.

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