Taxonomic and floristic novelties for Echeveria (Crassulaceae) in Central Michoacan, Mexico

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 Echeveria purhepecha and Echeveria patriotica, with whom it shares the closest morphological affinities. Additionally, Echeveria 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.


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, Th iede 1995, Meyrán and López-Chavez 2003, Pérez-Calix and Franco 2004, Vázquez et al. 2013). Among the infrageneric groups of this genus, ser. Gibbifl orae (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. Gibbifl orae (García and Pérez-Calix 2007, Jimeno-Sevilla and Carrillo-Reyes 2010, Reyes and González 2010, Reyes et al. 2011a, 2011b, García and Costea 2014, Jimeno-Sevilla et al. 2015, which suggests an incomplete knowledge of the species diversity in this group. Th e 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). Th is area is a part of the Trans-Mexican Volcanic Belt and has a particularly rich fl ora 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 fl oristic inventory of the malpaís surrounding San Andrés Corú. Th e malpaís ("badlands") is a landform that consists of relict yet recognizable lava fi elds that exhibit various degrees of erosion and vegetation succession stages depending on their age (Neuendorf et al. 2005). In some of the fi eld trips undertaken NW and W-SW of the village, an unknown Echeveria belonging to ser. Gibbifl orae 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. Th us, the fi rst objective of this article is to describe the new species, which we named E. coruana, and to explore its morphological affi nities with other species of ser. Gibbifl orae. Th e second aim is to report E. yalmanantlanensis as a new species for Michoacan.

Materials and methods
In addition to herbarium specimens, fl owers and leaves of E. coruana and E. yalmanantlanensis were fi xed 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 fi xed fl owers 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 fl owers 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
Th e new species, E. coruana belongs to ser. Gibbifl orae, 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; infl orescences 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, fl eshy; styles whitish to dark-red or nearly black. : the presence of corolla appendages at the base of antipetalous staminal fi laments. However, it markedly diff ers from these species in having smaller leaf rosettes, a diff erent leaf morphology, shorter infl orescences, cincini with fewer fl owers, 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. Th e most recently described species with corolla appendages, E. rulfi ana, diff ers 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).

Echeveria coruana I.García, D.Valentín & Costea, sp. nov.
urn:lsid:ipni.org:names:77158795-1 Figures 1, 2 Diagnosis. Echeveria coruana morphologically resembles most E. patriotica and E. purhepecha, with which it shares a similar fl ower morphology, but diff ers from both in having acaulescent or inconspicuous stems, acuminate leaves, and corolla appendages at the base of antipetalous stamen fi laments. It diff ers from E. patriotica in having smaller leaf rosettes, 10-15 cm in diameter, smaller infl orescences, 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.
Ecology. Th e 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. Th e tree layer is dominated by Quercus magnoliifolia Née, Ficus membranacea C. Phenology. November to January. Etymology. Th e specifi c 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 signifi cant 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). Th erefore, using the IUCN (2012) criteria B2 biii, we preliminarily categorize this species as Critically Endangered (CR). More research in the fi eld will be carried out in the future to determine the best strategy to mitigate the above mentioned threats. Additional

Echeveria yalmanantlanensis new for the flora of Michoacán
Th e exploration of the malpaís located at ca. 6 km SE of San Andrés Corú also led to an important fl oristic discovery: a new record of E. yalmanantlanensis (Fig. 3). Th is 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 fi nd 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. Th is fi nding suggests a disjunct distribution of E. yalmanantlanensis, which although rare may also be present at other localities in Central Michoacan.
Habitat and phenology of E. yalmanantlanensis. In Michoacan, E. yalmanantlanensis grows on volcanic rocks and occasionally as epiphyte in shady habitats that maintain suffi cient humidity even during the dry season (Fig. 3). Th e 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. Th e 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. Th e 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 re- ported from the type locality. Th e phenology is also somewhat diff erent between the two sites: it extends to December at the new locality in Michoacan, while in Sierra of Manantlán plants were noted to fl ower 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´)(w 2 ) (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 Ofi cial 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 km 2 and 8 km 2 , 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.