Salvia reginae and S. spellenbergii (Lamiaceae), two new species from Chihuahua, Mexico

During botanical explorations in the highlands of NW Mexico, two new Salvia L. species were discovered in the state of Chihuahua: S. reginae J. G. González & J. H. Vega and S. spellenbergii J. G. González. The first one is morphologically similar to S. concolor Lamb. ex Benth., from which it differs by having smaller floral bracts, a longer upper corolla lip, stamens parallel to the dorsal corolla line, longer filament and connective, the latter ornate with an antrorse tiny acute tooth, longer thecae, longer and exserted styles, and bigger mericarps. Salvia spellenbergii resembles S. fruticulosa Benth., S. goldmanii Fernald and S. pruinosa Fernald; however, it can be distinguished from these because of its shorter petioles, smaller leaf blades, usually fewer floral nodes, fewer flowers per floral node, and regularly shorter calyces. Both species are described and illustrated. Tables with morphological comparisons, illustrations, conservation assessment, and a distribution map are also presented.


Introduction
Salvia L. is the largest genus within Lamiaceae with an estimated diversity among 900-1000 species worldwide (Frodin 2004;Harley & al. 2004;Drew & al. 2017). However, considering recent taxonomic rearrangements (Drew & al. 2017) and constant description of new species around the globe (Fernández-Alonso 2014; Celep & al. 2015;Hu & al. 2017;Zamudio & Bedolla-García 2018; as some examples), an updated and more stable account is still needed. The systematic research on the genus is very active with several efforts attempting to readjust its taxonomy and classification in order to recognize several smaller monophyletic genera (Will & Claßen-Bockhoff 2017) or a broader natural genus (Drew & al. 2017). The rearrangements in the traditional Salvia circumscription and classification (Bentham 1832(Bentham -1836(Bentham , 1848(Bentham , 1876 are compulsory because the results of phylogenetic analyses have proved that these are largely artificial (Walker & al. 2004;Walker & Sytsma 2007). Between the different alternatives to deal with the polyphyly of Salvia, the transfer of the genera Dorystaechas Boiss. & Heldr. ex Benth., Meriandra Benth., Perovskia Kar., Rosmarinus L. and Zhumeria Rech. f. & Wendelbo to a broader Salvia circumscription has been defended as the most equitable solution based on molecular and morphological evidence, and which is congruent with practical and ethical commitments, i.e. avoiding excessive taxonomic changes that would destabilize the taxonomy of the group creating confusion and hindering communication between the systematic community and general users of the nomenclature (Drew & al. 2017). The latter approach is the one followed and accepted herein.
The overwhelming Salvia diversity at global scale is mirrored in Mexico with more than 300 species currently recognized (Martínez-Gordillo & al. 2017), being the country with the highest diversity of the genus worldwide. In fact, according to the most recent inventory of the vascular plants in Mexico, Salvia is the most speciose genus of the Mexican Flora (Villaseñor 2016). This outstanding diversity is reflected in the wide array of morphological variation, ecological preferences, wide distribution and diversity of geographical patterns exhibited by the Mexican species (Cornejo-Tenorio & Ibarra-Manríquez 2011;. However, besides the relevance of the genus, the knowledge of its diversity is still deficient, and research efforts have resulted in continuous discovery of novelties in both distribution and taxonomy (Bedolla-García & Zamudio 2015Fragoso-Martínez & al. 2015;González-Gallegos 2015a, 2015bGonzález-Gallegos & López-Enríquez 2016;Martínez-Gordillo & al. 2016a, 2016bOlvera-Mendoza & al. 2017;Zamudio & Bedolla-García 2018). As part of ongoing research on the diversity of Mexican Salvia, in concert with exploration of Mohinora mountain in NW Mexico, two undescribed species were discovered; both belong to S. subg. Calosphace (Benth.) Epling, according to stamen morphology (elongated connective with only two fertile thecae at apex of anterior arms, and the posterior ones connate between them). Consequently, the new taxa are here described and illustrated as part of the growing information towards an updated monograph of Salvia diversity in Mexico.

Material and methods
Herbarium specimens of both taxa were collected on August 2016 and 2018, respectively; these were herborized and prepared according to standard procedures (Lot & Chiang 1986). The herbarium specimens collected of both new species for this study, and those of Salvia spellenbergii sp. nov. already deposited in CIIDIR and MEXU herbaria, were thoroughly examined and collated against specialized literature for its identification (Epling 1939;Ramamoorthy 2005;Klitgaard 2012;, as well as compared with type specimens of morphologically similar species at JSTOR Global Plants (JSTOR 2019). After the previous step, it was clear that these specimens belonged to undescribed species, accordingly, qualitative and quantitative characters were assessed using a dissecting microscope Zeiss Stemi 508, and the descriptions were prepared. The conservation status of the species was evaluated according to IUCN (2012) categories and criteria, and with the help of GeoCAT (Bachman & al. 2011). However, S. reginae deviates from the latter because of its smaller floral bracts, longer upper corolla lips, stamen position (parallel to corolla dorsal line instead of oblique in respect to this), these exserted by 8 -10 mm, longer filaments and connectives, the latter ornate with an an- trorse tiny acute tooth, longer thecae, longer and exserted styles by 11 -17 mm, and bigger mericarps.
Distribution and ecology -Salvia reginae is an endemic species from Chihuahua, Mexico (Fig. 2). It is known only from two localities, the base of Mohinora mountain peak and Cañón Prieto near Mesa de Las Guacamayas. It grows in very humid ravines, mainly at the surroundings of small streams, in pine forest or riparian vegetation. Conservation status -Until further botanical explorations in the area are carried out and more data compiled, Salvia reginae should receive a preliminary conservation status of Data Deficient. However, there is no doubt that, under geographical criteria, the species could be classified as Critically Endangered (CR) based on a calculated Extent of Occurrence (EOO) of 0.004 km 2 , and a calculated Area of Occupancy (AOO) of 8 km 2 (IUCN 2012), these were estimated using a cell width of 2 km.
Etymology -The epithet of this species is dedicated to Regina Vega González, daughter of the second author, who at her young age (eight years old), has started to appreciate the beauty and diversity of wild plants.
Remarks -Salvia reginae is morphologically similar to S. concolor, which belongs to S. sect. Dusenostachys (Epling) Epling. This section is one of those in need of a restructuring because not all its species have been recovered as part of the same monophyletic group (Jenks & al. 2011(Jenks & al. , 2013. Salvia reginae can be differentiated from S. concolor by having smaller floral bracts, longer upper corolla lips, stamens exserted by 8 -10 mm, longer filaments, longer connectives, ornate with an antrorse tiny acute tooth, longer thecae, longer styles and exserted by 11 -17 mm, and bigger mericarps (Table 1).
Additionally, the connective in Salvia concolor is oblique to the corolla dorsal line, blocking the entrance to corolla tube; hence, the pollinators are forced to push it back when trying to get the nectar, and doing so, they activate the staminal lever mechanism. During this process the stamens descend, the thecae get exposed (from upper corolla lip) and the pollen is deposited on pollinator's body (Claßen-Bockhoff & al. 2003). In S. reginae, the stamens are parallel along dorsal line of the corolla tube; hence, the corolla tube entrance is not blocked, and the staminal lever mechanism could not be activated. Besides, the long corolla tubes and the exserted and immovable stamens suggest that in S. reginae the pollination is restricted to birds (Wester & Claßen-Bockhoff 2007).
Wester & Claßen-Bockhoff (2011) classified S. concolor as a species with a transitional pollination syndrome between bees and birds (ornithophilous to melithophilous, or intermediate). They consider that the ample lower corolla tube of S. concolor plays a role as landing platform for bees, although the corolla tube length in morphs with the longer corollas would exclude bees from reaching nectar at the corolla bottom. The difference in stamen position between both species can have deep ecological implications in terms of how these species interact with their pollinators and floral visitors, it could also be an example of an evolutionary transition from one pollination syndrome to another, like to what was hypothesized for S. platyphylla Briq. and Diagnosis -Salvia spellenbergii is morphologically similar to S. fruticulosa Benth., S. goldmanii Fernald and S. pruinosa Fernald. However, it differs from them because of its shorter petioles, smaller leaf blades, usually fewer floral nodes, fewer flowers per floral node, and regularly shorter calyces. It is also distinguished from S. fruticulosa and S. goldmanii by having smaller floral bracts and corolla tubes, and shorter filaments and styles. It is separate from S. fruticulosa and S. pruinosa due to the trimucronate upper calyx lips, and from S. goldmanii because of the lack of two folds inside the basal portion of corolla tube.
Phenology -Flowering and fruiting from the end of July, most likely until November or December.
Conservation status -The species is known only from five localities, four in the protected area of Cascadas de Basaseachi National Park, and another nearby Urique. Based on geographical criteria, it is suggested to assign Salvia spellenbergii a preliminary conservation status of Critically Endangered (CR) or Endangered (EN) following IUCN Red List categories and criteria (IUCN 2012). The Extent of Occurrence (EOO) was calculated as 88.608 km 2 and the Area of Occupancy (AOO) was estimated as 12 km 2 based on a cell width of 2 km. However, the species grows in an orographically complex area with several inaccessible sites, so other populations might eventually be found. Moreover, con-  sidering that the species grows within a National Park population decline and conservation threats should be minor. The species can remain as Data Deficient until a thorough evaluation is conducted.
Etymology -The epithet is dedicated to Richard W. Spellenberg, Emeritus Curator of the NMC herbarium (Las Cruces, New Mexico), one of the first in collecting the new species, and enthusiastic contributor to the knowledge of the NW Mexican flora. One of his contributions consists of a floristic inventory of Basaseachi National Park (Spellenberg & al. 1996). In that publication, the specimen Spellenberg & al. 8807 (MEXU,NMC) was included under the name Salvia chamaedryoides Cav.; however, this belongs to S. spellenbergii.
Remarks -Salvia spellenbergii can be assigned to S. sect. Tomentellae (Epling) Epling because of the perennial habit, branched hairs, deciduous floral bracts, 5 -7-veined upper calyx lip, non-invaginated corolla tube at base, included stamens, geniculate connective and densely pubescent mericarps (Epling 1939). Among the species of this section, the new taxon is morphologically similar to S. fruticulosa, S. goldmanii and S. pruinosa in having ovate, deltoid-ovate to oblong-lanceolate leaf blades, and pubescent mericarps. However, there are several characters that warrant the recognition of S. spellenbergii as a different species. It can be distinguished from S. fruticulosa in having shorter petioles, slightly smaller leaf blades, fewer floral nodes, more lax inflorescences, fewer flowers per node, and a trimucronate and 5-veined upper calyx lip (Table 2). Salvia spellenbergii differs from S. goldmanii by the shorter petioles, leaf blade shape, fewer flowers per floral node, smaller floral bracts, shorter calyces and 5-veined upper calyx lips, shorter corolla tubes, corolla tube naked inside, shorter filaments, and shorter styles (Table 2). In contrast to S. pruinosa, the new species possesses smaller petioles, smaller leaf blades, bigger floral bracts, and trimucronate upper calyx lips (Table 2). Moreover, of the three similar species, only Salvia goldmanii is distributed in the state of Chihuahua; whereas, S. pruinosa also inhabits the Sierra Madre Occidental, but not in the same state. Salvia fruticulosa is the most geographically distant species, distributed in the Sierra Madre del Sur biogeographic province in Oaxaca and Puebla (Table 2).
It should be noted that several of the specimens examined of this species, and that in the published list of vascular plants growing in Cascada de Basaseachi National Park (Spellenberg & al. 1996), were identified as Salvia chamaedryoides, a species of S. sect. Flocculosae (Epling) Epling. However, this species can be easily differentiated by having an entire upper calyx lip and 7-veined, ventricose and invaginated corolla tube, connective ornate with a retrorse acute tooth, and glabrous mericarps.