Populus primaveralepensis sp. nov. (Salicaceae, Malpighiales), a new species of white poplar from the Bosque La Primavera Biosphere Reserve in western Mexico

Abstract. Populus primaveralepensis A.Vázquez, Muñiz-Castro & Zuno sp. nov., a new species from relict gallery cloud forest in Bosque La Primavera Biosphere Reserve (Mexico), is described and illustrated. The new species belongs to P. subsect. Tomentosae Hart., and is morphologically similar to P. luziarum A.Vázquez, Muñiz-Castro & Padilla-Lepe, but differs from it in having taller trees without root suckers, white and ringed young stems and branches, a branching angle of ca 45o, leaves with higher blade to petiole ratio, leafs frequently elliptic or ovate to widely ovate (vs widely ovate to ovatedeltoid), denser infl orescences, and shorter capsules. The conservation status of the species was assessed as Critically Endangered (CR).


Material and methods
Populus primaveralepensis sp. nov. was fi rst collected at the BLPBR in 2009 from a single small tree, and the specimen was kept at IBUG (Harker et al. 4045 leg.). However, it remained cryptic since it was determined and fi led in the IBUG herbarium as P. simaroa Rzed. Recently, in February 2013, J. Padilla-Lepe, a member of a seed-collecting team at the BLPBR, led by O. Zuno-Delgadillo, found it again, but this time as the dominant canopy tree in the relict gallery cloud forest of the eastern Tala, Jalisco. The biologist J. Padilla-Lepe only collected a single sterile terminal twig, because he thought it was a second locality of P. luziarum, a recently described species that he had found a year earlier in western Tesistán, in Zapopan, Jalisco (Vázquez-García et al. 2017). A month later (March 2013), A. Vázquez, J. Padilla-Lepe, and O. Zuno-Delgadillo revisited the population for a closer examination, unveiling substantial qualitative and quantitative differences from the latter in the habit (non-soboliferous and taller trees with whitish branches), narrower leaves, and denser male and female infl orescences (Table 1), allowing us to conclude that we were dealing with an undescribed species of P. (sect. Populus) subsect. Tomentosae.
The morphological description and the illustrations are based on fresh and herbarium material. Leaf description and terminology of reproductive structures follow Radford et al. (1974), Eckenwalder (2010, and Dickmann & Kuzovkina (2014). The herbarium acronyms follow Thiers (2017). Detailed examination of herbaria type specimens and electronic images of type material for both P. guzmanantlensis (holotype: ZEA; isotypes: BRIT, CAS, CHAPA, CIIDIR, ENCB, F, GH, LE, MEXU, MICH; MO, TEX, UAMIZ, WIS) and P. simaroa (holotype: ENCB; isotypes: CAS, ENCB, G, MEXU, MICH, MO, NY, OS, P, US), available at the Global Plant JSTOR website (except for the holotype of P. guzmanantlensis), allowed us to determine the morphological differences among the taxa (Table 1). For the accepted names we followed POWO (2018). Authors and names of plants follow the IPNI (2018). The conservation status was assessed based on the criteria of IUCN (2012).    Sep. to Nov.

Mar. to May
Aug. to Oct.
Feb. to Apr.
Mar. to Jun.

Fruiting
Oct. to Nov.
Oct. to Jan.
Apr. to Jun.
Oct. to Nov.

Differential diagnosis
Populus primaveralepensis sp. nov. is morphologically close to P. luziarum, but it differs from the latter in possessing various qualitative and quantitative characters, such as having taller trees with nonsoboliferous habit, branching angle of ca 45º with white and ringed bark, and leaves with higher blade to petiole ratio (large leaves with petioles 2.9-3.9 vs 5.4-6 cm long, leaf blades frequently elliptic or ovate to widely ovate vs widely ovate to ovate-deltoid, 17-18.5 vs 15.5-16 cm long, infl orescences dense vs sparse, and shorter capsules, 1.0-1.8 vs 2.0-2.5 mm (Table 1). Isotypes MEXICO • Same data as for the holotype; K, MEXU, MO, ZEA.

Etymology
The epithet honors the collective conservation accomplishments at Bosque La Primavera for its twelfth anniversary as a MaB-UNESCO Biosphere Reserve as well as the biologist Jesús Padilla Lepe, a young and enthusiastic botanical explorer graduated from the Universidad de Guadalajara who discovered the species.

Distribution, habitat and phenology
Western Mexico: State of Jalisco, Bosque La Primavera Biosphere Reserve, along the tributaries of Río La Lobera and Río Caliente, in the municipalities of Tala and Arenal, respectively (Fig. 5).  Table 1). The fl owering occurs from August to November, the fruiting from October to November, and deciduous foliage can be observed during winter, from January to early March.

Taxonomic remarks
Because of its bifacial leaves, broad ciliate bracts; persistent, entire and oblique disk, two carpels, and 4-6 seeds, P. primaveralepensis sp. nov. falls within P. sect. Populus, the most speciose section of the genus (13 species); it belongs to P. subsect. Tomentosae, a subsection consisting of white poplars with abaxially pubescent leaves (Eckenwalder 1977a(Eckenwalder , 1977b. Populus primaveralepensis sp. nov. is morphologically close to P. luziarum in having abaxially tomentose leaves and buds; however, it differs from the latter in having a taller habit (25-30 vs 15-20 m), a different type of spread (exclusively by seeds vs both by seeds and by means of root-borne sucker shoots), branches white and ringed vs brown and not ringed, branching angle (usually ca 45 vs > 75º), longer large-sized leaves with shorter petioles, elliptic to ovate to widely ovate vs widely ovate to ovate-deltoid, rounded to subcordate at the base vs obtuse to rounded to subcordate, and acute at the apex vs rounded, acute to shortly apiculate (Table 1). Additionally, P. primaveralepensis sp. nov. differs from P. luziarum in terms of its phenology, losing leaves during winter vs autumn.

Ethnobotany
The species is locally known as "álamo". There is no available information on the use of the species in Jalisco; however, sometimes it is kept as a shade tree for cows. Like other species in the genus Populus, P. primaveralepensis sp. nov. is a potential source of cellulose fi bers, and can be used as an ornamental tree, or for restoration of watersheds in central Jalisco.
The known Extent of Occurrence (EOO) of P. primaveralepensis sp. nov. is ca 97.88 km 2 , but from this area, only an Area of Occupancy (AOO) of ca 48.29 km 2 is represented by its habitat (relict gallery cloud forests in humid ravines); the rest is occupied by human settlements (Tala city and La Primavera town), country roads, highways, agriculture, and pasturelands, even inside the BLPBR. Hence, according with IUCN Red List criteria B1ab(iii) (IUCN 2012), P. primaveralepensis sp. nov. should be categorized as Critically Endangered, an addition to the fl ora of conservation concern at BLPBR ( Table 2), because it has an EOO < 100 km 2 , very small and restricted subpopulations which are severely fragmented; there are less than 120 individuals known, and there is a continuing observed and projected decline in the area and quality of its habitat (relict gallery cloud forest).
Populus primaveralepensis sp. nov. is extremely rare, thus it should be protected immediately. It is important to disseminate this case and alert the general public that the fragmentation of habitats (mainly road expansion) represents a great threat for these fragile relict ecosystems, which have harboured numerous species for over one hundred millennia (Mahood 1980).

Conservation status
Populus primaveralepensis sp. nov. and P. luziarum belong to the P. subsect. Tomentosae and are likely closely related phylogenetically. Based on cpDNA sequences, it has been confi rmed that P. sect. Populus represents a monophyletic group, although the phylogenetic relationships within the section are still uncertain (Wang et al. 2015;Zhang et al. 2017). This section has a relatively young evolutionary history, and because of fossil records, and morphological and molecular phylogenetic analyses (Eckenwalder 1996;Wang et al. 2014Wang et al. , 2015, it is inferred that this group originated from the rapid radiation of Table 2. Plant species of conservation concern at Bosque La Primavera Biosphere Reserve, Jalisco, Mexico (Hernández-López 2006;Hernández-López et al. 2006, 2009a, 2009bSEMARNAT 2010;IUCN 2012 an ancestral member of P. sect. Leucoides Spach. The relative recent morphological and evolutionary divergence is presented by the similarities exhibited by P. luziarum and P. primaveralepensis sp. nov., which could have migrated from a Pleistocene refuge in the Sierra Madre Occidental to the geologically recent Sierra La Primavera volcanic complex (western Transmexican Neovolcanic Belt), which was formed by several eruptions that happened between 120 000 and 20 000 years ago (Mahood 1980). Both species are linked to ravines and permanent streams, and have certainly played an important role in the maintenance and continuity of these ecosystems for at least 120 000 years. Even though the geographical ranges of the two species are only 13.5 km apart, they occur in different basins (Río Ameca and Río Santiago, respectively), exhibiting distinct geomorphological features, and atmospheric and climatic conditions (SEMADES 2006).

Floristic relevance
The riparian communities of P. primaveralepensis sp. nov. and P. luziarum do not share any tree species (100% dissimilar). Hence, according with their current fl oristic composition (Table 1), it is evident that the two areas represent two distinct biogeographical histories, with no recent exchange between them, which deserve more attention; they will provide a great opportunity to study the incipient evolutionary history of various fl oristic elements that have presumably migrated to the La Primavera Forest from the older Sierra Madre Occidental.
Mexico, now with eleven species of Populus, represents one third of the worldwide richness of this genus (POWO 2018), and is the richest in the continent followed by USA (eight species) and Canada (fi ve species). Jalisco, with a 45% (fi ve species) of the Mexican species of Populus, now matches Chihuahua in terms of absolute richness of species of Populus, even though the latter area is nearly three times larger in area (247 460 vs 79 080 km 2 ).
Populus primaveralepensis sp. nov. is now the fi rst species categorized as Critically Endangered (CR) within BLPBR, out of the 14 species of conservation concern in this protected area (Table 2), a reserve with more than 1000 species of vascular plants.