Diversity of the Pteridoflora of Montane Northwestern Mexico

Abstract

This study compiles and updates the checklist of ferns and lycophytes from the Sierra Madre Occidental (SMOc). For this, we revised information on these taxa from regional floristic studies, databases, and herbaria. Our updated list includes 312 species, of which 276 are ferns and 36 are lycophytes integrated into 27 families and 75 genera. The richest families are Pteridaceae (118), Polypodiaceae (31), Selaginellaceae (30), Aspleniaceae (25), and Dryopteridaceae (25). The three most diverse genera were Selaginella (30), Asplenium (25), and Myriopteris (22). The species-rich Mexican states that include the SMOc are Durango (166 species), Chihuahua (149), and Jalisco (146). As in other tropical mountains, species richness in the SMOc is concentrated at the elevation interval of 1500 to 2000 m (236 species). The mid-mountain vegetation forests (Quercus and Pinus-Quercus forests) harbor the most pteridoflora richness (52% of the species). Four species of ferns are listed as threatened in the Mexican Official Norm NOM-059-SEMARNAT-2010, 17 species are listed in the IUCN, and only one tree ferns are in CITES. The SMOc has a Nearctic affinity, and its fern and lycophyte diversity are lower than in other Mexican Transition Zone mountain chains, such as the Sierra Madre del Sur, the Trans-Mexican Volcanic Belt, and the Sierra Madre Oriental. Notwithstanding, its biological composition is unique and distinctive. The species number reported in the SMOc represents 31% of the pteridoflora diversity recorded in Mexico.

1. Introduction

Ferns and lycophytes are seedless vascular plants that are highly diverse worldwide, especially in the montane areas of tropical regions [1,2,3]. For example, the territory of Mexico, where almost 75% of it consists of mountains, represents one of the countries in the Neotropics with a highly diverse pteridoflora diversity [2], with nearly 1043 species [4,5]. This number represents nearly 5% of the total vascular flora of the country (23,314 species sensu Villaseñor [6]), and 20% are endemic [4]. In addition, recently described new species increase this richness [7,8].

The Mexican fern flora has been extensively studied from a taxonomic point of view [9]. In addition, other states and regional floras are available [4,10,11], among others. However, it is necessary to study some regions where information is still scarce or scattered. The review of specimens in herbaria, fieldwork in different regions of the country, and studies of local floras show large areas that are so far little explored [5,12,13,14].

Previous floristic and biogeographic research related to ferns and lycophytes has been carried out in some of the main mountain chains of Mexico, such as the Sierra Madre del Sur [4], the Sierra Madre Oriental [15,16], and the Trans-Mexican Volcanic Belt [17]. In addition, there are general studies of pteridoflora in the Serranías Transístmicas in Chiapas [18] and the Sierra de la Giganta in Baja California Norte [19,20]. Although the Sierra Madre Occidental has not been studied entirely with regard to its pteridoflora, available information on herbaria and previous studies exists. Unfortunately, this mountain chain has no extensive regional inventories of ferns and lycophytes. Nevertheless, the arid–semiarid zone of northwestern Mexico (and the southwestern United States) has been considered an area of endemicity for this group of plants [21,22], which are regions that, in turn, are recognized as highly endemic for flowering plants [23,24].

Tropical mountains have been considered areas of high concentration of biodiversity and have been recognized as biodiversity hotspots [25,26,27]. In the case of ferns and lycophytes, tropical mountains play a central role in their diversity and diversification [1,26]. They are also clearly associated with the main hotspots recognized for these groups of vascular plants [1,3]. Furthermore, the Mexican ferns and lycophytes represent biological lineages that are relatively well-studied [9]; they are diverse (>1000 species) and have been relatively well-sampled in most of the Mexican mountain chains [4,17,28]. For these reasons, the studies and inventories of ferns and lycophytes in the mountain chains of Mexico are imperative and relevant in terms of plant diversity, mainly in areas that are poorly studied, such as the Sierra Madre Occidental.

Detailed studies to obtain information on plant taxonomic groups such as ferns and lycophytes at regional or local scales are essential to understand their evolution and biogeography and to evaluate their conservation status. This study aimed to carry out a floristic inventory of ferns and lycophytes in the Sierra Madre Occidental (SMOc) to unify the previous knowledge and update floristic information. We also offer information about the ecology, distribution, and conservation status of ferns and lycophytes inhabiting the SMOc. Also, we compared the species richness of the study area with the other Mexican mountain chains. Finally, we highlight the local endemism and threatened taxa.

2. Materials and Methods

2.1. Study Area

The SMOc is a morphotectonic and biogeographic province located in northwestern Mexico (Figure 1), with extreme coordinates of 30°35′–21°00′ N and 109°10′–102°25′ W. It is the most extensive mountainous complex in the country, covering almost 1200 km [29,30]. This Sierra connects the Rocky Mountains in the United States with the Trans-Mexican Volcanic Belt in the south and runs parallel to the Pacific coast. It has been considered an important biological corridor for both boreal species and tropical mountain elements [23].

The SMOc has the most extensive area with temperate forests in the country, for the confluence in its territory of floras of diverse origins, and for its great variety of vegetation types. The SMOc divides the subhumid Mexican tropical forest on the southwestern side (Jalisco to Sonoran) and desert scrub on the north and east sides (Sonoran-Chihuahuan desert) [31,32]. Therefore, this biogeographic province is crucial and considered part of the Mexican Transition Zone [32,33]. The SMOc mountain chain comprises parts of the following states: Aguascalientes, Chihuahua, Durango, Jalisco, Nayarit, Sinaloa, Sonora, and Zacatecas (Figure 1). This mountain chain has an average elevation of 2500 m, with a median of 1800 m on its eastern side facing the Mexican Plateau and a low elevation limit of 300 m on its western side facing the Pacific slope. In contrast, the highest points, such as Cerro Gordo (3347 m asl), Barajas (3310 m), and Mohinora (3307 m), reach more than 3300 m asl, with the first two located in Durango and the last one in Chihuahua [30]. This mountain chain is composed mainly of ignimbritic rocks (estimated at ca. 289,000 km² [34]), and the vegetation covers 251,648 km² [30].

The SMOc is a volcanic arc produced from magmatic and tectonic episodes related to the subduction of the Farallon tectonic plate beneath the North American plate, and it was constructed from north to south during 60 m.a., starting in the late Cretaceous and ending in the middle Miocene [29,35]. In the first stage, effusive volcanism in the SMOc was developed from its origin to near 32 m.a., changing later to explosive volcanism, which contributed to its extension and elevation increase [35]. Thus, this mountain chain is an example of the enormous volcanic activity in the Mexican territory and represents one of the larger silicic igneous areas in the world [29].

In the western part of the SMOc, the section facing the Pacific generally has a monsoon-type climate [36]. That area presents different humidity gradients. The orographic shadow effect causes a drier inner slope in the mountain, which decreases humidity from west to east from the Pacific Ocean Slope to the Mexican Plateau. The intertropical convergence zone sheds rain in the summer in Nayarit, Jalisco, and southeastern Mexico. The northern part is influenced by the subtropical belt of high atmospheric pressure and by the cold oceanic current of California, with increasing humidity from north to south. Although intermittent, the summer–autumn hurricanes originating in the Pacific Ocean run from south to north and leave moisture in northwestern Mexico. The landscape heterogeneity is also related to a wide range of climates: it is dry in the north and eastern slopes, temperate and semi-cold in the highlands, and warm in the lowland zones of the western slopes facing the Pacific Ocean [37]. The SMOc represents the driest Mexican temperate mountain system (seasonal temperate forests), so it does not harbor as great a diversity of ferns and lycophytes as the wetter Mexican mountains. In the SMOc, the understory of the seasonal forest is frequently covered with leaves, thus preventing the establishment of other plants.

Figure 1. Map of northwestern Mexico. (A) Localization of the Sierra Madre Occidental (SMOc) and Sky Islands [33] and (B) vegetation types and land use in the SMOc [38]. AGS = Aguascalientes.

Figure 1. Map of northwestern Mexico. (A) Localization of the Sierra Madre Occidental (SMOc) and Sky Islands [33] and (B) vegetation types and land use in the SMOc [38]. AGS = Aguascalientes.

There are four general climatic zones in the SMOc: (a) dry and semi-dry climates (type BS) in the foothills to the east, north, and northwest; (b) temperate climates and semi-cold (C and C(E), respectively) in the upper part and middle part, semi-dry towards the eastern slope, and sub-humid towards the western; (c) semi-warm (A(C)) on the western slope; and (d) warm (A) in the lower parts and ravines. The rainy season occurs in summer with a marked climatic seasonality [30].

About 14 vegetation types exist in the SMOc (Figure 1) and change dramatically from slope to slope, as well as among different elevation sites [30,38]. Pines, pine-oak, other conifer forests, and oak forests cover the highlands (57% of the surface). This region harbors the greatest diversity associations of pines, oaks, and Arbutus worldwide [39]. In addition, there are tropical deciduous and semideciduous forests on the western slopes. The northern and eastern slopes of the SMOc, facing the Mexican Plateau, are dominated by semi-arid landscapes with xeric scrublands. The riparian forest and other wetlands constitute azonal vegetation types [30]. Two mega centers of diversity are recognized in the SMOc: one in the northern part and the other in the high basin of the San Pedro Mezquital River. [30,40,41].

2.2. Distributional Data and Analysis

We constructed a database with updated taxonomic and phylogenetic information on ferns and lycophytes from four primary sources: (1) the review of floristic studies carried out in the SMOc [11,42,43,44,45,46,47,48,49,50]; (2) revision of the herbarium specimens in some Mexican botanical collections, including the national herbarium of the Instituto de Biología, UNAM (MEXU), the herbarium of the Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional (ENCB), the herbarium of the Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Unidad Durango, Instituto Politécnico Nacional (CIIDIR), and the herbarium of the Universidad Autónoma de Aguascalientes (HUAA); (3) revision of the digital databases, e.g., the New York Botanical Garden (NYBG), the Missouri Botanical Garden (https://www.tropicos.org/home, accessed on 3 August 2021), the Pteridophyte Collections Consortium (PCC) (https://www.pteridoportal.org/portal/index.php, accessed on 3 August 2021), and the Red de Herbarios del Noroeste de México (https://herbanwmex.net/portal/, accessed on 3 August 2021); (4) field surveys in some poorly collected areas. Some of these areas are the Sky Islands in the northern part of the SMOc; protection areas of fauna and flora in Campo Verde in Sonora, northern SMOc; protection areas of fauna and flora in Tutuaca, between Chihuahua and Sonora, in the central part of the SMOc; the gorges region in Durango, western SMOc; and the Sierra del Nayar, southern SMOc.

Voucher specimens collected during the fieldwork were deposited at the national herbarium (MEXU) and the herbarium of the Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Unidad Durango (CIIDIR). For each specimen examined, we verified the identity of the species and updated the nomenclature to the latest taxonomic revisionary studies, mainly based on the Phylogeny Pteridophyte Group, or PPG I [51]. In addition, we depurated and updated the taxa names without clear identities, voucher references, and accurate geographic data from the Missouri and New York Botanical Gardens and the Red de Herbarios del Noroeste databases.

We consulted the following monographic, taxonomic, and phylogenetic studies to update the nomenclature of genera and species: Amauropelta [52], Austroblechnum [53], Botrypus [54], Christella [52], Cyclosorus [55], Ephemeropteris [56], Gaga [57], Gastoniella [58], Goniopteris [52], Leptogramma [55], Pelazoneuron [55], Phlegmariurus [59], Pleopeltis [60], Myriopteris [61], Sceptridium [54], and Vandenboschia [62]. The taxonomic study of Mickel and Smith [9] was reviewed for the remaining genera and species.

From all these information sources, we compiled a final checklist of accepted taxa based on the validation of names through referenced phylogenetic studies, the cross reference of databases, and the revised vouchers from herbaria. In the final checklist (Appendix A), the classification follows the PPG I [51].

From these sources, our final database contains information on fern and lycophyte species, including locality (state and geographical coordinates), elevation, and life form. The vegetation types followed the proposal of González-Elizondo et al. [30]. This information was obtained from the herbaria labels and web databases. The SMOc presents a wide elevation range, so we delimited seven elevation intervals of 500 m to represent the tendency of species in a graph. These intervals were used for comparative purposes (e.g., [1,63,64,65]). Finally, the study of Mickel and Smith [9] was used as a general framework to assess the limits of fern and lycophyte species’ geographic distributions and endemism. For this, we determined eight categories related to the geographic distribution of each species as follows: (1) Cosmopolitan—taxa distributed worldwide; (2) American— taxa distributed in the American continent; (3) Nearctic—taxa distributed in Mexico and North America; (4) Neotropical—taxa distributed in Mexico, Central, and South America, including, in some cases, Florida in the United States of America; (5) Mesoamerican—taxa distributed in Mexico and Central America; (6) Endemic to Mexico—taxa whose known distribution is restricted to Mexico; (7) Endemic to the SMOc—taxa whose known distribution is restricted to the limits of the SMOc; (8) Regional endemic to northwestern Mexico—taxa whose known distribution is limited to the SMOc and adjacent states of the United States of America (Arizona, New Mexico, and Texas) and northern Mexico (Coahuila).

In general, the flora richness is expressed as the species number or a biodiversity index that considers the number of species per area in a logarithmic sense. Therefore, using biodiversity indexes is essential for comparing sampled areas with different sizes. In this study, we are comparing the SMOc with other Mexican mountain chains. Therefore, we calculated the floristic richness (taxonomic biodiversity index) following the suggestion of Squeo et al. [66]: R = N/ln A (where: N = species number; lnA = natural logarithm of the area in km). With this formula, we compared the species richness among geographic regions.

We revised the Mexican Official Norm NOM-059-SEMARNAT-2010 [67] to recognize how many fern and lycophyte species of the SMOc are listed and to verify their corresponding risk category. The NOM-059-SEMARNAT-2010 is the official document generated by the Mexican government that encompasses the environmental protection of the wild flora, fauna, and fungi species native to Mexico [67]. This document includes the specifications for including and analyzing those species in some risk categories. For example, the threatened category in the Mexican Official Norm NOM-059-SEMARNAT-2010 is equivalent to the vulnerable category of the IUCN. Meanwhile, the special protection category of the NOM-059-SEMARNAT-2010 includes some minor categories of the IUCN [68]. Finally, we proposed other fern and lycophyte species as candidates based on their restricted distribution, low population density, and rareness. We complemented this information with those species included in the IUCN Red List [69] and CITES [70].

3. Results

3.1. Floristics

Based on herbarium specimens, web databases, specialized literature, and specimens collected during fieldwork, we obtained a final checklist that included 312 species from the SMOc belonging to 27 families and 75 genera (

Table 1. Families of ferns and lycophytes represented in the SMOc. We recorded the number of species and genera in each family, the species endemic to the SMOc, and the species included in the Mexican Official Norm NOM-059-SEMARNAT-2010 [67].

Families	Species	Genera	Endemic Species	NOM-059
Anemiaceae	11	1	3
Aspleniaceae	25	1	3
Athyriaceae	5	3
Blechnaceae	7	3
Cyatheaceae	1	1		Cyathea costaricensis
Cystopteridaceae	2	1
Dennstaedtiaceae	4	2
Dryopteridaceae	25	6
Equisetaceae	5	1
Gleicheniaceae	1	1
Hymenophyllaceae	2	2
Isoetaceae	3	1
Lycopodiaceae	3	2
Lygodiaceae	1	1
Marsileaceae	4	2
Nephrolepidaceae	1	1
Ophioglossaceae	8	4
Osmundaceae	1	1
Plagiogyriaceae	1	1
Polypodiaceae	31	6	Polypodium 1	Campyloneurum phyllitidis
Psilotaceae	2	1		Psilotum × complanatum P. nudum
Pteridaceae	118	23	Argyrochosma 1, Myriopteris 1, Notholaena 2
Salviniaceae	2	1
Selaginellaceae	30	1	1	Selaginella porphyrospora
Tectariaceae	2	1
Thelypteridaceae	10	6
Woodsiaceae	7	1	1
Total 27	312	75	13	4

, Appendix A). Of these species, 276 are ferns and 36 are lycophytes. The most diverse families (10 or more species) are Pteridaceae (118), Polypodiaceae (31), Selaginellaceae (30), Aspleniaceae (25), Dryopteridaceae (25), Anemiaceae (11), and Thelypteridaceae (10). The Pteridaceae is the richest family in the area. The numbers registered in our study show that Pteridaceae is around four times more genera and species-diverse than the next most diverse family (Table 1). The remaining pteridoflora families have nine or fewer species (Table 1). Six families are represented by only one species (Cyatheaceae, Gleicheniaceae, Lygodiaceae, Nephrolepidaceae, Osmundaceae, and Plagiogyriaceae).

Eleven genera have ten or more species (Figure 2). The three most diverse genera are Selaginella (30), Asplenium (25), and Myriopteris (22). The remaining genera inhabiting the SMOc have from nine to one species. From these, 32 genera are represented by only one species; some of them are common in other humid parts of Mexico (i.e., Ctenitis, Cyathea, Goniopteris, Hymenophyllum, Diplazium, Melpomene, Nephrolepis).

3.2. Taxonomic Biodiversity Index

The floristic richness calculated for the surface of the SMOc was 25 species per km². Notwithstanding that it is the largest mountain chain in Mexico (

Table 2. Taxonomic biodiversity index (TBI) of the study area compared with other areas and mountain chains of Mexico.

Study Area	Elevation Ranges	Area * (km2)	Number of Pteridophyte Species	TBI (S/InA)
SMOc (present study)	300–3500	251,648	312	25.17
SMOr [16]	200–3694	220,192	424	34.47
TMVB (Tejero-Díez pers. data)	300–5636	163,015	~415	34.58
SMS [4]	300–3700	±143,447	614	51.71
ST [18]	300–3284	±59,161	~550	50.05

Acronyms: SMOc: Sierra Madre Occidental; SMOr: Sierra Madre Oriental; TMVB: Trans-Mexican Volcanic Belt; SMS: Sierra Madre del Sur; ST: Serranías Transístmicas. * The area size follows the study’s authors; in those cases where the authors did not mention them, we obtained information from different sources (±). ~ Data calculated from the database of the first author or the cited authors.

), the richness of ferns and lycophytes is low in comparison to the other Mexican wet montane areas due to the absence of appropriate substrates and wide aridity. The other Mexican mountain chains have higher species numbers per km² because they house more humid temperate forests and proper phorophytes.

3.3. Threatened Species

Only four species that inhabit the SMOc are included in the Mexican Official Norm NOM-059-SEMARNAT-2010 [67]. Two of them in the threatened category: Campyloneurum phyllitides (L.) C. Presl, and Psilotum × complanatum Sw. Two are in danger of extinction: (Cyathea costaricensis (Mett. ex Kuhn) Domin and Selaginella porphyrospora A. Braun). There are 16 species included in the IUCN Red List in the less concern category (LC), and only Psilotum nudum is critically endangered (CR) (

Table 3. Conservation status of the fern and lycophyte species represented in the SMOc and their risk categories in the Mexican Official Norm NOM-059-SEMARNAT-2010, IUCN, and CITES.

Family	Species	NOM-059	IUCN	CITES
Aspleniaceae	Asplenium formosum		LC
Aspleniaceae	Asplenium monanthes		LC
Aspleniaceae	Asplenium trichomanes		LC
Cyatheaceae	Cyathea costaricensis	P		Appendix II
Dennstaedtiaceae	Pteridium latiusculum		LC
Equisetaceae	Equisetum hyemale		LC
Hymenophyllaceae	Hymenophyllum tunbrigense		LC
Lycopodiaceae	Palhinhaea cernua		LC
Nephrolepidaceae	Nephrolepis undulata		LC
Ophioglossaceae	Ophioglossum nudicaule		LC
Ophioglossaceae	Ophioglossum reticulatum		LC
Osmundaceae	Osmunda regalis		LC
Polypodiaceae	Campyloneurum phyllitidis	A
Psilotaceae	Psilotum × complanatum	A
Psilotaceae	Psilotum nudum		CR
Pteridaceae	Adiantum capillus-veneris		LC
Pteridaceae	Anogramma leptophylla		LC
Pteridaceae	Pteris cretica		LC
Salviniaceae	Azolla microphylla		LC
Selaginellaceae	Selaginella porphyrospora	P
Thelypteridaceae	Cyclosorus interruptus		LC
Total		4	17	1

Abbreviations for NOM-059-SEMARNAT-2010 categories: threatened (A) and in danger of extinction (P). IUCN Red List: Less concern category (LC) and critically endangered (CR).

). Only Cyathea costaricensis is included in CITES. Unfortunately, more species need to be analyzed to consider their inclusion in Mexican and international lists.

3.4. Pteridodiverse States of the SMOc

Durango contains the greatest number of species of ferns and lycophytes (166 species), followed by Chihuahua (149), Jalisco (146), Sonora (134), Sinaloa (131), and Nayarit (127). Aguascalientes and Zacatecas have fewer species (55 and 74, respectively) (Appendix A and Figure 3). Sonora includes more endemic species (7 species), followed by Durango, Nayarit, and Sinaloa (6 species). Restricted endemics are present in Chihuahua and Jalisco, with four species each. Some of them are shared between these two states.

3.5. Life Forms

Most species occurring in the SMOc are epipetric (183 species) and terrestrial (168), followed by epiphytes (39) and aquatics (22); there was only one tree fern and a climbing fern (Appendix A). The arborescent habit is represented by Cyatheaceae (Cyathea), and the single climbing species belongs to Lygodiaceae (Lygodium). The epipetric species were recorded mainly in Aspleniaceae (Asplenium), Pteridaceae (in almost all genera), Woodsiaceae (Woodsia), and Selaginellaceae (Selaginella). The epiphytic species belong mainly to Polypodiaceae (in almost all genera). Finally, aquatic plants were found mainly in the families Isoetaceae (Isoetes), Marsileaceae (Marsilea and Pilularia), and Salviniaceae (Azolla) (Appendix A). The annual life form is rare among ferns. However, we found three species with this life form: Anogramma leptophylla (L.) Link, Gastoniella novogaliciana (Mickel) Li Bing Zhang andLiang Zhang, and Selaginella porphyrospora.

3.6. Elevation

Ferns and lycophytes are distributed all over the elevation interval of the SMOc (300 to 3200 m asl). As usually occurs in tropical mountains, the highest diversity in the SMOc was observed at mid-elevations. The highest species concentration occurred between 1500 to 2000 m (236 species) (Figure 4). This diversity decreased toward both high and low elevations.

3.7. Vegetation Types Distribution

The Quercus and mixed Pinus–Quercus forests stand out for their pteridoflora richness (52% of the species) and cover the largest surface of the SMOc (110,882 km²) [30]. Atmospheric humidity is high in these areas; oak species are well represented and are excellent phorophytes and soil formers [71,72]. On the other hand, conifer forests (including pine forests) contain at least 32% of the pteridophytes and cover a surface of 30,841 km² [30]. In comparison, the tropical deciduous and semideciduous forests occupy less surface and cover 17,827 km² and 3950 km², respectively [30], and contain 35% of the species. The remaining plant communities contain less than 70 species (Appendix A).

3.8. Geographic Distribution

Concerning the geographic distribution of ferns and lycophytes that inhabit the SMOc, the Neotropical and Mesoamerican components are the best represented, with 65 species each. They are followed by the endemic to Mexico component, with 61 species (Figure 5). In northwestern Mexico, our data support that the Nearctic component is more significant than in other parts of the country, being represented by 50 species. Furthermore, the high proportion of Mesoamerican and Neotropical components in the SMOc contributes to enhancing the significance of this montane area in America (Appendix A). The other geographic components have less than 35 species each.

We recorded 13 species that are endemic to the SMOc: Anemia affinis Hook. and Baker, Anemia brandegeei Davenp., Anemia intermedia Copel. ex M.E. Jones, Argyrochosma lumholtzii (Maxon andWeath.) Windham, Asplenium arcanum A. R. Sm., Asplenium modestum Maxon, Asplenium tryonii Correll, Myriopteris yatskievychiana (Mickel) Grusz andWindham, Notholaena aurantiaca D.C. Eaton, Notholaena jaliscana Yatsk. andArbeláez, Polypodium praetermissum Mickel andTejero, Selaginella macrathera Weath., and Woodsia cystopteroides Windham andMickel (Table 1). At least eight other species are closely linked to the SMOc distribution and adjacent regions (Appendix A).

4. Discussion

Our study updated the number of ferns and lycophytes in the SMOc. The recognition of 312 species in the pteridoflora of the SMOc contributes to the knowledge of these groups. Therefore, we can say that this Mexican orographic system has an extraordinary taxonomic biodiversity of ferns and lycophytes, which reflects the current pteridoflora diversity in the driest Mexican mountain chain. Our results represent an increment of 50 species of pteridoflora (18%) compared to the 262 species previously estimated [4]. Recent studies considered 1043 species of ferns and lycophytes occurring in Mexico [4,5]. Therefore, the new number of species reported here in the SMOc represents 31% of the diversity recorded for the country.

The SMOc represents an exciting area harboring one of the world’s most extensive subtropical conifer forests [30,31,32]. Morrone [32] recently suggested that the SMOc is closely related to areas from the Nearctic biogeographical realm, where some fern and lycophyte families and genera are poorly represented. In the SMOc, the tropical humid fern families, such as Cyatheaceae (one species) and Hymenophyllaceae (two species), are underrepresented compared with other Mexican chains located in eastern and southern Mexico, as in the case of the Sierra Madre del Sur, which contains a solid Neotropical component, where the two families mentioned above have 13 and 31 species, respectively [4]. Among the mountainous areas of Mexico, the SMOc has the most significant North American biological influence [73] with regard to fern and lycopod diversity.

The best-represented families in species number are Pteridaceae (118), Polypodiaceae (31), Selaginellaceae (30), Aspleniaceae (25), and Dryopteridaceae (25). Cheilanthoid ferns mainly represent Pteridaceae (Argyrochosma, Astrolepis, Gaga, Myriopteris, Notholaena, Pellaea) and are distributed predominantly on the eastern slope facing the Mexican Plateau, which has xerophytic and seasonal temperate vegetation types.

Selaginella is the most diverse in the SMOc. This genus is included in a monotypic family and represents the largest one, with 700 to 800 species worldwide that inhabit an impressive range of habitats, including rocky deserts and xeric scrublands [74]. Among the species adapted to xeric habitats, Selaginella lepidophylla and other species are commonly named resurrection plants due to their ability to survive extreme and long-term droughts [75]. In the SMOc, Selaginella species are mainly distributed on the eastern slope facing the Mexican Plateau with xerophytic vegetation.

On the other hand, the western slopes of the SMOc have more Nearctic affinity [31] except on the lower zones [30]. In this last area, the Dryopteridaceae, Aspleniaceae, and the non-cheilanthoid genera of Pteridaceae (e.g., Adiantum, Pteris, and Pityrogramma) are well-represented. Finally, Polypodiaceae and Dryopteraceae (Elaphoglossum) are represented by temperate genera and species, mainly in the medium and high montane areas [60]. A Mediterranean or monsoon climate [36,37] allows for the coexistence of several taxonomic groups. Our study supports that the SMOc is a diversity center for Argyrochosma (Pteridaceae). Fourteen species of this genus occur in Mexico and the southwestern United States, which is considered mainly an American genus of about 20 species, with 5 in South America and 1 in China [51], and we recorded eleven species in the SMOc. Apparently, the SMOc represents a diversification center for Argyrochosma, as suggested for other fern and lycophyte genera linked to the Andean region. In this last case, the mountain chain has played a crucial role in the diversification of Phlegmariurus [26] and Polystichum [76].

Pteridaceae is the most diverse family of ferns in the SMOc. The genera and species number included in Pteridaceae are around four times more diverse than the next most diverse family. This family has a cosmopolitan distribution concentrated in wet tropical and arid regions. It differs notably from other fern families by encompassing xeric-adapted species [77]. Among these, cheilanthoids represent uncommon ferns that do not live in the temperate or tropical, moist, shaded habitats of “typical” ferns, because most species grow in exposed rocky habitats with an extended annual dry period [78]. The cheilanthoid ferns comprise several separate lineages distributed in the SMOc, such as Argyrochosma, Bommeria, Cheilanthes, Gaga, Hemionitis, Myriopteris, Notholaena, and Pellaea, which occupy the diverse xeric niches of this mountain chain. This richness of Pteridaceae contrast with the low diversity of other families with a higher diversity in rainfall regions.

Some groups of ferns and lycophytes are poorly represented in the SMOc in comparison with other Mexican mountain chains, such as the Sierra Madre del Sur [4] and the Sierra Madre Oriental [15,16]. This is because many families and genera of the tropical and subtropical groups reach their northern distributional limit before reaching the SMOC, e.g., Cyatheaceae. Other families decrease their species richness towards the north, e.g., Anemiaceae, Gleicheniaceae, and Hymenophyllaceae, with few species recorded in the flora of North America [79].

Tropical and subtropical mountains harbor unequal biodiversity, and ferns and lycophytes are no exception [3]. The southern portion of the SMOc has recently been included in the Mesoamerican hotspot of fern diversity proposed by Suissa et al. [3]. In this sense, a significant decrement in species richness has been detected, from southwest to northeast, in other biological groups of the SMOc [31]. Notwithstanding, this mountain chain is recognized as one of the main biodiversity areas in the country [30,32].

Ferns and lycophytes go along with biological and geographical characteristics, and some species are used as environmental indicators [80]. For example, it is necessary to consider endemic species that inhabit seasonal subhumid conditions. In addition, some locations have been used to feed cattle [81,82], which reduces the fern populations. Therefore, this aspect is an essential characteristic to be considered in Mexican and international risk lists.

We found at least 13 species of ferns that are endemic to the SMOc. Some of these species (e.g., Anemia brandegeei, Anemia intermedia, Asplenium modestum, Asplenium tryonii, Argyrochosma lumholtzii, Myriopteris yatskievychiana, Notholaena jaliscana) meet the criteria (restricted distribution, low-density populations, and habitat sensitive to reduction by the human impact) to be included in the Mexican Official Norm NOM-059-SEMARNAT-2010 [67] and the IUCN [69]. In our study, we are proposing these species as candidates to be included in the NOM-059-SEMARNAT-2010.

Some other species, which were rare in the study area but widespread in other Mexican localities, must be considered candidates to be included in the Mexican Official Norm NOM-059-SEMARNAT-2010 [67] or at least to be treated differently. This is the case for Phlegmariurus (Lycopodiaceae), which in Mexico is represented by 13 species, two of which occur in the SMOc (P. cuernavacensis and P. taxifolius). Phlegmariurus species are distributed in undisturbed areas of mature pine-oak and humid montane forests. Because of this, the populations of Phlegmariurus are highly susceptible to disturbance and were represented by few individuals in each site.

Unfortunately, deforestation and land-use change have reduced the pine-oak and humid montane forests due to agriculture and animal husbandry. Furthermore, these plants are rare or absent in cleared areas because they are vascular epiphytes of mature host canopy trees [83]. This information allows us to conclude that both species of Phlegmariurus may be considered threatened or endangered, as is the case in other areas of Mexico [83]. Therefore, more species must be included in the Mexican Official Norm NOM-059-SEMARNAT-2010 [67] due to their restricted distribution, rarity, and continuous loss and fragmentation of humid montane forests.

The SMOc includes another group of species endemic to Mexico that are rare throughout the country, like those represented in a few localities and collections (e.g., Argyrochosma palmeri (Baker) Windham, Asplenium pringlei Davenp., A. sanchezii A. R. Sm., Gaga pellaeopsis (Mickel) Fay-Wei Li and Windham, Gastoniella novogaliciana, Pleopeltis rzedowskiana (Mickel) A.R. Sm. and Tejero, and Selaginella schaffneri Hieron.). On the other hand, Botrychium tolucaense W. H. Wagner and Mickel, Argyrochosma pilifera (R.M. Tryon) Windham, Selaginella macrathera, and Selaginella carnerosana T. Reeves are only known from type or a few herbaria specimens. These species were collected more than 30 years ago and could be considered extinct.

The proportion of restricted endemics supports the proposals of Tryon [21,22] and Mickel and Smith [9], in the sense that northwestern Mexico (including the southwestern United States) are considered an endemism center for this group of plants, essentially for those inhabiting the seasonal montane forests and semi-arid vegetation types (regions that, in turn, are recognized as highly endemic for flowering plants by Rzedowski [23,24]). On the other hand, the tropical mountains are highly diverse in the elevation interval from 1000–2500 m; despite this, a peak of endemism is located at higher elevations [1].

The Mexican ferns and lycophytes are underrepresented in the Red Lists, where only 3% of them are listed. A good example is the comparison of the pteridoflora of Mexico and Bolivia, with similar sizes (1191 species in Bolivia [2]). In the case of Bolivia, nearly 11% of species are registered in some risk category [84].

The SMOc and other Mexican mountain chains constitute the Mexican Mountain Component [32], which was recently recognized as one of the main fern hotspots and globally named the “Mesoamerican hotspot” [3] and has a higher richness than the neighboring non-hotspot regions. A similar situation occurs in northwestern Mexico at a regional level, because the SMOc holds a higher richness of fern and lycophyte species than the neighboring biogeographic provinces, such as the Chihuahuan Desert and Pacific lowland provinces (see Morrone [32]).

In the SMOc, ferns and lycophytes are mainly concentrated between 1500 to 2000 m asl where mild weather occurs. The same elevation interval was recognized by Hernández-Rojas et al. [85] along eight study transects across Mexico. Similar results have been reported in other countries and areas of the Neotropical region, such as the Andes [63], Costa Rica [1], Colombia [65], Bolivia [85], and Argentina [86]. These studies support that fern and lycophyte diversity show a well-defined, hump-shaped richness pattern on high tropical mountains, with the highest diversity between 1500 to 2000 m and decreasing toward high and low elevations [1,63,87]. The same phenomenon occurs in the central part of the Himalayas in Nepal [88]. Such mid-elevation peaks in fern richness have also been found in other regions, such as Borneo, Costa Rica, and Bolivia, by Kessler [1].

The most extraordinary diversity of ferns and lycophytes is linked to atmospheric humidity, which, in tropical mountains, is concentrated at mid-elevations, where cloud or temperate forest develops [1,85]. The low reactivity of foliar stomata partly explains why the richness of lycophytes and ferns is replaced by seed plants in drier environments [89], and, on the contrary, in humid forests, these groups are better represented [23,90,91,92]. Therefore, it is not a coincidence that the best representativeness of the richness of ferns and lycopods coincides with the mid-mountain area (1500 to 2000 m asl) of the oceanic slope, where semi-warm and temperate climates prosper, and mixed forests develop, mainly those of Quercus and Pinus-Quercus. The facts mentioned above are common in other areas of the Neotropics, in which the richness of pteridophytes reaches a maximum [87]. This also can be explained by the heterogeneity and contrasted elevational levels in mountains that practically constitute the most extended biological corridor parallel to the sea, which is the longest on the planet [93].

The lycophytes and ferns of the SMOc occupy specific and specialized niches. Most species are epipetric, and the understory forest is very poor in species. This fact is caused because the conifer and mixed pine-oak forests, which account for ca. 42.5% of the extension of the SMOc, develop from mid to high elevations, from 1300 to 3300 m asl [30]. Furthermore, the accumulation of needles on the understory inhibits the growth of other species, especially ferns, because the dense leaf litter affects gametophyte growing on the ground [94]. In addition, soils are acidic, and the presence of terpenes promotes recurrent fires; also, the decayed bark of the trees rejects epiphytes [95,96]. Therefore, the high richness of lycophytes and ferns in the temperate zone of the SMOc is due to a large number of rocky microenvironments, such as protected escarpments and, in several cases, in the ravines, where the conifer forest acquires a riparian nature, as is the case for the forests of Cupressus, Pseudotsuga, and Abies.

The SMOc hosts 24 pine species, 54 oaks, 7 Arbutus species, and other tree species [39]. These amounts are high, considering that the greatest diversity of pines, Arbutus, and oak trees are located in Mexico. However, despite its environmental, economic, and scientific importance, the SMOc is still one of Mexico’s most biologically and ecologically poorly known regions, where different communities need to be deeply analyzed.

The epiphytic ferns (39 species, 8%) are poorly represented in the SMOc, in comparison with other Mexican areas, such as the Sierra Madre del Sur (183 species, 30%) [4]. The SMOc has a xeric character where the main phorophytes are different species of oaks; however, in contrast to other Mexican mountain ranges, the highest concentration of ferns and lycophytes occurs in ravines on northern slopes, growing mainly at the base of the trunks, sometimes on the lower sub-horizontal branches. Ferns and lycophytes are more diverse in wet and mild habitats, which are conditions that occur on the Atlantic slope of Mexico. In the Pacific slope, where the SMOc is located, these plants are affected by stressful climatic factors [85].

The SMOc was considered by Villers-Ruiz and Trejo-Vázquez [97] among the temperate forest areas more sensitive to climatic and land-use changes. Unfortunately, deforestation and land-use change have reduced the temperate forests due mainly to agriculture and animal husbandry. The coniferous and oak forests are the more affected vegetation types [98,99]. As a result, the SMOc experienced a significant loss of temperate forest cover during 1986–2012 (about 34%), with an annual forest area loss rate of 1.3%, an amount considered intermediate relative to other parts of Mexico [100]. Notwithstanding, this human impact limits the existence of fern and lycophyte species and has an influence on habitat distribution [88].

Among Mexico’s mountainous areas, the SMOc has the most considerable Nearctic influence [73]. Even though the pteridoflora component is not above average diversity compared to other Mexican mountain ranges, the existence of a large proportion of Nearctic elements in the SMOc is greater than in other Mexican mountains. The SMOc ferns present a mixture of Neotropical and Nearctic affinities, unlike the other mountain ranges with a more significant influence of Neotropical elements. This Sierra lacks the typical association of Neotropical ferns due to its low humidity levels. Deep knowledge and conservation of the biological diversity and ecosystems of the SMOc are urgent for various reasons. This synthesis aims to contribute to the biological studies carried out in this mountain chain and to add to the detailed knowledge of the biological diversity of the SMOc.

Tropical mountains are the global centers of fern and lycophyte diversity [1,3]. Among these areas, the Mexican mountain chains, including the SMOc, were recently considered as part of one of the main hotspots recognized worldwide by Suissa et al. [3] for ferns. The Mesoamerican hotspot constitutes a biologically complex area [101] and contains an exceptional species richness of ferns and lycophytes, where the SMOc contributes to this biodiversity.