Patterns of Richness and Endemism in the Gypsicolous Flora of Mexico

Abstract

Gypsum soils occur around the world, mainly in arid regions. These harsh environments promote unusual flora with high degrees of endemism. Mexico has extensive gypsum outcrops, but their flora has been poorly studied. However, the highest species richness and endemism are expected to be concentrated in Mexico’s northern dry regions. To promote the study of this flora and its conservation, we estimate how well sampled it is, quantify species richness, identify centers of endemism, and detect which gypsum outcrops lie within federal protected natural areas (PNA). We conducted exhaustive literature and herbaria reviews to generate a database of botanical records on gypsum soils. The total species and gypsophyte richness were calculated using cell grids. Centers of endemism were identified using the corrected weighted endemism index (CWE). We mapped the gypsum outcrops within PNA polygons. The most collected sites are Cuatro Ciénegas (Coahuila) and Santo Domingo Tonalá (Oaxaca), which also had the highest total species richness. Nevertheless, gypsophyte richness was higher in Cuatro Ciénegas and Nuevo León. The CWE identified seven gypsophyte centers of endemism. Mexico hosts the most diverse gypsophile flora in the world, despite having been only partially studied and collected. The regions with the highest species richness and endemism are unprotected.

Full text

Citation: Ortiz-Brunel, J.P.;
Ochoterena, H.; Moore, M.J.;
Aragón-Parada, J.; Flores, J.;
Munguía-Lino, G.; Rodríguez, A.;
Salinas-Rodríguez, M.M.;
Flores-Olvera, H. Patterns of
Richness and Endemism in the
Gypsicolous Flora of Mexico.
Diversity 2023,15, 522. https://
doi.org/10.3390/d15040522
Academic Editor: Julio Peñas de
Giles
Received: 1 March 2023
Revised: 13 March 2023
Accepted: 23 March 2023
Published: 4 April 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
diversity
Article
Patterns of Richness and Endemism in the Gypsicolous Flora
of Mexico
Juan Pablo Ortiz-Brunel 1, Helga Ochoterena 2, Michael J. Moore 3, Juvenal Aragón-Parada 1, Joel Flores 4,
Guadalupe Munguía-Lino 5, Aarón Rodríguez 1, María Magdalena Salinas-Rodríguez 6
and Hilda Flores-Olvera 2, *
1Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias,
Universidad de Guadalajara, Zapopan 45200, Mexico; jpablo.ortiz@alumnos.udg.mx (J.P.O.-B.);
juvenal.aparada@alumnos.udg.mx (J.A.-P.); aaron.rodriguez@academicos.udg.mx (A.R.)
2Departamento de Botánica, Instituto de Biología, Circuito Exterior s.n., Ciudad Universitaria,
Ciudad de México 04510, Mexico; helga@ib.unam.mx
3Department of Biology, Oberlin College, Oberlin, OH 44074, USA; mmoore@oberlin.edu
4IPICYT/División de Ciencias Ambientales, San Luis Potosí78216, Mexico; joel@ipicyt.edu.mx
5Cátedras CONACyT-Universidad de Guadalajara, Centro Universitario de Ciencias Biológicas y
Agropecuarias, Universidad de Guadalajara, Zapopan 45132, Mexico;
guadalupe.munguia95@academicos.udg.mx
6
Herbario Jorge Marroquín, Facultad de Ciencia Biológicas, Universidad Autónoma de Nuevo León, Avenida
Pedro de Alva, s/n, San Nicolas de los Garza 66451, Mexico; mane.salinasrdr@uanl.edu.mx
*Correspondence: mahilda@ib.unam.mx
Abstract:
Gypsum soils occur around the world, mainly in arid regions. These harsh environments
promote unusual flora with high degrees of endemism. Mexico has extensive gypsum outcrops,
but their flora has been poorly studied. However, the highest species richness and endemism are
expected to be concentrated in Mexico’s northern dry regions. To promote the study of this flora and
its conservation, we estimate how well sampled it is, quantify species richness, identify centers of
endemism, and detect which gypsum outcrops lie within federal protected natural areas (PNA). We
conducted exhaustive literature and herbaria reviews to generate a database of botanical records on
gypsum soils. The total species and gypsophyte richness were calculated using cell grids. Centers of
endemism were identified using the corrected weighted endemism index (CWE). We mapped the
gypsum outcrops within PNA polygons. The most collected sites are Cuatro Ciénegas (Coahuila)
and Santo Domingo Tonalá(Oaxaca), which also had the highest total species richness. Nevertheless,
gypsophyte richness was higher in Cuatro Ciénegas and Nuevo León. The CWE identified seven
gypsophyte centers of endemism. Mexico hosts the most diverse gypsophile flora in the world,
despite having been only partially studied and collected. The regions with the highest species
richness and endemism are unprotected.
Keywords:
biodiversity; Cuatro Ciénegas; edaphic endemism; gypsophile; gypsophyte;
gypsum; plants
1. Introduction
Gypsum soils occur worldwide. They are especially common in arid or semiarid
regions, although they occur as small outcrops in wetter areas [
1
–
4
]. These soils are com-
posed mainly of sedimentary deposits resulting from ancient high salinity environments [
3
].
In North America, most gypsum deposits formed in the Paleozoic or Mesozoic eras and
were later exposed by Cenozoic uplift and erosion [
5
]. Due to its high solubility, gypsum
mixes easily with adjacent soils [
6
]. Desert climatic conditions allow the conservation
of gypsum horizons because the low precipitation slows their erosion and intermixing
with different soils and greatly reduces the accumulation of organic matter [
7
]. The phys-
ical characteristics of gypsum soils (gypsisols) vary depending on their origin and the
Diversity 2023,15, 522. https://doi.org/10.3390/d15040522 https://www.mdpi.com/journal/diversity

Diversity 2023,15, 522 2 of 17
local climate [
3
]. Gypsum can be present as anhydrite, crystalline selenite, evaporite
bedrock, secondary evaporites, or even sand dunes [
6
]. In Mexico, gypsum is generally
found as alluvial deposits, crusts, crystals, rocks, and sand dunes in bedrocks, cliffs, hills,
and plains [6,8].
Mexico has multiple gypsisol areas distributed throughout the country. Accord-
ing to the Servicio Geológico Mexicano [
9
], gypsum soils occur in Baja California, Baja
California Sur, Campeche, Chihuahua, Coahuila, Colima, Durango, Guerrero, Hidalgo,
Jalisco, Michoacán, Morelos, Nuevo León, Oaxaca, Puebla, San Luis Potosí, Sinaloa, Sonora,
Tamaulipas, and Zacatecas states. The highest concentration occurs in the north and north-
eastern part of the country in the states of Chihuahua, Coahuila, Nuevo León, and San Luis
Potosí[
4
,
10
,
11
]. These zones correspond mainly to the Chihuahuan Desert (CHIH) and
the Sierra Madre Oriental (SMOr) biogeographic provinces (following Morrone et al. [
12
]).
Gypsisols are widespread over these provinces, but the size of individual gypsum expo-
sures ranges from several square kilometers to a few square meters [
8
,
13
]. Consequently,
soil maps from Mexico do not have the necessary scale to depict all the outcrops present in
the country. In Baja California and Baja California Sur, the records of gypsum are scarce [
14
].
Additionally, gypsum soils are reported in areas in biogeographic provinces with tropical
affinity in the Pacific Lowlands (PL), the Balsas Basin (BB), and the Yucatán Peninsula.
These outcrops are found in the states of Campeche [
15
], Colima [
16
,
17
], Guerrero [
18
],
Jalisco [19], Oaxaca [20,21], and Puebla [22].
Plants that live on gypsum are often called gypsicolous plants. Many of these have de-
veloped physical and physiological traits that promote their survival, so much so that many
of them are found only in this type of soil. Some examples are seeds with a mucilaginous
coat, tolerance to high (e.g., S and Ca) and/or low (e.g., P) nutrient levels, and strong roots
that break through soil crusts [
7
,
23
,
24
]. The species that inhabit gypsum are mostly herbs,
shrubs, and rarely trees [
25
]. Gypsicolous plants are often grouped by their frequency
of occurrence on gypsum. Following Mota et al. [
26
], plants found only on gypsum are
gypsophytes, plants that occur mostly on gypsum are gypsoclines, and those that grow
on and off gypsum are called gypsovags. The proportion of these three types of plants
in a gypsum community has been found to depend on the gypsum concentration in the
soil and the climatic conditions [
3
,
27
]. Additionally, high concentrations of foliar sulfur
and magnesium have been shown to play an important role in the adaptation of plants to
gypsum [
28
]. Globally, the diversity of physical characteristics of the gypsum, together
with the different reliefs and climates, promotes the development of many types of vege-
tation in gypsum [
29
]. In Mexico, gypsum is reported in xerophilous scrubland [
6
,
21
,
30
],
grasslands [
31
–
33
], dune vegetation [
34
], tropical deciduous forests [
16
,
17
,
35
], and oak and
pine forests [10,22,36,37] (Figure 1).
Most gypsum communities studied in Mexico are located within the CHIH [
5
,
8
,
13
,
34
,
38
]
and the SMOr [
37
,
39
–
41
]. Unfortunately, most gypsum outcrops in Mexico are either poorly
explored botanically or even unexplored, especially those in the western and southern
portions of the country. Floristic studies on gypsophytes in Mexico have focused on a few
taxonomic groups, such as pteridophytes [
42
], gymnosperms [
36
], Amaranthaceae [
43
],
and Euphorbiaceae [
22
]. Alternatively, a few studies have focused on distinct areas, such
as the Cuatro Ciénegas basin [
44
]. Recently, the exploration and study of some areas of
these interesting communities in Oaxaca have resulted in outstanding novelties such as
the genus Mixtecalia Redonda-Mart., García-Mend. and D. Sandoval (Asteraceae) [
21
],
and several new species within the genera Agave L. (Asparagaceae), Bletia Ruiz and Pav.
(Orchidaceae), Cephalocereus Pfeiff. (Cactaceae), Hechtia Klotzsch (Bromeliaceae), and
Pinguicula L. (Lentibulariaceae) [35,45–49].

Diversity 2023,15, 522 3 of 17
Diversity 2023, 15, x FOR PEER REVIEW 3 of 18
Figure 1. Vegetation types in gypsum soils of Mexico: (a) xerophilous scrubland in San Juan Teita,
Oaxaca, (b) xerophilous scrubland in Aramberri, Nuevo León, (c) palmetto woodland in Galeana,
Nuevo León, (d) coniferous forest in Galeana, Nuevo León, (e) dune vegetation in Cuatro Cienégas,
Coahuila, (f) grassland in Vanegas, San Luis Potosí, (g) tropical deciduous forest in Santiago Jux-
tlahuaca, Oaxaca, (h) grassland and tropical deciduous forest in Tolimán, Jalisco, and (i) tropical
deciduous forest in Tecomán, Colima. Photographs: (a) Juvenal Aragón, (b–i) J. P. Ortiz-Brunel.
Most gypsum communities studied in Mexico are located within the CHIH
[5,8,13,34,38] and the SMOr [37,39–41]. Unfortunately, most gypsum outcrops in Mexico
are either poorly explored botanically or even unexplored, especially those in the western
and southern portions of the country. Floristic studies on gypsophytes in Mexico have
focused on a few taxonomic groups, such as pteridophytes [42], gymnosperms [36], Am-
aranthaceae [43], and Euphorbiaceae [22]. Alternatively, a few studies have focused on
distinct areas, such as the Cuatro Ciénegas basin [44]. Recently, the exploration and study
of some areas of these interesting communities in Oaxaca have resulted in outstanding
novelties such as the genus Mixtecalia Redonda-Mart., García-Mend. and D. Sandoval
(Asteraceae) [21], and several new species within the genera Agave L. (Asparagaceae),
Bletia Ruiz and Pav. (Orchidaceae), Cephalocereus Pfeiff. (Cactaceae), Hechtia Klotzsch (Bro-
meliaceae), and Pinguicula L. (Lentibulariaceae) [35,45–49].
Despite the works mentioned above, a great proportion of the gypsicolous flora of
Mexico remains unrecorded. Moore et al. [6] estimated at least 200 gypsophyte species in
the CHIH, including its portions in USA and Mexico. However, this number includes only
gypsophytes and lacks gypsocline and gypsovag species. Furthermore, the number of
these three kinds of gypsicolous plants throughout Mexico is unknown. Generally, gyp-
sisol areas host an elevated number of endemic taxa [3,7]. In Mexico, Sosa and De-Nova
[50] identified two hotspots of angiosperm endemism that in part comprise gypsum soils:
the Northeastern rosette scrub and the Gypsum grasslands. Additionally, Salinas-
Rodríguez et al. [51] identified one hotspot for the endemic vascular plants of the SMOr
that includes the gypsum outcrops from Nuevo León and Tamaulipas states. Given this,
it is expected that northern Mexico has the widest extent of gypsum soils and the highest
Figure 1.
Vegetation types in gypsum soils of Mexico: (
a
) xerophilous scrubland in San Juan Teita,
Oaxaca, (
b
) xerophilous scrubland in Aramberri, Nuevo León, (
c
) palmetto woodland in Galeana,
Nuevo León, (
d
) coniferous forest in Galeana, Nuevo León, (
e
) dune vegetation in Cuatro Cienégas,
Coahuila, (
f
) grassland in Vanegas, San Luis Potosí, (
g
) tropical deciduous forest in Santiago Juxt-
lahuaca, Oaxaca, (
h
) grassland and tropical deciduous forest in Tolimán, Jalisco, and (
i
) tropical
deciduous forest in Tecomán, Colima. Photographs: (a) Juvenal Aragón, (b–i) J. P. Ortiz-Brunel.
Despite the works mentioned above, a great proportion of the gypsicolous flora of
Mexico remains unrecorded. Moore et al. [
6
] estimated at least 200 gypsophyte species
in the CHIH, including its portions in USA and Mexico. However, this number includes
only gypsophytes and lacks gypsocline and gypsovag species. Furthermore, the number of
these three kinds of gypsicolous plants throughout Mexico is unknown. Generally, gypsisol
areas host an elevated number of endemic taxa [
3
,
7
]. In Mexico, Sosa and De-Nova [
50
]
identified two hotspots of angiosperm endemism that in part comprise gypsum soils: the
Northeastern rosette scrub and the Gypsum grasslands. Additionally, Salinas-Rodríguez
et al. [
51
] identified one hotspot for the endemic vascular plants of the SMOr that includes
the gypsum outcrops from Nuevo León and Tamaulipas states. Given this, it is expected
that northern Mexico has the widest extent of gypsum soils and the highest species richness
and endemism of gypsophytes in the country. Meanwhile, tropical gypsum outcrops
from central and southern Mexico should also be expected to host a high species richness
because angiosperm richness is higher in tropical and subtropical regions [
52
]. However, it
is necessary to explicitly test these patterns with occurrence data.
To promote additional research and conservation of these ecologically and evolu-
tionarily important but generally underappreciated habitats, this study provides the first
comprehensive overview of the general state of knowledge of the gypsicolous flora in
Mexico. For the first time, we identify and map the botanical records that explicitly refer to
gypsum in Mexico. We also determine how well botanically sampled these sites are and
estimate the spatial distribution of vascular plant species richness and centers of endemism

Diversity 2023,15, 522 4 of 17
within them. We also assess which of these gypsum areas fall within the Protected Natural
Areas (PNAs) of Mexico to detect which are currently under federal protection.
2. Materials and Methods
2.1. Botanical Records on Mexican Gypsum Soils
We conducted an exhaustive literature review of ecological and floristic studies, mono-
graphs, revisions, and species descriptions involving gypsophytes. Then, we searched
for the records that included any of the following words: gipsícola, gipsófila, gypseous,
gypsicolous, gypsophile, gypsophyte, gypsum, yeso, and yesoso. This allowed us to iden-
tify many gypsum areas that have botanical records in Mexico, facilitating the review of
records in herbaria and electronic databases. Later, we reviewed herbarium records from
ANSM, GBH, IBUG, MEXU, OAX, SERO, SLPM, TEX/LL, and ZEA (acronyms according
to Thiers [
53
]) that included any of the words mentioned for the literature review. Addition-
ally, we added records from the Global Biodiversity Information Facility (GBIF [
54
]) and
IBdata [
55
], following the same search methodology and for which the species determina-
tion was verifiable. All the species with herbarium vouchers explicitly mentioning gypsum
were included in a database and, when necessary, the localities were carefully georefer-
enced using Google Earth Pro 4.2. We identified the states and municipalities of Mexico to
which these areas corresponded. Consequently, we aggregated records from works that
explicitly used herbarium voucher references, such as the endemic vascular plants of the
Sierra Madre Oriental [
56
], selected angiosperm groups in Mexico [
57
], the Cuatro Ciénegas
Basin [
44
], and the endemic vascular plants of the Sierra Madre del Sur [
58
]. Gypsum is
often localized in small outcrops; therefore, we excluded doubtful localities. Additionally,
the records that mentioned growing on gypsum but without a herbarium voucher were
not included. Several herbarium specimens were personally identified when there was
conflicting identification among duplicates. To avoid bias due to different classification
systems, all the species names were standardized with the Missouri Botanical Garden’s
Tropicos database using the Taxonomic Name Resolution Service [
59
]. Other taxonomical
updates for higher taxonomic ranks followed APG IV [60] for angiosperms, Christenhusz
et al. [61] for gymnosperms, and Christenhusz et al. [62] for pteridophytes.
From the final database, duplicated and doubtful entries were deleted using collector
numbers and data filtering. All remaining records were converted into points and processed
in QGIS version 2.14.3 (QGIS Development [
63
]). We generated a map with these points
to identify the botanical records that explicitly refer to gypsum across Mexico and their
biogeographic affinity following Morrone et al. [
12
]. We then incorporated the localities
reported by the Servicio Geológico Mexicano (SGM [
9
]) to identify the presence of gypsum
for which we were unable to find herbarium records. To estimate the intensity of botanical
collections, we used the observation richness tool in DIVA-GIS 4.2 [
64
]. The cell size
was the same as that in the species richness analyses. We are aware that the use of this
approach overstates the extent of some gypsum sites. However, the purpose of this map
was only to estimate the sampling status of the potential gypsicolous flora throughout
Mexico according to herbarium vouchers and the literature.
2.2. Species Richness
The distinction between gypsovag, gypsocline, and gypsophyte is often overlooked
in herbarium labels and databases; thus, we used the literature and locality comparisons
to assign these categories in our database. Most species facultatively growing on gypsum
in Mexico lack detailed ecological information; thus, we avoided the use of the term
gypsocline. For each species, we searched all available records in digital and herbarium
collections and the literature. The species that included more than two records in localities
without gypsum were considered as gypsovags.
The spatial distribution of species richness was estimated by two approaches. We
used both gypsophytes and gypsovags in one analysis and only gypsophytes in the other.
This allowed us to identify the total species richness patterns on gypsum soils as whole

Diversity 2023,15, 522 5 of 17
plant communities and to detect where the greatest number of gypsophytes grow all
together. We performed a richness analysis by cell grid in DIVA-GIS 4.2 with a cell size of
0.18
◦×
0.18
◦
. The cell size was obtained using the Maximum Distances method established
in Willis et al. [
65
] and modified by Suárez-Mota and Villaseñor [
66
]. Even though some
gypsum outcrops are considerably smaller than the cell size used, we chose this method
because it is a good strategy to analyze the spatial distribution of species richness and
allowed us to compare our results with other patterns of plant species richness across
the country. The results from these analyses were visualized in QGIS. Finally, to test if
the species richness depended on the number of observations, we applied a regression
analysis between the grid results of the total species richness and those of the number of
observations in DIVA-GIS.
2.3. Endemism
Analyzing centers of endemism is useful to identify areas for conservation [
67
].
Weighted endemism (WE) evaluates a cell based on the endemism level of all the species
present within it. Meanwhile, the corrected weighted endemism (CWE) index adjusts the
WE value of a cell as a function of its species richness [
68
,
69
]. The endemism analysis
was only performed with gypsophytes because if a species is considered a gypsovag, it is
assumed to have a wider distribution area, and our database does not include its complete
distribution. Since the gypsophyte richness analysis shows the cells with the highest num-
ber of gypsophytes growing together, we only used WE to calculate the CWE index. This
allowed us to recognize those cells with few, but very restricted, gypsophyte species. Both
parameters were estimated in the program Biodiverse [
70
] using the same cell size as in the
richness analyses.
2.4. Conservation Status of the Mexican Gypsicolous Flora
We used the QGIS geoprocessing tools to overlay our recorded gypsum areas with
the current polygons of the Protected Natural Areas (PNAs) of Mexico as stated by the
“Comisión Nacional de Áreas Naturales Protegidas” (CONANP [
71
]). This allowed us to
identify which gypsicolous communities in Mexico are currently protected by federal law.
Additionally, we identified the plant species recorded on gypsum that are protected by the
Mexican Federal Law NOM-059-SEMARNAT-2010 [72].
3. Results
3.1. Botanical Records on Mexican Gypsum Soils
We identified botanical records reporting gypsum sites in 14 states of Mexico: Baja
California, Baja California Sur, Chihuahua, Coahuila, Colima, Durango, Guerrero, Jalisco,
Nuevo León, Oaxaca, Puebla, San Luis Potosí, Tamaulipas, and Zacatecas (Figure 2a). The
states with the highest number of gypsum sites recorded were Nuevo León and Coahuila.
In these two states, most outcrops occur in pine oak forests and xerophilous scrubland in
the municipalities of Cuatro Ciénegas, Galeana, Aramberri, and Zaragoza. In San Luis
Potosí, gypsophile grasslands are frequent in the municipalities of Matehuala and Vanegas,
while xerophilous scrubland is common in Guadalcázar, San Nicolás Tolentino, and Villa
Juárez. Many scattered sites were identified across Chihuahua and Coahuila, mainly in
xerophilous scrubland or grassland and even in gypsum dunes, such as the ones in the
Cuatro Ciénegas Basin. In Baja California and Baja California Sur, gypsum records were
scarce. In Baja California there are reports between Chapala and Punta Prieta and in
Baja California Sur at Isla San Marcos in Mulegémunicipality. Four isolated areas were
identified in Durango, while all the sites from Zacatecas were located along its borders with
Coahuila or San Luis Potosí(Figure 2a). In Tamaulipas, gypsum records are concentrated
in the southwestern portion of the state, on xerophilous shrubland close to Nuevo León
and San Luis Potosí. In western Mexico, small gypsum outcrops occur in Colima and
Jalisco, on a very restricted area of mostly limestone-derived soils with tropical deciduous
forests. This also occurs in Guerrero, Puebla, and in the Santiago Juxtlahuaca and Santo

Diversity 2023,15, 522 6 of 17
Domingo Tonalámunicipalities in Oaxaca. The other sites in Oaxaca were reported as
xerophilous scrubland.
Diversity 2023, 15, x FOR PEER REVIEW 6 of 18
Vanegas, while xerophilous scrubland is common in Guadalcázar, San Nicolás Tolentino,
and Villa Juárez. Many scattered sites were identified across Chihuahua and Coahuila,
mainly in xerophilous scrubland or grassland and even in gypsum dunes, such as the ones
in the Cuatro Ciénegas Basin. In Baja California and Baja California Sur, gypsum records
were scarce. In Baja California there are reports between Chapala and Punta Prieta and in
Baja California Sur at Isla San Marcos in Mulegé municipality. Four isolated areas were
identified in Durango, while all the sites from Zacatecas were located along its borders
with Coahuila or San Luis Potosí (Figure 2a). In Tamaulipas, gypsum records are concen-
trated in the southwestern portion of the state, on xerophilous shrubland close to Nuevo
León and San Luis Potosí. In western Mexico, small gypsum outcrops occur in Colima and
Jalisco, on a very restricted area of mostly limestone-derived soils with tropical deciduous
forests. This also occurs in Guerrero, Puebla, and in the Santiago Juxtlahuaca and Santo
Domingo Tonalá municipalities in Oaxaca. The other sites in Oaxaca were reported as
xerophilous scrubland.
Figure 2. Current distribution of botanical collections on gypsum: (a) gypsisols with botanical rec-
ords in Mexico and (b) number of observations in gypsum sites. The blue dots constitute all the
botanical records. The red crosses represent gypsisol sites reported by the SGM [9] without botanical
records. State abbreviations: BC = Baja California, BCS = Baja California Sur, CAMP = Campeche,
COAH = Coahuila, COL = Colima, CHIH = Chihuahua, DUR = Durango, GRO = Guerrero, HGO =
Hidalgo, JAL = Jalisco, MICH = Michoacán, MOR = Morelos, NL = Nuevo León, OAX = Oaxaca, PUE
= Puebla, SIN = Sinaloa, SLP = San Luis Potosí, SON = Sonora, T = Tamaulipas, ZAC = Zacatecas.
According to the herbarium records, the CHIH province presented the highest con-
centration of gypsum sites, widely distributed across it (Figure 2a). However, potential
gypsisols in the SMOr are abundant along its northern portion and in some cases, they
were larger in extent than those in the CHIH. Additionally, there were three gypsum lo-
calities in the Tamaulipas province. Only two gypsum localities were recorded for the Baja
Californian province. There were many gypsum sites recorded in biogeographic prov-
inces with tropical affinities. In western Mexico, gypsum outcrops were documented in a
reduced area pertaining to the Pacific Lowlands. Meanwhile, the gypsisols of the southern
portion of the country were situated in the Balsas Basin (BB) and the Sierra Madre del Sur
(SMS) provinces.
We recorded 4880 plant collections on Mexican gypsisols, but their distribution was
markedly heterogeneous (Figure 2b). The Cuatro Ciénegas Basin hosted the highest sam-
pling concentration with 784 records. Another highly sampled site, with 408 accessions,
was identified in southern Mexico in the Santo Domingo Tonalá municipality in Oaxaca
(Figure 2b). Finally, some areas with 51–100 and 101–200 records were localized mainly
across Coahuila, Nuevo León, and San Luis Potosí. The rest of the documented sites across
the country had less than 50 records, with most less than 20 (Figure 2b).
Figure 2.
Current distribution of botanical collections on gypsum: (
a
) gypsisols with botanical
records in Mexico and (
b
) number of observations in gypsum sites. The blue dots constitute all the
botanical records. The red crosses represent gypsisol sites reported by the SGM [
9
] without botanical
records. State abbreviations: BC = Baja California, BCS = Baja California Sur, CAMP = Campeche,
COAH = Coahuila, COL = Colima, CHIH = Chihuahua, DUR = Durango, GRO = Guerrero,
HGO = Hidalgo, JAL = Jalisco, MICH = Michoacán, MOR = Morelos, NL = Nuevo León,
OAX = Oaxaca, PUE = Puebla, SIN = Sinaloa, SLP = San Luis Potosí, SON = Sonora, T = Tamaulipas,
ZAC = Zacatecas.
According to the herbarium records, the CHIH province presented the highest con-
centration of gypsum sites, widely distributed across it (Figure 2a). However, potential
gypsisols in the SMOr are abundant along its northern portion and in some cases, they
were larger in extent than those in the CHIH. Additionally, there were three gypsum locali-
ties in the Tamaulipas province. Only two gypsum localities were recorded for the Baja
Californian province. There were many gypsum sites recorded in biogeographic provinces
with tropical affinities. In western Mexico, gypsum outcrops were documented in a re-
duced area pertaining to the Pacific Lowlands. Meanwhile, the gypsisols of the southern
portion of the country were situated in the Balsas Basin (BB) and the Sierra Madre del Sur
(SMS) provinces.
We recorded 4880 plant collections on Mexican gypsisols, but their distribution was
markedly heterogeneous (Figure 2b). The Cuatro Ciénegas Basin hosted the highest sam-
pling concentration with 784 records. Another highly sampled site, with 408 accessions,
was identified in southern Mexico in the Santo Domingo Tonalámunicipality in Oaxaca
(Figure 2b). Finally, some areas with 51–100 and 101–200 records were localized mainly
across Coahuila, Nuevo León, and San Luis Potosí. The rest of the documented sites across
the country had less than 50 records, with most less than 20 (Figure 2b).
3.2. Species Richness
We recorded 1470 species growing on gypsum soils in Mexico. The highest total
species richness (gypsophytes and gypsovags) was found in northern Mexico at the Cu-
atro Ciénegas Basin in Coahuila, with 288 species, and in the Santo Domingo Tonalá
municipality in Oaxaca, with 266 (Figure 3a). Cells with 81–150 species were identified
in the municipalities of Aramberri, Galeana, and Zaragoza in Nuevo León, and cells with
51–80 species were found in Nuevo León and San Luis Potosí. The remaining gypsum sites
had less than 50 species (Figure 3a). The regression analysis showed that the variation in
the total species richness pattern is strongly associated with the variation in the number of
records (R2= 0.9, p< 0.001).

Diversity 2023,15, 522 7 of 17
Diversity 2023, 15, x FOR PEER REVIEW 7 of 18
3.2. Species Richness
We recorded 1470 species growing on gypsum soils in Mexico. The highest total spe-
cies richness (gypsophytes and gypsovags) was found in northern Mexico at the Cuatro
Ciénegas Basin in Coahuila, with 288 species, and in the Santo Domingo Tonalá munici-
pality in Oaxaca, with 266 (Figure 3a). Cells with 81–150 species were identified in the
municipalities of Aramberri, Galeana, and Zaragoza in Nuevo León, and cells with 51–80
species were found in Nuevo León and San Luis Potosí. The remaining gypsum sites had
less than 50 species (Figure 3a). The regression analysis showed that the variation in the
total species richness pattern is strongly associated with the variation in the number of
records (R2 = 0.9, p < 0.001).
Figure 3. Spatial distribution of species richness within the gypsicolous flora in Mexico: (a) all spe-
cies recorded and (b) gypsophytes.
Among all species, 205 were cataloged as gypsophytes (with 1878 records). The high-
est gypsophyte species richness was found in northern Mexico (Figure 3b). There were 37
gypsophytes recorded in the Cuatro Ciénegas Basin. Other cells with 23–36 species were
found in Nuevo León in the municipalities of Galeana and Aramberri-Zaragoza. Gyp-
sisols with 16–22 species were detected in the states of Coahuila and Nuevo Léon. All
remaining sites had fewer than 15 gypsophytes, and Baja California, Baja California Sur,
Jalisco, and Puebla had none (Figure 3b).
3.3. Endemism
The CWE analysis detected many cells across the country with high levels of local
endemism (Figure 4). We identified seven important centers of endemism based on the
highest valued cells and their concentration. Centers 1 and 2 were located in the CHIH,
specifically in the Cuatro Ciénegas Basin, Coahuila (twelve exclusive gypsophytes), and
in Mina, Nuevo León (six exclusive gypsophytes). Centers 3 and 4 occurred along the Si-
erra Madre Oriental. Center 3 is located in southern Nuevo León and hosts the largest
number of exclusive gypsophytes (62 species), while Center 4 occurred in San Luis Potosí
(eight exclusive gypsophytes). The fifth center corresponds to Colima and it is supported
by two microendemic species. The last two centers were found in southern Mexico at the
confluences of the BB with the SMS in Oaxaca, at the municipalities of Santo Domingo
Tonalá, Santiago Juxtlahuaca, and San Juan Teita, and both sites had three microendemic
gypsophytes, respectively. Table 1 shows the gypsophytes that support the proposal of
centers of endemism.
Figure 3.
Spatial distribution of species richness within the gypsicolous flora in Mexico: (
a
) all species
recorded and (b) gypsophytes.
Among all species, 205 were cataloged as gypsophytes (with 1878 records). The
highest gypsophyte species richness was found in northern Mexico (Figure 3b). There were
37 gypsophytes recorded in the Cuatro Ciénegas Basin. Other cells with 23–36 species were
found in Nuevo León in the municipalities of Galeana and Aramberri-Zaragoza. Gypsisols
with 16–22 species were detected in the states of Coahuila and Nuevo Léon. All remaining
sites had fewer than 15 gypsophytes, and Baja California, Baja California Sur, Jalisco, and
Puebla had none (Figure 3b).
3.3. Endemism
The CWE analysis detected many cells across the country with high levels of local
endemism (Figure 4). We identified seven important centers of endemism based on the
highest valued cells and their concentration. Centers 1 and 2 were located in the CHIH,
specifically in the Cuatro Ciénegas Basin, Coahuila (twelve exclusive gypsophytes), and
in Mina, Nuevo León (six exclusive gypsophytes). Centers 3 and 4 occurred along the
Sierra Madre Oriental. Center 3 is located in southern Nuevo León and hosts the largest
number of exclusive gypsophytes (62 species), while Center 4 occurred in San Luis Potosí
(eight exclusive gypsophytes). The fifth center corresponds to Colima and it is supported
by two microendemic species. The last two centers were found in southern Mexico at the
confluences of the BB with the SMS in Oaxaca, at the municipalities of Santo Domingo
Tonalá, Santiago Juxtlahuaca, and San Juan Teita, and both sites had three microendemic
gypsophytes, respectively. Table 1shows the gypsophytes that support the proposal of
centers of endemism.
Diversity 2023, 15, x FOR PEER REVIEW 8 of 18
Figure 4. Centers of endemism detected for the gypsophytes in Mexico.
Table 1. Restricted species that support the gypsophyte endemism centers.
Endemism Center Supporting Species
1
Cuatro Ciénegas Basin
Amaranthaceae: Tidestromia rhizomatosa I.M. Johnst.; Asteraceae: Erigeron cuatrocienegensis G.L.
Nesom, Gaillardia gypsophila B.L. Turner, Haploesthes robusta I.M. Johnst., Solidago gypsophila
G.L. Nesom, Xanthisma restiforme (B.L. Turner) D.R. Morgan and R.L. Hartm., Xylothamia
truncata G.L. Nesom; Cactaceae: Ancistrocactus pinkavanus García-Mor., Gonz.-Bot. and Rodr.
González; Euphorbiaceae: Euphorbia scopulorum Brandegee; Gentianaceae: Sabatia tuberculata
J.E. Williams; Poaceae: Bouteloua johnstonii Swallen, Sporobolus spiciformis Swallen.
2
Mina, Nuevo León
Asteraceae: Erigeron heleniae G.L. Nesom; Boraginaceae: Cryptantha geohintonii B.L. Turner;
Caryophyllaceae: Drymaria pattersonii B.L. Turner; Ehretiaceae: Tiquilia tuberculata A.T.
Richardson; Polemoniaceae: Giliastrum gypsophilum (B.L. Turner) J.M. Porter; Solanaceae:
Chamaesaracha geohintonii Averett and B.L. Turner.
3
Galeana-Aramberri-
Zaragoza
Asparagaceae: Jaimehintonia gypsophila B.L. Turner; Asteraceae: Ageratina gypsophila B.L.
Turner, Erigeron gypsoverus G.L. Nesom, E. pattersonii G.L. Nesom, Helianthella gypsophila B.L.
Turner, Heterotheca gypsophila B.L. Turner, Hieracium gypsophilum B.L. Turner, Isocoma gypsophila
B.L. Turner, Sanrobertia gypsophila B.L. Turner, Tridax hintoniorum B.L. Turner, Verbesina
aramberrana B.L. Turner, V. hintoniorum B.L. Turner, V. zaragosana B.L. Turner; Boraginaceae:
Antiphytum hintoniorum L.C. Higgins and B.L. Turner, Cryptantha gypsites I.M. Johnst.;
Cactaceae: Aztekium hintonii Glass and Fitz Maurice, Geohintonia mexicana Glass and Fitz
Maurice, Rapicactus beguinii subsp. hintoniorum (A.Hofer) Lüthy, R. booleanus (G.S.Hinton)
D.Donati, R. zaragozae (Glass and R.A.Foster) D.Donati, Turbinicarpus hoferi Lüthy and A.B.
Lau; Campanulaceae: Calcaratolobelia margarita (E. Wimm.) Wilbur, C. pringlei (B.L. Rob.)
Wilbur; Caryophyllaceae: Arenaria hintoniorum B.L. Turner; Commelinaceae: Callisia
hintoniorum B.L. Turner, Gibasis gypsophila B.L. Turner; Crassulaceae: Sedum booleanum B.L.
Turner; Cyperaceae: Carex gypsophila Reznicek and S. González; Euphorbiaceae: Euphorbia
correlli M.C. Johnst., E. neilmulleri M.C. Johnst.; Fabaceae: Dalea gypsophila Barneby,
Dermatophyllum juanhintonianum (B.L. Turner) B.L. Turner; Frankeniaceae: Frankenia margaritae
Medrano; Hydrophyllaceae: Phacelia hintoniorum B.L. Turner, P. vossii N.D. Atwood; Iridaceae:
Sisyrinchium microbracteatum G.L. Nesom; Lamiaceae: Hedeoma ciliolata (Epling) R.S. Irving, H.
pusilla (R.S. Irving) R.S. Irving, Salvia gypsophila B.L. Turner, Scutellaria hintoniorum Henrickson,
S. lutilabia T.M. Lane and G.L. Nesom; Lentibulariaceae: Pinguicula immaculata Zamudio and
Lux, P. nivalis Luhrs and Lampard, P. rotundiflora Studnička; Liliaceae: Calochortus marcellae
G.L. Nesom; Linaceae: Linum gypsogenium G.L. Nesom, L. modestum C.M. Rogers; Namaceae:
Nama hitchcockii J.D. Bacon; Oleaceae: Menodora gypsophila B.L. Turner, M. hintoniorum B.L.
Figure 4. Centers of endemism detected for the gypsophytes in Mexico.

Diversity 2023,15, 522 8 of 17
Table 1. Restricted species that support the gypsophyte endemism centers.
Endemism Center Supporting Species
1
Cuatro Ciénegas Basin
Amaranthaceae: Tidestromia rhizomatosa I.M. Johnst.; Asteraceae: Erigeron cuatrocienegensis G.L.
Nesom, Gaillardia gypsophila B.L. Turner, Haploesthes robusta I.M. Johnst., Solidago gypsophila G.L.
Nesom, Xanthisma restiforme (B.L. Turner) D.R. Morgan and R.L. Hartm., Xylothamia truncata G.L.
Nesom; Cactaceae: Ancistrocactus pinkavanus García-Mor., Gonz.-Bot. and Rodr. González;
Euphorbiaceae: Euphorbia scopulorum Brandegee; Gentianaceae: Sabatia tuberculata J.E. Williams;
Poaceae: Bouteloua johnstonii Swallen, Sporobolus spiciformis Swallen.
2
Mina, Nuevo León
Asteraceae: Erigeron heleniae G.L. Nesom; Boraginaceae: Cryptantha geohintonii B.L. Turner;
Caryophyllaceae: Drymaria pattersonii B.L. Turner; Ehretiaceae: Tiquilia tuberculata A.T.
Richardson; Polemoniaceae: Giliastrum gypsophilum (B.L. Turner) J.M. Porter; Solanaceae:
Chamaesaracha geohintonii Averett and B.L. Turner.
3
Galeana-Aramberri-Zaragoza
Asparagaceae: Jaimehintonia gypsophila B.L. Turner; Asteraceae: Ageratina gypsophila B.L. Turner,
Erigeron gypsoverus G.L. Nesom, E. pattersonii G.L. Nesom, Helianthella gypsophila B.L. Turner,
Heterotheca gypsophila B.L. Turner, Hieracium gypsophilum B.L. Turner, Isocoma gypsophila B.L.
Turner, Sanrobertia gypsophila B.L. Turner, Tridax hintoniorum B.L. Turner, Verbesina aramberrana B.L.
Turner, V. hintoniorum B.L. Turner, V. zaragosana B.L. Turner; Boraginaceae: Antiphytum
hintoniorum L.C. Higgins and B.L. Turner, Cryptantha gypsites I.M. Johnst.; Cactaceae: Aztekium
hintonii Glass and Fitz Maurice, Geohintonia mexicana Glass and Fitz Maurice, Rapicactus beguinii
subsp. hintoniorum (A.Hofer) Lüthy, R. booleanus (G.S.Hinton) D.Donati, R. zaragozae (Glass and
R.A.Foster) D.Donati, Turbinicarpus hoferi Lüthy and A.B. Lau; Campanulaceae: Calcaratolobelia
margarita (E. Wimm.) Wilbur, C. pringlei (B.L. Rob.) Wilbur; Caryophyllaceae: Arenaria hintoniorum
B.L. Turner; Commelinaceae: Callisia hintoniorum B.L. Turner, Gibasis gypsophila B.L. Turner;
Crassulaceae: Sedum booleanum B.L. Turner; Cyperaceae: Carex gypsophila Reznicek and S.
González; Euphorbiaceae: Euphorbia correlli M.C. Johnst., E. neilmulleri M.C. Johnst.; Fabaceae:
Dalea gypsophila Barneby, Dermatophyllum juanhintonianum (B.L. Turner) B.L. Turner;
Frankeniaceae: Frankenia margaritae Medrano; Hydrophyllaceae: Phacelia hintoniorum B.L. Turner,
P. vossii N.D. Atwood; Iridaceae: Sisyrinchium microbracteatum G.L. Nesom; Lamiaceae: Hedeoma
ciliolata (Epling) R.S. Irving, H. pusilla (R.S. Irving) R.S. Irving, Salvia gypsophila B.L. Turner,
Scutellaria hintoniorum Henrickson, S. lutilabia T.M. Lane and G.L. Nesom; Lentibulariaceae:
Pinguicula immaculata Zamudio and Lux, P. nivalis Luhrs and Lampard, P. rotundiflora Studniˇcka;
Liliaceae: Calochortus marcellae G.L. Nesom; Linaceae: Linum gypsogenium G.L. Nesom, L.
modestum C.M. Rogers; Namaceae: Nama hitchcockii J.D. Bacon; Oleaceae: Menodora gypsophila B.L.
Turner, M. hintoniorum B.L. Turner; Onagraceae: Oenothera stubbei W. Dietr., P.H. Raven and W.L.
Wagner; Orobanchaceae: Agalinis gypsophila B.L. Turner, Castilleja galehintoniae G.L. Nesom;
Papaveraceae: Hunnemannia hintoniorum G.L. Nesom; Poaceae: Muhlenbergia jaime-hintonii P.M.
Peterson and Valdés-Reyna; Polygalaceae: Polygala oedophylla S.F. Blake; Polygonaceae: Eriogonum
fimbriatum W.J. Hess and Reveal; Pteridaceae: Gaga hintoniorum (Mendenh. and G.L. Nesom) F.W.
Li and Windham; Rubiaceae: Galium dempsterae B.L. Turner, G. juniperinum Standl.;
Scrophulariaceae: Leucophyllum alejandrae G.L. Nesom, L. hintoniorum G.L. Nesom
4
San Luis Potosí
Asteraceae: Neonesomia johnstonii (G.L. Nesom) Urbatsch and R.P. Roberts, Tridax candidissima A.
Gray, Verbesina potosina B.L. Rob.; Iridaceae: Sisyrinchium zamudioi Espejo, López-Ferr. and Ceja;
Lentibulariaceae: Pinguicula gypsicola Brandegee, P. takakii Zamudio and Rzed.; Liliaceae:
Calochortus mendozae Espejo, López-Ferr. and Ceja; Linaceae: Linum macradenium Brandegee
5
Colima
Crassulaceae: Graptopetalum glassii Acev.-Rosas and Cházaro; Lentibulariaceae: Pinguicula
colimensis McVaugh and Mickel
6
Oaxaca-Mixteca
Bromeliaceae: Hechtia gypsophila López-Ferr., Espejo and Hern.-Cárdenas; Crassulaceae: Echeveria
subcorymbosa Kimnach and Moran; Lentibulariaceae: Pinguicula pygmaea Rivadavia, E.L.Read and
A.Fleischm.
7
Oaxaca-Teita
Asparagaceae: Xochiquetzallia magnifolia García-Mend. and J.Gut.; Asteraceae: Mixtecalia teitaensis
Redonda-Mart., García-Mend. and D. Sandoval; Cactaceae: Cephalocereus parvispinus S. Arias, H. J.
Tapia and U. Guzmán
3.4. Conservation Status of the Mexican Gypsicolous Flora
The geoprocessing methodology identified nine federal PNAs that contain gypsum
soil areas in Mexico (Figure 5a–f). Two of them were located in the Baja California Peninsula
(a, b) and corresponded to the “Área de Protección de Flora y Fauna (APFF) Valle de Los

Diversity 2023,15, 522 9 of 17
Cirios” and “APFF Islas del Golfo de California”. In Chihuahua, one gypsum locality
occurred at the “APFF Cañón de Santa Elena” (c). The gypsisols of the Cuatro Ciénegas
Basin and the adjacent areas are protected by two PNAs: the “APFF Cuatro Ciénegas”
and the “Área de Protección de los Recursos Naturales Cuenca Alimentadora del Distrito
Nacional de Riego (CADNR) 4 Don Martín” (d). Within the limits of Coahuila and Nuevo
León, we found that the “Parque Nacional Cumbres de Monterrey” and the “CADNR 26
Bajo Río San Juan” hosted gypsum areas (e). Finally, we identified two PNAs that have
gypsum outcroppings in Oaxaca (f): the “APFF Boquerón de Tonalá”, in the Mixteca region,
and the “Reserva de la Biosfera Tehuacán-Cuicatlán”, which is shared with Puebla.
Diversity 2023, 15, x FOR PEER REVIEW 10 of 18
Figure 5. Protected Natural Areas (PNAs) of Mexico with gypsum records. (a) Área de Protección
de Flora y Fauna (APFF) Valle de Los Cirios, (b) APFF Islas del Golfo de California, (c) APFF Cañón
de Santa Elena, (d) APFF Cuatro Ciénegas and Área de Protección de los Recursos Naturales Cuenca
Alimentadora del Distrito Nacional de Riego (CADNR) 4 Don Martín, (e) Parque Nacional Cumbres
de Monterrey and CADNR 26 Bajo Río San Juan, and (f) APFF Boquerón de Tonalá and Reserva de
la Biosfera Tehuacán-Cuicatlán.
4. Discussion
4.1. Botanical Records on Mexican Gypsum Soils
Gypsum sites are scattered throughout Mexico. Even though we recorded references
to gypsum sites in 14 states of the country, we are aware that there are many unexplored
gypsum outcrops that we failed to detect with our workflow. For example, the SGM [9]
reports the presence of gypsum soil in Campeche, Hidalgo, Michoacán, Morelos, Sinaloa,
and Sonora, but we did not find botanical records for gypsum in these states. Martínez
and Galindo-Leal [15] reported plants growing on gypsum in the state of Campeche, but
we were unable to locate herbarium collections. There are numerous botanical collections
on gypsum in Mexico whose collecting labels do not identify the collecting site as pos-
sessing gypsisols. An important fact is that gypsum is often confused with calcium car-
bonate or saline soils [73]. To corroborate this, different approaches such as satellite re-
mote sensing, geological surveys, soil samplings, and ecological data should be used in
an integrative way. These are complicated and time-consuming tasks in a country as large
as Mexico, especially considering information is often lacking (e.g., soil sampling and eco-
logical data). Additional work is necessary to complete the gypsicolous flora of Mexico
and to corroborate if the presence of gypsum reported by the SGM [9] represents surface
outcrops and have direct contact with plants or if the deposits are located in mines. Nev-
ertheless, our results are an important first step to detect potential gypsum outcrops in
Mexico and to understand their flora.
For much of the botanical history of Mexico, only the gypsophile flora from the CHIH
have received significant botanical research interest [5,8,10,13,38]. However, we identified
Figure 5.
Protected Natural Areas (PNAs) of Mexico with gypsum records. (
a
)Área de Protección de
Flora y Fauna (APFF) Valle de Los Cirios, (
b
) APFF Islas del Golfo de California, (
c
) APFF Cañón de
Santa Elena, (
d
) APFF Cuatro Ciénegas and Área de Protección de los Recursos Naturales Cuenca
Alimentadora del Distrito Nacional de Riego (CADNR) 4 Don Martín, (
e
) Parque Nacional Cumbres
de Monterrey and CADNR 26 Bajo Río San Juan, and (
f
) APFF Boquerón de Tonaláand Reserva de la
Biosfera Tehuacán-Cuicatlán.
Of the 1470 species recorded growing on gypsum, 56 are included under the NOM-059-
SEMARNAT-2010. Six of these are catalogued as endangered, twenty-two are threatened,
and twenty-eight are subject to special protection. Among these fifty-six catalogued species,
only six were classified as gypsophytes.
4. Discussion
4.1. Botanical Records on Mexican Gypsum Soils
Gypsum sites are scattered throughout Mexico. Even though we recorded references
to gypsum sites in 14 states of the country, we are aware that there are many unexplored
gypsum outcrops that we failed to detect with our workflow. For example, the SGM [
9
]
reports the presence of gypsum soil in Campeche, Hidalgo, Michoacán, Morelos, Sinaloa,

Diversity 2023,15, 522 10 of 17
and Sonora, but we did not find botanical records for gypsum in these states. Martínez and
Galindo-Leal [
15
] reported plants growing on gypsum in the state of Campeche, but we
were unable to locate herbarium collections. There are numerous botanical collections on
gypsum in Mexico whose collecting labels do not identify the collecting site as possessing
gypsisols. An important fact is that gypsum is often confused with calcium carbonate or
saline soils [
73
]. To corroborate this, different approaches such as satellite remote sensing,
geological surveys, soil samplings, and ecological data should be used in an integrative
way. These are complicated and time-consuming tasks in a country as large as Mexico,
especially considering information is often lacking (e.g., soil sampling and ecological data).
Additional work is necessary to complete the gypsicolous flora of Mexico and to corroborate
if the presence of gypsum reported by the SGM [
9
] represents surface outcrops and have
direct contact with plants or if the deposits are located in mines. Nevertheless, our results
are an important first step to detect potential gypsum outcrops in Mexico and to understand
their flora.
For much of the botanical history of Mexico, only the gypsophile flora from the CHIH
have received significant botanical research interest [
5
,
8
,
10
,
13
,
38
]. However, we identified
that, with the exception of the Cuatro Ciénegas Basin [
34
,
44
], most of the gypsum outcrops
in CHIH have poor botanical records (Figure 2b). This is particularly evident in the region
of west central Coahuila, which has some of the most extensive and least accessible gypsum
exposures in North America, as part of the Acatita Formation [
44
]. The flora associated
with the gypsum outcrops from the SMOr seems to be better known, mostly due to the
fieldwork conducted in Nuevo León by the Hinton family [
41
] and in San Luis Potosíby
Rzedowski [
74
]. However, our results showed that many areas of the SMOr need more
intensive exploration, even in the relatively well-explored states of Nuevo León and San
Luis Potosí. For example, San Luis Potosíhas two gypsiferous regions, one in the Middle
Zone that occupies 203,950 Ha and another in the Highland Zone which has 193,309 Ha [
75
],
but the flora of the Middle Zone is less studied.
Meanwhile, we found very few records from the outcrops of Baja California, Baja
California Sur, Colima, Durango, Jalisco, Puebla, and Zacatecas. With the exception of
one recent floristic inventory in Colima [
17
], research on these gypsum outcrops is scarce
and focused on particular groups [
16
,
76
,
77
]. On the other hand, the recent exploration of
some gypsum communities in Oaxaca has revealed a highly localized endemic flora [
78
].
Perhaps the most outstanding example is the genus Mixtecalia, a tree-like Asteraceae [
21
].
Due to the lack of collections and the particularities of gypsisols in Mexico, we are sure that
the intensification of botanical exploration in these communities will lead to the description
of many new taxa.
4.2. Species Richness
The highest total species richness was documented in the Cuatro Ciénegas Basin,
which is the most sampled gypsum area of the country and has been previously recognized
as a region of outstanding diversity [
34
,
44
,
79
]. Additionally, the area surrounding Santo
Domingo Tonaláin Oaxaca hosts an elevated number of species (Figure 3a). This zone has
received extensive attention, with many botanical collections and technical studies [
80
,
81
].
It is situated in the Balsas Basin, a biogeographic province with tropical affinity and
with wetter conditions than the gypsisols of northern Mexico. In tropical gypsisols, the
rain washes the surface of the soil and hinders the formation of a hard gypsum crust,
which allows the establishment of a greater proportion of gypsovag species [
3
,
7
], but
comparatively fewer gypsum endemics. Nevertheless, Oaxaca hosts the highest species
richness of angiosperms in Mexico [
82
,
83
], which contributes to the diversity of plants on
gypsum outcrops there.
In Mexico, the highest species richness levels of vascular plants are concentrated in
the southern portion of the country [
84
], following the global latitudinal pattern [
52
]. It
is feasible that the gypsicolous floras of Mexico as a whole follow this pattern too. Total
species richness was highly correlated with the number of occurrence records; thus, it

Diversity 2023,15, 522 11 of 17
is possible that if the number of records in southern and western Mexico increases, the
number of species may be higher than in those in northern Mexico. The pattern of spatial
distribution of the total species richness in the country will change as the poorest explored
areas increase their records, particularly those from southern and western Mexico. However,
this pattern is different when species richness is analyzed only with gypsophytes.
Gypsophyte species richness is concentrated in northern Mexico, mainly in the SMOr,
but also in the CHIH (Figure 3b). Gypsum soils are widely distributed in these regions,
with individual outcrops, the extent of which varies in size from many square kilometers
to a few square meters [
6
,
8
,
9
]. It is believed that gypsophyte floras evolved from groups
that have their diversity centers in the same regions [
6
]. Within the SMOr and CHIH,
the combination of isolation of individual outcrops from one another, a wide range of
different climatic conditions, and the relative climatic stability of the gypsum outcrops
throughout the Pleistocene have promoted the evolution of gypsophyte plant lineages that
occur there [
6
,
8
,
38
,
85
]. Several studies have demonstrated the existence of gypsophyte
clades in the CHIH and SMOr (with as many as 10 gypsophyte species in a single clade),
implying that speciation occurred after the shift to a gypsophyte ecology [
13
,
86
–
90
]. In
the case of the SMOr, the large topographical and climatic variation has promoted plant
diversification [
51
,
91
,
92
]. Our results follow this pattern also for the gypsum outcrops
within this biogeographic province at Nuevo León. Within the CHIH, the Cuatrociénegas
Basin hosts outstanding levels of diversity [
79
]. Most of the bolson consists of surface
gypsisols; thus, gypsum plays a main role in community assembly and differentiation.
Here, species assemblages have been shown to be related to the effect of topographic factors,
altitude, and slope [
93
]. The gypsophyte diversity estimated in the municipality of Cuatro
Ciénegas by Ochoterena et al. [44] and this work exemplify this well.
Mexico has a megadiverse flora, which results from many factors, including its geo-
graphic location that lies at the contact of Neotropical and Nearctic elements; its climatic
history, comprising of periods of fluctuations and stability; and a highly varied topography,
physiography, and geology [
57
,
94
]. The total number of plant species in the country is
estimated to be 22,969 [
95
]. Our work reports that 1470 (6.4%) of those species grow on
gypsum, from which 205 (14% of the gypsicolous plants in Mexico) are gypsophytes. Hence,
gypsophytes represent almost 1% of the total flora of the country. This is the first work to
attempt such approximations; thus, we are aware that these numbers are far from definitive.
On the one hand, it is possible that some of the putative gypsophytes are simply yet to
be recorded outside gypsum. On the other hand, in-depth taxonomic and phylogenetic
studies, as well as botanical exploration of the gypsum outcrops in Mexico, are highly
incomplete, and the discovery of additional gypsophytes (perhaps many more) is to be
expected. Regardless, Mexico hosts a highly species-rich gypsophyte flora, considering
that the first preliminary estimate of the number of gypsophytes across all of the Palearctic
and Australia resulted in 378 species, from which Iran has the highest number, with 91 [
96
].
Consequently, given the current knowledge, our work places Mexico as the country with
the highest recorded number of gypsophyte species worldwide. A detailed taxonomic
analysis of the gypsophyte flora of Mexico is in preparation.
4.3. Endemism
The use of the CWE index allowed us to identify the centers of endemism with the
highest numbers of localized gypsophyte species. Our results recovered seven such centers
of endemism across Mexico (Figure 4a). Center 1, the Cuatro Ciénegas basin, has been
recognized as an important center of endemism and biodiversity for many organisms and
is home to many narrowly endemic gypsophytes [
11
,
34
,
44
,
79
]. Centers 2 and 3, in the
SMOr, have been identified as angiosperm diversity hotspots [
50
,
51
,
97
]. The high number
of endemic species that occur in these zones is remarkable [
37
,
56
]. Center 4, which includes
the gypsophilous grasslands in the CHIH and a small portion of the SMOr, with xerophilous
scrubland in Guadálcazar, San Luis Potosí, hosts an important level of endemism [
50
,
51
].
Center 5, in western Mexico at the Microcuenca La Salada in Colima, is another area with

Diversity 2023,15, 522 12 of 17
recognized high diversity and endemism [
17
]. Despite the geographic proximity of the
two nearby centers of endemism in Oaxaca (6 and 7), they have very different species
compositions. Center 6 is composed mainly of species characteristic of tropical deciduous
forests, while center 7 is composed of xerophilous scrubland. Even though these sites do
not possess high gypsophyte richness, those that occur are microendemic. Overall, the
gypsum outcrops of Mexico contain elevated rates of endemism, with those in the CHIH
and the SMOr hosting many endemic gypsophyte taxa, but those in western and southern
Mexico uniformly hosting very rare gypsophyte species (Figure 6).
Diversity 2023, 15, x FOR PEER REVIEW 13 of 18
Figure 6. Examples of gypsophytes of Mexico. Asparagaceae: (a) Jaimehintonia gypsophila B.L.
Turner; Asteraceae: (b) Mixtecalia teitaensis Redonda-Mart., García-Mend. and D. Sandoval, (c)
Sartwellia mexicana A. Gray, (d) Xanthisma restiforme (B.L. Turner) D.R. Morgan and R.L. Hartm.;
Cactaceae: (e) Aztekium hintonii Glass and Fitz Maurice, (f) Geohintonia mexicana Glass and Fitz Mau-
rice, (g) Rapicactus booleanus (G.S.Hinton) D.Donati; Caryophyllaceae: (h) Drymaria lyropetala I.M.
Johnst.; Commmelinaceae: (i) Callisia hintoniorum B.L. Turner; Crassulaceae: (j) Graptopetalum glassii
Acev.-Rosas and Cházaro; Fouquieriaceae: (k) Fouquieria shrevei I.M. Johnst.; Hydrophyllaceae: (l)
Phacelia marshall-johnstonii N.D. Atwood and Pinkava; Lentibulariaceae: (m) Pinguicula gypsicola
Brandegee; Liliaceae: (n) Calochortus marcellae G.L. Nesom; Linaceae: (o) Linum macradenium
Brandegee; Namaceae: (p) Nama stevensii C.L. Hitchc. Photographs: (a,c–p) by J. P. Ortiz-Brunel, (b)
by Juvenal Aragón.
4.4. Conservation Status of the Mexican Gypsicolous Flora
Nine federal PNAs currently contain gypsum outcrops (Figure 5). Unfortunately,
only the “APFF Cuatro Ciénegas” and the “CADNR 4 Don Martín” occur in a zone (Cu-
atro Ciénegas Basin) with high gypsophyte richness and endemism. Even though the
“Parque Nacional Cumbres de Monterrey” and the “CADNR 26 Bajo Río San Juan” host
some gypsum outcrops, the highest concentration of records, species richness, and ende-
mism of gypsophytes in the SMOr occurs just south of them. This problem has also been
identified for the endemic vascular plants of the SMOr [51]. If the “CADNR 26 Bajo Río
San Juan” in Nuevo León were enlarged, it would cover the aforementioned gypsum ar-
eas. Additionally, this would protect other important ecosystems in one of the most rele-
vant hotspots of endemism and diversity in Mexico [50,51]. Meanwhile, some gypsum
outcrops in Chihuahua and Oaxaca with few gypsophyte taxa are protected within the
“APFF Cañón de Santa Elena” and the “Reserva de la Biósfera Tehuacán-Cuicatlán”,
Figure 6.
Examples of gypsophytes of Mexico. Asparagaceae: (
a
)Jaimehintonia gypsophila B.L.
Turner; Asteraceae: (
b
)Mixtecalia teitaensis Redonda-Mart., García-Mend. and D. Sandoval,
(
c
)Sartwellia mexicana A. Gray, (
d
)Xanthisma restiforme (B.L. Turner) D.R. Morgan and R.L. Hartm.; Cac-
taceae: (
e
)Aztekium hintonii Glass and Fitz Maurice, (
f
)Geohintonia mexicana Glass and Fitz Maurice,
(
g
)Rapicactus booleanus (G.S.Hinton) D.Donati; Caryophyllaceae: (
h
)Drymaria lyropetala I.M. Johnst.;
Commmelinaceae: (
i
)Callisia hintoniorum B.L. Turner; Crassulaceae: (
j
)Graptopetalum glassii Acev.-
Rosas and Cházaro; Fouquieriaceae: (k)Fouquieria shrevei I.M. Johnst.; Hydrophyllaceae: (l)Phacelia
marshall-johnstonii N.D. Atwood and Pinkava; Lentibulariaceae: (
m
)Pinguicula gypsicola Bran-
degee; Liliaceae: (
n
)Calochortus marcellae G.L. Nesom; Linaceae: (
o
)Linum macradenium Bran-
degee; Namaceae: (
p
)Nama stevensii C.L. Hitchc. Photographs: (
a
,
c
–
p
) by J. P. Ortiz-Brunel, (
b
) by
Juvenal Aragón.
4.4. Conservation Status of the Mexican Gypsicolous Flora
Nine federal PNAs currently contain gypsum outcrops (Figure 5). Unfortunately, only
the “APFF Cuatro Ciénegas” and the “CADNR 4 Don Martín” occur in a zone (Cuatro
Ciénegas Basin) with high gypsophyte richness and endemism. Even though the “Parque

Diversity 2023,15, 522 13 of 17
Nacional Cumbres de Monterrey” and the “CADNR 26 Bajo Río San Juan” host some
gypsum outcrops, the highest concentration of records, species richness, and endemism of
gypsophytes in the SMOr occurs just south of them. This problem has also been identified
for the endemic vascular plants of the SMOr [
51
]. If the “CADNR 26 Bajo Río San Juan” in
Nuevo León were enlarged, it would cover the aforementioned gypsum areas. Additionally,
this would protect other important ecosystems in one of the most relevant hotspots of en-
demism and diversity in Mexico [
50
,
51
]. Meanwhile, some gypsum outcrops in Chihuahua
and Oaxaca with few gypsophyte taxa are protected within the “APFF Cañón de Santa
Elena” and the “Reserva de la Biósfera Tehuacán-Cuicatlán”, respectively. Fortunately, one
of the areas with the highest total species richness is protected by the “APFF Boquerón de
Tonalá” in Oaxaca.
Despite the existence of the above protected areas, our results show that most of
the gypsum plant communities with the highest species richness and endemism of the
gypsophyte flora of Mexico are unprotected. This problem is coupled with the fact that
only six gypsophytes are officially protected by Mexican law [
72
], despite the fact that most
gypsophytes have a very narrow geographic distribution and grow on a substrate frequently
exploited by mining. Gypsum mining represents one of the most significant threats to
gypsum biodiversity worldwide [
3
], and those of Mexico are no exception. Gypsum is
not abundant in much of the country; thus, exposed outcrops are often economically
exploited [
98
], and it is important that this activity is regulated based on species diversity
and endemism. Finally, new PNAs should be developed to promote the conservation of
these unique communities, particularly in zones with high species richness and endemism.
5. Conclusions
Our work represents the first attempt to integrate information about plant species
growing on gypsum outcrops throughout Mexico based on botanical collections. We find
that most of the potential gypsum outcrops in Mexico are poorly explored and deserve
more attention, as in general, the gypsicolous flora of Mexico is diverse and unique. Even
though the gypsophyte flora of Mexico is not completely known, our work demonstrates
that it is the most species-rich in the world, and that nearly 1% of Mexican plant species
are gypsophytes. The botanical exploration of gypsum communities is likely to result in
the discovery of new gypsophytes and in an increase in the total number of species of
the gypsicolous flora in the country. This seems particularly likely and relevant for those
exposures in western and southern Mexico, which largely occur in tropical seasonal forests
rather than in the more typical arid and semi-arid vegetation. Despite the high diversity and
endemism of gypsum outcrops in Mexico, those with higher numbers of gypsophytes and
those that contain narrowly endemic species are unprotected, with the exception of Cuatro
Ciénegas. We found that enlarging the PNA CADNR 26 Bajo Río San Juan in Nuevo León
would protect one of the most important hotspots of endemism in Mexico. Additionally,
most gypsophytes need to be evaluated by IUCN criteria to assess their conservation status.
We hope that this work will encourage the botanical exploration of gypsum outcrops in
Mexico, and will set a necessary baseline for future ecological, taxonomic, and evolutionary
research to understand these communities and conserve their biodiversity.
Author Contributions:
Conceptualization, J.P.O.-B., H.O., M.J.M. and H.F.-O.; data curation, J.P.O.-B.,
H.O., M.J.M., J.A.-P., G.M.-L., A.R., M.M.S.-R. and H.F.-O.; formal analysis, J.P.O.-B.; investigation,
J.P.O.-B., J.F., G.M.-L., A.R., M.M.S.-R. and H.F.-O.; methodology, J.P.O.-B., H.O., M.J.M. and H.F.-O.;
resources, J.F.; visualization, J.A.-P. and J.F.; writing—original draft, J.P.O.-B. and H.F.-O.; writing—
review and editing, J.P.O.-B., H.O., M.J.M., J.A.-P., J.F., G.M.-L., A.R., M.M.S.-R. and H.F.-O. All
authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Data Availability Statement:
The database with the botanical records of vascular plants on gypsum
is free and available upon request.

Diversity 2023,15, 522 14 of 17
Acknowledgments:
We thank George Yatskievych and the Billie L. Turner Plant Resources Center of
the University of Texas at Austin for their invaluable help. We are grateful to Arantzazu L. Luzuriaga
for their help, comments, and suggestions. We thank Rosa de Lourdes Romo Campos for her technical
support. The authors thank the Gypworld project for promoting collaboration and ideas interchange.
Conflicts of Interest:
The authors have no competing interest to declare that are relevant to the
content of this article.
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