2023-Briones-Salas, et al. Mamíferos Chinantla

Diversity and conservation of mammals
in indigenous territories of southern
Mexico: proposal for an ‘‘Archipelago
Reserve’’
Miguel Briones-Salas1 , Rosa E. Galindo-Aguilar1 , Graciela E. González1 and
María Delfina Luna-Krauletz2
1
Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Unidad Oaxaca, Instituto
Politécnico Nacional, Santa Cruz Xoxocotlan, Oaxaca, México
2
Instituto de Estudios Ambientales, Universidad de la Sierra Juárez, Ixtlán de Juárez, Oaxaca, México
ABSTRACT
Submitted 23 March 2023
Accepted 3 October 2023
Published 7 November 2023
Corresponding author
Rosa E. Galindo-Aguilar,
[email protected]
Academic editor
Sandrine Pavoine
Additional Information and
Declarations can be found on
page 23
Southern Mexico’s tropical forests are home to the country’s highest richness of
mammal species; La Chinantla region is situated within this area, its name from the
indigenous group residing in the area and holding territorial ownership, namely the
Chinantecos. In La Chinantla, there are no Protected Areas; instead, there are Areas
Destined Voluntarily for Conservation (ADVC) and ‘‘Voluntary Conservation Areas’’
(VCA), that are managed by local inhabitants through social consensus. These ADVC
may function as an archipelago reserve, which represents regional diversity, including
the social context, through complementarity. To verify its biodiversity, we analyzed the
richness, composition, distribution, and conservation of wild mammals in the region.
Records were obtained from four sources—primary data collection, databases, scientific
literature, and community monitoring—and were organized into four zones based on
altitudinal and vegetation gradients. We compared the diversity between zones for
three categories of mammals: small (<100 gr.), bats, and medium and large (>100
gr.). 134 species were identified comprising 11 orders, 26 families and 86 genera. The
zone with highest elevation presented the greatest species richness for the assemblage
of mammals and terrestrial mammals, while the zone with the lowest elevation had
the highest richness of bats. For each mammal category, the zone with the most species
also registered the highest number of exclusive species. For the assemblage of mammals
and for medium and large mammals, the similarity index was highest between the two
intermediate zones, while for small mammals and bats, the greatest similarity occurred
between the areas of higher altitude. The study region was found to have the second
highest richness of mammals in Mexico. Finally, we suggest that the conservation
proposals by indigenous people could function as a set of ‘‘islands’’ that promote the
conservation of biodiversity, possibly as an Archipelago Reserve.
DOI 10.7717/peerj.16345
Subjects Biodiversity, Biogeography, Conservation Biology, Ecology, Zoology
Copyright
2023 Briones-Salas et al.
Keywords Áreas destinadas voluntariamente a la conservación, Tropical rainforest, Cloud forest,
Chinantla, Bats, Sierra Madre de Oaxaca
Distributed under
Creative Commons CC-BY 4.0
OPEN ACCESS
How to cite this article Briones-Salas M, Galindo-Aguilar RE, González GE, Luna-Krauletz MíD. 2023. Diversity and
conservation of mammals in indigenous territories of southern Mexico: proposal for an ‘‘Archipelago Reserve’’. PeerJ 11:e16345
http://doi.org/10.7717/peerj.16345
INTRODUCTION
A recurring pattern in biodiversity is that species richness increases as latitude decreases
(Rodhe, 1999), which is one of the reasons why the most biodiverse ecosystems in the world
are in equatorial regions. In addition, the mountains in the tropics have high biological
diversity, since they contain species with different origins and evolutionary histories along
their altitudinal gradient (Graham et al., 2014). Of this biological diversity, beta diversity is
most notable, mainly due to geographic isolation and speciation processes (Mastretta-Yanes
et al., 2015).
The Sierra Madre del Sur is in southern Mexico, in addition to being composed of
temperate vegetation, is home to tropical forests. Species richness is high in these forests,
not only in terms of taxonomic diversity but also phylogenetic and functional diversity
(Espinosa, Ocegueda-Cruz & Luna-Vega, 2016; Aguilar-Tomasini, Martin & Speed, 2021).
One of the largest humid tropical forests in Mexico is located in a region in the
north of the state of Oaxaca called La Chinantla; the region has been inhabited since the
pre-Columbian era by the Chinantecs, an ethnic group that maintains the milpa system,
which relies on subsistence livestock and hunting in some areas (Legarreta, 2010) and
it is considered a priority terrestrial region for conservation in Mexico (Arriaga et al.,
2000) and a priority conservation area for Mesoamerica because of its biodiversity and
endemic species (De Albuquerque et al., 2015). It is a mountainous area whose lowlands has
large areas of tropical rainforest (TRF) and montane cloud forest (MCF), both of which
house extremely biodiverse plant communities (Rzedowski, 1996), while its highlands
contain pine-oak-forests (P-OF). Being composed mainly of TRF and MCF, this region
is an important source of supply of water resources, carbon sequestration, and other
environmental services (Galicia & Zarco-Arista, 2014).
Several studies have revealed a great richness of vertebrate species in La Chinantla
(Noria-Sánchez, Prisciliano-Vázquez & Patiño Islas, 2015; Briones-Salas, Cortés-Marcial
& Lavariega, 2015; Simón-Salvador et al., 2021), particularly of mammals (Pérez-Lustre,
Contreras-Diaz & Santos-Moreno, 2006; Pérez-Irineo & Santos-Moreno, 2012; Del RioGarcía et al., 2014). Moreover, recent records have highlighted species of paramount
importance for conservation efforts, as they are classified as threatened at both national
and international levels (except for Caluromys. derbianus): Tapirus Bairdii, Panthera onca,
Ateles geoffroyi, and C. derbianus (Lira-Torres et al., 2006; Figel et al., 2009; Ortiz-Martínez
et al., 2012; Galindo-Aguilar et al., 2019). The region has also been recognized as a biological
corridor for jaguar (P. onca) conservation in southern and northern Mexico (Rodríguez-Soto
et al., 2011), and researchers have recently begun suggesting that it could be a viable region
for jaguar conservation (Jȩdrzejewski et al., 2018; Lavariega et al., 2020).
Despite the high diversity recorded in the region, La Chinantla does not contain any
Protected Areas (PAs)—where the federal or state government exercises jurisdiction.
However, Chinantecs have established almost 31 communitarian conservation areas which
are volunteered elected for biodiversity conservation, namely ‘‘Areas Destined Voluntarily
for Conservation’’ (ADVC, 27) and ‘‘Voluntary Conservation Areas’’ (VCA, 4). The former
is federally certified by the National Commission of Protected Natural Areas (CONANP,
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
2/30
by its Spanish acronym) while the latter is not. In both cases, these spaces are managed
by the inhabitants themselves through social consensus, which establishes rules of use,
including restrictions on hunting and looting plant species and removing plant cover for
agricultural and livestock activities (Anta-Fonseca & Mondragón-Galicia, 2006; Lele et al.,
2010). ADVCs and VCAs cover variable extensions of forest and aim to protect the most
fragile natural environments. They are in areas with high biological and cultural diversity
and are commonly inhabited by species that fall into some national and international threat
category.
The ADVC in La Chinantla are distributed at an altitudinal gradient of 50–2,500 masl
and comprise a little more than 58,765.78 ha (CONANP-Chinantla Office), almost half of
which is certified by the state of Oaxaca (125,923 ha) (CONANP, 2020).
While that there are no PAs, such as national parks and biosphere reserves, in the region,
which would represent a conservation strategy due to their unique and variable-sized areas
(Halffter, 2007; Moctezuma, Halffter & Arriaga-Jiménez, 2018), alternative strategies could
be considered. One proposed approach is the establishment of small, protected areas to
safeguard the entire regional diversity and enhancing beta diversity. This model has been
referred to in other studies as the ‘‘Archipelago Reserve’’ (AR) (Halffter, 2007; Moctezuma,
Halffter & Arriaga-Jiménez, 2018). The objective of this model is to represent regional
diversity, including the social context, through complementarity. The use of multiple
areas aims to increase species exchange among remnants in fragmented landscapes or
between traditional and rustic agroecosystems with high biological diversity, valuing
productive practices and sustainable development (Halffter, 2007; Moctezuma, Halffter &
Arriaga-Jiménez, 2018). Given the biological and social significance of La Chinantla and
considering the presence of small communitarian conservation areas (ADVC y VCA)
geographically distributed within a priority site and encompassing a significant altitudinal
gradient in a mountainous zone, we propose that the region may function as an archipelago
reserve with substantial potential for biodiversity conservation. Therefore, we establish the
following objectives: (1) analyze the distribution of mammals as a focus group along an
altitudinal gradient; (2) to determine whether species richness distribution is homogeneous
along this gradient or if there is species turnover among different altitudinal steps.
MATERIALS & METHODS
Study area
La Chinantla is in northeast Oaxaca, in the foothills of the Sierra Madre de Oaxaca and in
the Papaloapan River basin. It comprises 14 municipalities that are in the subregions of
Sierra Madre de Oaxaca and Planicie Costera del Golfo (Ortiz-Pérez, Hernandez-Santana
& Figueroa-Mah-Eng, 2004) (Fig. 1).
The climate in La Chinantla is hot and humid in the lowlands, and cool and humid in
the highlands with an average annual temperature of 16 ◦ C and 25 ◦ C, respectively (Meave,
Rincón & Romero-Romero, 2006). The region has high humidity and annual rainfall between
3,600 and 5,800 mm. Its altitude ranges from 0 to 3,000 masl, with slopes between 6◦ and
45◦ in 80% of the territory (Meave, Rincón & Romero-Romero, 2006). Tropical rainforests
(TRF) and montane cloud forests (MCF) predominate (INEGI, 2016).
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
3/30
Figure 1 Geographical location and sources of data on wild mammals in La Chinantla region, northeast of Oaxaca, Mexico. Zone 1 = 4–400, Zone 2 = 400–1,000, Zone 3 = 1,000–1,500, Zone 4 = 1,500–
3,000. Altitude is in masl.
Full-size DOI: 10.7717/peerj.16345/fig-1
Dividing the study area into zones
Based on the altitudinal gradient and the types of vegetation, we divided the study region in
four zones. Zone 1: 0 to 400 masl and warm climates, lowland TRF dominates, combined
with secondary vegetation (SV), agriculture (A), and livestock areas; contains 10 ADVCs.
Zone 2: 401 to 1000 masl, with warm and semi-warm climates, TRF in the midlands, subdeciduous tropical forest (SDTF) combined with SV, A, and livestock areas; contains nine
ADVCs. Zone 3: 1,001 to 1,500 masl, with humid subtropical climates, MCF vegetation,
mixed with small fragments of highland TRF, SV, and to a lesser extent A; contains four
ADVCs. Zone 4: >1,501 masl, with temperate and humid climates and temperate pine-oak
forests (P-OF) mixed with small fragments of MCF, SV, and A; contains three VCAs and
one ADVC (Fig. 1).
Obtaining records
The records used for this study came from four sources:
1. Primary data collection. The collection of specimens was carried out by four research
teams, led by the authors. Approximately 40 visits were made to the study area, around
four per year, with an average of three consecutive days each, covering both the rainy and
dry seasons, from the year 2010 to 2020. During each visit, efforts were made to cover
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
4/30
the widest area both inside and outside the ADVCs, considering all altitudinal gradients
present, and changing sampling sites daily.
Conventional sampling techniques were used for different mammal groups: small
mammals (<100 g), such as shrews and rodents; bats; and medium to large mammals
(>101 g) (Medellín, 1994). During each visit, small mammals were captured using an
average of 100 Sherman traps (7.6 × 8.9 × 22.5 cm) baited with a mixture of peanut butter,
vanilla extract, and oats. The traps were set daily along two 500 m linear transects, either
within the vegetation or near water bodies, with a 10 m spacing between each trap. The
sampling effort was 2,171 trap-nights per year of work. Additionally, 100 pitfall traps were
placed during each sampling period at 2 m intervals in areas with leaf litter and near fallen
logs, with a depth of 30 cm. For both cases, the traps were set in the afternoon and checked
the following morning.
Bats were captured using mist nets (12 × 2.6 m). During each visit, an average of three
nets were set up in locations near water bodies or within the vegetation. The nets remained
open for eight hours each night, over three consecutive days. The sampling effort per site
was calculated by multiplying the length and width of the mist nets by the number of hours
they were open, in addition to the number of nights and the number of nets used. The
result was expressed as m2 net/hour based on the method proposed by Medellín (1994). The
total sampling effort per year was 1,123 m of net in 96 h, divided into 12 nights sampling.
Thus, the sampling effort was 26,880 m of net per night.
For small mammals and bats, once captured, somatic measurements, reproductive
condition, weight, sex, and age data were obtained. Most of the specimens were released
at the same capture site, except for a minimum number of individuals that were
collected and prepared as museum specimens using taxidermy techniques following the
recommendations of Hall (1981). Subsequently, they were deposited in the Mastozoological
Collection of the Centro Interdisciplinario de Investigación para el Desarrollo Integral
Regional, Unidad Oaxaca (OAX.MA.026.0497). Specimens were collected under a scientific
collection permit issued by the Mexican Ministry of Environment and Natural Resources
(FAUT-0037; SEMARNAT).
For medium to large mammals, two randomly distributed linear transects of
approximately 2.5 km in length were traversed in each locality to search for signs (tracks
and feces) during each visit. The transects were walked daily by two observers. Once
signs were located, data on tracks was collected (geographic location, length and width
measurements), photographs were taken, and plaster casts were made. To complete the
inventory, four Tomahawk-type traps with double folding doors (24 × 6 × 6 inches) were
used, baited with ripe fruits and sardines. The traps were placed within the vegetation and
near water bodies on the first day of work and checked daily in the morning. In case of
any capture, photographs of the individual were taken, and data on species, sex, age, and
if possible, somatic measurements was recorded. All specimens were released at the same
capture site.
For all collection sites, geographic coordinates and elevation were obtained using a
Global Positioning System (GPS) with the WGS84 datum.
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
5/30
2. Databases. We obtained records of wild mammals in museums and scientific
collections; five domestic: la Colección Nacional de Mamíferos (CNMA), la Colección
de la Escuela Nacional de Ciencias Biológicas del IPN (ENCB), la Colección del Museo de
Zoología de la Facultad de Ciencias de la UNAM (MZFC), la Colección de la Universidad
Autónoma Metropolitana-Iztapalapa(UAMI) y la Colección del Centro Interdisciplinario
de Investigación para el Desarrollo Integral Regional, Unidad Oaxaca (CIIDIR-OAX.), IPN
(OAXMA). The foreign collections were ten: Field Museum Natural History (FMNH),
American Museum of Natural History(AMNH), Texas A&M University (TWWC), Angeles
County Museum (LACM), Museum of Zoology, University of Michigan (UMMZ), Texas
Tech University(TTU), University of New Mexico, Museum of Southwestern Biology
(MSB), Carnie Museum of Natural History (CM), University of Florida, Florida Museum
of Natural History (UF) y Natural History Museum, Kansas University (KU). Data were
also obtained from the Global Biodiversity Information Facility (GBIF) portal.
3. Literature review. A review of the scientific literature was carried out in databases
including Scopus, Scielo, Redalyc, Google Scholar, and Elsevier for the years 1969–2022. We
use the keywords ‘‘mammals’’, ‘‘mamíferos’’ or ‘‘Chinantla’’. Topics such as distribution,
new records of species, and expansion of taxa distribution areas were reviewed. Each
scientific article discovered underwent a meticulous review to ascertain the presence of the
required information. After this evaluation, the ensuing data was extracted: municipality,
type of vegetation, and species.
4. Community monitoring. The community monitoring was done by the local
inhabitants. The authorities, as well as the residents of each community where the
camera traps were deployed, provided their endorsement to the National Commission
of Protected Natural Areas (CONANP). We formally request the information that has been
generated through community monitoring within the Chinantla ADVCs from CONANP
(DRFSIPS-0095-2019). We have carefully reviewed all the photos and videos captured
during the monitoring conducted between 2011 and 2014, with the aim of creating a
database containing independent events (see details below). Community monitors placed
5 camera trap models (Bushnell. n = 97; Moultrie; n = 26; Wildview, n = 3; Ltl Acorn,
n = 2; and Stealth Cam, n = 1). The cameras were programmed to operate 24 h a day and
to capture photos (1–5 photos) and/or videos (10–30 s long). The traps were placed on
trees or stakes 10–40 cm above the ground, generally one meter from the roads where the
monitors had observed fauna or tracks. We use for the analysis only the independent events:
(1) consecutive photographs of different individuals of the same or different species, (2)
consecutive photographs of individuals of the same species taken more than 24 h apart, (3)
nonconsecutive photos of individuals of the same species (O’Brien, Kinnaird & Wibisono,
2003). Our analysis used data from 129 camera trapping stations over a four-year period
(2011–2014) in 18 indigenous communities in the region. The total sampling effort was of
4,373 trap-nights; 2,257 in Zone 1 (61 camera traps), 1,354 in Zone 2 (45 camera traps),
540 in Zone 3 (19 camera traps) and 222 in Zone 4 (four camera traps). The details of dates
and time in which the camera traps in the field can be observed in Fig. S1.
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
6/30
Data analysis
The collected specimens were identified using specialized guides (Ceballos & Oliva,
2005; Aranda-Sánchez, 2012; Álvarez Castañeda, Álvarez & Gonzáles-Ruiz, 2017). The
nomenclature was updated following Ramírez-Pulido et al. (2014), with some recent
modifications. Specialized literature (Hall, 1981; Ceballos & Oliva, 2005; Carraway, 2007;
Briones-Salas, Cortés-Marcial & Lavariega, 2015) was consulted to identify taxa endemic to
Mexico and Oaxaca.
Species richness was counted as the total number of species recorded in the entire region
and the four zones. We created species accumulation curves for species richness based on
rarefaction and extrapolation (Chao & Jost, 2012) using the program iNEXT (Chao, Ma &
Hsieh, 2022).
Beta diversity was obtained using the Jaccard qualitative similarity index; this index
compares species communities between two sites to determine which species are shared
and which are distinct. Using this measure, we assess the disssimilarity between pairs of
communities for all mammals, small mammals, bats, and medium to large mammals
from the four sites and ranged from 0 (shared species between two sites) and 1(sites do
not have the same composition). We measured total β diversity and the turnover and
nestedness components between zones based on the Jaccard index (Baselga et al., 2018).
We calculated: (1) total β diversity (βju), (2) turnover β diversity (βtu), and (3) nestedness
β diversity (βne). These parameters were computed using the betapart package (Baselga et
al., 2018) in R (version 3.3.3; R Core Team, 2017), utilizing the Incidence-based pair-wise
dissimilarities function, beta.pair. Additionally, we employed the unweighted pair group
method for arithmetic averages (UPGMA). The analyzes were performed in the program
PAST.
Conservation and protection statuses for the species were recorded based on the IUCN
Red List (IUCN, 2022), the appendices of the CITES (CITES, 2013), and NOM-059SEMARNAT-2010 (SEMARNAT, 2010).
RESULTS
Species richness
A total of 134 species were recorded for the entire region, comprising 11 orders, 26
families, and 86 genera, representing 62%, 100%, 89.6%, and 72.8%, respectively, of all
the mammals in the state of Oaxaca (Table 1). The orders with the highest number of
species were Chiroptera (n = 52) and Rodentia (n = 38). Only one species was recorded in
each of the following orders: Cingulata, Pilosa, Primates, and Perissodactyla (Table 1). By
categories, small mammals accounted for 41 species, bats for 52, and medium and large
for 41. Seventy-three species were recorded during collection and 26 through community
monitoring; 103 and 54 species records were recovered from databases and literature
search (Alfaro, García-García & Santos-Moreno, 2006; Ibarra et al., 2011; Lira-Torres et al.,
2006; Ortiz-Martínez et al., 2012; Perez-Lustre, Contreras-Diaz & Santos-Moreno, 2006; Del
Rio-García et al., 2014), respectively (Table 1; Fig. 2). In terms of the types of vegetation
cover, the highest species richness was recorded in the Pine Oakforest (n = 88), followed
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
7/30
Table 1 Terrestrial mammals recorded in La Chinantla Oaxaca, Mexico.
Taxonomic category
Size
Record type
Zone
Vegetation type
Year
NOM
IUCN
Caluromys derbianus
(Waterhouse, 1841)
M-L
CM
1
TRF
2012
A
LC
Didelphis marsupialis
Linnaeus, 1758
M-L
C, D, L
1, 2, 3
MCF, SDTF, TRF
1964–2015
LC
Didelphis virginiana
Kerr, 1792
M-L
C, D, L
1, 2, 3
MCF, P-OF, SDTF, TRF
1901–2016
LC
Marmosa mexicana
Merriam, 1897
S
C, D
2, 3, 4
MCF, P-OF, TRF
1962–2005
LC
Philander opossum
(Linnaeus, 1758)
M-L
CM, D
1, 2, 3
MCF, SDTF, TRF
1962–2014
LC
M-L
C, CM, L
1, 2, 3
MCF, SDTF, TRF
2005–2015
LC
M-L
CM, D, L
1, 2, 3
MCF, SDTF, TRF
1990–2014
P
LC
Cryptotis berlandieri
(Baird, 1858)
S
C
4
P-OF
2009
Pr
LC
Cryptotis goldmani
(Merriam, 1895) MX
S
D
4
TRF
1972
Pr
LC
Cryptotis magnus
(Merriam, 1895)
OAX
S
D
1, 2, 3, 4
MCF, P-OF, TRF
1959–1991
Pr
VU
Cryptotis mexicanus
Coues, 1877 MX
S
D, C
3, 4
MCF, P-OF
1964–2009
Sorex macrodon
Merriam, 1895
S
D
3
MCF
1969–1975
Sorex saussurei
Merriam, 1892
S
D
3, 4
MCF
1964–1986
LC
Sorex ventralis
Merriam, 1895
S
D
3
MCF
1995
LC
Sorex veraecrucis
Jackson, 1925
S
D, C
3
MCF, P-OF, TRF
1964–1993
A
LC
Sorex veraepacis
Alston, 1877
S
D, C
3, 4
MCF, P-OF, TRF
1964–2005
A
LC
CITES
Orden Didelphimorphia
Familia Didelphidae
Orden Cingulata
Familia Dasypodidae
Dasypus novemcinctus
Linnaeus, 1758
Orden Pilosa
Familia Myrmecophagidae
Tamandua mexicana
(de Saussure, 1860)
Orden Eulipotyphla
Familia Soricidae
LC
A
VU
(continued on next page)
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
8/30
Table 1 (continued)
Taxonomic category
Size
Record type
Zone
Vegetation type
Year
NOM
IUCN
Balantiopteryx io
Thomas, 1904
B
D, L
1
SDTF. TRF
1962–2006
VU
Balantiopteryx plicata
Peters, 1867
B
C, D, L
1, 4
P-OF, SDTF
1962–2009
LC
Diclidurus albus
Wied-Neuwied, 1820
B
C
1
SDTF
2014
LC
Peropteryx macrotis
(J.A. Wagner, 1843)
B
D
1
SDTF, TRF
1962–1988
LC
Rhynchonycteris naso
(Wied-Neuwied,
1820)
B
D
1
SDTR
1990
Saccopteryx bilineata
(Temminck, 1838)
B
D, C
1,4
P-OF, SDTR, TRF
1962–2014
LC
Molossus aztecus de
Saussure, 1860
B
D
2
SDTR, TRF
1962
LC
Molossus rufus
E.Geoffroy SaintHilaire, 1805
B
D
1, 2
SDTR, TRF
1960–1969
LC
Tadarida brasiliensis (I. Geoffroy SaintHilaire, 1824)
B
D
4
P-OF
1988
LC
Mormoops megalophylla (Peters, 1864)
B
D
1, 3
P-OF, SDTF. TRF
1962–1988
LC
Pteronotus fulvus
Thomas, 1892
B
D
1
TRF
1988
LC
Pteronotus mesoamericanus Smith, 1972
B
C, D
1, 4
P-OF, SDTF, TRF
1960–2009
LC
Pteronotus psilotis
(Dobson, 1878)
B
D
1
SDTF
1969
LC
Anoura geoffroyi
Gray, 1838
B
D, C, L
2, 3, 4
MCF. P-OF, TRF
1964–2009
LC
Artibeus jamaicensis
Leach, 1821
B
D, C, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
1960–2014
LC
Artibeus lituratus
(Olfers, 1818)
B
D, C
1, 3, 4
MCF, P-OF, SDTF, TRF
1962–2009
LC
Carollia perspicillata
(Linnaeus, 1758)
B
D, C
1, 2, 3
MCF, SDTF, TRF,
1960–2014
LC
CITES
Orden Chiroptera
Familia Emballonuridae
Pr
LC
Familia Molossidae
Familia Mormoopidae
Familia Phyllostomidae
(continued on next page)
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
9/30
Table 1 (continued)
Taxonomic category
Size
Record type
Zone
Vegetation type
Year
NOM
Carollia sowelli
R.J. Baker, Solary y
Hoffmann, 2002
Carollia subrufa
(Hahn, 1905)
B
D, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
1962–2006
LC
B
D, C,
1, 4
P-OF, SDTF, TRF
1969–2014
LC
Centurio senex
Gray, 1842
B
D, C, L
1, 3, 4
P-OF, SDTF, TRF
1960–2014
LC
Choeroniscus godmani
(Thomas, 1903)
B
C
4
P-OF
2009
LC
Chiroderma villosum
Peters, 1860
B
D
1
TRF
2001
LC
Chrotopterus auritus
(Peters, 1856)
B
D
2
TRF
1966
LC
Dermanura phaeotis
Miller, 1902
B
D, C
1, 3
MCF, TRF, SDTF
1962–2014
LC
Dermanura tolteca
(Saussure, 1860)
B
D, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
1964–2006
LC
Desmodus rotundus
(E. Geoffroy SaintHilaire, 1810)
B
D, C, L
1, 3, 4
P-OF, SDTF, TRF
1960–2014
LC
Enchisthenes hartii
(Thomas, 1892)
B
L
1, 2
MCF, SDTF
2005–2006
Glossophaga commissarisi Gardner, 1962
B
D, C
1, 2, 4
P-OF, SDTF, TRF
1962–2009
LC
Glossophaga leachii
(Gray, 1844)
B
D, C, L
1, 4
P-OF, SDTF, TRF
1969–2009
LC
Glossophaga morenoi
Martínez y Villa, 1938
MX
B
C
4
P-OF
2009
LC
Glossophaga soricina
(Pallas, 1766)
B
D, C, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
1962–2014
LC
Hylonycteris underwoodi Thomas, 1903
B
D
1,3
MCF, P-OF, SDTF, TRF
1962–1981
LC
Leptonycteris
yerbabuenae*
Martínez y Villa,
1940
B
D, C
1, 4
P-OF, SDTF
1962–2009
NT
Micronycteris microtis
Miller, 1898
B
D
1
SDTF
1962–1969
LC
Mimon cozumelae
Goldman, 1914
B
L
1
SDTF
2006
Platyrrhinus helleri
(Peters, 1866)
B
D
1, 3
SDTF, TRF
1962–1988
LC
Phyllostomus discolor
(J.A. Wagner, 1843)
B
D, L
1, 2
MCF, SDTF
1974–2006
LC
Pr
A
IUCN
CITES
LC
LC
(continued on next page)
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
10/30
Table 1 (continued)
Taxonomic category
Size
Record type
Zone
Vegetation type
Year
NOM
Sturnira hondurensis
Goodwin, 1940
Sturnira parvidens
Goldman, 1917
B
D, C, L
2, 3, 4
MCF, P-OF, TRF
1960–2009
LC
B
D, C, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
1960–2014
LC
Trachops cirrhosus
(Spix, 1823)
B
D
2
TRF
1989
LC
Uroderma bilobatum
Peters, 1866
B
D, C
1
SDTF
1988–2014
LC
Vampyressa thyone
Thomas, 1909
B
L
1
SDTF
2006
LC
Vampyrodes major G.M.Allen, 1908
(Thomas, 1889)
B
D, L
1, 3
SDTF, TRF
1961–2006
LC
Vampyrum spectrum
(Linnaeus, 1758)
B
D, L
1
SDTF, TRF
2005–2006
Eptesicus furinalis
(D’Orbigny y Gervais,
1847)
B
D, C
1
SDTF, TRF
1962–2014
LC
Aeroestes cinereus
(Palisot de Beauvois,
1796)
B
C
3
P-OF
1999
LC
Dasypterus intermedius H. Allen, 1862
B
D
1
TRF
1962–1969
LC
Dasypterus xanthinus
(Thomas, 1897)
B
D
1
TRF
1962
LC
Myotis keaysi J. A.
Allen, 1914
B
D
1, 3
MCF, P-OF, SDTF, TRF
1962–1981
LC
Myotis nigricans
(Schinz, 1821)
B
D, C
1, 3, 4
MCF, P-OF, SDTF
1969–2014
LC
Myotis volans
(H.Allen, 1866)
B
D
1
TRF
1960
LC
Perimyotis subflavus
(F. Cuvier, 1832)
B
D
1
TRF
1983
VU
M-L
D, L
1, 3
MCF, SDTF, TRF
2006–2012
Sylvilagus gabbi (Linnaeus, 1758)
M-L
D
1
TRF
1964
EN
Sylvilagus floridanus
(J. A. Allen, 1890)
M-L
C, L
1, 4
MCF, P-OF, SDTF
2010–2015
LC
P
IUCN
CITES
NT
Familia Vespertilionidae
Orden Primates
Familia Atelidae
Ateles geoffroyi* Kuhl,
1820
P
EN
Orden Lagomorpha
Familia Leporidae
(continued on next page)
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
11/30
Table 1 (continued)
Taxonomic category
Size
Record type
Zone
Vegetation type
Year
NOM
IUCN
Sciurus aureogaster F.
Cuvier, 1829
M-L
C, CM, D, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF,
1962–2015
LC
Sciurus deppei Peters,
1863
M-L
C, CM, D
1, 2, 3, 4
MCF, P-OF, TRF
1964–2015
LC
Heterogeomys hispidus
(Le Conte, 1852)
M-L
L
2
SDTF
2011
LC
Orthogeomys grandis
(Thomas, 1893)
M-L
D
4
P-OF
1969–1981
LC
Heteromys desmarestianus Gray, 1868
S
D, C, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
1962–2006
LC
Heteromys irroratus
(Gray, 1868)
S
C, L
1, 3, 4
P-OF, SDTF, A
2006–2018
LC
M-L
C, D, L
1, 2
SDTF, TRF
1992–2015
M-L
C, CM, D, L
1, 2, 3
A, MCF, SDTF, TRF
1947–2015
CR
M-L
C, CM, D, L
1, 2, 3
MCF, P-OF, SDTF, TRF
1964–2015
LC
Habromys chinanteco
(Robertson y Musser,
1976) OAX
S
C, D
4
MCF, P-OF
1970–2006
CR
Habromys ixtlani
(Goodwin, 1964)
OAX
S
C, D
3, 4
MCF, P-OF
1964–2006
CR
Habromys lepturus
(Merriam, 1898)
OAX
S
D
3, 4
MCF, P-OF
1964–1989
CR
Handleyomys alfaroi
(J. A. Allen, 1891)
S
D
2, 3, 4
MCF, P-OF, TRF
1962–1988
LC
Handleyomys chapmani Thomas, 1898
MX
S
C, D, L
1, 2, 3, 4
A, MCF, PAS, P-OF, SDTF, TRF
1901–2018
VU
Handleyomys melanotis Thomas, 1893
S
D
1, 3
MCF
1962–1972
LC
Handleyomys rostratus Merriam, 1901
S
D
1, 3
P-OK, TRF
1962
LC
Megadontomys
cryophilus (Musser,
1964) OAX
S
C, D
2, 3, 4
MCF, P-OF
1964–2006
EN
CITES
Orden Rodentia
Familia Sciuridae
Familia Geomyidae
Familia Heteromyidae
Familia Erethizontidae
Coendou mexicanus
Kerr, 1792
A
LC
Familia Dasyproctidae
Dasyprocta mexicana
de Saussure, 1860 MX
Familia Cuniculidae
Cuniculus paca (Linnaeus, 1766)
Familia Cricetidae
(continued on next page)
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
12/30
Table 1 (continued)
Taxonomic category
Size
Record type
Zone
Vegetation type
Year
NOM
IUCN
Microtus mexicanus
(Saussure, 1861)
Microtus oaxacensis
Goodwin, 1966 OAX
S
C, D
3, 4
P-OF
1962–1999
LC
S
C, D
3, 4
MCF, P-OF
1964–2006
EN
Nyctomys sumichrasti
(de Saussure, 1860)
S
D
1, 3, 4
MCF, P-OF, SDTF, TRF
1962–1991
LC
Oligoryzomys fulvescens (de Saussure,
1860)
S
C, D, L
1, 2, 3
MCF, P-OF, TRF
1962–2005
LC
Oryzomys couesi (Alston, 1877)
S
D
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
1961–1989
LC
Peromyscus aztecus
(de Saussure, 1860)
S
C, D, L
2, 3, 4
A, MCF, P-OF
1959–2018
LC
Peromyscus beatae
Thomas, 1903 MX
S
C, D
3, 4
A, P-OF
2018
LC
Peromyscus furvus J.
A. Allen y Chapman,
1897 MX
S
D
3
MCF, P-OF
1974
DD
Peromyscus gratus
Merriam, 1898
S
C
4
P-OF
1999–2005
LC
Peromyscus levipes
Merriam, 1898 MX
S
D, C
3, 4
MCF, P-OF
1963–2005
LC
Peromyscus labecula
(Wagner, 1845)
S
D
3
P-OF
1964
LC
Peromyscus
melanocarpus
Osgood, 1904 OAX
S
C, D
2, 3, 4
MCF, P-OF, TRF
1959–2015
EN
Peromyscus mexicanus
(de Sausure, 1860)
S
C, D, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
1962–2015
LC
Reithrodontomys fulvescens J.A. Allen,
1894
S
D
2, 4
P-OF, TRF
1964–1969
LC
Reithrodontomys mexicanus (de Saussure,
1860)
S
C, D
2, 3, 4
MCF, P-OF, TRF
1962–2015
LC
Reithrodontomys microdon Merriam, 1901
S
C, D
3, 4
A, MCF, P-OF
1962–2018
LC
Reithrodontomys
sumichrasti (de Saussure, 1860)
S
C, D
3, 4
MCF, P-OF, TFR
1968–1999
LC
Sigmodon hispidus Say
and Ord, 1825
S
D, L
1, 2, 3
MCF, P-OF, SDTF, TRF
1964–2006
LC
Sigmodon mascotensis
J.A. Allen, 1897
S
D
1
TRF
1987–1988
LC
Sigmodon toltecus (de
Saussure, 1860)
S
D
1, 3
P-OF, TRF
Tylomys nudicaudus
(Peters, 1866)
S
D, L
1, 2, 3
MCF, P-OF, SDTF, TRF
CITES
LC
1964–2006
LC
(continued on next page)
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
13/30
Table 1 (continued)
Taxonomic category
Size
Record type
Zone
Vegetation type
Year
NOM
IUCN
CITES
Puma yagouaroundi
(E. Geoffroy SaintHilaire, 1803)
M-L
CM, D, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
1962–2014
A
LC
I
Leopardus pardalis
(Linnaeus, 1758)
M-L
C, CM, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
2010–2015
P
LC
I
Leopardus wiedii
(Schinz, 1821)
M-L
C, CM, L
1, 2, 3
MCF, P-OF, SDTF, TRF
2005–2016
P
NT
I
Lynx rufus (Schreber,
1777)
M-L
L
4
P-OF
2010
LC
Herpailurus concolor
(Linnaeus, 1771)
M-L
C, CM, L
1, 2, 3, 4
MCF, P-OF, TRF
2003–2015
LC
II
Panthera onca* (Linnaeus, 1758)
M-L
C, CM, D, L
1, 2, 3
MCF, P-OF, SDTF, TRF
1998–2014
NT
II
Canis latrans Say,1822
M-L
CM, C, L
1, 4
MCF, P-OF, TRF
2013–2015
LC
Urocyon cinereoargenteus (Schreber, 1775)
M-L
C, L
2, 3, 4
MCF, P-OF, TRF
2003–2015
LC
Conepatus leuconotus
(Lichtenstein, 1832)
M-L
L
2
SDTF
2011
LC
Conepatus semistriatus (Boddaert, 1785)
M-L
CM, L
1, 2, 3, 4
P-OF, TRF
2010–2014
LC
Mephitis macroura
Lichtenstein, 1832
M-L
C, CM
1, 3, 4
MCF, P-OF, SDTF, TRF
2003–2015
LC
Spilogale angustifrons
A. H. Howell, 1902
M-L
C
4
P-OF
1999
LC
Eira barbara (Linnaeus, 1758)
M-L
CM, C, D, L
1, 2, 3
MCF, P-OF, SDTF, TRF
1965–2016
P
LC
Galictis vittata (Schreber, 1776)
M-L
CM
1
TRF
2013–2014
A
LC
Lontra longicaudis*
(Olfers, 1818)
M-L
C
1
MCF,
2009
A
NT
Mustela frenata Lichtenstein, 1831
M-L
C, CM, D
1, 2, 4
P-OF, TRF
1961–2014
Bassariscus astutus
(Lichtenstein, 1830)
M-L
C, L
4
MCF, P -OF
2010–2015
A
LC
Bassariscus
sumichrasti (de
Saussure, 1860)
M-L
CM, D
3
MCF, P -OF
1969–2014
Pr
LC
Nasua narica (Linnaeus, 1766)
M-L
C, CM, L
1, 2, 3
MCF, P-OF, SDTF, TRF
2005–2016
A
LC
Potos flavus (Schreber, 1774)
M-L
CM, D, L
1, 2, 3
P-OF, TRF, SDTF
1964–2012
Pr
LC
Procyon lotor (Linnaeus, 1758)
M-L
CM, C, D, L
1, 2, 3, 4
P-OF, TRF, SDTF
1964–2014
Orden Carnívora
Familia Felidae
P
Familia Canidae
Familia Mephitidae
Familia Mustelidae
I
LC
Familia Procyonidae
LC
(continued on next page)
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
14/30
Table 1 (continued)
Taxonomic category
Size
Record type
Zone
Vegetation type
Year
NOM
IUCN
M-L
C, CM, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
2005–2015
LC
Mazama temama
(Kerr, 1792)
M-L
CM, C, D, L
1, 2, 3, 4
MCF, P-OF, SDTF, TRF
1969–2016
DD
Odocoileus virginianus
*
(Zimmermann,
1780)
M-L
C
2, 4
MCF, P-OF, TRF
2015
LC
M-L
L
1
MCF
2004
CITES
Orden Artiodactyla
Familia Tayassuidae
Pecari tajacu (Linnaeus, 1758)
Familia Cervidae
Orden Perissodactyla
Familia Tapiridae
Tapirus bairdii* (Gill,
1865)
P
EN
I
Notes.
Keys: Size/class: S, small; B, bats; M-L, medium-large; Record type: D, Database; C, Collection; L, Literature; CM, Community monitoring; Zone 1, 0–400 masl; Zone 2, 401–
1,000 masl; Zone 3, 1,001–1,500 masl; Zone 4, >1,501 masl; Vegetation: MCF, Montane cloud forest; TRF, Tropical raiforest; P-OF, Pine-oak forest; SDTF, Sub-deciduous tropical forest; A, Agriculture; PAS, Pastures; Year, Year of first and last documented record; Conservation Status: IUCN: CR, Critically Endangered; EN, Endangered; VU, Vulnerable; NT, Near Threatened; EW, Extinct in the wild. CITES: I, II, III. NOM (Official Mexican Standard NOM-059-SEMARNAT-2010): E, Probably extinct in the wild; P, Endangered; A, Threatened; PR, Subject to special protection; Endemism: MX, Endemic to Mexico; OAX, Endemic to Oaxaca.
*Priority species for conservation present in Oaxaca are marked with an asterisk (*) according to SEMARNAT (2014).
Figure 2 Frequency of records of mammals (small, medium and large and bats) according to Zone,
record type and vegetation in La Chinantla, Oaxaca, Mexico. Zones: Z1, Zona 1; Z2, Zona 2; Z3, Zona 3;
Z4, Zona 4; Record type: D, Database; C, Collection; L, Literature; CM, Community monitoring; Vegetation: MCF, Montane cloud forest; TRF, Tropical raiforest; P-OF, Pine-oak forest; SDTF, Sub-deciduous
tropical forest; A, Agriculture; Pas, Pastures.
Full-size DOI: 10.7717/peerj.16345/fig-2
by the Tropical Rainforest (n = 85; Table 1; Fig. 2). For small mammals, five families were
recorded—Cricetidae had the most species (n = 29), while Geomyidae and Heteromyidae
had fewer (two species each). Five families of bats were recorded, with Phyllostomidae
presenting the highest number of species (n = 31) and Molossidae the lowest(n = 3). The
medium and large mammals group contained 17 families—Felidae had most species (n = 6;
Table 1).
A higher species richness was recorded in Zone 1 for the assemblage of mammals
(n = 89), bats (n = 43), and medium to large mammals (n = 32). However, in the case of
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
15/30
Figure 3 Rarefaction/Extrapolation curves of mammal species richness in regions of La Chinantla,
Oaxaca. Z1, Zone 1; Z2, Zone 2; Z3, Zone 3; Z4, Zone 4.
Full-size DOI: 10.7717/peerj.16345/fig-3
Figure 4 Rarefaction/Extrapolation curves for (A) Small mammals (B) Bats and (C) Medium-Large
mammals in La Chinantla, Oaxaca. Z1, Zone 1; Z2, Zone 2; Z3, Zone 3; Z4, Zone 4.
Full-size DOI: 10.7717/peerj.16345/fig-4
small mammals, species richness was Zone 3 (n = 35 and Zone 4; n = 29) (Figs. 3 and 4,
Table 2).
For all mammal groups, species extrapolation curves suggest that Zone 1 and 3 have
similar species diversity, higher than Zone 2 and 4, although, between Zone 1 and Zone
4, confidence intervals do not overlap (Fig. 3). For small mammals, the zones with higher
altitude (Zone 3 and Zone 4) showed the highest species richness, while the lower altitude
zones (Zone 1 and Zone 2) were more similar in their composition (Fig. 4A). For bats, the
highest species diversity was recorded in the lower zone (Zone 1, n = 43), while the diversity
was lower in higher zones, with overlap was only between Zone 1 and Zone 4, unlike to
Zone 2 and Zone 3, that it was statistically different (Fig. 4B). The curves for medium to
large mammals suggest that the lower altitude zones (Zone 1 and Zone 2) are more similar
and have higher diversity, while the higher altitude zones (Zone 3 and Zone 4) show lower
species diversity, although, all confidence intervals overlap (Fig. 4C). It is worth noting
that neither the diversity interpolation nor the extrapolation curves reached an asymptote
for any of the four groups in any of the zones, indicating the need for additional sampling
(Figs. 3 and 4).
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
16/30
Table 2 Beta diversity total and turnover and nestedness components of the different groups of wild mammals in the four zones of La Chinantla, Oaxaca. The values in bold indicate the total number of species in each zone, the number of exclusive species is noted in brackets. The Jaccard dissimilarity index values are italicized, and below it, in normal font, is the number of species shared between each pair of zones.
Zone 1
Zone 2
Zone 3
Zone 4
All mammals beta.total
Zone 1
89 (19)
0.61
0.55
0.70
Zone 2
41
57 (3)
0.52
0.66
Zone 3
52
44
79 (7)
0.55
32
46
69 (11)
Zone 4
36
All mammals beta.turnover
Zone 2
0.44
Zone 3
0.51
0.37
Zone 4
0.65
0.61
All mammals beta.nestedness
Zone 2
0.17
Zone 3
0.04
0.15
Zone 4
0.06
0.05
0.05
0.50
Small mammals beta.total
Zone 1
14 (1)
0.64
0.64
0.81
Zone 2
8
15 (0)
0.62
0.65
Zone 3
13
14
35 (5)
0.41
12
24
29 (4)
Zone 4
7
Small mammals beta.turnover
Zone 2
0.60
Zone 3
0.13
0.22
Zone 4
0.67
0.40
Small mammals beta.nestedness
Zone 2
0.04
Zone 3
0.51
0.40
Zone 4
0.14
0.25
0.08
0.33
Bats beta.total
Zone 1
43 (17)
0.79
0.65
0.67
Zone 2
10
15 (2)
0.69
0.71
Zone 3
16
8
19 (1)
0.62
8
11
21 (3)
Zone 4
16
Bats beta.turnover
Zone 2
0.50
Zone 3
0.27
0.64
Zone 4
0.38
0.64
Bats beta.nestedness
Zone 2
0.29
Zone 3
0.38
0.06
Zone 4
0.28
0.08
0.59
0.03
(continued on next page)
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
17/30
Table 2 (continued)
Zone 1
Zone 2
Zone 3
Zone 4
Medium–large mammals beta.total
Zone 1
32 (5)
0.34
0.32
0.65
Zone 2
23
27 (2)
0.24
0.63
Zone 3
23
22
25 (1)
0.66
Zone 4
13
12
11
19 (4)
Medium–large mammals beta.turnover
Zone 2
0.21
Zone 3
0.15
0.21
Zone 4
0.43
0.50
0.56
Medium–large mammals beta.nestedness
Zone 2
0.14
Zone 3
0.17
0.03
Zone 4
0.21
0.13
0.10
Beta diversity
Considering all mammal species, 18 were shared across the four zones (14%). In Zone 1,
19 species were exclusive, while in Zone 2, only three species were exclusive. Zones 1 and
4 had the highest degree of species dissimilarity (DI = 0.70; Table 2). For small mammals,
five were shared across the four zones. In Zone 3, five species were exclusive, while Zone 2
had no exclusive species. The highest dissimilarity index for small mammals was observed
between Zones 1 and 4 (DI = 0.81). For the bat, five species were shared across the four
zones. Zone 1 recorded the highest number of exclusive species (n = 17), while only one
exclusive species was recorded in Zone 3. Zones 1 and 2 presented the highest value of
dissimilarity (SI = 0.79). Finally for the medium to large mammal, eight species were shared
among the four zones. In the lower zone (Zone 1), five exclusive species were recorded,
while in Zone 3, only one exclusive species was registered. Zones 3 and 4 exhibited the
highest dissimilarity index (DI = 0.66; Table 2). In general terms, it was observed that the
species turnover component had a much greater impact on the total beta value for the four
groups compared to the nestedness component.
For the assemblage of mammals and small mammals, the similarity dendrograms
showed two groups, one for species from the highest altitude zone (Zone 4) and the other
containing the remaining zones. For bats, species from Zone 2 are separated from the other
zones. For medium to large mammals, species from Zones 2, 3, and 4 form a separate
group from those in the lower altitude zone (Zone 1) (Fig. 5).
State of conservation
Twenty-four species are listed in NOM-059 (SEMARNAT, 2010), 18 in the list of the
International Union for Conservation of Nature (IUCN), and seven in CITES (Table 1).
The first two lists shared seven species: Cryptotis magnus (Zone 1–4), Vampyrum spectrum
(Zone 1), Ateles geoffroyi (Zone 1 and 3), Leopardus wiedii (Zone 1, 2 and 3), Panthera onca
(Zone 1, 2 and 3), Lontra longicaudis (Zone 1), and Tapirus bairdii (Zone 1) (Table 1).
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
18/30
Figure 5 Jaccard dissimilarity among mammal assemblages considering all species, bats, small mammals, and medium and large-sized mammals in La Chinantla, Oaxaca.
Full-size DOI: 10.7717/peerj.16345/fig-5
DISCUSSION
Species richness and diversity
Our results highlight the value of indigenous lands for mammal conservation, specifically
through community conservation areas. Despite the absence of formal protected natural
areas in the region, the mammalian richness in this Mexican region remains remarkably
high. La Chinantla ranks as the second location in Mexico with the highest mammalian
richness (n = 134), below La Selva Zoque, which is located across three states in southern
Mexico: Oaxaca, Chiapas, and Veracruz (n = 149) (Lira-Torres, Galindo-Leal & BrionesSalas, 2012). Please note that La Selva Zoque (∼1,000,000 ha) is considerably larger than
La Chinantla (∼58,765.78 ha)(CONANP-Oficina Chinantla). Nevertheless, the recorded
species count is nearly identical, underscoring the significance of indigenous territories
for mammalian conservation. It is important to point out that mammalian richness in
La Chinantla is greater than at other highly biodiverse sites in Mexico, such as La Selva
Lacandona, Chiapas (n = 125) (March & Aranda, 1992); La Reserva de la Biósfera el
Triunfo, Chiapas (n = 112) (Espinoza-Medinilla, Anzures Dadda & Cruz-Aldan, 1998); and
La Sepultura Biosphere Reserve, Chiapas (n = 98) (Espinoza-Medinilla et al., 2004).
The great richness of species in La Chinantla is the result of the diversity of ecosystems
found there, such as the Montane cloud forest, Tropical rainforest, and Pine-Oak Forest,
which in most of our coverage were in a good state of conservation (Pennington & Sarukhán,
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
19/30
2005). Several factors may be contributing to this, such as the inaccessibility to certain areas,
but above all, the conservation work that the residents of La Chinantla carry out through
conservation zones, such as the ADVC (Acevedo, Lugo Espinosa & Ortiz Hernández, 2021).
In addition to the strategies employed by the Chinantecos to safeguard their territory,
they establish various rules of utilization and access within the framework of an internal
regulation. These rules include restrictions on hunting, extraction of plant species, removal
of vegetation cover for agricultural and livestock activities, among others (Anta-Fonseca &
Mondragón-Galicia, 2006).
Species richness was higher in the lower zone (Zone 1), mainly comprising well-preserved
Tropical Rainforest (TRF) and remnants of TRF with secondary vegetation (Pennington &
Sarukhán, 2005; Meave et al., 2017). These vegetation types are well-represented within the
10 ADVCs present in the area, which likely contributes to the presence of many species.
Zone 3 exhibited the second highest richness, despite having the lowest tree cover in the
region (INEGI, 2016). However, there are numerous well-preserved TRF remnants and
different successional stages interspersed with agricultural sites.
Bats had the greatest species richness, much of it in the lower zone. This could be
explained by high coverage of tropical rainforest and fruit crops, where the species have been
observed to find food and shelter in other tropical environments in America (Lira-Torres,
Galindo-Leal & Briones-Salas, 2012; Briones-Salas, Lavariega & Lira-Torres, 2019). On the
other hand, several species were recorded only in this area, some of which are considered
‘‘rare’’ such as Balantiopteryx io, Diclidurus albus, Micronycteris microtis, Mimon cozumelae,
and Vampyrum spectrum. Some studies have shown that the presence of these species are
good indicators of low habitat disturbance (Fenton et al., 1992; Wilson, Ascorra & Solari,
1996; Castro-Luna & Galindo-González, 2012). It is important to highlight that some bats
in La Chinantla are also distributed in North America (e.g., Dasypterus mexicanus, D.
xanthinus, and Myotis volans), South America (e.g., Balantiopteryx plicata, D. albus, and
Saccopteryx bilineata), and Mesoamerica (e.g., B.io, Dermanura tolteca and Glossophaga
leachii) (Villa & Cervantes, 2003). The area’s combination of tropical, semitropical, and
temperate environments contributes to this high diversity of bats and has been observed
elsewhere in Mexico (Briones-Salas & Sánchez-Cordero, 2004).
Small mammals exhibited the second highest species richness, dominated by species
from the family Cricetidae, which can establish themselves in a wide range of environments,
including disturbed sites (Linzey et al., 2012; Martin-Regalado et al., 2019). Another highly
represented family in La Chinantla was Soricidae, with nine species. Four of these species
were collected in sites with high humidity and good conservation status, primarily PineOak Forest and Montane Cloud Forest, as documented by other authors (Carraway, 2007).
Unlike bats, the highest species richness of small mammals was recorded in higher altitude
zones. In fact, over half of the species ( n = 30) were exclusively found in these areas,
including six species endemics to Oaxaca. Some authors have found high rodent diversity
at elevated altitudes (Mccain, 2005; Martin-Regalado et al., 2019). It is worth mentioning
that the six endemic species from Oaxaca, such as Habromys chinanteco and H. ixtlani, are
found in sites protected by indigenous communities. The pattern observed for rodents is
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
20/30
similar to that observed in the Andes of Peru and Chile, where speciation is proposed to
have occurred in the highlands (Marquet, 1994).
Regarding medium and large mammals, most species were recorded in the lowland
and warm areas of La Chinantla, although there was some overlap in confidence intervals
between Zones 1, 2, and 3, indicating that their assemblages are very similar. Several
species in Zone 1 were recorded in agricultural areas and secondary vegetation, such as
Odocoileus virginianus, Procyon lotor, Nasua narica, and Herpailurus yagouaroundi, many
of which are common and tolerant to disturbance (Briones-Salas, Lavariega & Lira-Torres,
2019). Similar findings have been described in the Istmo de Tehuantepec, Oaxaca, Mexico,
in human-modified environments dominated by agricultural and livestock activities
(Cortés-Marcial & Briones-Salas, 2014). It is important to mention that most of these
records were made within VCAs by community monitors, reflecting the crucial role of
indigenous communities in biodiversity knowledge and conservation.
The presence of all six species of felids distributed in Mexico is noteworthy, particularly
Panthera onca, which has a comparable density to the Eden Reserve located in Yucatan and
northern Sonora (Rosas-Rosas & Bender, 2012; Ávila Nájera et al., 2015; Lavariega et al.,
2020). Meanwhile, although no population studies have been conducted on Puma concolor,
the species has been recorded throughout La Chinantla (Figel et al., 2009; Silva-Magaña
& Santos-Moreno, 2020). On the other hand, the bobcat, Lynx rufus, was found in the
Pine-Oak Forest at the higher parts of the region. Another species of interest is Ateles
geoffroyi, which was found in Zones 1 and 3 in the Tropical Rainforest and Montane
Cloud Forest (Briones-Salas et al., 2006); even in the lowest zone, an ADVC called ‘‘Cerro
Chango’’ was established due to the presence of groups of this species. Zone 3 had the
lowest species richness, with only a few species recorded: the pocket gopher Orthogeomys
grandis, the bobcat L. rufus, the hog-nosed skunk Spilogale angustifrons, and the ringtail
Basariscus astutus.
Similarity indices
The greatest similarities between the four groups of mammals were recorded between
neighboring areas. This indicates that there is an exchange of species between nearby zones.
The analysis of beta diversity components indicates that the species turnover component
was larger than nestedness, contributing to beta diversity in the Chinantla region. The
intermediate zones may function as corridors that connect the upper and lower parts of La
Chinantla. The landscape of the region presents a mosaic composed of Tropical Rainforest,
Montane Cloud Forest, small areas of coffee plantations, cultivated areas, and pastures that
may allow organisms move through.
Conservation
The Chinantecos play a crucial role as custodians of endangered species, as 33% of
the total registered species are classified under some level of risk. For three of these
species, La Chinantla is the northern limit of their distribution in the American
continent with adequate habitat to maintain populations: the tapir Tapirus bairdii
(Vivas-Lindo et al., 2020); the spider monkey A. geoffroyi (Vidal-García & Serio-Silva, 2011;
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
21/30
Calixto-Pérez et al., 2018); and the spectral vampire V. spectrum, which finds refuge sites in
the remnants of the region’s Tropical Rain Forest.
The study region is also a potential habitat for four medium-sized cats—H. yagouaroundi,
Leopardus pardalis, Leoparuds weidii, and L. rufus—and for the last one, the zone represents
its most southeastern distribution area (Monroy-Vilchis, Zarco-González & Zarco-González,
2019). This area has a substantial population of P. onca, the largest of these cats (Lavariega
et al., 2020); it is also a biological corridor that connects populations in north of the country
(Rodríguez-Soto et al., 2011).
La Chinantla region has a mosaic of landscapes that makes it heterogeneous in terms of
vegetation, topography, and climate; this region also has high species richness and diversity
and should be considered in state and national conservation policies. The establishment of
31 ADVCs by indigenous communities has significantly contributed to the conservation of
mammals and other taxonomic groups. The Chinantecs who settle in the place have carried
out community monitoring actions over the past 12 years, not only with mammals but other
groups too such as birds (Ortega-Álvarez et al., 2012; Noria-Sánchez, Prisciliano-Vázquez
& Patiño Islas, 2015), amphibians, and reptiles (Simón-Salvador et al., 2021). This has
undoubtedly contributed to the knowledge and conservation of La Chinantla’s wild fauna.
Finally, the ADVCs in the region function as islands of conservation and protection
for germplasm of the native fauna. We believe that strategies such as the establishment of
biological corridors that connect these ADVCs will help enhancing the genetic exchange of
populations and the dispersal of mammals in the area. Our study reveals that beta diversity
is an important component in the region, as there is a high species turnover among
different altitudinal gradients in this mountainous system. This could represent a first step
towards identifying a suitable region for establishing an Archipelago Reserve, as proposed
by other studies in Mexico (Moctezuma, Halffter & Arriaga-Jiménez, 2018; Garcia-Grajales
& Buenrostro-Silva, 2009) and other Central American countries (Anderson & Ashe, 2000).
Archipelago Reserves also take a social approach that coincides with the Chinantecs’
strategies. This approach strengthen species conservation by using a community scheme
through local and regional strategies. In addition, government programs have played an
important role in channeling economic incentives through programs such as payment for
environmental services and ADVCs certification, which make it possible to meet various
conservation objectives. This would greatly support biodiversity, particularly for species
that are endemic to the country and/or are classified in some threat category by national
or international standards. Archipelago reserves are a novel and compelling proposal for
biodiversity conservation as they seek to protect a set of complementary areas, such as
the ADVCs in La Chinantla, which together safeguard an substantial portion of Mexican
biodiversity. Considering the region’s high richness of mammals and other taxonomic
groups, establishing protected areas by indigenous communities can be an alternative to
the lack of officially designated protected areas.
ACKNOWLEDGEMENTS
We thank N. Martín-Regalado for their comments on this manuscript. Special thanks to
the researchers who allowed access to the scientific collection visited.
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
22/30
ADDITIONAL INFORMATION AND DECLARATIONS
Funding
The project was supported by the Secretary of Research and Graduate Studies (SIP:
20220797) of the National Polytechnic Institute. CONANP provided information on
community monitoring in the region. REGA thanks the scholarship (#622396) granted by
the Mexican National Commission of Science and Technology (CONACyT) to pursue her
Ph.D. in Sciences in Management and Conservation of Natural Resources at the CIIDIR,
Oaxaca, Instituto Politécnico Nacional. MB-S thanks the Commission for the Operation
and Promotion of Academic Activities (COFAA) and the Research Incentive Program
(EDI) at Instituto Politécnico Nacional for the fellowship, as well as the National System
of Researchers (SNI) for its recognition. The funders had no role in study design, data
collection and analysis, decision to publish, or preparation of the manuscript.
Grant Disclosures
The following grant information was disclosed by the authors:
Secretary of Research and Graduate Studies of the National Polytechnic Institute: SIP:
20220797.
Mexican National Commission of Science and Technology (CONACyT): #622396.
Commission for the Operation and Promotion of Academic Activities (COFAA) and the
Research Incentive Program (EDI) at Instituto Politécnico Nacional.
Competing Interests
The authors declare there are no competing interests.
Author Contributions
• Miguel Briones-Salas conceived and designed the experiments, performed the
experiments, analyzed the data, prepared figures and/or tables, authored or reviewed
drafts of the article, and approved the final draft.
• Rosa E Galindo-Aguilar conceived and designed the experiments, performed the
experiments, analyzed the data, prepared figures and/or tables, authored or reviewed
drafts of the article, and approved the final draft.
• Graciela E González performed the experiments, authored or reviewed drafts of the
article, and approved the final draft.
• María Delfina Luna-Krauletz performed the experiments, authored or reviewed drafts
of the article, and approved the final draft.
Animal Ethics
The following information was supplied relating to ethical approvals (i.e., approving body
and any reference numbers):
Scientific collection issued by the Secretary of Environment and Natural Resources of
Mexico (FAUT-0037; SEMARNAT).
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
23/30
Field Study Permissions
The following information was supplied relating to field study approvals (i.e., approving
body and any reference numbers):
The Comisión Nacional de Areas Naturales Protegidas approved the study (DRFSIPS0095-2019).
Data Availability
The following information was supplied regarding data availability:
The raw data are available in the Supplemental Files.
Supplemental Information
Supplemental information for this article can be found online at http://dx.doi.org/10.7717/
peerj.16345#supplemental-information.
REFERENCES
Acevedo MA, Lugo Espinosa G, Ortiz Hernández YD. 2021. Percepciones comunitarias
sobre mecanismos de conservación de recursos naturales bajo un enfoque paisajístico
en tres ejidos de la Chinantla, Oaxaca. In: Recuperación transformadora de los
territorios con equidad y sostenibilidad. México City: UNAM-AMECIDER.
Aguilar-Tomasini MA, Martin MD, Speed JDM. 2021. Assessing spatial patterns of
phylogenetic diversity of Mexican mammals for biodiversity conservation. Global
Ecology and Conservation 31:e01834 DOI 10.1016/j.gecco.2021.e01834.
Alfaro AM, García-García JL, Santos-Moreno A. 2006. Mamíferos de los municipios
Santiago Jocotepec y Ayotzintepec, Chinantla Baja, Oaxaca. Naturaleza y Desarrollo
4(1):19–23.
Álvarez Castañeda ST, Álvarez T, Gonzáles-Ruiz N. 2017. Guía para la identificación de
los mamíferos de México. Baltimore: Johns Hopkins University Press.
Anderson RS, Ashe JS. 2000. Leaf litter inhabiting beetles as surrogates for establishing
priorities for conservation of selected tropical montane cloud forests in Honduras,
Central America (Coleoptera; Staphylinidae, Curculionidae). Biodiversity and
Conservation 9:617–653 DOI 10.1023/A:1008937017058.
Anta-Fonseca S, Mondragón-Galicia F. 2006. El Ordenamiento Territorial y los
estatutos comunales: el caso de Santa Cruz Tepetotutla, Usila, Oaxaca. In: Anta S,
Arreola AV, González MA, Acosta J, eds. Ordenamiento Territorial Comunitario:
un debate de la sociedad civil hacia la construcción de políticas públicas. México City:
Secretaría de Medio Ambiente y Recursos Naturales; Instituto Nacional de Ecología;
Instituto para el Desarrollo Sustentable en Mesoamérica, AC. Grupo Autónomo para
la Investigación Ambiental, A.C. Grupo de Estudios Ambientales, A.C. Methodus
Consultora, S, 191–208.
Aranda-Sánchez JM. 2012. Manual para el rastreo de mamíferos silvestres de México.
México City: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad
(CONABIO).
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
24/30
Arriaga L, Espinoza JM, Aguilar CEM, Gómez L, Loa E. 2000. Regiones Terrestres
Prioritarias para México. Available at http://www.conabio.gob.mx/conocimiento/
regionalizacion/doctos/terrestres.html (accessed on 11 April 2021).
Ávila Nájera DM, Chávez C, Lazcano-Barrero MA, Pérez-Elizalde S, Alcántara-Carbajal
JL. 2015. Estimación poblacional y conservación de felinos (Carnivora: Felidae)
en el norte de Quintana Roo, México. Revista de Biologia Tropical 63:799–813
DOI 10.15517/rbt.v63i3.15410.
Baselga A, Orme D, Villeger S, De Bortoli J, Leprieur F, Baselga MA. 2018. Package
‘betapart’. Partitioning beta diversity into turnover and nestedness components.
version, 1(0).
Briones-Salas M, Cortés-Marcial M, Lavariega MC. 2015. Diversidad y distribución
geográfica de los mamíferos terrestres del estado de Oaxaca, México. Revista
Mexicana de Biodiversidad 86:685–710 DOI 10.1016/j.rmb.2015.07.008.
Briones-Salas M, Lavariega MC, Lira-Torres I. 2019. Mammal diversity before the
construction of a hydroelectric power dam in southern Mexico. Animal Biodiversity
and Conservation 42:99–112 DOI 10.32800/abc.2019.42.0099.
Briones-Salas M, Luna Krauletz MD, Marín-Sánchez A, Servín J. 2006. Noteworthy
records of two species of mammals in the Sierra Madre de Oaxaca, México. Revista
Mexicana de Biodiversidad 77:309–310.
Briones-Salas MA, Sánchez-Cordero V. 2004. Mamíferos. In: García-Mendoza A, Ordoñez MDJ, Briones-Salas MA, eds. Biodiversidad de Oaxaca. México City: Instituto
de Biología, UNAM-Fondo Oaxaqueño para la Conservación de la Naturaleza-World
Wildlife Fund, 223–247.
Calixto-Pérez E, Alarcón-Guerrero J, Ramos-Fernández G, Dias PAD, Rangel-Negrín
A, Améndola-Pimenta M, Domingo C, Arroyo-Rodríguez V, Pozo-Montuy G,
Pinacho-Guendulain B, Urquiza-Haas T, Koleff P, Martínez-Meyer E. 2018.
Integrating expert knowledge and ecological niche models to estimate Mexican
primates’ distribution. Primates 59:451–467 DOI 10.1007/s10329-018-0673-8.
Carraway L. 2007. Shrews (Eulypotyphla: Soricida) Of Mexico. Monographs of the
Western North American Naturalist 3:1–91 DOI 10.3398/1545-0228-3.1.1.
Castro-Luna AA, Galindo-González J. 2012. Enriching agroecosystems with fruitproducing tree species favors the abundance and richness of frugivorous
and nectarivorous bats in Veracruz, Mexico. Mammalian Biology 77:32–40
DOI 10.1016/j.mambio.2011.06.009.
Ceballos G, Oliva G. 2005. Los mamíferos silvestres de México. Distrito Federal, México:
Comisión Nacional para el Uso y Conocimiento de la Biodiversidad. Fondo de
Cultura Económica.
Chao A, Jost L. 2012. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547 DOI 10.1890/11-1952.1.
Chao A, Ma K, Hsieh T. 2022. iNEXT online software for interpolation and extrapolation
of species diversity. Available at https://chao.shinyapps.io/iNEXTOnline/.
CONANP. 2020. Áreas Destinadas Voluntariamente a la Conservación. Available at
https://advc.conanp.gob.mx/sample-page/ (accessed on 09 December 2019).
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
25/30
Cortés-Marcial M, Briones-Salas M. 2014. Diversidad, abundancia relativa y patrones de actividad de mamíferos medianos y grandes en una selva seca del Istmo
de Tehuantepec, Oaxaca, México. Revista de Biologia Tropical 62:1433–1448
DOI 10.15517/rbt.v62i4.13285.
De Albuquerque FS, Benito B, Beier P, Assunção Albuquerque MJ, Cayuela L. 2015.
Supporting underrepresented forests in Mesoamerica. Natureza e Conservacao
13:152–158 DOI 10.1016/j.ncon.2015.02.001.
Del Rio-García I, Espinoza-Ramirez M, Luna-Krauletz M, López-Hernández N. 2014.
Diversidad, distribucion y abundancia de mamíferos en Santiago Comaltepec,
Oaxaca, México. Agroproductividad 7:17–23.
Espinosa D, Ocegueda-Cruz S, Luna-Vega I. 2016. Introducción al estudio de la
Biodiversidad de la Sierra Madre del Sur: Una visión general. Biodiversidad de la
Sierra Madre del Sur: Una síntesis preliminar. Ciudad de México, México: UNAM
528.
Espinoza-Medinilla E, Anzures Dadda A, Cruz-Aldan E. 1998. Mamíferos del a Reserva
el Triunfo, Chiapas. Revista Mexicana de Mastozoología 3:79–94.
Espinoza-Medinilla E, Cruz E, Lira I, Sánchez I. 2004. Mammals of La Sepultura
biosphere reserve, Chiapas, México. Revista de Biologia Tropical 52:249–259
DOI 10.15517/rbt.v52i1.14941.
Fenton MB, Acharya L, Audet D, Hickey MBC, Merriman C, Obrist MK, Syme DM,
Adkins B. 1992. Phyllostomid bats (Chiroptera: Phyllostomidae) as indicators of
habitat disruption in the neotropics. Biotropica 24:440–446 DOI 10.2307/2388615.
Figel JJ, Durán E, Barton Bray D, Prisciliano-Vázquez J-R. 2009. New jaguar records
from montane forest at a priority site in southern Mexico. CATnews 50:14–15.
Galicia L, Zarco-Arista AE. 2014. Multiple ecosystem services, possible trade-offs
and synergies in a temperate forest ecosystem in Mexico: a review. International
Journal of Biodiversity Science, Ecosystem Services & Management 10:275–288
DOI 10.1080/21513732.2014.973907.
Galindo-Aguilar RE, Lavariega MC, Rueda JA, Prisciliano JR, Pérez-Hernández
MJ. 2019. Registros recientes de Caluromys derbianus (Didelphimorphia: Didelphidae), Tamandua mexicana (Pilosa: Myrmecophagidae) y Coendou mexicanus
(Rodentia: Erethizontidae) en Oaxaca, México. Mammalogy Notes 5:20–24
DOI 10.47603/manovol5n2.20-24.
Garcia-Grajales AJ, Buenrostro-Silva A. 2009. ¿Reserva archipiélago?, una propuesta de
conservación complementaria para la costa de Oaxaca. Ciencia y Mar 39:3–8.
Graham CH, Carnaval AC, Cadena CD, Zamudio KR, Roberts TE, Parra JL, Mccain
CM, Bowie RCK, Moritz C, Baines SB, Schneider CJ, Vanderwal J, Rahbek C,
Kozak KH, Sanders NJ. 2014. The origin and maintenance of montane diversity: Integrating evolutionary and ecological processes. Ecography 37:711–719
DOI 10.1111/ecog.00578.
Halffter G. 2007. Reservas archipiélago: Un nuevo tipo de área protegida. In: Hacia
una cultura de conservación de la diversidad biológica. México: España: Sociedad
Entomológica Aragonesa (SEA), Zaragoza, España. Comision Nacional Para El
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
26/30
Conocimiento Y Uso De La Biodiversidad (Conabio) México. Comisión Nacional De
Áreas Naturales Protegidas (CONANP). Consejo Nacional De Ciencia Y Tecnología.
Hall RE. 1981. The mammals of North America II. New York: John Wiley and Sons.
Ibarra JT, Del Campo C, Barreau A, Medinaceli A, Camacho C, Puri RK, Martin GJ.
2011. Etnoecología chinanteca: conocimiento, práctica y creencias sobre fauna y
cacería en un área de conservación comunitaria de la Chinantla, Oaxaca, México.
Etnobiología 9(1):36–58.
INEGI. 2016. Uso del suelo y vegetación, escala 1:250000, serie VI (continuo nacional).
Available at http://geoportal.conabio.gob.mx/metadatos/doc/html/usv250s6gw.html
(accessed on 30 April 2021).
CITES. 2013. Apéndices I, II y III. Available at http://cites.org/esp/app/appendices.php.
IUCN. 2022. The IUCN Red List of Threatened Species. Available at https://www.
iucnredlist.org .
Jȩdrzejewski W, Robinson HS, Abarca M, Zeller KA, Velasquez G, Paemelaere EAD,
Goldberg JF, Payan E, Hoogesteijn R, Boede EO, Schmidt K, Lampo M, Viloria ÁL,
Carreño R, Robinson N, Lukacs PM, Nowak JJ, Salom-Pérez R, Castañeda F, Boron
V, Quigley H. 2018. Estimating large carnivore populations at global scale based on
spatial predictions of density and distribution - Application to the jaguar (Panthera
onca). PLOS ONE 13(3):e0194719 DOI 10.1371/journal.pone.0194719.
Lavariega MC, Ríos-Solís JA, Flores-Martínez JJ, Galindo-Aguilar RE, SánchezCordero V, Juan-Albino S, Soriano-Martínez I. 2020. Community-Based Monitoring of Jaguar (Panthera onca) in the Chinantla Region, Mexico. Tropical Conservation
Science 13:194008292091782 DOI 10.1177/1940082920917825.
Legarreta P. 2010. Miradas sobre la integración. RURIS 3:125–150.
Lele S, Wilshusen P, Brockington D, Seidler R, Bawa K. 2010. Beyond exclusion:
alternative approaches to biodiversity conservation in the developing tropics. Current
Opinion in Environmental Sustainability 2:94–100 DOI 10.1016/j.cosust.2010.03.006.
Linzey AV, Reed AW, Slade NA, Kesner MH. 2012. Effects of habitat disturbance on a
Peromyscus leucopus (Rodentia: Cricetidae) population in western Pennsylvania.
Journal of Mammalogy 93:211–219 DOI 10.1644/11-MAMM-A-130.1.
Lira-Torres I, Galindo-Leal C, Briones-Salas M. 2012. Mamíferos de la selva Zoque,
México: riqueza, uso y conservación. Revista de Biología Tropical 60:781–797.
Lira-Torres I, Naranjo-Piñera EJ, Hilliard D, Camacho-Escobar MA, De Villa Meza
A, Reyes-Chargoy MA. 2006. Status and Conservation of Baird’s Tapir in Oaxaca,
México. Tapir Conservation 15:21–28.
March IJ, Aranda M. 1992. Mamíferos de la Selva Lacandona. In: Vázquez M, Ramos
M, eds. Reserva de la Biosfera Montes Azules, Selva Lacandona: investigación para
su Conservación. San Cristóbal de las Casas, México: Publicaciones Especiales
ECOSFERA, 201–220.
Marquet PA. 1994. Diversity of small mammals in the pacific coastal desert of peru and
chile and in the adjacent andean area: Biogeography and community structure.
Australian Journal of Zoology 42:427–442 DOI 10.1071/ZO9940527.
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
27/30
Martin-Regalado CN, Briones-Salas M, Lavariega MC, Moreno CE. 2019. Spatial
incongruence in the species richness and functional diversity of cricetid rodents.
PLOS ONE 14:1–20 DOI 10.1371/journal.pone.0217154.
Mastretta-Yanes A, Moreno-Letelier A, Piñero D, Jorgensen TH, Emerson BC. 2015.
Biodiversity in the Mexican highlands and the interaction of geology, geography
and climate within the Trans-Mexican Volcanic Belt. Journal of Biogeography
42:1586–1600 DOI 10.1111/jbi.12546.
Mccain CM. 2005. Elevetional gradiants in diversity of small mammals. Ecology
86:366–372 DOI 10.1890/03-3147.
Meave JA, Rincón A, Romero-Romero MA. 2006. Oak forests of the hyper-humid
region of La Chinantla, Northern Oaxaca Range, Mexico. In: Ecology and
conservation of neotropical montane oak forests. Berlin: Springer, 113–125
DOI 10.1007/3-540-28909-7_9.
Meave JA, Rincón-Gutiérrez A, Ibarra-Manríquez G, Gallardo-Hernández C, RomeroRomero MA. 2017. Checklist of the vascular flora of a portion of the hyperhumid
region of La Chinantla, Northern Oaxaca Range, Mexico. Botanical Sciences
95:722–759 DOI 10.17129/botsci.1812.
Medellín RA. 1994. Mammal diversity and conservation in the Selva Lacandona, Chiapas,
Mexico. Conservation Biology 8(3):780–799
DOI 10.1046/j.1523-1739.1994.08030780.x.
Moctezuma V, Halffter G, Arriaga-Jiménez A. 2018. Archipelago reserves, a new option
to protect montane entomofauna and beta-diverse ecosystems. Revista Mexicana de
Biodiversidad 89:927–937 DOI 10.22201/ib.20078706e.2018.3.2446.
Monroy-Vilchis O, Zarco-González Z, Zarco-González MM. 2019. Potential distribution and areas for conservation of four wild felid species in Mexico: conservation
planning. Mammalian Biology 98:128–136 DOI 10.1016/j.mambio.2019.09.003.
Noria-Sánchez JL, Prisciliano-Vázquez J-R, Patiño Islas JJ. 2015. Monitoreo comunitario de aves en la Chinantla, Oaxaca: un esfuerzo para la conservación de la
biodiversidad. In: Ortega-Álvarez R, Sanchez-González LA, Berlanga García H, eds.
Plumas de multitudes: integración comunitaria en el estudio y monitoreo de aves en
México. 7. México City: CONABIO, 1–88.
O’Brien TG, Kinnaird MF, Wibisono HT. 2003. Crouching tigers, hidden prey: Sumatran tiger and prey populations in atropical forest landscape. Animal Conservation
6:131–139 DOI 10.1017/S1367943003003172.
Ortega-Álvarez RR, Sánchez-González LA, Rodríguez-Contreras V, Vargas-Canales
VMVM, Puebla-Olivares F, Berlanga H. 2012. Birding for and with people:
integrating local participation in avian monitoring programs within high biodiversity
areas in Southern Mexico. Sustainability 4:1984–1998 DOI 10.3390/su4091984.
Ortiz-Martínez T, Pinacho-Guendulain B, Mayoral-Chávez P, Carranza-Rodríguez
JC, Ramos-Fernández G. 2012. Demografía y uso de hábitat del mono araña
(Ateles geoffroyi) en una selva húmeda tropical del norte de Oaxaca, México. Therya
3:381–401 DOI 10.12933/therya-12-95.
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
28/30
Ortiz-Pérez MJ, Hernandez-Santana JR, Figueroa-Mah-Eng JM. 2004. Reconocimiento
fisiográfico y geomorfológico. In: García-Mendoza AJ, Ordóñez M, Briones-Salas
M, eds. Biodiversidad de Oaxaca. México City: Universidad Nacional Autonoma de
México; Fondo Oaxaqueño para la conservacion de la Naturaleza; World Wildlife
Fund, 43–54.
Pennington T, Sarukhán J. 2005. Arboles tropicales de México. Manual para la identificación de las principales especies. México City: UNAM, Fondo de Cultura Económica.
Pérez-Irineo G, Santos-Moreno A. 2012. Diversidad de mamíferos terrestres de talla
grande y media de una selva subcaducifolia del noreste de Oaxaca, México. Revista
Mexicana de Biodiversidad 83:164–169.
Perez-Lustre M, Contreras-Diaz RG, Santos-Moreno A. 2006. Mamíferos del bosque
mesófilo de montaña del municipio de San Felipe Usila, Tuxtepec, Oaxaca, Mexico
martín. Revista Mexicana de Mastozoología 10:29–40
DOI 10.22201/ie.20074484e.2006.10.1.140.
Ramírez-Pulido J, González-Ruiz N, Gardner A, Arroyo-Cabrales J. 2014. List of recent
land mammals of Mexico, 2014. Lubbock: Special Publications Museum of Texas
Tech University, Museum of Texas Tech University DOI 10.1177/002194368302000404.
R Core Team. 2017. R: a language and environment for statistical computing. Version
3.3.3. Vienna: R Foundation for Statistical Computing. Available at http://www.rproject.org/.
Rodhe K. 1999. Latitudinal gradients in species diversity and rapoport’s rule revisited:
a review of recent work and what can parasites teach us about the causes of the
gradients? Ecography 22:593–613 DOI 10.1111/j.1600-0587.1999.tb00509.x.
Rodríguez-Soto C, Monroy-Vilchis O, Maiorano L, Boitani L, Faller JC, BrionesSalas M, Núñez R, Rosas-Rosas O, Ceballos G, Falcucci A. 2011. Predicting
potential distribution of the jaguar (Panthera onca) in Mexico: identification
of priority areas for conservation. Diversity and Distributions 17:350–361
DOI 10.1111/j.1472-4642.2010.00740.
Rosas-Rosas OC, Bender LC. 2012. Population status of jaguars (Panthera onca) and
pumas (Puma concolor) in northeastern Sonora. Mexico. Acta Zoológica Mexicana
28:86–101 DOI 10.21829/azm.2012.281818.
Rzedowski J. 1996. Análisis preliminar de la flora vascular de los bosques mesófilos de
montaña de México. Acta Botanica Mexicana 25–44 DOI 10.21829/abm35.1996.955.
SEMARNAT. 2010. Norma Oficial Mexicana NOM-059-SEMARNAT-2010. México City:
Diario Oficial de la Federación.
SEMARNAT. 2014. Acuerdo por el que se da a conocer la lista de especies y poblaciones
prioritarias para la conservación. México City: Diario Oficial de la Federación.
Silva-Magaña N, Santos-Moreno A. 2020. The pardalis effect: its spatial and temporal
variation. Revista Mexicana de Biodiversidad 91
DOI 10.22201/IB.20078706E.2020.91.3201.
Simón-Salvador PR, Arreortúa M, Flores CA, Santiago-Dionicio H, González-Bernal
E. 2021. The role of indigenous and community conservation areas in herpetofauna
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
29/30
conservation: A preliminary list for Santa Cruz tepetotutla, Oaxaca Mexico. ZooKeys
2021:185–208 DOI 10.3897/zookeys.1029.62205.
Vidal-García F, Serio-Silva JC. 2011. Potential distribution of Mexican primates:
modeling the ecological niche with the maximum entropy algorithm. Primates
52:261–270 DOI 10.1007/s10329-011-0246-6.
Villa B, Cervantes FA. 2003. Los mamíferos de México. México City: Grupo editorial
Iberoamericano, Instituto de Biología, UNAM.
Vivas-Lindo R, Hernández-Ordóñez O, Rodríguez-Salazar MA, Reynoso VH, SernaLagunes R. 2020. Recent records of Tapirella bairdii and Panthera onca in a region
highly transformed by human activities in Southern Veracruz, México. Therya
11:151–156 DOI 10.12933/therya-20-768.
Wilson DE, Ascorra CF, Solari S. 1996. Bats as indicators of habitat disturbance. Lima:
Smithsonian Institution Press.
Briones-Salas et al. (2023), PeerJ, DOI 10.7717/peerj.16345
30/30