Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

Effects of human disturbance on medium and large mammals

in primary and secondary tropical forests in southern Mexico

Rosa Elena Galindo-Aguilar1, 2; https:// orcid.org/0000-0002-2842-3449

Mario C. Lavariega2; https://orcid.org/0003-2513-8244

María Jesús Pérez Hernández3; https://orcid.org/0001-6890-5939

Carlos A. López González4; https://orcid.org/0003-2925-9545

Octavio César Rosas-Rosas5*; https://orcid.org/0003-0504-7193

1. Colegio de Postgraduados Campus Montecillo, Montecillo, Texcoco, Estado de México, México; rgalindoa@ipn.mx

2. Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional-Unidad Oaxaca, Instituto Politécnico

Nacional, Santa Cruz Xoxocotlán, Oaxaca, México; mlavariegan@ipn.mx

3. Universidad Autónoma Chapingo, Texcoco, Estado de México, México; mperezhe@chapingo.mx

4. Universidad Autónoma de Querétaro, Juriquilla, Querétaro, México; carlos.lopez@uaq.mx

5. Colegio de Postgraduados, programa en Innovación en Manejo de Recursos Naturales, Campus San Luis Potosí,

México; octaviocrr@colpos.mx(*Correspondence)

Received 26-I-2024. Corrected 04-XII-2024. Accepted 23-IV-2025.

ABSTRACT

Introduction: In tropical forests, populations of medium and large mammals are being impacted by human

activities. Understanding how species respond to land use conversion, fragmentation, and the encroachment of

roads density and settlements is of conservation interest in highly biodiverse regions.

Objetive: To assess the effect of human disturbance and environmental variables on trophic guilds of medium

and large mammals in the tropical forests of the Sierra Negra-Mazateca in southern Mexico.

Methods: We characterized the landscape (land use and vegetation, number of fragments, and edge density)

through supervised classification of Landsat 8 images. We recorded species using camera-trap stations and evalu-

ated the relationship between the presence and relative abundance of species with human disturbance variables

using zero-inflated regression models.

Results: The landscape of the Sierra Negra-Mazateca is dominated by fragments of secondary forests (48.6 %)

with a small proportion of primary forests (9.6 %). We found no differences in the overall relative abundance

of species between primary and secondary forests, but differences were observed for omnivore and carnivore

guilds. Human disturbances had a disparate effect among guilds, negatively affecting carnivores and positively

herbivores.

Conclusions: Secondary forests are refuges for tolerant species. Nevertheless, we emphasize the need to conserve

primary forests and safeguard medium and large mammals, especially the carnivore guild. Extensive manage-

ment in secondary forests is recommended to conserve remaining primary forests, alongside community aware-

ness and empowerment for coexistence with wildlife.

Keywords: carnivores; defaunation; human disturbance; landscape analyses; landsat; montane cloud forest; zero-

inflated models.

https://doi.org/10.15517/rev.biol.trop..v73i1.58524

CONSERVATION

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

INTRODUCTION

Human activities can have significant neg-

ative impacts on mammals, threatening their

survival, causing biodiversity loss, and alter-

ing the ecosystems in which they inhabit. For

example, tropical forests play an important role

in maintaining biodiversity and global ecologi-

cal services, however, human disturbance has

caused alarming rates of loss, fragmentation

and degradation in this type of forest (Brad-

shaw et al., 2009; Curtis et al., 2018 Díaz-

Gallegos et al., 2010; Gibson et al., 2011). The

fragmentation produces patches of vegetation

surrounded by a matrix of different land use

or vegetation (Saunders et al., 1991). Currently,

large fragments of tropical forests are being

reduced to mosaics of small fragments (Hansen

et al., 2020) and exhibit degradation processes

(Gibson et al., 2011; Phillips et al., 2017). This

means that forests lose their capacity to pro-

vide ecosystem services or undergo significant

changes in species composition (Millennium

Ecosystem Assessment, 2005). Among the main

causes are the intensification of slash and burn

agriculture, an agricultural system that trans-

forms the forest into a mosaic of vegetation

patches represented by various stages of suc-

cession or secondary vegetation (Brady, 1996;

Phillips et al., 2017). Such changes are produc-

ing profound effects on the presence, abun-

dance, interactions, spatial distribution and

behavior of species (Bowyer et al., 2019; Gibson

et al., 2011; Pires et al., 2023).

Wild mammal communities show a rela-

tionship between the intensity of landscape

fragmentation and degradation with species

composition. Slightly fragmented or moderate-

ly degraded landscapes can maintain a number

of species similar to those occurring in primary

forests but showing changes in the dominance

of resilient generalist species (Barlow et al.,

2007; Borges, 2007; Gibson et al., 2011; Phil-

lips et al., 2017; Scales & Marsden, 2008; Tilker

et al., 2019). Forest fragments tend to contain

less diverse mammalian communities with a

RESUMEN

Efectos de la perturbación humana en los mamíferos medianos y grandes de

los bosques tropicales primarios y secundarios en sur de México

Introducción: En los bosques tropicales las poblaciones de mamíferos medianos y grandes están siendo afectadas

por las actividades humanas. Es de interés para la conservación de áreas altamente biodiversas conocer cómo

responden las especies a la conversión de uso de suelo, la fragmentación de la vegetación y la creación de caminos

y poblados.

Objetivos: Evaluar el efecto de la perturbación humana y las variables ambientales sobre los mamíferos medianos

y grandes, así como en los gremios tróficos, en los bosques tropicales de la Sierra Negra-Mazateca, en el sur de

México.

Métodos: Caracterizamos el paisaje (uso de suelo y vegetación, porcentaje de cobertura vegetal, número de frag-

mentos y densidad de borde) por medio de una clasificación supervisada de imágenes Landsat 8. A las especies

las registramos por medio de estaciones de fototrampeo y evaluamos la relación entre presencia y la abundancia

relativa de las especies con variables de perturbación humana con modelos de regresión inflados de ceros.

Resultados: El paisaje de la Sierra Negra-Mazateca tiene predominio de fragmentos de bosques secundarios (48.6

%) y una baja proporción de bosques primarios (9.6 %). Encontramos que no hubo diferencias en la abundancia

relativa de las especies entre bosques primarios y secundarios, pero sí para los gremios de omnívoros y carnívoros.

Las perturbaciones humanas tuvieron un efecto negativo sobre carnívoros, y positivo en herbívoros.

Conclusiones: El bosque secundario es refugio de las especies generalistas, sin embargo, enfatizamos la necesidad

de conservar los bosques primarios para conservar a los mamíferos medianos y grandes y sobre todo al gremio

de los carnívoros. Se recomienda un manejo extensivo en los bosques secundarios y conservar los bosques pri-

marios restantes, junto con la concientización y el empoderamiento de la comunidad para la coexistencia con la

vida silvestre.

Palabras clave: carnívoros; defaunación; perturbación humana; análisis del paisaje; landsat; bosque mesófilo de

montaña; modelos inflados por ceros.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

predominance of species with small home rang-

es (Meyer et al., 2015). In addition, in highly

fragmented and degraded landscapes mam-

malian communities tend to become homo-

geneous, due to local and regional extinctions,

where even generalist species occur in low

abundances (Bovendorp et al., 2019; Knowlton

et al., 2019 Phillips et al., 2017).

In fragmented landscapes, edges substan-

tially influence the magnitude to which spe-

cies use the fragments, notably affecting those

species dependent on primary forests such as

carnivores (Balme et al., 2010; Brodie et al.,

2015; Slater et al., 2023). On the other hand,

herbivorous species do not present a negative

effect (Brodie et al., 2015; Kiffner et al., 2013).

Concurrently, other human disturbances such

as roads and human settlements negatively

affect mammal occupancy (Boron et al., 2019).

Medium and large sized mammals (those

that weigh more than 100 g, Medellín, 1994),

are more susceptible to disappearing due to

either extrinsic or intrinsic factors (Davidson

et al., 2017). These mammals are important

in the dynamics of forests, performing the

roles of herbivory, including seed consumption

and dispersal, and as top predators (Dirzo &

Miranda, 1990; Lacher et al., 2019). Therefore,

the loss of species and decrease in abundance

of medium and large sized mammals produces

severe cascading effects that impact several

lower trophic levels, causing “extinction cas-

cades” (Bovendorp et al., 2019; Garmendia et

al., 2013; Michalski & Peres, 2007).

The tropical forests located in southern

Mexico have been identified as priority places

for the conservation of mammals (García-Mar-

molejo et al., 2008; Jenkins et al., 2013), due to

their high diversity of species and endemism

(Briones-Salas et al., 2015; Sánchez-Cordero et

al., 2014). The largest fragments of mountain

cloud forests and tropical rainforests in Mexico

occur there (Challenger, 1998). Particularly,

the forests of La Sierra Negra-Mazateca show

evidence of species of conservation importance,

such as jaguars (Panthera onca) and ocelots

(Leopardus pardalis, Briones-Salas et al., 2015;

Galindo-Aguilar et al., 2016); this locale acts

as a potential corridor for them, by linking the

populations of northern and southern Mexico

(Cacelin-Castillo et al., 2020; Ceballos et al.,

2021). However, the region presents intense

processes of fragmentation and degradation

(Velázquez et al., 2003). It is estimated that hab-

itat loss rates of rainforest and mountane cloud

forest between 2000 and 2016 were -2.63 % and

-2.29 %, respectively and that few fragments are

considered suitable to maintain ocelot popula-

tions (Galindo-Aguilar et al., 2019).

Although second growth forests, derived

from human disturbance, are increasing in

area around the world (Food and Agriculture

Organization of the United Nations & United

Nations Environmental Programme, 2020), few

studies have explored changes in the presence

and abundance of medium and large sized

mammals, with respect to primary forests with

little disturbance (e.g. Azlan, 2006; Zhang et al.,

2019). In a multi-taxonomic study, Barlow et al.

(2007) found group-dependent responses, with

greater species richness of birds, amphibians,

arachnids, butterflies, lizards, beetles and bats

in primary forests than in second growth forests

or plantations. However, the authors found no

differences in richness in either small or large

mammals. In other studies, second growth for-

ests harbor substantial bird richness compared

to other more degraded environments (Harvey

et al., 2006). In small mammals, fragment size

and structure complexity influenced diversity

more than condition of the forest per se (da

Fonseca, 1989; da Fonseca & Robinson, 1990).

In medium and large sized mammals, the

importance of second growth forest fragments

immersed in monoculture matrices has been

highlighted, favoring occupation (McShea et

al., 2009; William et al., 2023). In Brazil, species

composition was not different between primary

and second growth forests, but there were sub-

stantial changes in abundances, particularly in

herbivores and small primates that were more

frequent in second growth forests (Parry et al.,

2007). In central China, it was observed that

richness was not different between primary,

secondary or plantation forests, but changes in

abundance were observed (Zhang et al., 2019).

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

Likewise, in southern Mexico, no differences

were found in species richness between palm

plantations and fragments of secondary forests,

but a high proportion of species showed greater

abundance in the fragments, although there

were no differences in average relative abun-

dance (Knowlton et al., 2019). In Lacandona,

Chiapas, it was observed that the number of

mammal species is higher when forest cover

is greater; in fragmented forests, species not

recorded in continuous forests were found, as

is the case with Cabassous centralis (Garmendia

et al., 2013). In general, most studies agree on

a low effect on the specific richness between

primary, secondary forests or plantations, but

significant changes affect the occupancy or

abundance of several species.

In this context, our objective was to evalu-

ate the influence of human disturbances on

the composition and relative abundance of

medium and large sized mammals, as well as on

the trophic guilds that make up these commu-

nities. We wanted to test two hypotheses. First,

it is postulated that there is a species-specific

response of the relative abundance of medium

and large mammals to the landscape condition

(Garmendia et al., 2013; Michalski & Peres,

2007; Naughton-Treves et al., 2003). It is antici-

pated that generalist species will show greater

abundance in disturbed environments, while

less tolerant species will have lower abundance

(Bovendorp et al., 2019). Our second hypoth-

esis, we proposed that at the guild level, carni-

vores will show a negative effect on disturbed

environments, due to their needs for food,

shelter and large home areas (Kruuk, 2002). In

contrast, it is expected that herbivores will have

a positive effect on disturbed environments,

by having a greater food supply in sites with

secondary vegetation or agriculture (Gallegos-

Peña et al., 2010).

MATERIALS AND METHODS

Study area: Our study was carried out in

the Negra and Mazateca mountains, located in

the states of Puebla and Oaxaca, respectively,

in southern Mexico. The climate of this region

is warm and humid with temperatures ranging

between 16 and 26 °C, and it has annual rainfall

of 3 000-4 500 mm (García, 1964). The main

types of vegetation are humid tropical forests,

mountane cloud forests and pine-oak forests,

all in primary and secondary states. Land uses

include seasonal and perennial agriculture, and

induced grasslands for livestock raising (Insti-

tuto Nacional de Estadística, Geografía e Infor-

mática [INEGI], 2015).

The area is made up of communal lands

(“ejidos”) belonging to indigenous peoples

(Nahuas and Mazatecs), and includes two

municipalities: San Sebastián Tlacotepec (State

of Puebla, 18°14’-18°32’ N & 96°43’-96°55’ W;

altitude between 60 and 1 580 m (Fig. 1), with

13 534 inhabitants distributed in 61 localities

with a density of 56.9 inhabitants/km² ( INEGI,

2010); and Santa María Chilchotla (State of

Oaxaca, 18°10’-18°24’ N & 96°35’-96°52’ W;

altitude from 0 to 2 100 m, with 20 584 inhabit-

ants distributed in 110 localities with a density

of 72.3 inhabitants/km2 (INEGI, 2010).

Data collection: To determine the study

area, we used GIS to create a polygon of 110

km². This size was chosen because it matches

the home range required by the largest mam-

mal potentially inhabiting the area, the jaguar

(150 km² in Abra Tanchipa, SLP, Silva-Cabal-

lero, 2019). Within the polygon, we established

an imaginary grid containing 18 squares of 3

km² each. In each square, we placed 2-3 cam-

era trap stations, spaced 1-3 km² apart, during

three different time periods. This sampling

design meets the criteria for obtaining inde-

pendent data and covering the largest possible

area (Noss et al., 2013) (Table 1; Fig. 1). The

cameras were in primary forests (21 stations)

and in secondary forests (19 stations). The total

sampling effort was 1 693 nights/trap (943 in

primary forests and 750 in secondary forests)

to ensure a similar number of cameras in each

type of forest.

The cameras were placed 3 m apart from

mammal trails with spoor evidence (Aranda-

Sánchez, 2012), and we secured them to a tree

at 40 cm above the ground (Noss et al., 2013).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

We use StealthCam® Delta8 cameras model

STC-Q8X / STC-D8BZ, Cuddeback® Ambush

Black Flash Model 1194 and Bushnell® Tro-

phyCam HD Essential 119736C and Covert®.

We placed a single camera in 34 stations, and

we placed two facing cameras in six stations. In

these sites we used Obsession® CK perfume as

an attractant for felids. The cameras were pro-

grammed to take photographs throughout the

day and were checked monthly for maintenance

and battery replacement. We used field guides

to identify photographed mammals to the spe-

cies level (Aranda-Sánchez, 2012; Ceballos &

Oliva, 2005).

Landscape analysis: To characterize the

landscape and obtain a map of land use and

vegetation in the study area, a Landsat 8 (OLI-

TIRS) image (Route 24 / Row 47; April 28,

2016) was analyzed with a resolution of 30 m,

obtained from the Glovis platform (U.S. Geo-

logical Survey, 2016). We use infrared bands

Table 1

Camera trap survey effort to document medium and large sized mammals in Sierra Negra-Mazateca, Mexico.

Sampling periods Days Distance between

cameras

Number of cameras Trap days

Primary Secondary Primary Secondary

December 2013-January 2014 30 1 km 9 8 270 240

April 2014 11-48 3 km 5 3 182 71

July-October 2014 10-101 3 km 7 8 491 439

Total 21 19 943 750

Fig. 1. Land cover in Sierra Negra-Mazateca, México, obtained through supervised classification of Landsat 8 images, and

camera traps locations. The color of the camera indicates the number of species recorded.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

5, 4 and 3 because their combination is more

useful to discriminate between types of cover

and/or vegetation (Chuvieco, 1995). The spa-

tial resolution of the image was resampled

to 15 m due to the highly fragmented land-

scape. Subsequently, supervised classification

was performed with the maximum likelihood

algorithm (Moumane et al., 2022; Zhang et

al., 2022). For the resulting image, a majority

filter with a 5 x 5 pixel window was applied.

The processing was carried out in the ENVI 4.7

software (ITT, 2009). From the resulting land

use and vegetation map, the following metrics

that characterize the landscape were calculated:

area of vegetation cover, percentage of veg-

etation cover, number of patches (NumP) and

average patch area (APA). For the calculation

of the last two metrics, the edge effect (100 m)

was eliminated to preserve only the core area of

the patches.

Data Analysis: Species richness was

obtained from photographic records, both for

primary and secondary forests. The trophic

guilds that we used correspond to carnivores,

omnivores, insectivores, frugivores, and herbi-

vores, which were obtained following Ceballos

& Oliva (2005).

Camera trapping rate was used as an index

of relative abundance (Rovero & Marshall,

2009). Relative abundance indices (RAI) were

calculated using the ratio of the number of

independent events of each species / trap night

x 1 000 (Jenks et al., 2011). As independent

events, those photographic records that met the

following characteristics were considered: 1)

consecutive photographs of different individu-

als (that is, identified by spot patterns) of the

same species; 2) and consecutive photographs

of the same species taken > 24 hours apart (O’

Brien et al., 2003). We performed a Mann-

Whitney test to determine if there were differ-

ences between the RAIs of the species and the

trophic groups to which they belong between

primary and secondary forests.

Sample coverage and diversity: We used

coverage-based rarefaction-extrapolation

sampling curves, based on standardized level

of sample completeness. This approach inte-

grates rarefaction and extrapolation of the Hill

numbers in a unified standardization method

for quantifying and comparing species diver-

sity across multiple assemblages with different

sampling effort (Chao & Jost 2015; Hsieh et al.,

2016). Diversity was estimated with the refor-

mulation of the Hill numbers done by Chao and

Jost (2015). Hill numbers are parameterized by

a diversity order q, which determines the mea-

sures’ sensitivity to species relative abundances

(Hsieh et al., 2016). Here, we used q = 0, which

estimate the species diversity without regard

to their relative abundances of species (Chao

& Jost, 2015), and can also be interpreted as a

species accumulation curve (Chao et al., 2014).

Estimates confidence intervals were obtained

with 1 000 bootstrap iterations (Chao & Jost,

2015); to extrapolate the species diversity, we

used the double of the larger sample in assem-

blages, and for rarefaction-extrapolation calcu-

lus we used 80 every-spaced knots (Chao et al.,

2014). Calculus were done in iNext package for

R (Hsieh et al., 2016).

Rank-abundance curves: Rank-abun-

dance curves were constructed for each zone

following the methodology described by Feins-

inger (2001). The analyses were conducted

using BiodiversityR version 2.13-1and vegan’

version 2.6-4 in R software version 4.0.2

(R Core Team, 2012).

Regression models with excess of zeros:

To relate the relative abundance of the guilds

with the environmental variables we used

regression models with excess of zeros. These

regression models have two components, the

first with a binomial distribution evaluates the

probability of having excesses of zeros; and the

second, models the counts, using a Poisson

distribution, and unlike truncated models of

zeros, zeros are considered within the model,

whether the species is not present or was not

detected (Zuur et al., 2009). The excess of zeros

in camera traps can be due to two types of fac-

tors, sampling and structural. Sampling errors

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

(“false zeros”) may include cameras placed in

habitats not used by the species (e.g. urban

areas), out-of-season sampling (e.g. migratory

species), and identification errors; structural

errors are due to species not using a par-

ticular site in response to environmental vari-

ables (“true zeros”). In this work we ruled out

sampling errors, given that the stations were

arranged in habitats reported as used by the

species, the sampling time was long enough

to detect or not detect the species in the sites,

they are not migratory species and the identi-

fication of the species can be reviewed until a

consensus is reached (photographic evidence is

available). The binomial part, when modeling

the probability that a value of zero is observed,

measures the relationship of the variables with

the absence of the species in the sites. To com-

pensate for variation in the resulting response

we used sampling effort (i.e. the specific days

each station operated) as an offset variable.

Environmental and human disturbance

covariates: We chose human disturbance

and environmental covariates that have been

shown to have an effect on mammal occu-

pancy (Cavada et al., 2019; Pardo et al., 2018):

the Euclidean distance to the nearest human

settlement, the Euclidean distance to the near-

est road, elevation, type of cover (primary/

secondary), and percentage of natural vegeta-

tion (primary/secondary) and edge density in

500 m buffers. At each camera trap station,

we recorded elevation with a Garmin global

positioning system and land use or vegetation

cover (primary or secondary). On the other

hand, using the ArcMap program, 500 m buf-

fers were created in the land use and vegetation

map for each camera-trap station (Pardo et al.,

2018). In FragStat, within each buffer the per-

centage of primary and secondary tree cover

and edge density were calculated (McGarigal

& Marks, 1995). In addition, from each station,

the Euclidean distance to the nearest human

settlement and the distance to the nearest road

were measured as variables that may have an

effect on the abundance of mammals. The vari-

ables were standardized, and collinearity was

evaluated with the variance inflation factors

and 2 as a threshold. Additionally, we obtained

correlation coefficients between covariates and

when | r | > = 0.7, one of the variables was

excluded. The models were made in the R envi-

ronment with the car and pscl packages (Jack-

man, et., 2015; R Core Team, 2012).

RESULTS

Landscape analysis: Secondary tropical

forests are the main type of vegetation cover in

La Sierra Negra-Mazateca covering 48.6 % of

the study area; agricultural land, cattle pastures

and without vegetation cover another 37.9 %;

and the primary forest occupies 9.6 % (Table 2).

1 098 tropical forest patches were identified,

of which 963 patches correspond to second-

ary tropical forests and 135 to primary forests,

of which 53 are tropical cloud forest and 82

Table 2

Land cover types in Sierra Negra-Mazateca, Mexico.

Land cover types Area (km2)Percentage Average patch area (ha) Number of patch

Secondary tropical forest 252.98 48.60 3.08 963

Cattle pastures 74.11 14.24 1.50 248

Without vegetation 68.41 13.14 1.97 189

Agricultural land 53.49 10.28 1.96 140

Tropical rainforest 29.05 5.58 1.04 82

Tropical cloud forest 20.99 4.03 0.85 53

Water 20.06 3.85 12.27 37

Human settlements 1.48 0.28

Total 520.57 100 22.67 1 712

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

are tropical rainforest (Table 2, Fig. 1, Fig. 2).

Most patches of primary forest are found in

the most remote sites, far from population

centers (Fig. 1).

Community composition of medium and

large mammals: We obtained 497 independent

events from 16 species of medium and large

mammals, distributed in 13 families and six

orders. Regarding the total number of spe-

cies, the order Carnivora was the best repre-

sented (37.5 %), followed by Rodentia (18.7 %;

Table 3). Five trophic guilds were observed, the

omnivores were the ones that occurred in the

highest proportion (37.5 %) and the insecti-

vores and carnivores in the lowest proportion

(12.5 %) (Fig. 3). In the primary forest patches

all species were recorded, while in the sec-

ondary forest patches, Coyote (Canis latrans)

and Northern tamandua (Tamandua mexi-

cana) were not recorded. The largest carnivore

recorded was the Ocelot (Leopardus pardalis)

and of the herbivores, the Collared pecca-

ry (Dicotyles crassus) and the American red

brocket (Mazama temama). Most species were

more frequent in the primary forests, although

the Nine banded armadillo and American red

brocket were more frequent in secondary tropi-

cal forest.

Relative abundance: The species with the

highest relative abundance was the Mexican

Table 3

Detected species, guild, and Relative Abundance Index (RAI) of medium and large mammals in Sierra Negra-Mazateca,

México.

Orden

Scientific name

Common

name Guild EI

RAI

STF

RAI

STF

total

RAI

Total

Didelphimorphia

Didelphis spp.Opossum O 16 17 3 4 19 11.2

Philander opossum Gray four-eyed opossum O 7 7.4 7 9.3 14 8.2

Cingulata

Dasypus novemcinctus Nine banded armadillo I 3 3.2 21 28 24 14.2

Pilosa

Tamandua mexicanaaNorthern tamandua I 2 2.1 0 0.0 2 1.2

Rodentia

Sciurus aureogaster Mexican gray squirrel F 18 19 3 4 21 12.4

Cuniculus paca Spotted paca F 32 34 28 37.3 60 35.4

Dasyprocta mexicana Mexican aguti F 160 170 63 84 223 132.0

Lagomorpha

Sylvilagus spp. Cottontail H 2 2.12 1 1.3 3 1.8

Carnivora

Canis latrans Coyote O 1 1.1 0 0.0 1 0.6

Leopardus pardalis Ocelot C 18 19.1 4 5.3 22 13

Leopardus wiedii Margay C 1 5.1 1 1.8 2 1.1

Conepatus semistriatus Striped hog-nosed skunk O 12 13 13 17.3 25 14.8

Nasua narica White-nosed coati O 41 43.5 7 9.3 48 28.4

Procyon lotor Northern raccoon O 5 5.3 1 1.3 6 3.6

Artiodactyla

Dicotyles crassus Collared peccary H 10 10.6 4 5.3 14 8.3

Mazama temama Central American red brocket H 3 3.2 10 13.3 13 7.7

Total Total 331 166 497

Independent events (EI). Trophic guild: C, carnivore; F, frugivore; H, herbivore; I, insectivore; Or, omnivore. Tropical

rainforest (BT) and Secondary tropical forest (STF). / a Excluded from zero-inflated models due to their arboreal habits.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

aguti (Dasyprocta mexicana), both in second-

ary and primary forests (RAI = 84 and 170,

respectively). The Coyote was the least detected

species in primary forests (RAI = 1.1) and

Cottontail (Sylvilagus spp.), Margay (Leopar-

dus wiedii) and Northern raccoon (P. lotor)

in secondary forests (RAI = 1.3, Table 3). No

significant statistical differences were found

in the RAI for mammals between primary and

secondary forests (U = 260.0, T = 329.0, p =

0.104). However, within the trophic guilds we

found significant differences for omnivores (U

= 298.0, T= 291.0, p = 0.006) and carnivores (U

= 275.0, T= 314.0, p = 0.019), but neither for

frugivores (U = 219.0, T = 370.0, p = 0.605) or

herbivores (U = 207.0, T = 382.0, p = 0.820).

Sample coverage and diversity: Sample

completeness was high for the forest types and

conditions (Fig. 4). We found that the estimated

species diversity was slightly higher in primary

forests (q0= 16.86 effective species, CI 11.73-

22.00) than in secondary forests (q0 = 15.89

effective species, CI 10.50-21.28) (Fig. 5). In

rainforests, the difference was more notice-

able, with greater diversity in primary than

secondary fragments (primary 15.04, CI 5.92-

24.17; secondary 9.85, CI 6.59-13.10) (Fig. 6A),

Fig. 2. Patch size per land cover types in Sierra Negra-Mazateca, México. The color indicates the size of the patches.

Fig. 3. Composition of trophic guilds documented in Sierra Negra-Mazateca, Mexico.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

than in the cloud forests (primary 14.12, CI

8.17-20.08; secondary 16.91, CI 7.94-25.88)

(Fig. 6B).

Rank-abundance curves: The rank-abun-

dance curves revealed that the dominant spe-

cies in both primary and secondary forests are

similar, whereas the rare species differ; L. wiedii

in conserved forests, whereas Sylvilagus in dis-

turbed forests (Fig. 7).

Relationship between mammals and

guilds with environmental and human distur-

bance variables: The two zero-inflated models

showed that no variable explained the pres-

ence and abundance of the species. The unions

showed that some variables had a negative rela-

tionship; for example, carnivores with elevation

(β = -0.739, p = 0.0003) and secondary cover (β

= -1.756, p = 0.0012); omnivores with elevation

(β = -1.152, p = 0.000254), secondary cover (β =

-2.428, p = 0.000341), edge density (β = -2.84, p

= 0.001362); herbivores had a negative relation-

ship with elevation (β = -1.112, p = 0.0207).

Omnivores also had a positive relationship with

the distance to rivers (β = 1.652, p = 0.00072),

and the percentage of tree cover (β = 2.31, p =

0.001796, Table 4). In the case of insectivores,

Fig. 4. Curve of the sample completeness of mammals recorded in primary and secondary forests in Sierra Negra-Mazateca,

Mexico.

Fig. 5. Curve of rarefaction and extrapolation of mammals recorded primary and secondary forests in Sierra Negra-Mazateca,

Mexico.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

there were limited data available to conduct

analyses within this guild.

DISCUSSION

In this study we explore the effect of human

disturbances on medium and large mammal

communities in tropical forests. Unlike what

we expected, the richness and composition of

species between secondary and primary for-

ests in La Sierra Negra-Mazateca was similar;

likewise, the relative abundance indices did not

present significant differences between forests.

Regarding species richness, a similar finding

Fig. 6. Curve of rarefaction and extrapolation of mammals recorded in A. primary and secondary cloud forest and B. tropical

rainforest in Sierra Negra-Mazateca, Mexico.

Fig. 7. Curve of rank-abundance of mammals recorded in primary forest (black line) and secondary forest (purple line) in

Sierra Negra-Mazateca, Mexico. Dmex = Dasyprocta mexicana, Cpac = Cuniculis paca, Plot = Procyon lotor, Sylvilagus, Mtem

= Mazama temama, Dnov = Dasypus novemcinctus, Lpar = Leopardus pardalis, Cla t= Canis latrans, Nnar = Nasua narica,

Popos = Philander opossum, Saur = Sciurus aureogaster, Lwie = Leopardus wiedii, Csem = Conepatus semistriatus, Tmex =

Tamandua mexicana.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

was reported in forests of central China, where

in primary forests, secondary forests and plan-

tations, richness varied by only one species.

However, in this region there were notable

differences in relative abundances, with high

values in primary forests (Zhang et al., 2019).

Considering the RAI values in Sierra Neg-

ra-Mazateca, we can observe that the species

that tolerate human presence (e.g., the Ameri-

can red brocket and Nine-banded armadillo

Dasypus novemcinctus (Newman, 1913; Sala-

zar-Ortiz et al., 2022) have higher values than

species that are less tolerant and require a larger

home range (e.g., Dicotyles crassus). Although

the species recorded here, such as Ocelot or

Collared peccary, had higher RAI in primary

forests than in secondary forests, these values

were notably lower compared to other tropi-

cal forests (Lira-Torres & Briones-Salas, 2012;

Muench & Martínez-Ramos, 2016). It is possi-

ble that there is overexploitation of the species,

since many of them are captured for different

purposes, such as preventing and reducing

damage to crops, for food, trade, ornament,

traditional medicine or because people con-

sider them to have magical-religious attributes

(Galindo-Aguilar, 2015). It has been observed

in various forests that hunting has direct nega-

tive effects on the survival of mammals (Cullen

et al. 2000; Peres, 1997).

In contrast, we found that the Nine-band-

ed armadillo and American red brocket, two

of the main prey of large and medium-sized

carnivores, had a higher abundance index in

secondary forests than in primary forests. One

of the reasons is the tolerance that these species

have to human activities and that, in addi-

tion, secondary forests provide abundant food

for herbivores, through fast-growing plants

(Naughton-Treves et al., 2003; Zapata-Ríos et

al., 2006). On the other hand, the Mexican aguti

had a greater abundance in primary forests, a

result similar to the tropical forests of Los Chi-

malapas, Oaxaca, where this species used sec-

ondary forests to a lesser extent (Lira-Torres &

Briones-Salas, 2012), this finding confirms the

importance of primary forests for mammals.

At the guild level, not only carnivores

showed a negative effect to the disturbance,

but also omnivores, but this was not the case

for herbivores, as we had predicted. Carnivores

had a negative relationship with secondary

cover, that is, they prefer conserved or primary

vegetation environments (Ferreira et al., 2018;

Ferreira et al., 2020; Graham et al., 2019). On

the other hand, they had a negative relationship

with elevation, this means that sites with lower

elevation have a greater abundance of carni-

vores. In the region, low-altitude areas present

a mosaic of primary and secondary forests, in

Table 4

Zero-inflated count component model for guilds in Sierra Negra-Mazateca, México.

Guild Estimate Std.Error Z value p

Carnivores

(Intercept) -0.1232 0.2549 -0.483 0.629

elevation -0.7393 0.2045 -3.615 < 0.005

secondary cover -1.7569 0.5457 -3.22 < 0.005

Omnivores

(Intercept) 2.0698 0.3326 6.223 < 0.005

elevation -1.1526 0.3151 -3.658 < 0.005

distance to rivers 1.6523 0.4886 3.382 < 0.005

secondary cover -2.8406 0.7929 -3.582 < 0.005

percentage of tree cover 2.3109 0.7402 3.122 < 0.005

edge density -2.4285 0.7583 -3.203 < 0.005

Herbivores

(Intercept) -0.4305 0.3232 -1.332 0.183

elevation -1.1127 0.4808 -2.314 0.021

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

addition to livestock and crop areas, therefore,

these sites can be ideal for carnivores to hunt

their prey. It has been documented that vegeta-

tion structure is an important variable for cap-

ture success (Watine et al., 2022). In this case,

agroforestry systems can offer better visibility

to predators. Another possible reason are that

the prey of carnivores is usually found in these

modified habitats: Nasua narica (White-nosed

coati), Cuniculus paca (Spotted paca), Mexican

aguti, Collared peccary, American red brocket,

since they feed on corn and beans from the

milpa (Magioli et al., 2019).

The abundance of omnivores was relat-

ed to more variables, preferring low altitude

and conserved areas (primary cover zones)

and lower edge density. In such a fragmented

region, it is possible that the primary forest is

playing an important role in the survival of this

guild, since although they are generalist species,

they require primary forest; they may also be

playing a key functional role as seed dispersers

for forest conservation (Ferreira et al., 2020;

Magioli et al., 2021).

Herbivores had a negative relationship

with elevation; it is possible that in low-altitude

areas where there are more crops, they are tak-

ing advantage of these resources by feeding on

bean crops, as well as on the growing plants

that occur in the acahuales (it is a stage of eco-

logical succession in tropical forests, typically

vegetation that grows in an area abandoned

for agricultural land use), however conserved

forests continue to be a necessary element

for them to remain present (Bodmer, 1989;

Salazar-Ortiz et al., 2022).

The Sierra Negra-Mazateca has experi-

enced processes of deforestation and, main-

ly, continuous degradation since the 1980s

(Velázquez et al., 2003). This work allowed

us to see that these processes are still present,

where 60 % of the vegetation cover of these

mountains is forest, but only 10 % is primary,

the rest is secondary in different stages of suc-

cession. Although secondary vegetation func-

tions as habitat for different species, they are

not a substitute for primary forests (Gibson et

al., 2011; Mendenhall et al., 2016). In the area,

a mosaic of primary and secondary vegetation

was observed, with patches so small that they

seem incapable of hosting populations of some

species of medium and large mammals (Men-

doza et al., 2005; Michalski & Peres, 2007).

The number of species we recorded (16)

represents a little more than a third (38 %)

of the mammals that were historically found

in the region (Briones-Salas et al., 2015). The

absence of species, both large and medium-

sized, suggests that the area is experiencing a

defaunation process, similar to that observed

in other tropical forests (Flores et al., 2014;

Ortiz-Lozada et al., 2017). Studies with cam-

era traps show a greater number of species,

for example, in the Chimalapas and La Selva

Lacandona, 20 and 18 medium- and large-sized

species were detected, respectively, including

three globally threatened species: jaguar (Pan-

thera onca), tapir (Tapirus bairdii) and White-

lipped peccary (Tayassu pecari) (Garmendia et

al., 2013; Lira-Torres & Briones-Salas, 2012).

Among the medium-sized threatened species

not recorded in the Sierra Negra-Mazateca, but

with historical distribution are Derby’s woolly

opossum (Caluromys derbianus), Jaguarundi

(Puma yagouaroundi), Greater grison (Galictis

vittata) and Tayra (Eira barbara; Lavariega et

al., 2017). We also did not record large species

such as Puma (Puma concolor), White-tailed

deer (Odocoileus virginianus) and jaguar. In the

case of the jaguar, not only the transformation

of the landscape contributed to its extirpation,

according to the interviews that were carried

out in the region, the jaguar was persecuted

until it was eliminated (Galindo-Aguilar, 2015).

Although well-conserved protected patch-

es could support a significant proportion of

wildlife, they are generally insufficient to main-

tain long-term populations of most large mam-

mals (Mendoza et al., 2005; Ortiz-Lozada et al.,

2017). Therefore, connectivity through vegeta-

tion restoration should be a necessary measure

to contain species and ecological services in La

Sierra Negra-Mazateca (Hansen et al., 2020;

Knowlton et al., 2019). In addition, awareness-

raising work must be proposed and real oppor-

tunities generated with the rural communities

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

where the potential corridors are located so that

ecological connectivity can be effective. It is

urgent to work multidisciplinary and together

with local inhabitants, academic institutions,

private initiative and the government, generat-

ing alternatives for the effective restoration and

conservation of tropical forests.

Ethical statement: The authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are fully

and clearly stated in the acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

ACKNOWLEDGMENT

R. E. Galindo-Aguilar thanks the National

Council of Humanities, Sciences and Technolo-

gies (CONAHCyT) for the scholarship awarded

to complete his Master’s degree (No 351897).

We would like to thank the local people who

contributed information and guidance during

the fieldwork. The Priority Species Support

Program, the National Commission of Protect-

ed Natural Areas (CONANP) and the College

of Postgraduates (trust 167304). To J. Figel for

his observations and suggestions that improved

this manuscript.

REFERENCES

Aranda-Sánchez, J. M. (2012). Manual para el rastreo de

mamíferos silvestres de México. Comisión Nacional

para el Conocimiento y Uso de la Biodiversidad

(CONABIO).

Azlan, J. M. (2006). Mammal diversity and conservation in

a secondary forest in Peninsular Malaysia. Biodiversity

& Conservation, 15(3), 1013–1025.

Balme, G. A., Slotow, R., & Hunter, L. T. B. (2010).

Edge effects and the impact of non-protected

areas in carnivore conservation: Leopards in the

Phinda-Mkhuze Complex, South Africa. Ani-

mal Conservation, 13(3), 315–323. https://doi.

org/10.1111/j.1469-1795.2009.00342.x

Barlow, J., Gardner, T. A., Araujo, I. S., Ávila-Pires, T. C.,

Bonaldo, A. B., Costa, J. E., Esposito, M. C., Ferreira,

L. V., Hawes, J., Hernandez, M. I. M., Hoogmoed, M.

S., Leite, R. N., Lo-Man-Hung, N. F., Malcolm, J. R.,

Martins, M. B., Mestre, L. A. M., Miranda-Santos,

R., Nunes-Gutjahr, A. L., Overal, W. L., … Peres,

C. A. (2007). Quantifying the biodiversity value of

tropical primary, secondary, and plantation forests.

Proceedings of the National Academy of Sciences of

the United States of America, 104(47), 18555–18560.

https://doi.org/10.1073/PNAS.0703333104/SUPPL_

FILE/03333TABLE4.PDF

Bodmer, R. E. (1989). Ungulate biomass in relation to fee-

ding strategy within Amazonian forests. Oecologia,

81(4), 547–550. https://doi.org/10.1007/BF00378967

Borges, S. H. (2007). Bird assemblages in secondary

forests developing after slash-and-burn agricul-

ture in the Brazilian Amazon. Journal of Tropical

Ecology, 23(4), 469–477. https://doi.org/10.1017/

S0266467407004105

Boron, V., Deere, N. J., Xo, P., & Link, A. (2019). Richness,

diversity, and factors influencing occupancy of mam-

mal communities across human-modified landscapes

in Colombia. Biological Conservation, 232, 108–116.

https://doi.org/10.1016/j.biocon.2019.01.030

Bovendorp, R. S., Brum, F. T., McCleery, R. A., Baiser, B.,

Loyola, R., Cianciaruso, M. V., & Galetti, M. (2019).

Defaunation and fragmentation erode small mammal

diversity dimensions in tropical forests. Ecography, 42,

23–35. https://doi.org/10.1111/ecog.03504

Bowyer, R. T., Boyce, M. S., Goheen, J. R., & Rachlow, J. L.

(2019). Conservation of the world’s mammals: Status,

protected areas, community efforts, and hunting.

Journal of Mammalogy, 100(3), 923–941. https://doi.

org/10.1093/JMAMMAL/GYY180

Bradshaw, C. J. A., Sodhi, N. S., & Brook, B. W. (2009).

Tropical turmoil: A biodiversity tragedy in progress.

Frontiers in Ecology and the Environment, 7(2), 79–87.

https://doi.org/10.1890/070193

Brady, N. C. (1996). Alternatives to slash-and-

burn: a global imperative. Agriculture, Ecosys-

tems & Environment, 58(1), 3–11. https://doi.

org/10.1016/0167-8809(96)00650-0

Briones-Salas, M., Cortés-Marcial, M., & Lavariega, M. C.

(2015). Diversidad y distribución geográfica de los

mamíferos terrestres del estado de Oaxaca, México.

Revista Mexicana de Biodiversidad, 86(3), 685–710.

https://doi.org/10.1016/j.rmb.2015.07.008

Brodie, J. F., Giordano, A. J. & Ambu, L. (2015). Differen-

tial responses of large mammals to logging and edge

effects. Mammalian Biology, 80, 7–13.

Cacelin-Castillo, L. A., Rosas-Rosas, O. C., Martínez-

Meyer, E., García-Chávez, J. H., & Torres-Romero,

E. J. (2020). Potential distribution of the Ocelot

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

(Leopardus pardalis) in southern Sierra Madre Orien-

tal and Sierra Negra, México. Therya, 11(2), 232–238.

Cavada, N., Worsøe-Havmøller, R., Scharff, N., & Rovero,

F. (2019). A landscape-scale assessment of tropical

mammals reveals the effects of habitat and anthro-

pogenic disturbance on community occupancy. PLoS

ONE, 14(4), e0215682.

Ceballos, G., & Oliva, G. (2005). Los mamíferos silvestres

de México (1a ed.). Comisión Nacional para el Cono-

cimiento y Uso de la Biodiversidad (CONABIO),

Fondo de Cultura Económica.

Ceballos, G., de la Torre, J. A., Zarza, H., Huerta, M.,

Lazcano-Barrero, M. A., Barcenas, H., Cassaigne, I.,

Chávez, C., Carreón, G., Caso, A., Carvajal, S., García,

A., Morales, J. J., Moctezuma, O., Monroy-Vilchis,

O., Ruiz, F., & Torres-Romero, E. J. (2021). Jaguar

distribution, biological corridors and protected areas

in Mexico: from science to public policies.Landscape

Ecology,36, 3287–3309.

Challenger, A. (1998). Utilización y conservación de los eco-

sistemas terrestres de México: Pasado, presente y futuro.

Comisión Nacional para el Conocimiento y Uso de

la Biodiversidad (CONABIO), Instituto de Biología

de la Universidad Nacional Autónoma de México,

Agrupación Sierra Madre S.C.

Chao, A., & Jost, L. (2015). Estimating diversity and entropy

profiles via discovery rates of new species. Methods in

Ecology and Evolution, 6(8), 873–882.

Chao, A., Gotelli, N. J., Hsieh, T. C., Sander, E. L., Ma, K. H.,

Colwell, R. K., & Ellison, A. M. (2014). Rarefaction

and extrapolation with Hill numbers: a framework for

sampling and estimation in species diversity studies.

Ecological Monographs, 84, 45–67.

Chuvieco, E. (1991). Fundamentos de teledetección espacial.

Ediciones Rialp.

Cullen, L., Bodmer, R. E., & Valladares-Pádua, C. (2000).

Effects of hunting in habitat fragments of the Atlantic

forests, Brazil. Biological Conservation, 95(1), 49–56.

https://doi.org/10.1016/S0006-3207(00)00011-2

Curtis, P. G., Slay, C. M., Harris, N. L., Tyukavina, A., &

Hansen, M. C. (2018). Classifying drivers of global

forest loss. Science, 361(6407), 1108–1111. https://doi.

org/10.1126/science.aau3445

da Fonseca, G. A. (1989). Small mammal species diversity

in Brazilian tropical primary and secondary forests

of different sizes. Revista Brasileira de Zoologia, 6,

381–422.

da Fonseca, G. A., & Robinson, J. G. (1990). Forest size

and structure: Competitive and predatory effects on

small mammal communities. Biological Conservation,

53(4), 265–294.

Davidson, A. D., Shoemaker, K. T., Weinstein, B., Costa,

G. C., Brooks, T. M., Ceballos, G., Radeloff, V. C.,

Rondinini, C., & Graham, C. H. (2017). Geography

of current and future global mammal extinction risk.

PLoS ONE, 12(11), e0186934. https://doi.org/10.1371/

JOURNAL.PONE.0186934

Díaz-Gallegos, J. R., Mas, J. F., & Velázquez, A. (2010). Trends

of tropical deforestation in Southeast Mexico. Singa-

pore Journal of Tropical Geography, 31(2), 180–196.

https://doi.org/10.1111/j.1467-9493.2010.00396.x

Dirzo, R., & Miranda, A. (1990). Contemporary neotro-

pical defaunation and forest structure, function, and

diversity-A equel to John Terborgh. Conservation

Biology, 4(4), 444–447.

Feinsinger, P. (2001). Designing field studies for biodiversity

conservation. Island Press.

Ferreira, A. S., Peres, C. A., Bogoni, J. A., & Cassano, C.

R. (2018). Use of agroecosystem matrix habitats by

mammalian carnivores (Carnivora): A global-scale

analysis. Mammal Review, 48(4), 312–327. https://doi.

org/10.1111/MAM.12137

Ferreira, A., Peres, C. A., Dodonov, P., & Cassano, C.

(2020). Multi-scale mammal responses to agrofores-

try landscapes in the Brazilian Atlantic Forest: The

conservation value of forest and traditional shade

plantations. Agroforestry Systems, 94(6), 2331–2341.

https://doi.org/10.1007/s10457-020-00553-y

Flores, J. J., Coates, R. I., Sánchez-Cordero, V., & Mendieta,

V. J. (2014). Mamíferos terrestres de la Estación de

Biología Tropical de los Tuxtlas. Revista Digital Uni-

versitaria, 15(4), 1–10.

Food and Agriculture Organization of the United Nations,

& United Nations Environmental Programme. (2020).

The State of the World’s Forests 2020. Forests, biodiver-

sity and people. FAO, UNEP. https://doi.org/10.4060/

ca8642en

Galindo-Aguilar, R. E. (2015). Distribución, abundancia

y conservación del jaguar y sus presas en los bosques

tropicales de dos municipios de la Sierra Negra de Pue-

bla y la Sierra Mazateca de Oaxaca, México [Master’s

tesis, Institución de Enseñanza e Investigación en

Ciencias Agrícolas, México]. Colegio de Postgra-

duados. http://colposdigital.colpos.mx:8080/jspui/

handle/10521/2683

Galindo-Aguilar, R. E., Cacelin-Castillo, L. A., Rosas-Rosas,

O. C., Bravo-Vinaja, M. G., Alcántara-Carbajal, J. L.,

& Vázquez-García, V. (2016). Primeros registros de

ocelote en los bosques tropicales de la Sierra Negra

de Puebla y la Sierra Mazateca de Oaxaca, México.

Therya, 7, 205–211.

Galindo-Aguilar, R. E., Pérez-Hernández, M. J., Reynoso-

Santos, R., Rosas-Rosas, O., & González-Gervacio,

C. (2019). Cambio de uso de suelo, fragmentación

del paisaje y la conservación de Leopardus pardalis

16 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

Linnaeus, 1758. Revista Mexicana de Ciencias Fores-

tales, 10(52), 149–169. https://doi.org/10.29298/rmcf.

v10i52.395

Gallegos-Peña, A., Bello-Gutiérrez, J., & Jesús de la Cruz,

A. (2010). Cuantificación del daño ocasionado por

mamíferos terrestres a cultivos de maíz en el ejido

Oxolotán del municipio de Tacotalpa, Tabasco. En

M. Guerra-Roa, S. Calme, S. Gallina-Tessaro, & E.

Naranjo-Piñera (Eds.), Uso y manejo de fauna silvestre

en el norte de Mesoamérica (pp. 297–314). Secretaria

de Educación del Estado de Veracruz.

García, E. (1964). Modificaciones al sistema de clasificación

climática de Köppen (para adaptarlo a las condiciones

de la República Mexicana). Instituto de Geografía,

Universidad Nacional Autónoma de México.

García-Marmolejo, G., Escalante, T., & Morrone, J. J.

(2008). Establecimiento de prioridades para la con-

servación de mamíferos terrestres neotropicales de

México. Mastozoologia Neotropical, 15, 41–65.

Garmendia, A., Arroyo-Rodríguez, V., Estrada, A., Naran-

jo, E. J., & Stoner, K. E. (2013). Landscape and

patch attributes impacting medium- and large-sized

terrestrial mammals in a fragmented rain forest. Jour-

nal of Tropical Ecology, 29(4), 331–344. https://doi.

org/10.1017/S0266467413000370

Gibson, L., Lee, T. M., Koh, L. P., Brook, B. W., Gardner,

T. A., Barlow, J., Peres, C. A., Bradshaw, C. J. A.,

Laurance, W. F., Lovejoy, T. E., & Sodhi, N. S. (2011).

Primary forests are irreplaceable for sustaining tropi-

cal biodiversity. Nature, 478(7369), 378–381. https://

doi.org/10.1038/nature10425

Graham, S. I., Kinnaird, M. F., O’Brien, T. G., Vågen, T. G.,

Winowiecki, L. A., Young, T. P., & Young, H. S. (2019).

Effects of land-use change on community diversity

and composition are highly variable among functio-

nal groups. Ecological Applications, 29(7), e01973

https://doi.org/10.1002/EAP.1973

Hansen, M. C., Wang, L., Song, X. P., Tyukavina, A., Turu-

banova, S., Potapov, P. V., & Stehman, S. V. (2020).

The fate of tropical forest fragments. Science Advan-

ces, 6(11), eaax8574. https://doi.org/10.1126/sciadv.

aax8574

Harvey, C. A., Medina, A., Sánchez, D. M., Vílchez, S.,

Hernández, B., Saenz, J. C., Maes, J. M., Casanoves, F.,

& Sinclair, F. L. (2006). Patterns of animal diversity in

different forms of tree cover in agricultural landsca-

pes. Ecological Applications, 16(5), 1986–1999.

Hsieh, T. C., Ma, K. H., & Chao, A. (2016). iNEXT: An R

package for interpolation and extrapolation of species

diversity (Hill numbers). Methods in Ecology and Evo-

lution, 7, 1451–1456.

Instituto Nacional de Estadística, Geografía e Informática.

(2010). Censo de población y vivienda [Conjunto de

datos]. Información demográfica y social. https://

www.inegi.org.mx/programas/ccpv/2010/

Instituto Nacional de Estadística, Geografía e Informática.

(2015). Land cover and use, scale 1:250,000. Instituto

Nacional de Estadística y Geografía. http://www.inegi.

org.mx/geo/contenidos/recnat/usosuelo/

ITT. (2009). ENVI 4.7 [Software]. ITT Visual Information

Solutions.

Jenkins, C. N., Pimm, S. L., & Joppa, L. N. (2013). Global

patterns of terrestrial vertebrate diversity and conser-

vation. Proceedings of the National Academy of Sciences

of the United States of America, 110(28), 2603–2610.

https://doi.org/10.1073/PNAS.1302251110/

Jenks, K. E., Chanteap, P., Damrongchainarong, K., Cutter,

P., Cutter, P., Redford, T., Lynam, J. A., Howard, J., &

Leimgruber, P. (2011). Using relative abundance indi-

ces from camera trapping to test wildlife conservation

hypotheses an example from Khao Yai National Park,

Thailand. Tropical Conservation Science, 4(2), 113–

131. https://doi.org/10.1177/194008291100400203

Kiffner, C., Stoner, C., & Caro, T. (2013). Edge effects

and large mammal distributions in a national park.

Animal Conservation, 16(1), 97–107. https://doi.

org/10.1111/j.1469-1795.2012.00577.x

Knowlton, J. L., Mata-Zayas, E. E., Ripley, A. J., Valenzuela-

Cordova, B., & Collado-Torres, R. (2019). Mammal

diversity in oil palm plantations and forest fragments

in a highly modified landscape in Southern Mexico.

Frontiers in Forests and Global Change, 2, 67. https://

doi.org/10.3389/ffgc.2019.00067

Kruuk, H. (2002). Hunter and hunted: Relationships between

carnivores and people. Cambridge University Press.

Lacher, T. E., Davidson, A. D., Fleming, T. H., Gómez-Ruiz,

E. P., McCracken, G. F., Owen-Smith, N., Peres, C.

A., & Vander-Wall, S. B. (2019). The functional roles

of mammals in ecosystems. Journal of Mammalogy,

100(3), 942–964. https://doi.org/10.1093/jmammal/

gyy183

Lavariega, M. C., Martín-Regalado, N., Monroy-Gamboa,

A. G., & Briones-Salas, M. (2017). Estado de con-

servación de los vertebrados terrestres de Oaxaca,

México. Ecosistemas y Recursos Agropecuarios, 4(10),

135–146. https://doi.org/10.19136/ERA.A4N10.855

Lira-Torres, I., & Briones-Salas, M. (2012). Abundancia

relativa y patrones de actividad de los mamíferos

de los Chimalapas, Oaxaca, México. Acta Zoológica

Mexicana, 28(3), 566–585.

Magioli, M., de Barros-Ferraz, K. M. P. M., Garcia-Chiare-

llo, A., Galetti, M., Setz, E. Z. F., Pereira-Paglia, A. P.,

Abrego, N., Ribeiro, M. C., & Ovaskainen, O. (2021).

Land-use changes lead to functional loss of terrestrial

mammals in a Neotropical rainforest. Perspectives in

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

Ecology and Conservation, 19(2), 161–170. https://doi.

org/10.1016/J.PECON.2021.02.006

Magioli, M., Moreira, M. Z., Fonseca, R. C. B., Ribeiro, M.

C., Rodrigues, M. G., & de Barros-Ferraz, K. M. P.

M. (2019). Human-modified landscapes alter mam-

mal resource and habitat use and trophic structure.

Proceedings of the National Academy of Sciences of

the United States of America, 116(37), 18466–18472.

https://doi.org/10.1073/PNAS.1904384116

McGarigal, K., & Marks, B. J. (1995). FRAGSTATS: spatial

pattern analysis program for quantifying landscape

structure [Software]. U.S. Department of Agriculture,

Forest Service, Pacific Northwest Research Station.

McShea, W. J., Stewart, C., Peterson, L., Erb, P., Stuebing,

R., & Giman, B. (2009). The importance of secon-

dary forest blocks for terrestrial mammals within an

Acacia/secondary forest matrix in Sarawak, Malaysia.

Biological Conservation, 142(12), 3108–3119.

Medellín, R. A. (1994). Mammal Diversity and Con-

servation in the Selva Lacandona, Chiapas, Mexi-

co. Conservation Biology, 8(3), 780–799. https://doi.

org/10.1046/j.1523-1739.1994.08030780.x

Mendenhall, C. D., Shields-Estrada, A., Krishnaswami, A.

J., & Daily, G. C. (2016). Quantifying and sustaining

biodiversity in tropical agricultural landscapes. Proce-

edings of the National Academy of Sciences, 113(51),

14544–14551.

Mendoza, E., Fay, J., & Dirzo, R. (2005). A quantitati-

ve analysis of forest fragmentation in Los Tuxt-

las, southeast Mexico: Patterns and implications for

conservation. Revista Chilena de Historia Natural,

78(3), 451–467. http://www.redalyc.org/articulo.

oa?id=369944275008

Meyer, N., Esser, H. J., Moreno, R., van Langevelde, F.,

Liefting, Y., Oller, D. R., Vogels, C. B. F., Carver, A. D.,

Nielsen, C. K., & Jansen, P. A. (2015). An assessment

of the terrestrial mammal communities in forests of

Central Panama, using camera-trap surveys. Journal

for Nature Conservation, 26, 28–35.

Michalski, F., & Peres, C. A. (2007). Disturbance-media-

ted mammal persistence and abundance-area

relationships in Amazonian forest fragments. Con-

servation Biology, 21(6), 1626–1640. https://doi.

org/10.1111/j.1523-1739.2007.00797.x

Millennium Ecosystem Assessment. (2005). Ecosystems and

human well-being: Synthesis. Island Press.

Moumane, A., Al Karkouri, J., Benmansour, A., El Ghazali,

F. E., Fico, J., Karmaoui, A., & Batchi, M. (2022).

Monitoring long-term land use, land cover change,

and desertification in the Ternata Oasis, Middle

Draa Valley, Morocco. Remote Sensing Applications:

Society and Environment, 26, 100745. https://doi.

org/10.1016/J.RSASE.2022.100745

Muench, C., & Martínez-Ramos, M. (2016). Can commu-

nity-protected areas conserve biodiversity in human-

modified tropical landscapes? The case of terrestrial

mammals in southern Mexico. Tropical Conservation

Science, 9(91), 178–202.

Naughton-Treves, L., Mena, J. L., Treves, A., Alvarez, N., &

Radeloff, V. C. (2003). Wildlife survival beyond park

boundaries: The impact of slash-and-burn agricul-

ture and hunting on mammals in Tambopata, Peru.

Conservation Biology, 17(4), 1106–1117. https://doi.

org/10.1046/j.1523-1739.2003.02045.x

Newman, H. H. (1913). The natural history of the nine-

banded armadillo of Texas. The American Naturalist,

47(561), 513–539.

Noss, A., Polisar, J., Maffei, L., & Garcia, R. (2013). Evalu-

ando la densidad de jaguares con trampas cámara.

Programa para la Conservación del Jaguar, Programa

para Latinoamérica y el Caribe, Wildlife Conserva-

tion Society.

O’Brien, T. G., Kinnaird, M. F., & Wibisono, H. T. (2003).

Crouching tigers, hidden prey: Sumatran tiger and

prey populations in a tropical forest landscape. In Ani-

mal Conservation Forum (Vol. 6, No. 2, pp. 131–139).

Cambridge University Press.

Ortiz-Lozada, L., Pelayo-Martínez, J., Mota-Vargas, C.,

Demeneghi-Calatayud, A. P., & Sosa, V. J. (2017).

Absence of large and presence of medium-sized mam-

mal species of conservation concern in a privately

protected area of rain forest in Southeastern Mexico.

Tropical Conservation Science, 10, 1940082917738093.

https://doi.org/10.1177/1940082917738093

Pardo, L. E., Campbell, M. J., Edwards, W., Clements,

G. R., & Laurance, W. F. (2018). Terrestrial mam-

mal responses to oil palm dominated landscapes in

Colombia. PLoS ONE, 13(5), e0197539.

Parry, L., Barlow, J., & Peres, C. A. (2007). Large-vertebrate

assemblages of primary and secondary forests in the

Brazilian Amazon. Journal of Tropical Ecology, 23(6),

653–662.

Peres, C. A. (1997). Evaluating the sustainability of subsis-

tence hunting in tropical forest. Centre for Social and

Economic Research on the Global Environment.

Phillips, H. R. P., Newbold, T., & Purvis, A. (2017). Land-

use effects on local biodiversity in tropical forests

vary between continents. Biodiversity and Conser-

vation, 26(9), 2251–2270. https://doi.org/10.1007/

s10531-017-1356-2

Pires, M. M., Benchimol, M., Cruz, L. R., & Peres, C. A.

(2023). Terrestrial food web complexity in Ama-

zonian forests decays with habitat loss. Current

Biology, 33(2), 389–396. https://doi.org/10.1016/j.

cub.2022.11.066

18 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73: e58524, enero-diciembre 2025 (Publicado Abr. 29, 2025)

T. N. E., Rawson, B. M., Guegan, F., Kissing, J., Weg-

mann, M., & Wilting, A. (2019). Habitat degrada-

tion and indiscriminate hunting differentially impact

faunal communities in the Southeast Asian tropical

biodiversity hotspot. Communications Biology, 2, 396.

https://doi.org/10.1038/s42003-019-0640-y

Velázquez, A., Durán, E., Ramírez, I., Mas, J. F., Bocco,

G., Ramírez, G., & Palacio, J. L. (2003). Land use-

cover change processes in highly biodiverse areas:

The case of Oaxaca, Mexico. Global Environmen-

tal Change, 13(3), 175–184. https://doi.org/10.1016/

S0959-3780(03)00035-9

Watine, L. N., Willcox, E. V., Clark, J. D., & Harper, C.

A. (2022). Rainforest carnivore ecology in a mana-

ged forest reserve: Differential seasonal correlates

between habitat components and relative abundan-

ce. Biological Conservation, 276, 109814. https://doi.

org/10.1016/J.BIOCON.2022.109814

William, W. O., van Manen, F. T., Sharp, S. P., & Ratnayeke,

S. (2023). Secondary forest within a timber plantation

concession in Borneo contributes to a diverse mam-

mal assemblage. Global Ecology and Conservation, 43,

e02474. https://doi.org/10.1016/j.gecco.2023.e02474

Zapata-Ríos, G., Suárez, R. E., Utreras, B. V., Vargas, O. J.,

Zapata Ríos, G., & Vargas, J. (2006). Evaluation of

anthropogenic threats in Yasuní National Park and its

implications for wild mammal conservation. Lyonia,

10, 47–57.

Zhang, B., Li, W., & Zhang, C. (2022). Analyzing land

use and land cover change patterns and population

dynamics of fast-growing US cities: Evidence from

Collin County, Texas. Remote Sensing Applications:

Society and Environment, 27, 100804. https://doi.

org/10.1016/J.RSASE.2022.100804

Zhang, Y., Liu, X., Lv, Z., Zhao, X., Yang, X., Jia, X., Sun,

W., He, X., He, B., Cai, Q., & Zhu, Y. (2019). Animal

diversity responding to different forest restoration

schemes in the Qinling Mountains, China. Ecological

Engineering, 136, 23–29.

Zuur, A. F., Ieno, E. N., Walker, N., Saveliev, A. A.,

& Smith, G. M. (2009). Mixed effects models and

extensions in ecology with R. Springer. https://doi.

org/10.1007/978-0-387-87458-6

R Core Team. (2012). The R project for statistical computing.

R. https://www.r-project.org

Rovero, F., & Marshall, A. R. (2009). Camera trapping pho-

tographic rate as an index of density in forest ungu-

lates. Journal of Applied Ecology, 46(5), 1011–1017.

Salazar-Ortiz, J., Barrera-Perales, M., Bravo-Vinaja, M. G.,

Serna-Lagunes, R., Ocaña-Parada, C. de J., & Gaste-

lum-Mendoza, F. I. (2022). Populational attributes of

the central american red brocket deer (Mazama tema-

ma) in the Sierra de Zongolica, Veracruz, Mexico.

Agrociencia, 56(3), 492–517. https://doi.org/10.47163/

AGROCIENCIA.V56I3.2805

Sánchez-Cordero, V., Botello, F., Flores-Martínez, J. J.,

Gómez-Rodríguez, R. A., Guevara, L., Gutiérrez-

Granados, G., & Rodríguez-Moreno, Á. (2014). Bio-

diversity of Chordata (Mammalia) in Mexico. Revista

Mexicana de Biodiversidad, 85, 496–504.

Saunders, D. A., Hobbs, R. J., & Margules, C. R. (1991).

Biological consequences of ecosystem fragmentation:

A review. Conservation Biology, 5(1), 18–32.

Scales, B. R., & Marsden, S. J. (2008). Biodiversity in small-

scale tropical agroforests: A review of species richness

and abundance shifts and the factors influencing

them. Environmental Conservation, 35(2), 160–172.

https://doi.org/10.1017/S0376892908004840

Silva-Caballero, L. A. (2019). Preferencias alimentarias y

su relación con la bioenergética del jaguar (Panthera

onca) en la Reserva de la Biósfera Sierra del Abra Tan-

chipa, San Luis Potosí, México [Doctoral dissertation,

Institución de Enseñanza e Investigación en Cien-

cias Agrícolas, México]. Colegio de Postgraduados.

http://colposdigital.colpos.mx:8080/jspui/bitstream/

handle/10521/3851/Silva_Caballero_LA_DC_Gana-

deria_2019.pdf?sequence=1

Slater, H. D., Gillingham, P. K., Pratt, V., Eaton, B., Fletcher,

S., Abdullah, A., & Korstjens, A. H. (2023). Living

on the edge: Forest edge effects on microclimate and

terrestrial mammal activity in disturbed lowland

forest in Sumatra, Indonesia. Oryx: The International

Journal of Conservation, 58(2), 228–239.

Tilker, A., Abrams, J. F., Mohamed, A., Nguyen, A., Wong,

S. T., Sollmann, R., Niedballa, J., Bhagwat, T., Gray,