Mammalian Biology 98 (2019) 173–178

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Mammalian Biology
journal homepage: www.elsevier.com/locate/mambio

Original investigation

Jaguar density in a mosaic of disturbed/preserved areas in

southeastern Mexico
Mircea G. Hidalgo-Mihart a,b,∗ , Alejandro Jesús-de la Cruz a,b ,
Fernando M. Contreras-Moreno a,d , Rugieri Juárez-López a , Yaribeth Bravata-de la Cruz a ,
Diana Friedeberg b , Pedro Bautista-Ramírez c
a
División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco, Villahermosa, Tabasco, 86039, Mexico
b
Panthera Mexico, San Miguel de Allende, Guanajuato, 37700, Mexico
c
Academia de Ingeniería Ambiental, Instituto Tecnológico Superior de los Ríos, Balancán, Tabasco, 86930, Mexico
d
Proyecto GEF Especies en Riesgo. CONANP-PNUD, Reserva de la Biósfera de Calakmul, Calakmul, Campeche, 24640, Mexico

a r t i c l e i n f o a b s t r a c t

Article history: Jaguar populations in Mexico have been extensively reduced to the point where the species is consid-
Received 21 February 2018 ered Endangered. In south-eastern Mexico, jaguar density estimations have focused in the largest Jaguar
Accepted 20 September 2019 Conservation Units (JCUs) but are lacking for the small, isolated JCUs where natural habitats are usu-
Available online 22 September 2019
ally combined with farming areas. We installed 103 camera trap stations across an area in the small
Handled by Mauro Lucherini and isolated JCU of Laguna de Terminos and estimated the jaguar density using spatially explicit capture-
recapture (SECR) models with the sex of the identified jaguars as a covariate. We obtained 126 pictures of
Keywords:
adult jaguars in 7052 camera trap days, corresponding to seven females, seven males and three individuals
Carnivore of unidentified sex. We estimated a density of 1.934 ± 0.529 jaguars/100 km2 . Our jaguar density esti-
Conservation mation was in the lower range of those reported elsewhere in preserved areas of south-eastern Mexico,
Panthera onca probably because habitat quality has been reduced by agriculture and cattle grazing.
Laguna de Terminos © 2019 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
Wetland

Introduction
As the top predator in the Neotropics, the jaguar (Panthera onca)
may have large impacts on prey populations and play an important
role in trophic cascades and ecosystem regulation (Cavalcanti and
Gese, 2010). However, due to habitat modification and conflicts
with humans jaguar populations have been extensively reduced
across their range (Sanderson et al., 2002; de la Torre et al., 2017a)
and listed as “Near Threatened” by the International Union for Con-
servation of Nature (IUCN) (Quigley et al., 2017).
In Mexico, jaguar populations have been eradicated from 60%
of their original distribution area (Rodríguez-Soto et al., 2011)
and the species is currently considered Endangered in the country
(SEMARNAT, 2010) mostly due to habitat loss and fragmentation,
∗ Corresponding author at: División Académica de Ciencias Biológicas, Universi-
dad Juárez Autónoma de Tabasco, Villahermosa, Tabasco, 86039, Mexico.
E-mail addresses: mhidalgo@yahoo.com (M.G. Hidalgo-Mihart),
alexjc05@hotmail.com (A. Jesús-de la Cruz), fernandom28@yahoo.com
(F.M. Contreras-Moreno), ecolrugieri@hotmail.com (R. Juárez-López),
yarybravata@gmail.com (Y. Bravata-de la Cruz), dfriedeberg@panthera.org
(D. Friedeberg), cherico 92@hotmail.com (P. Bautista-Ramírez).
direct hunting, prey depletion, and the construction of new infras-
tructure (Zarco-González et al., 2013; Ceballos et al., 2016; de la
Torre et al., 2017a). The Mexican Conservation Action Program for
the Jaguar (CONANP, 2009) established the necessity to assess the
abundance of jaguar populations across the country and several
efforts have been made to accomplish this goal (e.g. de la Torre
and Medellín, 2011; Ávila-Nájera et al., 2015; Carrera-Treviño et al.,
2016) including a national jaguar census (Ceballos et al., 2016).
In southeastern Mexico, the major Jaguar Conservation Units
(JCUs, defined as areas with a stable prey community, known or
believed to contain a resident population of at least 50 breeding
individuals; Sanderson et al., 2002) are located in the largest con-
tinuous areas of tropical forests, but a series of more isolated JCUs
are still considered viable (JCUs of Petenes-Ria Celestun and Pan-
tanos de Centla-Laguna de Terminos; Rabinowitz and Zeller, 2010).
Whereas jaguar densities have been estimated in the large areas of
tropical forests (e.g. de la Torre and Medellin, 2011; Ávila-Nájera
et al., 2015; Ceballos et al., 2016), to our knowledge no studies
have been made in the more isolated JCUs. The Pantanos de Centla-
Laguna de Terminos JCU (hereafter called Laguna de Terminos JCU),
with an area of approximately 8904 km2 (Rabinowitz and Zeller,
2010), is considered the JCU with the highest risk of becoming

https://doi.org/10.1016/j.mambio.2019.09.009
1616-5047/© 2019 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
174 M.G. Hidalgo-Mihart et al. / Mammalian Biology 98 (2019) 173–178
isolated from others in southeastern Mexico and is in critical dan-
ger of disappearing (Chávez et al., 2016; de la Torre et al., 2017a;
Hidalgo-Mihart et al., 2017a). In a continental analysis de la Torre
et al. (2017a) estimated that 26–52 jaguars could potentially live
in Laguna de Terminos. However, because this number was based
on extrapolated data from other areas, the urgency of local density
estimations in all the identified jaguar subpopulations (including
Laguna de Terminos JCU) remains a priority.
Jaguar density estimations in disturbed areas are scarce across
jaguar distribution range, (Paviolo et al., 2008; Boron et al., 2016) in
Mexico they have only been performed in the northern (Gutiérrez-
González et al., 2012) and western (Figel et al., 2016) portions of the
country. In southern Mexico jaguar density has been estimated only
in regions where natural habitats are largely preserved and human
activities are low (eg. de la Torre and Medellín, 2011; Ávila-Nájera
et al., 2015). The objective of this paper was to determine the jaguar
density in the southwestern portion of the critically endangered
JCU Laguna de Terminos, where large cattle grazing and agricultural
areas are mixed with patches of preserved forest.
Material and methods
Study area
The study area is located in the coastal plains of the Gulf
of Mexico, in the municipalities of Carmen and Palizada, in the
southwest portion of the state of Campeche, Mexico (91◦ 45’50”
W; 18◦ 19’50” N; Fig. 1). The area forms part of the Mesoameri-
can Gulf-Caribbean mangroves and Pantanos de Centla terrestrial
ecosystems (Olson et al., 2001). The climate in the region is warm-
humid, with a mean temperature of 27 ◦ C and up to 2000 mm of
annual precipitation (INEGI, 2015a). Most of the region is subject to
seasonal flooding that can last from 2 to 8 months (June–February)
depending on the topography. The natural vegetation of the area is
greatly contingent upon the flooding regime and includes wetlands,
flooded savannahs, mangroves, sub-evergreen flooded rain forests,
and tropical deciduous flooded forests (Ocaña and Lot, 1996).
The study area is near the federal protected area of Laguna de
Terminos Flora and Fauna Protection Area (Fig. 1). Land tenure in
the region is composed of a series of privately-owned ranches, and
less than 10% is under the ejido land tenure regime (a form of prop-
erty right based on common-use of resources by rural settlements).
The area has been used mostly for industrial agriculture and cattle
grazing, and currently more than 50% of the natural forests of the
region have been transformed (Soto-Galera et al., 2010). However,
since 2010, several private properties covering c.a. 150 km2 located
in the eastern portion of the study area removed all cattle from
their properties and have destined the land only for conservation
purposes (hereafter called Private Conservation Areas).
Camera trapping survey and design
We estimated the jaguar density in the study area using cam-
era traps and spatially explicit capture-recapture (SECR) models
(Borchers and Efford, 2008). We carried out a camera trapping sur-
vey in the study area from March to August 2016. We followed
Tobler and Powell’s (2013) recommendations when setting up the
camera trap survey and installed 103 camera trap stations in an area
of 36 × 15 km (540 km2 ). Though the original design of the study
had cameras separated by 1.5 to 2 km from each other, in order
to increase the capture probability, we installed them in habitats
that are frequently used by jaguars (Hidalgo-Mihart et al., 2015).
This resulted in having 100 of the camera stations distributed in
zones covered by primary or secondary forests, and only three sta-
tions deployed in habitats consisting of agriculture and induced
grasslands (Fig. 1). Jaguar density estimations using SECR models
require that all animals in the study area be exposed to traps and in
theory have a capture probability of >0 (Tobler and Powell, 2013).
Because the access to three private properties inside the grid was
not granted, we were forced to leave several forested areas without
camera stations. However, because these properties were sepa-
rated from each other and the forest area in each one is less than
50 km2 , we do not consider that excluding them from the analysis
will affect our estimations. Additionally, because the home range of
the females in the region is larger than the private areas where the
cameras were not installed (home range size for female jaguars in
the nearby areas is smaller than males and varies between 184 km2
and 204 km2 ; Chávez, 2010; de la Torre et al., 2017b), we are con-
fident that the capture probability of all the adult jaguars living in
the study area is >0.
We installed sixty-five camera stations consisting of two Pan-
theracams model IV or V, or two Cuddeback Camera Long Range IR
cameras and 38 stations of only one Pantheracam. Cameras were
located in trails and roads and attached to trees at a height of 50 cm
above the ground and programmed to operate 24 h per day. We
placed a partially opened sardine can at about 5 m in front of each
camera to function as a lure. Placing lures has been shown to not
bias density estimates in large carnivores but may improve indi-
vidual identifications or detectability (Gerber et al., 2012; du Preez
˛
et al., 2014; Jedrzejewski et al., 2017).
Cameras were active in the field for at least 72 consecutive days,
yet due to logistic constrains we did not operate all the camera
stations simultaneously and the survey was performed in three
consecutive blocks. The first block consisted of 37 camera stations
that operated from March to May 2016 in the eastern portion of the
study area, mostly within the private conservation areas (Fig. 1).
The second block consisted of 34 camera traps that operated from
May to July 2016 within 3 private proprieties of the western por-
tion of the study area. Finally, the third block consisted of 27 camera
traps that operated in two private properties and two ejidos located
in the central portion of the study area from June to August 2016
(Fig. 1).
The sampling effort per camera was obtained by adding the
number of camera days that each individual camera station func-
tioned in the field, from the date when the camera was first active
to the date of the last photograph taken. We considered a double
station operational when at least one of the two cameras was work-
ing, and for all SECR models we used the exact number of days each
station was operational in order to reduce bias caused by camera
failure (Foster, 2008).
We identified jaguar individuals in photographs based on their
unique spot patterns and identified gender by secondary sexual
traits (Silver et al., 2004). If a photo could not be clearly assigned
to an individual it was removed from the analysis. We performed
the analysis using all the individuals identified by both sides. In
the cases where we did not have both sides of the individual as
occurred in the single camera stations, we used the identification
of the side where we had more identified individuals to estimate
the minimum number of individuals present in the area (Paviolo
et al., 2008).
Jaguar density estimation
To estimate jaguar densities in the study area, we applied maxi-
mum likelihood SECR models with a half-normal detection function
using the secr 3.0.1 R package (Borchers and Efford, 2008; Efford
et al., 2009; Efford, 2017). We obtained the encounter rate at the
home range center (g0), and the scale parameter ␴ which describes
how the encounter rate decreases with increasing distance from the
home range center and is related to the home range radius (Tobler
et al., 2013). To calculate the home range size, we used the Calhoun
 M.G. Hidalgo-Mihart et al. / Mammalian Biology 98 (2019) 173–178 175

Fig. 1. The figure shows the location of the camera stations throughout the study area, the location of the camera stations where jaguars where detected, and the effective
trapping area of the survey. The camera station blocks represent the timing when the cameras where active during the survey. The first block operated from March to May
2016, the second block from May to July 2016 and the third block from June to August 2016. The land use type in the study area was obtained from the Inventario Nacional
Forestal Serie V (INEGI, 2015b).

and Casby (1958) method and defined it as the circle of 2.45␴ radius
around the center of the home range that concentrates 95% of activ-
ity records in a circular bivariate normal home range (Petit et al.,
2017).
To determine the effect of the sex of the jaguars on the den-
sity estimation, we performed the SECR modelling using sex as a
covariate. We compared four resulting models (null model, g0, ␴
and g0 + ␴) using the Akaike Information Criterion corrected for
small sample sizes (AICc; Anderson and Burnham, 2002). Also, we
tested for differences between the best candidate models and the
null model using the likelihood ratio test.
Results
We recorded data from 98 camera trap stations (five of the 103
original camera stations were vandalized). Sixty-two of the cam-
era stations were installed in six private proprieties and two ejidos
where the main activities are agriculture and cattle grazing; the
remaining camera stations (32) were installed in Private Conser-
vation Areas. The final separation between camera stations varied
from 935 to 6798 m.
With a final trapping effort of 7052 camera days, we obtained
126 adult jaguar pictures corresponding to seven females (74 cap-
tures), seven males (49 captures) and three from unidentified sex
(three captures). We also obtained one picture of a jaguar kitten
of unidentified sex, but it was not included in the analysis. Due to
the low quality of some images, 12 jaguar photographs could not
be clearly assigned to an individual and were removed from the
analysis. The number of captures per individual female jaguar was
36, 14, 8, 7, 6, 2, and 1; in the case of male jaguars, the number
of captures per individual was 24, 8, 5, 5, 3, 2, and 2. The jaguars
of unidentified sex had only one capture per individual. In 38.8%
of the total camera stations we had at least one jaguar picture (38
cameras; Fig. 1). The maximum number of individuals captured in
one camera station was six.
The best model (Table 1) had a sex-specific ␴ and a constant g0.
We found differences between the best model and the null model
(likelihood ratio test: ␹2 = 14.621, df = 1, p = 0.00013) as well as
with the second candidate model (sex-specific ␴ and g0; likelihood
ratio test: ␹2 = 12.48, df = 1, p = 0.00041). Mean population den-
sity obtained with the best model was 1.934 ± 0.529 jaguars/100
km2 . We found that the estimated ␴ and home range for females
was 1883.41 m and 66.86 km2 respectively, and that it was smaller
than for males (4401.86 m and 365.38 km2 , respectively; Table 1).
The encounter probability g0 was 0.01401 for both sexes (Table 1).
Discussion
Even under the current conditions of habitat alteration and frag-
mentation in the study area, we found evidence of an established
176 M.G. Hidalgo-Mihart et al. / Mammalian Biology 98 (2019) 173–178
Table 1
Comparison of jaguar density estimates obtained from Spatially Explicit Capture Recapture (SECR) models, based on camera trap data surveyed in a mosaic of dis-
turbed/preserved areas in southeastern México. Density.- jaguar density (ind/100 km2 ); g0, encounter rate (capture occasion); ␴, scale parameter (m); AICc, Akaike Information
Criterion corrected for small sample sizes: AIC wt, Akaike Information Criterion weights.
Model Sex Density ± SE g0 ± SE
␴ M
+ 1.934 ± 0.529 0.01401 ± 0.00201
F 1883.41 ± 197.46
Sex
g0 M 0.01629 + 0.00289
+ 1.924 ± 0.533
F 0.01015 ± 0.00267
g0
␴ M 0.01730 ± 0.00298
+ 1.427 ± 0.360
F 0.00574 ± 0.00134
Sex
Null model 1.343 ± 0.335 0.01244 ± 0.00003
jaguar population that includes the presence of several females and
at least one jaguar kitten, indicating a reproductive population in
the area (Karanth et al., 2006; MacDonald et al., 2010; Andersen
et al., 2012). Although the estimated jaguar density was in the lower
range of those reported elsewhere in preserved areas of south-
eastern Mexico, it was comparable to those obtained in some areas
of the west and northwest of Mexico (see Supplementary Material
1).
The recorded low density could be the effect of the landscape
composition in the study area which consists of a mosaic of dis-
turbed and preserved habitats. Jaguar densities across landscapes
where human activities are predominant tend to be lower than
in preserved areas (e.g. Paviolo et al., 2008; Boron et al., 2016).
Nevertheless, if relatively large natural areas are preserved and
there is limited hunting of jaguars and their prey, the conservation
of jaguar populations has been considered possible in agricul-
ture/cattle grazing landscapes (Boron et al., 2016).
Our best density estimation model included the sex covariate.
We found that females had smaller home ranges than males. A
consequence of this difference is that in our best model the jaguar
density estimation that included the individual sex as a covariate
was 44% higher than the density estimated by the null model. Previ-
ous work has shown that home range size and movement patterns
can vary between male and female jaguars and that including these
covariates can improve density estimates (Sollmann et al., 2011;
Tobler et al., 2013; Boron et al., 2016; Petit et al., 2017).
In order to cover a larger survey area, our survey was per-
formed in three blocks and active for six months. As with all closed
capture–recapture models, SECR models assume a closed popula-
tion for the duration of the study (Tobler et al., 2013). Currently,
there is insufficient data from jaguar studies to indicate for how
long population closure can be assumed (Tobler and Powell, 2013),
and it is uncertain if our survey could influence the population clo-
sure assumption of the SECR models. However, the operation of
numerous stations and a large survey size area permitted the acqui-
sition of photographs of 17 individual jaguars with a relatively large
number of recaptures, compared with surveys where the number
of captured individuals ranged from 5 to 12 (e.g. de la Torre and
Medellín, 2011; Ávila-Nájera et al., 2015). Therefore, even with the
uncertainty of compliance with the closed population assumption
of the SECR, the higher number of captures improves the reliability
of our jaguar density estimation.
Using our density estimation for the entire area of 8904 km2
covered by the Laguna de Terminos JCU, we calculated that the JCU
could potentially host a jaguar population of 172 individuals (± 47
jaguars). However, this number could be inaccurate because it con-
siders that the entire JCU has the same conditions that we had in
our survey. We performed the study in an area were cattle ranching
is the most important use of the land and is mixed with preserved
forests, yet across the JCU the habitat conditions and human activ-
ities have considerable variations. Hydrophilic vegetation is one
of the most important vegetation types in the JCU covering more
than 1230 km2 in Laguna de Terminos (Soto-Galera et al., 2010)
␴ ± SE AICc  AICc AICc wt K
4401.86 ± 362.76
1631.08 0.00 0.79 5
4285.19 ± 347.84
1633.76 2.68 0.21 6
2077.73 ± 286.21
3919.40 ± 296.34 1641.29 10.22 0.00 5
3965.115 ± 306.18 1651.79 20.72 0.00 4
and ca. 1760 km2 in the Centla region (de la Rosa et al., 2017).
Jaguar detection in hydrophilic vegetation is infrequent and has
not been achieved in areas where this vegetation type is dominant
(Hidalgo-Mihart et al., 2017a,b). This suggests that jaguars’ use of
this type of vegetation is probably reduced, which would signify a
reduction in the available habitat for the species in the region. Also,
mangroves cover extensive areas in the JCU (ca. 795 km2 in Laguna
de Terminos and 134 km2 in Centla; Soto-Galera et al., 2010; de
la Rosa et al., 2017) and although in has historically been consid-
ered that jaguars could occur in these habitats in Mexico(Leopold,
1965; Aranda, 1996), and they have been previously detected in this
type of vegetation in the Laguna de Terminos JCU (Hidalgo-Mihart
et al., 2015), it is uncertain if our density estimation would hold for
mangroves.
At an international level, the Laguna the Terminos JCU has been
listed as an important conservation area for the species (Rabinowitz
and Zeller, 2010; Hidalgo-Mihart et al., 2017b; de la Torre et al.,
2017a), yet the Mexican Conservation Action Program for the Jaguar
(CONANP, 2009) has indicated that it is not a conservation pri-
ority for the country. Furthermore, a nationwide analysis did not
identify the area as important for jaguar conservation in Mexico
(Rodríguez-Soto et al., 2011). Our results showed that in spite of
a considerably disturbed landscape, a small but significant jaguar
population is surviving in the area. Our results increase the knowl-
edge of the jaguar population in this small JCU in Mexico and should
be considered in further conservation plans for jaguar populations
in the country as well as in future studies that identify conser-
vation priorities or corridors. This is especially important because
the Laguna de Terminos JCU is under increasing threat of isolation
from other jaguar conservation areas (Chávez et al., 2016; Hidalgo-
Mihart et al., 2017a; de la Torre et al., 2017a).
In the south of Mexico, jaguar density estimations have been
generally calculated using small survey areas (<100km2 ; e.g. Chávez
et al., 2007; de la Torre and Medellín, 2011; Ávila-Nájera et al., 2015;
CONANP, 2015). Although the results obtained from these stud-
ies have contributed to the knowledge and development of jaguar
conservation plans in Mexico (e.g. Ceballos et al., 2016), Tobler and
Powell (2013) found that the use of small survey areas and a lim-
ited number of camera trap stations consistently produced density
estimates that are biased and therefore reduce the reliability of
comparisons. Our study is the first in the south of Mexico to ful-
fill the recommendations provided by Tobler and Powell (2013).
We suggest that in order to reduce biases in jaguar density estima-
tions, future studies in Mexico should increase both the sampling
effort and the area, especially because the federal environmen-
tal authorities base most of their relevant management decisions
regarding jaguar conservation on jaguar density estimations (e.g.
Ceballos et al., 2016; CONANP, 2018).
Acknowledgements
Panthera México provided the financial support for the field
work. División Académica de Ciencias Biológicas-Universidad
 M.G. Hidalgo-Mihart et al. / Mammalian Biology 98 (2019) 173–178
Juárez Autónoma de Tabasco (DACBiol-UJAT), Nicte Ha, Xim-Balam
and Fundación Pedro y Elena Hernández A.C provided logistical
support for the project. We thank to the owners of the El Sinai,
El Limonar, Las Piedras and Santa Cecilia and the inhabitants of el
Tumbo de la Montaña-Zapote for granting us access to their pro-
prieties. RJL was supported by CONACYT - FOMIX 2014-03-245836,
“Fortalecimiento de la Maestría en Ciencias Ambientales para su
permanencia en el Padrón Nacional de Posgrados de Calidad del
Conacyt”, and FCM received a scholarship from CONACYT (schol-
arship 271627) for their MSc and Ph.D at DACBiol-UJAT. We thank
Mauro Lucherini and three anonymous reviewers for their sugges-
tions to improve the final version of the manuscript.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in
the online version, at doi:https://doi.org/10.1016/j.mambio.2019.
09.009.
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