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ORIGINAL PAPER
Density and population structure of the jaguar (Panthera onca)
in a protected area of Los Llanos, Venezuela, from 1 year
of camera trap monitoring
Włodzimierz Jędrzejewski
1
&Maria F. Puerto
1
&Joshua F. Goldberg
2
&
Mark Hebblewhite
3
&María Abarca
1
&Gertrudis Gamarra
4
&Luis E. Calderón
4
&
José F. Romero
4
&Ángel L. Viloria
1
&Rafael Carreño
1
&Hugh S. Robinson
5,6
&
Margarita Lampo
1
&Ernesto O. Boede
7
&Alejandro Biganzoli
8
&Izabela Stachowicz
1
&
Grisel Velásquez
1
&Krzysztof Schmidt
9
Received: 8 November 2016 / Accepted: 10 November 2016
#The Author(s) 2016. This article is published with open access at Springerlink.com
Abstract Density is crucial for understanding large carnivore
ecology and conservation, but estimating it has proven meth-
odologically difficult. We conducted 1 year of camera trap-
ping to estimate jaguar (Panthera onca)densityandpopula-
tion structure in the Los Llanos region of Venezuela on the
Hato Piñero ranch, where hunting is prohibited and livestock
are excluded from half of ranch lands. We identified 42 dif-
ferent jaguars and determined their sex, age class, and repro-
ductive status. We estimated adult jaguar densities with spatial
capture-recapture models, using sex/reproductive state and
session as covariates. Models without temporal variation re-
ceived more support than models that allowed variation be-
tween sessions. Males, reproductive females, and nonrepro-
ductive females differed in their density, baseline detectability,
and movement. The best estimate of total adult jaguar popu-
lation density was 4.44 individuals/100 km
2
. Based on
reproductive female density and mean number of offspring
per female, we estimated cub density at 3.23 individuals/
100 km
2
and an overall density of 7.67 jaguars/100 km
2
.
Estimated jaguar population structure was 21% males, 11%
nonreproductive females, 26% reproductive females, and 42%
cubs. We conclude that extending the sampling period to
1 year increases the detectability of females and cubs and
makes density estimates more robust as compared to the more
common short studies. Our results demonstrate that the
Venezuelan Llanos represent important jaguar habitat, and
further, they emphasize the importance of protected areas
and hunting restrictions for carnivore conservation.
Keywords Carnivore conservation .Felid ecology .Hato
Piñero .Jaguar breeding .Populationdensity estimate .Spatial
capture-recapture
Communicated by: Karol Zub
Electronic supplementary material The online version of this article
(doi:10.1007/s13364-016-0300-2) contains supplementary material,
which is available to authorized users.
*Krzysztof Schmidt
kschmidt@ibs.bialowieza.pl
1
Centro de Ecología, Instituto Venezolano de Investigaciones
Científicas (IVIC), Carretera Panamericana km 11, Caracas 1020-A,
Venezuela
2
Evolution, Ecology and Organismal Biology Program, University of
California, Riverside, CA 92521, USA
3
Wildlife Biology Program, Department of Ecosystem and
Conservation Sciences, University of Montana,
Missoula, MT 59812, USA
4
Hato Piñero–UPSAT Piñero, El Baúl, Cojedes 2213, Venezuela
5
Panthera, New York, NY 10018, USA
6
College of Forestry and Conservation, University of Montana,
Missoula, MT 59812, USA
7
Fundación para el Desarrollo de las Ciencias, Físicas, Matemáticas y
Naturales–FUDECI, Caracas 1010-A, Venezuela
8
Departamento de Biología, Facultad de Ciencias, Universidad de Los
Andes ULA, Mérida 5101, Venezuela
9
Mammal Research Institute, Polish Academy of Sciences,
17-230 Białowieża, Poland
Mamm Res
DOI 10.1007/s13364-016-0300-2
Introduction
Population density is central to understanding the ecology, spatial
distribution, and abundance of all organisms (Krebs 2001), yet
estimating density reliably remains a challenging problem in
applied ecology. This issue remains especially persistent for eco-
logically important large carnivores. Carnivore population den-
sity is one of the major components that determines the impacts
of predation on prey populations (Holling 1959; Messier 1994;
Jędrzejewska and Jędrzejewski 1998). Accurate density esti-
mates are also critical to evaluate population size and trends of
large carnivores, an increasingly important aim given worldwide
declines of many of these species (Gros et al. 1996; Treves and
Karanth 2003; Ripple et al. 2014).
For large carnivores, like other threatened and endangered
species, the knowledge of population structure and demogra-
phy can help predict population trends and long-term persis-
tence (Shaffer 1981; Coulson et al. 2001;Cooleyetal.2009).
Demographic parameters may depend upon species biology
but also reflect the breeding performance of a population. A
high proportion of breeding females and cubs suggests a high
reproduction rate and potentially a growing population.
Conversely, carnivore populations with few breeding individ-
uals may have a higher extinction risk. Thus, integrating
methods to estimate large carnivore population breeding struc-
ture with density could improve population trend predictions
and promote effective conservation (Woodroffe 2011;
Rosenblatt et al. 2014).
As the top predator in the Neotropics, the jaguar
(Panthera onca) may have large impacts on prey popula-
tions, and an important role in trophic cascades and eco-
system regulation (Terborgh et al. 2001; Cavalcanti and
Gese 2010; Estes et al. 2011). Like many large carnivores,
the jaguar has experienced a rapid contraction of its nat-
ural range due to anthropogenic influences, especially
habitat alteration and fragmentation (Quigley and
Crawshaw 1992; Nowell and Jackson 1996;Sanderson
et al. 2002a;Zeller2007). Moreover, the reported densi-
ties of the jaguar vary substantially across its present dis-
tribution, but the factors that shape this variation are poor-
ly understood (see Maffei et al. 2011 and Tobler and
Powell 2013 for review).
A variety of field and statistical methods have been
used to estimate large carnivore population densities
(e.g., Gros et al. 1996; Karanth and Nichols 1998;
Stander 1998; Wilson and Delahay 2001). Initial attempts
at estimating jaguar density were based on radio-tracking
(Schaller and Crawshaw 1980;C
rawshaw1995;Ceballos
et al. 2002). In the last decade, camera trapping combined
with capture-recapture statistical methods has become
common (Maffei et al. 2011). The recent development of
spatially explicit capture-recapture (SCR) methods has
further improved the quality of density estimates
(Borchers and Efford 2008;Nossetal.2012;Royle
et al. 2014). However, application of these methods may
still present unresolved issues, such as the large differ-
ences among estimates from consecutive seasons within
the same study area (e.g., de la Torre and Medellin 2011;
Foster and Harmsen 2012;Tobleretal.2013). This vari-
ation among estimates may result not only from study
areas of insufficient size but also from low detectability,
especially of females and juveniles. The low number of
detections may be partially attributable to short study pe-
riods (1–3 months), which are commonly used to address
the assumption of population closure in capture-recapture
models (Karanth and Nichols 1998;Silveretal.2004;
Maffei et al. 2011). In theory, prolonged study periods
may allow for immigration, emigration, births, and deaths
in the study area and lead to overestimates or underesti-
mates of abundance by the closed population models ap-
plied in SCR packages (White et al. 1982; Kendall et al.
1997;EffordandFewster2013;Royleetal.2014).
However, extending study duration may bring important
benefits, such as an increased number of detections. For
example, better detectability of all sex/age groups would
allow estimating population breeding structure and would
broaden the applicability of camera trapping to an array of
other ecological and conservation questions (du Preez
et al. 2014). While the open population models are still
less established and have been rarely applied to density
estimates (e.g., Gardner et al. 2010; Whittington and
Sawaya 2015), it would be practical to find solutions for
applying the commonly used SCR methods based on
closed population models to long-term camera trapping
data.
Here, we study a jaguar population in Los Llanos, a region
of vast plains interspersed with numerous rivers, marshes,
open grasslands, and forests, extending through large parts
of Venezuela and Colombia. This unique region constitutes
an important habitat for jaguar in northern South America
(Hoogesteijn and Mondolfi 1992; Sanderson et al. 2002b;
Rabinowitz and Zeller 2010); however, human-jaguar con-
flicts related to frequent jaguar attacks on cattle threaten pop-
ulations of this carnivore in the area (Hoogesteijn et al. 1993).
Conservation measures implemented on cattle ranches can
improve the prospects of jaguar persistence in this region
(Hoogesteijn and Chapman 1997).
In this work, we assessed the impact of study design on the
estimates of jaguar density and population structure in the
partially protected Hato Piñero ranch in the Venezuelan Los
Llanos. First, we examined the impact of sampling period on
population density estimates with SCR methods. To fulfill the
assumptions of the closed population model, we divided our
long study to shorter sessions and used these sessions as a
covariate in our SCR models. We tested whether increased
study duration leads to increased detectability, especially of
Mamm Res
females and cubs, and if it improves robustness of the density
estimates. We further estimated basic reproductive parameters
and structure of the jaguar population to assess the status of
this species in our study area and the efficacy of the protection
measures applied in Hato Piñero. Based upon our findings, we
made recommendations for conservation and future studies of
jaguars and other large carnivores.
Methods
Study area
Hato Piñero ranch encompasses a total area of 800 km
2
in the
south-eastern part of Cojedes state of Venezuela. It includes
the hills of Macizo de El Baúl and vast plains between the
rivers Cojedes, Portuguesa, Chirgua, and Pao. We conducted
the study in the north-central portion of Hato Piñero, between
68.0334° W, 8.9827° N and 68.2148° W, 8.8562° N (Fig. A1).
The landscape is dominated by a mosaic of open lowland
savanna, partially converted to pastures, open marshes, decid-
uous and dry forests, and chaparral on the hillsides (Huber
et al. 2006). Precipitation drives the seasonal climate with
most rain occurring between June and November. Average
annual rainfall is approximately 1400 mm (Polisar et al.
2003); however, there is profound variation between years
(data of the meteorological station of El Baúl). The main rivers
are located on the borders of the ranch, but a network of small
streams, channels, and artificial ponds and lakes is well devel-
oped inside these borders. Between July and October, large
parts of the ranch are normally flooded, and in the driest peri-
od—between February and May—only the largest rivers and
a small number of artificial ponds retain water.
Until 2009, Hato Piñero was a private cattle ranch with ap-
proximately 50% of its area maintained as a nature reserve that
strived to preserve the jaguar and its prey communities. Hunting
was prohibited within ranch boundaries. In 2010, the Venezuelan
government expropriated Hato Piñero as a state farm but retained
the conservation protections of the ranch. However, after expro-
priation, the number of cattle increased from about 11,000 in
2009 to approximately 13,000 in 2014. In recent years, the num-
ber of domestic buffalo has also increased, reaching approxi-
mately 2000 in 2014. In addition to livestock, common prey
species include peccaries (Pecari tajacu and Tayassu pecari),
capybaras (Hydrochoerus hydrochaeris), white-tailed deer
(Odocoileus virginianus), tapir (Tapir us t erre str is ), caimans
(Crocodilus crocodilus), and giant anteater (Myrmecophaga
tridactyla)(Polisaretal.2003; Scognamillo et al. 2003;
Jędrzejewskietal.2014). Sympatric carnivores include puma
(Puma concolor), ocelot (Leopardus pardalis), jaguarundi
(Puma yagouaroundi), and crab-eating fox (Cerdocyon thous).
Camera trapping
From July 2013 to July 2014 (376 days), we conducted a con-
tinuous camera trapping effort in the study area (Table 1,
Fig. A1). We used 27–56 camera-traps at any given time, mostly
HC 500 (Reconyx Inc., Holmen, WI, USA) and TrophyCam HD
Max (Bushnell, Overland Park, MI, USA). We aimed to distrib-
ute the cameras in a regular grid of 2 km by 2 km; however, we
adjusted camera positions in response to local topography, site
accessibility, and the presence of jaguar trails indicated by track
records (Fig. A1). Normally, we placed cameras along small dirt
roads, animal trails, and water-bodies, one camera per site. The
total area of the polygon encompassing all camera stations was
168.1 km
2
. To improve the quality of imagery for individual
identification, we placed a small piece of carpet (10 cm × 10 cm)
soaked with a beaver castoreum/catnip oil lure in front of the
cameras (usually at a distance of 3–4m)(Schmidtand
Kowalczyk 2006;Schlexer2008). Placing lures does not bias
density estimates but may improve individual identifications or
detectability (Gerber et al. 2012; du Preez et al. 2014).
Table 1 Summary of camera-
trapping effort for jaguar
(Panthera onca) study conducted
in Hato Piñero, Venezuela, over
six sessions during July 2013–
July 2014
Session N
days
Ntrap
sites
Polygon
size
Photos
identifiable
N adult jaguars
identified
Captures Recaptures
1 47 48 142.7 252 20 215 195
2 40 56 135.3 175 22 152 130
3 65 27 114.5 171 20 138 118
4 69 42 157.4 315 23 264 241
5 57 32 146.1 168 21 148 127
6 98 31 113.7 288 23 230 207
mean 62.7 39.3 134.9 228.2 21.5 191 170
Total 376 194 168.1 1369 28 1147 1018
The following parameters are presented: the numbers of trapping days, camera trap sites, and all photos with
identifiable individuals (taken with at least 10-min difference), numbers of jaguar captures and recaptures, and
minimum convex polygon of all cameras during each session. The number of captures and recaptures per session
has been defined using one capture per occasion (day)
Mamm Res
We divided our sampling period into six sessions that
corresponded with camera maintenance and data download.
Mean session duration was 63 days (range 47–99 days,
Tab le 1). During each site visit, we inspected the cameras to
adjust camera settings and, if required, the spatial location of
cameras due to landscape changes (i.e., flooding, droughts,
fires, etc.), observation of jaguar tracks, or technical problems.
We also refreshed the lure when servicing each camera.
We identified individual jaguars based on unique spot patterns
(Silver et al. 2004). We distinguished four sex/age groups: males,
nonreproductive females, reproductive females, and cubs. Cubs
included obviously young and immature individuals recorded
with adult females. Sex of adult individuals was determined by
the presence/absence of testicles or nipples and other reproduc-
tive signs. We classified females as reproductive if they were
recorded with cubs at any point during the study year, and as
nonreproductive, if they were never recorded with cubs. We
treated presence of cubs as an objective criterion for evidence
of breeding. Classification of breeding or non was held constant
for the entire study period. Although simplified, we believe this
classification justified by the long reproductive cycle of female
jaguars (i.e., 3 months gestation and 17 months care of cubs) and
long (3–4 years) time to first reproduction (Crawshaw and
Quigley 1991; De Paula et al. 2013). We make the assumption
that reproductive females maintain their territories for long pe-
riods (i.e., years) and any short-term event (i.e., losing cubs)
would not change their territory size. Furthermore, we generally
recorded older cubs (>3 months old), which would have survived
the presumed very early peak in juvenile mortality documented
in other large carnivores (Jędrzejewska et al. 1996; Palomares
et al. 2005). The identification process was performed by two
authors independently (MFP and MA) and verified by a third
(WJ). Unidentifiable captures were excluded from subsequent
analyses. For capture-recapture models, we defined daily sam-
pling occasions such that we considered only one capture per day
per trap, i.e., binomial detection histories (Royle et al. 2009;
Goldberg et al. 2015).
Population density estimation for adult jaguars
We applied maximum likelihood SCR models within the secr
2.10.3 R package (Efford et al. 2004,2009; Borchers and
Efford 2008;Efford2016) to estimate jaguar densities. These
hierarchical models define (1) a spatial model of the distribution
of animal activity centers and (2) a spatial observation model
relating the probability of detecting an individual at a particular
trap to the distance from the animal’s activity center (Efford
2004). For the observation model, we used a hazard half-
normal detection function:
λdðÞ¼1−exp −λ0exp −d2
2σ2
ð1Þ
where λ
0
represents the baseline detection probability at an
individual’s activity center, σdefines the shape of the decline
in detection away from the activity center and can be interpreted
in terms of the animal movement distribution, and dspecifies
the distance between a detector (camera trap) and the activity
center (Efford et al. 2009;Efford2016). This detection model
implies a Binomial distribution of detections of an individual at
a particular detector (Efford and Fewster 2013; Royle et al.
2014). We used a 15-km buffer around the study area to include
the activity centers of any individuals that may have been ex-
posed to sampling. We checked the adequacy of the buffer size
by examining likelihoods and estimates from models with larg-
er buffers. We applied full likelihood models with three sex/
reproductive status groups (adult males, adult reproductive fe-
males, and adult nonreproductive females) and six shorter ses-
sions as covariates (Borchers and Efford 2008). By doing this,
we also fulfilled the assumptions of the closed population mod-
el in analyzing our long dataset. We fit models with all possible
additive combinations of sex/reproductive status groups and
sessions as covariates on density (D), λ
0
,andσ. For density,
we always used sex/female reproductive state as a covariate to
provide an estimate of population structure and did not consider
intercept-only models. We assessed how D,λ
0
,andσdiffered
across sessions and sex/reproductive status groups and how this
variation influenced the overall density estimate. We evaluated
models with AICc (corrected Akaike information criterion) and
AICc weights (Hurvich and Tsai 1989; Wagenmakers and
Farrell 2004). To test the effect of study duration on estimates
of all parameters, we compared models that included session
covariates in the parameters D,λ
0
,andσ(corresponding to the
situation when model parameters were estimated based on sep-
arate sessions, as in short-term studies) with the best model that
did not include any session covariates.
The spatial scale parameter, σ, implies an estimate of indi-
vidual space use and the scale of movement about an activity
center. These estimates provide another means of addressing
the reliability of our model results through comparison to
telemetry-derived home range sizes. We transformed the σ
values for each sex/reproductive state into the radius of an in-
dividual activity range, encompassing 95% of animal locations
during the observation period. We made this conversion using
the hra function in the R package SCRbook (Royle et al. 2013;
https://sites.google.com/site/spatialcapturerecapture/scrbook-r-
package), since an analytical solution with the hazard half-
normal detection function is not readily available. The hra func-
tion approximates the 95% activity range of an individual, giv-
en parameter values, using a discrete meshwork of points about
the activity center. We calculated 95% activity range size for our
best model and compared them to home range size estimates
from radio-tracking.
To allow comparisons with earlier studies, we also applied
nonspatial capture-recapture methods to estimate adult jaguar
density (see Appendix Bfor methods and results).
Mamm Res
Estimating cub density and population structure
We estimated densities separately for males, reproductive fe-
males, and nonreproductive females. We attempted to fit
models directly to observations of cubs, but their sparse cap-
ture histories did not provide sufficient data for a maximum
likelihood analysis. To estimate cub density, we multiplied the
reproductive female density from our best model by mean
number of cubs per reproductive female. These estimates
allowed calculation of total jaguar density and population
structure for males, nonreproductive females, reproductive fe-
males, and cubs.
Results
Camera trapping and detection numbers for sex/age
groups
Our total sampling effort was 12,302 camera trap-nights. We
obtained 1465 captures, including 1369 with identifiable indi-
viduals (Table 1). In total, we identified 42 jaguars, including
14 adult males, 14 adult females, and 14 cubs. Of the 14
photographed adult females, 7 were actively reproducing
and photographed with cubs (Photos D1,D2). Although we
registered equal numbers of males, females, and cubs in the
study area, the capture frequency of each group differed: 58%
of identified photos were those of males (798 captures), 33%
of identifiable captures were those of females (452), and only
9% were those of cubs (119). On average, males were cap-
tured 56 times each, females 32 times, and cubs only 9 times.
Reproductive females had slightly higher total number of cap-
tures than nonreproductive females (257 versus 195, respec-
tively) and higher average number of captures per individual
(38 versus 28). Reproductive females were more frequently
captured alone (109 times) than accompanied by cubs (69
captures) during the period of known offspring dependency.
Conversely, cubs were recorded more frequently with their
mothers (83 individual captures) than alone (36 captures).
Density estimates of adult jaguars
Of the 32 models analyzed with the secr package with sex/
reproductive status and sessions as covariates, those which
did not allow density to vary across sessions obtained the
lowest AICc values. In contrast, models assuming density
variation across sessions received less support (Tables 2,
C1). The top secr model for adult jaguars included an
effect of sex/female reproductive status on D,λ
0
,andσ
and between session variation in λ
0
. All three parameters
differed significantly between sex/reproductive status
groups (Table 3). Baseline detection probability was low-
est for reproductive females (0.04 on average), whereas
nonreproductive females had the greatest baseline detect-
ability (0.13 on average) and males intermediate (0.08 on
average) to the two female reproductive classes. Males had
the largest values of estimated movement distribution
(σ= 2.97 ± 0.09 km), while reproductive and nonrepro-
ductive females obtained smaller σvalues (2.04 ± 0.11 and
2.32 ± 0.19 km, respectively). Estimated densities were
higher for reproductive females and males (1.97 ± 0.33
and 1.62 ± 0.22 individuals/ 100 km
2
, respectively) than
for nonreproductive females (0.85 ± 0.19 individuals/
100 km
2
). In total, the best model estimated 4.44 ± 1.16
adult jaguars/100 km
2
(Table 3).
Cub density and jaguar population structure
From observations of the seven reproductive females with
offspring during the study period, we estimated 1.64 cubs
per reproductive female on average. Additionally, one cub
was recorded alone on a single occasion and had an un-
known mother. We excluded this lone observation from
further analysis. On the basis of reproductive female den-
sity from the top model, we estimated 3.23 cubs/100 km
2
in the study area. Thus, we estimated a total density of
7.67 jaguars/100 km
2
. Jaguar population structure was
21% adult males, 11% nonreproductive females, 26% re-
productive females, and 42% cubs (Table 3).
Table 2 Model selection results
for selected models analyzed in
secr 2.10.3, with six sessions and
three sex/reproductive state
groups as covariates
Model AIC
c
ΔAIC
c
w
i
D∼sexg λ
0
∼sexg + session σ∼sexg 11,485.0 0.0 0.68
D∼sexg λ
0
∼sexg σ∼sexg 11,487.8 2.8 0.17
D∼sexg λ
0
∼sexg σ∼session + sexg 11,489.1 4.0 0.09
D∼sexg λ
0
∼sexg + session σ∼sexg + session 11,490.0 5.0 0.06
D∼sexg + session λ
0
∼sexg + session σ∼sexg + session 11,502.2 17.2 0.00
Selection parameters for all 32 analyzed models are presented in Table C1 (Supplementary materials)
Ddensity, λ
0
baseline detection probability, σmovement distribution parameter, sexg sex/reproductive state group
Mamm Res
Estimates of home range sizes
Based on the detection and movement parameter values, we
estimated 95% home range sizes. Males had the largest ranges
(167 km
2
), while nonreproductive females and reproductive
females moved in smaller ranges (103 and 79 km
2
,respective-
ly, Table 3).
Study duration and density estimates
The best secr model included seasonal variation in the base-
line detection probability, but not in density or the movement
distribution parameter. The top model that excluded seasonal
variation in all parameters had the second overall rank order in
our model set (ΔAIC
c
=2.8,w
i
=0.17,Table2) and produced
similar overall density estimates (D
total
= 4.47 ± 1.06 jaguars/
100 km
2
). In contrast, the model assuming between session
variation in all three parameters gave highly variable results:
from 3.65 to 5.62 jaguars/100 km
2
in different sessions
(Fig. 1, Table C2). This model received no support from our
model selection criterion (ΔAIC
c
=17.2).
Discussion
Our study provides a robust estimate of jaguar density from a
large, long-term photographic capture-recapture dataset. This
scope allowed us to address the concerns of many previous
jaguar studies, including small sample sizes, low detectability
of females and cubs, and limited spatial and temporal extent to
provide a more complete description of the jaguar population
in our study area. We estimate breeding and nonbreeding fe-
male density as well as cub density and total population struc-
ture for jaguars in Hato Piñero. We record high jaguar densi-
ties in the Venezuelan Llanos, providing evidence of the im-
portance of this habitat for conservation. Moreover, our ap-
proach to spatial and temporal study design may offer useful
guidance for future capture-recapture studies of jaguars and
other large carnivores.
Jaguar population density in Hato Piñero
and implications for conservation
Our estimates of jaguar density in Hato Piñero of 4.4 adults/
100 km
2
and 7.6 total jaguars/100 km
2
(including cubs) are
among the highest documented in South and Central America.
Comparable density estimates have been reported only in the
tropical forests of Peru, Belize, and Guatemala (Moreira et al.
2008; Harmsen et al. 2010; Tobler et al. 2013; Kelly and Rowe
2014) and in the wetlands of the Brazilian Pantanal (Soisalo and
Cavalcanti 2006). This high jaguar density most likely results
from high prey availability and productivity in our study area.
Karanth et al. (2004) demonstrated a similar relationship for ti-
gers in India. Polisar et al. (2003) estimated that the biomass of
potential jaguar prey in Hato Piñero was about 750 kg/km
2
of
wild prey and about 7700 kg/km
2
of livestock. These estimates
place Hato Piñero in a class of biomass availability and produc-
tivity with Manu National Park, Peru (270 kg/km
2
of wild prey),
Table 3 Parameter estimates from the top model of jaguar density
Model/parameter Session 1 Session 2 Session 3 Session 4 Session 5 Session 6 Mean
D∼sexg λ
0
∼sexg + session σ∼sexg (ΔAICc = 0)
λ
0
males (SE) 0.09 (0.01) 0.06 0.01 0.10 (0.02) 0.09 (0.01) 0.06 (0.01) 0.10 (0.01) 0.08
λ
0
reproductive females (SE) 0.04 (0.01) 0.03 (0.00) 0.04 (0.01) 0.04 (0.01) 0.02 (0.00) 0.04 (0.01) 0.04
λ
0
nonreproductive females (SE) 0.14 (0.03) 0.10 (0.02) 0.16 (0.05) 0.14 (0.02) 0.09 (0.02) 0.16 (0.04) 0.13
σmales (SE) 2.97 (0.09) 2.97 (0.09) 2.97 (0.09) 2.97 (0.09) 2.97 (0.09) 2.97 (0.09) 2.97
σreproductive females (SE) 2.04 (0.11) 2.04 (0.11) 2.04 (0.11) 2.04 (0.11) 2.04 (0.11) 2.04 (0.11) 2.04
σnonreproductive females (SE) 2.32 (0.21) 2.32 (0.21) 2.32 (0.21) 2.32 (0.21) 2.32 (0.21) 2.32 (0.21) 2.32
Dmales (SE) 1.62 (0.22) 1.62 (0.22) 1.62 (0.22) 1.62 (0.22) 1.62 (0.22) 1.62 (0.22) 1.62
Dreproductive females (SE) 1.97 (0.33) 1.97 (0.33) 1.97 (0.33) 1.97 (0.33) 1.97 (0.33) 1.97 (0.33) 1.97
Dnonreproductive females (SE) 0.85 (0.19) 0.85 (0.19) 0.85 (0.19) 0.85 (0.19) 0.85 (0.19) 0.85 (0.19) 0.85
Dadult jaguars total (SE) 4.44 (1.16) 4.44 (1.16) 4.44 (1.16) 4.44 (1.16) 4.44 (1.16) 4.44 (1.16) 4.44
Dcubs 3.23 3.23 3.23 3.23 3.23 3.23 3.23
95% home range males (km
2
) 167 167 168 167 167 168 167
95% home range reproductive females (km
2
)797979797979 79
95% home range nonreproductive females (km
2
) 103 102 103 103 102 103 103
For each sex/reproductive state group, values of λ
0
,σ,andDfor the top models are presented. Cub density was calculated by multiplying reproductive
female density by mean number of cubs/per female. Home range sizes were estimated from σand λ
0
values (see BMethods^)
Ddensity (individuals/100 km
2
), λ
0
baseline detection probability, σmovement distribution parameter, sexg sex/reproductive state group, SE standard
error
Mamm Res
and the Pantanal, Brazil (380 kg/km
2
), two famous jaguar
hotspots (Schaller 1983;Emmons1987).
The wet parts of Los Llanos, with mosaics of seasonally
flooded savannahs, marshes, dry or wet forests, and numerous
rivers and streams, may provide exceptionally good condi-
tions for jaguars. However, cattle breeding, human-jaguar
conflicts, and hunting likely limit jaguar population growth
outside the few protected areas in Los Llanos (Hoogesteijn
et al. 1993; González Fernández 1995; Hoogesteijn and
Hoogesteijn 2008). Boron et al. (2016) conducted camera-
trapping study in an unprotected part of the Colombian Los
Llanos and documented much lower adult jaguar density (2.2
jaguars/100 km
2
) than in Hato Piñero, despite the similarities
in primary productivity, forest cover, and human population
density between the two study areas. However, in the
Colombian study site, hunting of jaguars and its prey is com-
mon, as well as retaliatory killing of jaguars due to their at-
tacks on cattle (Boron et al. 2016). This contrast strongly
supports the efficacy of the jaguar conservation measures
adopted in Hato Piñero, including prohibition of hunting,
50% land excluded from cattle grazing, and development of
eco-tourism. Similar protections have benefitted jaguar con-
servation in the Pantanal of Brazil (Zimmermann et al. 2005b;
Greve 2014; Hoogesteijn et al. 2016).
Protected areas and other refuges play a crucial role for
maintaining other large carnivore populations in landscapes
with large human impacts (Mills 1991; Thapar 1999;
Naughton-Treves et al. 2005; Carroll and Miquelle 2006).
Our data confirm the importance of protected areas for jaguar
conservation. We show that large protected areas, like Hato
Piñero, can maintain robust jaguar populations at high density
and high reproductive output. As such, they may be a source
of dispersing individuals, supporting the persistence of jaguar
populations in the surrounding areas.
Differences between sex/reproductive groups
Consistent with previous studies accounting for sex dif-
ferences, we found higher detection and movement pa-
rameter estimates for males than females (Sollmann
et al. 2011;Tobleretal.2013). Our decision to discrim-
inate between reproductive and nonreproductive females
further refined the differences among females, based upon
whether we observed them caring for cubs. The low de-
tection probability of reproductive females may result
from protective maternal behavior. Females with cubs
may select the safest areas and reduce use of exposed
movement corridors, such as roads and trails, to avoid
male jaguars and pumas that may threaten young.
Infanticide by unrelated males is common in other felids
(e.g., Packer and Pusey 1983; Balme et al. 2013). The
higher detectability, larger movement ranges, and lower
Fig. 1 Comparison of jaguar total densities in Hato Piñero, Venezuela,
during July 2013–July 2014 estimated with three different models: (1) the
top model selected with AICc, (2) the model with all parameters constant
across sessions (corresponding to a long-term study), and (3) for the
model with all parameters free to vary between sessions (corresponding
to short-term studies). Error bars denote ±1 SE
Mamm Res
density of nonreproducing females may result from young
individuals using transient territories and moving large
distances in search of a territory (Beier 1995;Schmidt
1998;Zimmermannetal.2005a).
Length of study duration
The capture-recapture literature frequently emphasizes the im-
portance of the closed population (no birth, immigration,
death, or emigration) assumption of capture-recapture models
(White et al. 1982; Kendall et al. 1997). To address this con-
cern, most researchers have adopted the recommendation that
study periods should not exceed 3 months (Karanth and
Nichols 1998; Silver et al. 2004). Although the closed popu-
lation assumption is important, meeting this requirement does
not require such stringent limits on study period. In the anal-
ysis of our long-term data, we introduced sessions as a covar-
iate to act as a surrogate for the shorter time frames typically
employed by camera trapping studies. The best model allowed
for seasonal variation in one of the parameters (baseline de-
tection probability), but not in the other two (density and
movement distribution). Furthermore, the model that ignored
seasonal variation provided similar parameter estimates and
received some statistical support. In contrast, the model as-
suming variation between sessions in all parameters (corre-
sponding to short-term studies) received no statistical support
and produced much less precise density estimates.
Seasonal fluctuations in activity and density estimates have
been shown in other jaguar studies (de la Torre and Medellin
2011; Harmsen et al. 2011; Kelly and Rowe 2014; Tobler et al.
2013). This variation may be attributable to poor camera site
selection, camera failures, stolen cameras, local fires, or due to
seasonal changes in jaguar spatial activity patterns. Changes
in jaguar distribution may depend upon the availability of
water sources. During the dry season, only a few artificial
ponds, lakes, and streams persisted in our study area.
Alternatively, the spatial distribution of jaguars may depend
upon jaguar reproductive cycles. Scognamillo et al. (2002)
reported that the two jaguar females they radio-tracked in
Hato Piñero drastically reduced their activity ranges for about
2 months after giving birth to cubs. Comparable patterns of
seasonal activity changes related to reproductive cycles have
been demonstrated for other felids, e.g., for lynx in Białowieża
Primeval Forest (Schmidt 1998). Thus, seasonal changes in
activity patterns and territory use may have some impact on
detection probability and population assessments, as shown
by our results. Density estimates from data with a limited
temporal extent may have a greater stochastic component
and be less precise than those obtained in long-term studies.
The increased sampling duration in our study did not lead
to any obvious overestimates of population density and pro-
duced several key benefits. Most importantly, the long-term
monitoring increased detection numbers and led to better
parameter estimates for the most elusive groups within the
jaguar population. We could estimate densities separately for
each sex, age, and reproductive group to provide a more com-
plete description of jaguar population structure. Our estimate
of population structure with reproductive females and cubs
comprising 26 and 42%, respectively, of all individuals indi-
cates a healthy, productive jaguar population. Similar high
share of reproducing females and cubs has been observed in
radio-tracking studies of other large felid populations, e.g.,
lynx in partially protected Białowieża Forest in Poland
(Jędrzejewski et al. 1996).
In sum, the advantages of long-term studies suggest that
extended camera trap monitoring in combination with spatial
capture-recapture models may offer significant insights into
the population biology of target species.
Home range size estimates
Our estimates of year-round home range sizes (79 km
2
for
reproducing females, 103 km
2
for nonreproducing females,
and 167 km
2
for males) show, in general, a similar pattern to
estimates obtained with telemetry studies and further corrob-
orate our density estimates. Previous radio-telemetry research,
conducted on two male and two female jaguars in Hato Piñero
during 1996–1998, estimated average seasonal home range
sizes of 65 km
2
for females and 100 km
2
for males (Polisar
et al. 2003; Scognamillo et al. 2002,2003). In a GPS telemetry
study of jaguars conducted by Cavalcanti and Gese (2009)in
Pantanal, Brazil, a habitat similar to Hato Piñero, seasonal
female home ranges varied from 34 to 101 km
2
(average:
63 km
2
) and seasonal male home ranges varied from 58 to
263 km
2
(average: 156 km
2
). Slightly higher average esti-
mates obtained with SCR methods may result from the fact
that this technique assumes circular home ranges, while telem-
etry captures actual space use, which is rarely circular (e.g.,
Cavalcanti and Gese 2009). However, the higher estimates of
home range sizes of nonreproductive females can result from
their transient character which can cause a bias in movement
estimates (Royle et al. 2016).
Conclusions
Our study demonstrates that protected areas in Los Llanos are
potentially important jaguar habitat and that jaguar popula-
tions in this region may reach some of the highest densities
recorded for South America. Jaguar conservation plans and
actions should pay more attention to this region and promote
increasing the number of protected areas in Los Llanos.
Although today, Hato Piñero is an unquestionable jaguar
hotspot in northern South America, it needs more international
concern to maintain its good state of conservation, especially
in the context of the political instability, growing environmen-
tal risks, and uncertain future of this region.
Mamm Res
Our study also suggests new perspectives on future re-
search. Spatial capture-recapture studies of jaguars and similar
species, with camera traps, may benefit from extended moni-
toring not limited to 3 months. Based upon our experience, we
recommend large study areas with dense trap stations to max-
imize the number of individuals captured and number of de-
tections. Although we did not quantify the effect of lures, we
found them to increase picture quality and thus detectability.
Long-term camera trapping can provide additional insights
into carnivore population biology.
Acknowledgements Collecting data for this article was possible due to
financial support from the budgets of Instituto Venezolano de
Investigaciones Científicas (IVIC) and Mammal Research Institute of
the Polish Academy of Sciences and grants from Polish Ministry of
Science and Higher Education (grant NN304336339) and Panthera
Corporation (2010 Research and Conservation Grant and the Liz
Claiborne Art Ortenberg Jaguar Research Grants 2011, 2012, 2014).
We are grateful to all the personnel of Hato Piñero who made our work
possible. We are grateful to the IVIC Transportation Center, and especial-
ly to Argenis Hurtado and all IVIC drivers who participated in our expe-
ditions to Hato Piñero, also to Dinora Sánchez and Giovanni Colmenares
from Biodiven IVIC for making their car available for us. Special thanks
we direct to coordinators of Ecology Center of IVIC: Dr. Marta Francisco,
Dr. Astolfo Mata, Dr. Ascanio Rincón, and administration workers
Yugdalia García, Robert Vargas, and all staff of the Ecology Center for
their kind support to our work. Dr. Fernando Ruette and Miguel
Fernández (IVIC) shared their computers to assist with the analysis.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://
crea tiveco mmons. org/licenses/by/4.0/), which permits unrestricted
use, distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a link
to the Creative Commons license, and indicate if changes were made.
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