ZOOLOGIA 38: e63231

ISSN 1984-4689 (online)

zoologia.pensoft.net

RESEARCH ARTICLE

Temporal and spatial segregation of top predators (Felidae)

in a Mexican tropical Biosphere Reserve
Carlos A. Contreras-Díaz1 , Leroy Soria-Díaz2 , Yuriana Gómez-Ortiz3 , Rogelio Carrera-Treviño4 ,
Claudia C. Astudillo-Sánchez1 , Julio C. Chacón-Hernández2 , Luis Martínez-García2

1
Facultad de Ingeniería y Ciencias, Universidad Autónoma de Tamaulipas. Centro Universitario Victoria, C.P. 87149,
Victoria, Tamaulipas, Mexico.
2
Instituto de Ecología Aplicada, Universidad Autónoma de Tamaulipas. Av. División del Golfo, C.P. 87019, Victoria,
Tamaulipas, Mexico.
3
División de Desarrollo Sustentable, Universidad Intercultural del Estado de México. Libramiento Francisco Villa,
C.P. 50640, San Felipe del Progreso, Estado de México, Mexico.
4
Laboratorio de Fauna Silvestre, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Nuevo
León. Campus Ciencias Agropecuarias, C.P. 66050, Escobedo, Nuevo León, Mexico.
Corresponding author: Leroy Soria-Díaz (leroysoriadiaz@gmail.com, lesoria@uat.edu.mx)
http://zoobank.org/7854782F-4544-44E5-9684-054D3453FF42

ABSTRACT. Jaguars, Panthera onca (Linnaeus, 1758), and pumas, Puma concolor (Linnaeus, 1771) are the largest felids in
the neotropics. Both can overlap in niche axes (time, space and prey), and are therefore potentially competing species.
Segregation mechanisms presented by a low overlap in one of these axes of niche can facilitate the coexistence. Our aim
was to analyze jaguar and puma temporal and spatial overlap for understanding their segregation mechanisms. Between
2015 and 2017, twenty-six camera trap stations were located in five habitat types of El Cielo Biosphere Reserve (ECBR) in
northeastern Mexico. Temporal activity was analyzed using circular statistics and time overlap analysis. Spatial overlap was
calculated with the Pianka index and a selectivity habitat analysis. Our results showed that jaguars and pumas were nocturnal
and that the temporal overlap was high (∆4 = 0.77). We found an intermediate spatial overlap (Pianka index = 0.61). Jaguars
were more selective and preferred the deciduous forest. In comparison, pumas preferred oak-pine forest, but also used oak
and deciduous forest. Our results indicate that spatial segregation best explains the coexistence of jaguars and pumas in our
study area, probably due to both habitat diversity in the reserve and the generalist habits of the puma.
KEYWORDS. Camera trap, coexistence, El Cielo Biosphere Reserve, northeastern Mexico, Panthera onca, Puma concolor.

INTRODUCTION avoiding overlap, each species could have exclusive access to

time, space, or food, thereby reducing the risk of direct encoun-
Activity patterns and habitat use are important compo- ters and competition (Carothers and Jaksić 1984, Castro-Arellano
nents that describe the ecology and behavior of species and et al. 2010, Romero-Muñoz et al. 2010, Gómez-Ortiz et al. 2015).
may facilitate coexistence between species or individuals that As such, species with intra-guild competition potential provide a
experience intra-guild competition (Gause 1932, Hardin 1960, useful focal group to understand the mechanisms of segregation
Fedriani et al. 1999, Karanth and Sunquist 2000, Harmsen et that allow their coexistence (Hearn et al. 2018).
al. 2009). Top predators that have similar morphology, food Jaguars, Panthera onca (Linnaeus, 1758), and pumas, Puma
habits, distribution, and life history can develop mechanisms concolor (Linnaeus, 1771), constitute a large mammalian predator
of segregation in their use of the three main ecological niche guild that can affect the structure and pattern of associated eco-
axes (temporal, spatial, and trophic) to ensure their coexistence logical communities (Miller et al. 2001, Sunquist and Sunquist
(Schoener 1974, Pianka 1978, Di Bitetti et al. 2010, Morato et al. 2002). They also are the largest felids in the Neotropics and are
2016, Rayan and Linkie 2016). In a community where species sympatric top predators across the entire jaguar range in Central
make discriminate use of resources (time, space, and food) while and South America (Iriarte et al. 1990, Sunquist and Sunquist

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 C.A. Contreras-Díaz et al.

2002, Haines 2006). Jaguars are considered an endangered roundi) and described their mechanisms of coexistence in time
species in Mexico (SEMARNAT 2010). Both species can overlap and space (Carrera-Treviño et al. 2018). These mechanisms are
in temporal activity, habitat use, and prey species consumed unknown for jaguars and pumas.
(Núñez et al. 2000, Scognamillo et al. 2003, Romero-Muñoz et al. Given the variety of habitat types and the status of con-
2010). Thus, they potentially can compete with each other and servation of the ECBR, we hypothesized temporal and spatial
represent suitable subjects for the study on segregation strategies. segregation would be important mechanisms mediating the
Some authors suggest that competition between jaguars coexistence between jaguars and pumas. Our aim was to analyze
and pumas is low due to differences in diet (Aranda and Sán- temporal and spatial overlap between jaguars and pumas in
chez-Cordero 1996, Núñez et al. 2000, Novack et al. 2005, Cas- the ECBR to help understand the segregation mechanisms that
celli de Azevedo and Murray 2007, Flores-Turdera et al. 2021), ensure their coexistence.
temporal (Harmsen et al. 2009, Romero-Muñoz et al. 2010), and
spatial segregation (Scognamillo et al. 2003). MATERIAL AND METHODS
Generally, jaguars consume larger prey than pumas, and
pumas have a more diverse diet (Iriarte et al. 1990, Polisar et al. Study site
2003, Scognamillo et al. 2003, Flores-Turdera et al. 2021) and can We conducted our study in ECBR, which is in northeastern
easily switch to other prey when their primary prey population Mexico and is part of the state of Tamaulipas (Fig. 1). The ECBR
density falls (Soria-Díaz et al. 2018). Studies on the temporal has an area of 1, 445 km2 and elevation ranges from 100 to 2,
activity of jaguars show they are nocturnal in some places of 300 m of altitude (Steinberg et al. 2014). Mean annual precipi­
their distribution (Rabinowitz and Nothingham 1986, Emmons tation is 1000–2000 mm and mean annual temperatures are
1987, Núñez et al. 2002, Maffei et al. 2004, Di Bitteti et al. 2010). between 14 and 25.2 °C (INEGI 2013). The rainy season is from
Pumas tend to be active in crepuscular (dawn and dusk) and April to October and the dry season from November to March.
daylight hours (Di Bitteti et al. 2010, Hernández-SaintMartín et The reserve is a site of Nearctic and Neotropical biogeographic
al. 2013, Ávila-Nájera et al. 2016, De la Torre et al. 2017). Jaguars zones of transition with high species richness (both faunal and
are considered habitat specialists; they prefer dense vegetation floral) in a small geographic area (Steinberg et al. 2014). Habitat
and sites close to water (Sollmann et al. 2012). In contrast, pu- includes deciduous forest (DF), semi-deciduous forest (SDF), oak
mas are considered habitat generalists and are less dependent forest (OF), oak pine forest (OPF), mountain cloud forest (MCF),
on water sources (Logan and Sweanor 2001, Romero-Muñoz et submontane scrub (SS), and others (Fig. 1, González-Medrano
al. 2010, Sollmann et al. 2012, Monroy-Vilchis and Soria-Díaz 2005, INEGI 2013, Steinberg et al. 2014). The reserve hosts an
2013, Gutiérrez-González and López-González 2017). important mammalian biodiversity, including six felids’ species:
Other studies of overlapping temporal activity in popu­ Panthera onca, Puma concolor, Leopardus pardalis (Linnaeus, 1758),
lations of sympatric jaguars and pumas, noting that both Leopardus wiedii (Schinz, 1821), Puma yagouaroundi (É. Geoffroy
felids can change their behavioral patterns when exposed to Saint-Hilaire, 1803), and Lynx rufus (Schreber, 1777); and the
anthropogenic pressures such as agricultural burning, poaching, black bear, Ursus americanus (Pallas, 1780) (Vargas-Contreras
and logging (Scognamillo et al. 2003, Ávila-Nájera et al. 2016, and Hernández-Huerta 2001).
Briones-Salas et al. 2016). Habitat use can also vary according
to the level of human disturbance, mainly by the individual’s Sampling design
selection of less-disturbed areas (Foster et al. 2010, 2013, Hernán- We established 26 study camera trap stations in five
dez-SaintMartín et al. 2013). Areas that are protected from habitat types from January 2015 to December 2017. The mean
logging, poaching, and other human-caused disturbance, and distance between stations was approximately 6 ± 3 km. The
have high habitat heterogeneity allow for temporal and spatial number of stations in each habitat were chosen in proportion to
niche segregation, which promotes coexistence (Scognamillo the area of habitat it represented in the reserve: OF (414.6 km2,
et al. 2003). n = 9 stations), DF (329.7 km2, n = 8 stations), MCF (191.5 km2,
The Sierra Madre Oriental of northeastern Mexico repre­ n = 5 stations), OPF (80.3 km2, n = 2 stations), and SDF (69.6 km2,
sents one limit of the geographical distribution where jaguar n = 2 stations) (Fig. 1). These five habitat types cover 1,085.7 km2,
and puma populations occur simultaneously (Vargas-Contreras which represents 75% of the ECBR.
and Hernández-Huerta 2001, Sunquist and Sunquist 2002). El We installed two camera traps (Scoutguard HCO SG565)
Cielo Biosphere Reserve (ECBR) is located in the Sierra Madre at each of the 26 sampling stations along unpaved roads and
Oriental and presents a well preserved high-diversity area due man-made trails to maximize the detection probability of ja­guars
to low human impact, Nearctic and Neotropic convergence, ex- and pumas (Goulart et al. 2009, Srbek-Araujo and Chiarello
treme topographical conditions, and a large number of different 2013). Camera traps were attached to tree trunks at 30–50 cm
habitat types (Steinberg et al. 2014). A previous study in ECBR above ground, were active 24 hours and programmed to take
described the temporal and spatial interactions of sympatric one picture every 60 seconds. Date and time were also recorded
mesocarnivores (Leopardus pardalis, L. wiedii, and Puma yagoua- in each photograph. We checked cameras monthly to make

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 Temporal and spatial segregation of top predators

Figure 1. Geographical location of the El Cielo Biosphere Reserve in northeastern Mexico, with habitats and camera trap station locations.

sure they were working appropriately, replace batteries, and dawn, and with a mean of 19:44 h; our range = 18:44–20:44 h
downloaded images from memory cards. No bait or lures were for dusk).
used during the study. Temporal activity patterns for each species were analyzed us-
Photographs were classified as independent events to ing circular statistics implemented with the Oriana v. 4.02 software
avoid autocorrelation. We define these independent events as: (Kovach Computing Services, UK). Rayleigh’s Uniformity Test (Zar
a) consecutive photographs of different individuals of the same 2010, Sánchez et al. 2009) was used to verify whether the inde-
species; b) consecutive photographs of individuals of different pendent events of each species were non-randomly or uniformly
species; c) each individual in a group photograph; d) one hour distributed. Non-random timing of events could signal that the
between photographs only when it was not possible to identify animals were nocturnal, diurnal or crepuscular. If independent
individuals (O’Brien et al. 2003, Linkie and Ridout 2011). events were uniformly distributed throughout the day, the species
were classified as cathemeral (Zar 2010, Oliveira-Santos et al. 2012).
Temporal activity
We also compared the activity pattern of the jaguar and
We grouped independent photographic events into 24 puma between years (2015, 2016, and 2017) and seasons (dry and
one-hour categories starting at 00:00 h. Daily activity patterns wet) using parametric or nonparametric circular tests depending
for each species were further broken down into day, night, and on whether or not the data showed a von Mises distribution.
crepuscular (dawn and dusk). We determined the exact time of This distribution can be regarded as the circular analogue of the
dawn and dusk by using Sun Times software v. 7.1 (Kay and Du normal distribution on the line (Forbes et al. 2010).
Croz 2008, Carbajal-Borges et al. 2014), which considers the We calculated the temporal coefficient of overlap (∆) and its
latitude and time zone of the ECBR. In this way, we calculated 95% confidence interval from 10,000 bootstrap samples between
the range based on the monthly mean and considered one hour jaguar and puma activity patterns (Ridout and Linkie 2009). The
before and one hour after the corresponding dawn/dusk time coefficient of overlap is defined as the area under the curve which is
(e.g. with a monthly mean of 07:45 h; range = 06:45–08:45 h for formed by taking the minimum of two kernel density indices (one

ZOOLOGIA 38: e63231 | https://doi.org/10.3897/zoologia.38.e63231 | June 25, 2021 3 / 10

 C.A. Contreras-Díaz et al.

for jaguars, one for pumas) at each time point (Linkie and Ridout (Google Earth) and ArcGIS 10.2 to digitize the five habitat types
2011). The kernel density index is used to estimate time use for of the reserve and calculated the percentage of available area
each species by treating them as random samples from an under- for each habitat (DF [30.37%], SDF [6.41%], OF [38.19%], OPF
lying continuous distribution, instead of grouping photographic [7.40%], MCF [17.64%]). We used the index of selectivity (Ei)
events into discrete time categories. Overlap values ranged from 0 according to Krebs (1999): Ei = (ri – ni)/(ri + ni), where ri is the
(no overlap) to 1 (complete overlap). Low overlap was defined as percentage of jaguar or puma in each habitat type i; ni is the
∆ < 0.50, moderate overlap was 0.50 < ∆ < 0.70, and high overlap percentage of habitat type i available in ECBR. This index produ­
was ∆ > 0.70. Boundary values are intermediate to those of Massara ces values from –1 (habitat avoidance) to +1 (habitat selection);
et al. (2018) and are within estimated ranges from Monterroso et values close to zero indicate habitat is being used according to
al. (2014). Time overlap analysis was conducted in R v. 0.3.3 using its availability in the environment. The index data were resam-
the overlap package (R Development Core Team; Meredith and pled using bootstrap (10,000 replicates with replacement), 95%
Ridout 2020). Because we always had greater than 75 samples, we confidence intervals (CI) were estimated with R v. 3.1.3 (Glen
used the Dhat4 (∆4) estimator (Ridout and Linkie 2009). et al. 2012), and means reported with ± 1 SD.
Further, to know on a fine scale if both felids share the
Habitat use
same space, we determined the percentage of camera trap sta-
We grouped independent events of jaguars and pumas into tions where jaguars and pumas were photographed at the same
the five habitat types (DF, SDF, OF, OPF, MCF), and spatial overlap site, but at different times.
was subsequently calculated with the Pianka index. This index
ranges from 0 (no overlap) to 1 (complete overlap) and was per-
RESULTS
formed in EcoSim 7.0 software (http://www.garyentsminger.com/
ecosim) (Entsminger 2014). We compared our observed overlap in From January 2015 to December 2017, we had 28,220
the habitat between jaguars and pumas with null models of habitat camera trap days of survey effort and 1,063 photographs of
overlap generated by EcoSim. Null models used 10,000 randomly jaguars and pumas, 553 of which were identified as independent
generated interactions with a level of significance of 0.05. The events (371 jaguars; 182 pumas).
RA3 algorithm was used because it preserves the specialization
of each species but allows for the potential use of other resources Temporal activity
(Winemiller and Pianka 1990, Gómez-Ortiz et al. 2019). The activity pattern of jaguars was mainly nocturnal;
We also performed a selectivity habitat analysis to deter- 80% of independent events at night and activity peaks at 21:00,
mine if the jaguars and pumas used or avoid some habitat types 22:00, and 02:00 h (Fig. 2). The activity pattern of pumas was
of the ECBR according to availability. We used satellite imagery also nocturnal; 60% of independent events occurring at night

Figure 2. Circular histograms of activity patterns for jaguar (Panthera onca) and puma (Puma concolor) in El Cielo Biosphere Reserve, Tam-
aulipas, Mexico. Each bar is a discrete 1-hour time interval and is centered on the hour. The dependent variable (inner circles) is number
of times jaguars or pumas appeared in photographs at each time interval.

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 Temporal and spatial segregation of top predators

activity peaks at 20:00, 22:00, and 04:00 h (Fig. 2). However, the Habitat use
rest of the independent events for pumas (40%) were distributed The habitat use analysis showed that jaguars mostly used
at different times during the day and we even observed puma DF with 90% of independent records found in this habitat types,
activity peaks at 17:00, 06:00 and 07:00 h (Fig. 2). Rayleigh’s Uni- while pumas mostly used three different types of habitats in
formity Test (Z) did not show a uniform distribution throughout ECBR: OF (35%), DF (31%), and OPF (24%). The Pianka index
the day in jaguars (Z = 196.62, p < 0.01) or pumas (Z = 18.01, indicated an intermediate spatial overlap (0.61) between jaguars
p < 0.05), so neither species was classified as cathemeral (Zar and pumas. Therefore, pumas show behaviors of a generalist
2010, Oliveira-Santos et al. 2012). In both species, the data species by using a greater number of habitat types, which is
showed a greater tendency toward nighttime activity (Fig. 2). a potential strategy to avoid encounters with jaguars, and for
Jaguar and puma activity patterns did not show a Von both to coexist in the same landscape with similar habitats. We
Mises distribution (U2) in some years (jaguar: 2015 U2 = 0.23, p also recorded a low percentage (22.5%) of co-occurrence (sites
< 0.05; 2016 U2 = 0.04, p > 0.05; 2017 U2 = 0.32, p < 0.05; and where we photographed jaguars and pumas in the same space
puma: 2015 U2 = 0.05, p > 0.05; 2016 U2 = 0.02, p > 0.05; 2017 but at different times).
U2 = 0.03, p < 0.05). Based on these results we use a Mardia-Wat- Habitat selectivity analysis (Ei) showed segregation in
son-Wheeler (W) nonparametric multisample test to compare relation to habitat use. The jaguar selects the DF (Ei = 0.48), uses
jaguar and puma activity patterns among sampling years, and the SDF in proportion to availability (Ei = −0.08), and avoids
no significant differences were found (jaguar: W = 1.63, p > 0.05; using the MCF (Ei = −1), OF (Ei = −0.84), and OPF (Ei = −0.39).
and puma: W = 5.1, p > 0.05). In comparison, puma prefers the OPF (Ei = 0.41), uses the OF
We also compared the activity pattern of the jaguar (Ei = −0.04), DF (Ei = 0.09) and SDF (Ei = −0.18) in proportion to
between seasons (dry and wet) using the Watson-Williams (F) availability, and avoids using the MCF (Ei = −0.51). Based on the
parametric test (two samples) and the Von Mises distribution results of this analysis we believe that jaguars are more selective
(wet season: U2 = 0.41, p > 0.05; dry U2 = 0.14, p > 0.05). For than pumas (Fig. 4) in their use of habitat and it is probably
pumas we use Mardian-Watson-Wheeler (W) nonparametric test the main segregation mechanism that allows these felids to
(two samples), because the season did not show a Von Mises coexist in ECBR.
distribution (wet: U2 = 0.04, p < 0.05; dry: U2 = 0.03, p < 0.05).
However, there were also no significant differences in activity DISCUSSION
between wet and dry seasons (jaguar: F = 0.16, p > 0.05; and
puma W = 0.89, p > 0.05), so we did not consider those variables Jaguars and pumas are sympatric top predators across the
in the time overlap analysis. entire jaguar range, share a remarkably similar morphology, and
Time overlap analysis showed a high coefficient of overlap are obligate carnivores (Iriarte et al. 1990, Sunquist and Sun-
between jaguars and pumas (∆4 = 0.77) with confidence intervals quist 2002, Haines 2006). Both specialize in mammalian prey
of 0.71–0.84 (Fig. 3). and therefore experience significant intra guild competition.

Figure 3. Time overlap analysis of activity patterns between jaguar (Panthera onca) and puma (Puma concolor) in El Cielo Biosphere Reserve.
Time overlap is shown by the shaded area. The solid line represents the activity pattern of jaguars and dashed line shows the activity
pattern of pumas (∆4 = 0.77 is the result of the overlapping coefficient between jaguar and puma activity).

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 C.A. Contreras-Díaz et al.

periods but increase their activity at night. 2) At night, when

activity of both felids increases, some temporal segregation seems
to be present. Jaguars are most active from 21:00 to 22:00 h,
and 02:00 h, while puma activity peaks are in 20:00, 22:00 and
04:00 h (Fig. 2). However, based on these results (high temporal
overlap), we believe that the temporal mechanism may only be a
secondary strategy in the jaguar and puma interaction in ECBR.
Some authors suggest that pumas adjust their activity pattern
to local conditions on a finer scale as a strategy to avoid direct
encounters and coexist with jaguars (Scognamillo et al. 2003,
Moreno et al. 2006, Harmsen et al. 2009, Paviolo et al. 2009, Di
Bitetti et al. 2010, Hernández-SaintMartín et al. 2013).
Jaguars were nocturnal in the ECBR (80% of the inde-
pendent photographs) and did not show uniformity in their
daily activity and were not considered cathemeral. The jaguar
activity in this study is similar to that described in other studies
(Rabinowitz and Nottingham 1986, Núñez et al. 2002, Maffei
et al. 2004, Di Bitetti et al. 2010, Foster et al. 2013, Carrera-Tre-
viño et al. 2016, De la Torre et al. 2017) but differs from some
that classify them as cathemeral (being active throughout day)
(Emmons 1987, Gómez et al. 2005, Blake et al. 2012, Hernán-
dez-SaintMartín et al. 2013).
Pumas showed a greater tendency to be nocturnal but
showed activity at different times throughout the day; how-
ever, were not considered cathemeral. Other authors mention
that puma activity during the day is common and may be due
to low human activity and the availability of prey during the
Figure 4. Habitat selection by jaguars and pumas based on the Index day (Núñez et al. 2002, Scognamillo et al. 2003, Paviolo et al.
of selectivity (Ei) in El Cielo Biosphere Reserve, Tamaulipas, Mexico. 2009, Di Bitetti et al. 2010, Hernández-SaintMartín et al. 2013,
(DF) Deciduous forest, (SDF) semi-deciduous forest, (OF) oak forest, Ávila-Nájera et al. 2016, De la Torre et al. 2017). It’s possible
(OPF) oak-pine forest, (MCF) mountain cloud forest. that the activity shown by pumas during the day in the ECBR is
due to the presence of the jaguar and minimal human activity.
Carrera-Treviño et al. (2016) reported no sightings of pumas
Three axes of ecological niche (use of time, space, and food) during daylight hours on the periphery of the ECBR probably
are commonly used to decipher the intensity of interspecific because their study was carried out in disturbed areas and those
and intraspecific interaction between species (Schoener 1974, with human settlements.
Pianka 1978, Di Bitetti et al. 2010, Morato et al. 2016, Rayan and The reasons for nocturnal activity of jaguars and pumas
Linkie 2016). The theory predicts that high temporal overlap in are variable, but some authors hypothesize that hunting at
these axes promote a high rate of competition between species. night is advantageous because the two felids can get closer to
Low temporal overlap in one or more of the axes may signal a their prey without being detected (Sunquist and Sunquist 2002,
lower rate of competition, and thus species are more likely to Estrada-Hernández 2008), prey are more detectable or vulnera-
coexist without significant negative effects on each other that ble at night (Emmons 1987, Sunquist and Sunquist 2002), and
could lead to the complete exclusion (Gause 1932, Hardin 1960). cool nights allow felids to spend less energy hunting or when
Our results showed a high temporal overlap between moving from one place to another (Sunquist and Sunquist 2002,
jaguars and pumas in the ECBR (∆4 = 0.77). These observations Estrada-Hernández 2008, Foster et al. 2013).
concur with results of studies conducted in the Venezuelan lla- Understanding how large felids use habitat is essential to
nos (Scognamillo et al. 2003), Belizean rainforest (Harmsen et allow us to identify whether habitat use is a strategy for coexis-
al. 2009), Quintana Roo, Mexico (Ávila-Nájera et al. 2016), San tence in species that are potential competitors (Cristescu et al.
Luis Potosi, Mexico (Hernández-SaintMartín et al. 2013), and 2013). Our results of spatial overlap showed an intermediate
four Brazilian biomes (Foster et al. 2013). In the ECBR we think overlap between jaguars and pumas (Pianka index = 0.61).
that pumas use two strategies of temporal activity, considering Habitat use analysis showed that the jaguar prefers DF, uses SDF
the argument that jaguars dominate pumas (Elbroch and Ku- in proportion to availability and avoids the MCF, OF and OPF.
sler 2018). 1) Pumas are active during daylight and crepuscular In comparison pumas prefer OPF, also had records in OF, DF

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 Temporal and spatial segregation of top predators

and SDF, and used these types of vegetation according to their exclusively nocturnal; 4) Pumas used four habitat types; 5) We
availability and avoids the MCF (Fig. 4). Thus, it is possible that recorded a low percentage of co-occurrence (22.5%) in sites
jaguars are more selective in their use of habitat than pumas in where pumas and jaguars shared the same space.
the ECBR. Other researchers argue as well that the pumas are Our results yielded interesting conclusions of temporal
generalists and can be found in a wider range of habitats than and spatial interactions between jaguars and pumas and im-
the jaguar across their distribution (Iriarte et al. 1990, Sunquist proves our knowledge about the ecology of these Neotropical
and Sunquist 2002). Pumas can even live in proximity to hu- felids within a protected area (ECBR). We suggest that temporal
mans (Dickson and Beier 2007, De Angelo et al. 2011, Sollmann segregation is not the main coexistence mechanism between
et al. 2012), but they sometimes also avoid areas disturbed by these two felids because our temporal overlap results were high.
human activity (Paviolo et al. 2009, Di Bitetti et al. 2010, Foster Temporal segregation may only be a secondary strategy in the
et al. 2010, De Angelo et al. 2011). Finally, the low percentage jaguar and puma interaction. Instead, we suggest that spatial
of co-occurrence (22.5%) in sites where jaguars and pumas segregation may be the mechanism that best explains the coexis­
were photographed using the same space at different times may tence of the jaguar and puma in the ECBR. We believe that the
indicate they actively try to avoid each other. Scognamillo et presence of different habitat types allows these felids to avoid
al. (2003) suggest that differences in use of habitat patches by each other and coexist. In addition, the puma’s generalist habits
jaguars and pumas in the Venezuelan llanos was an important are an important factor to consider. In this study, pumas used
component of their ecological separation. a wider array of time and space. Finally, we recommend in a
Based on our results of spatial overlap (Pianka index future study in ECBR, to determine the diet of the jaguar and
= 0.61), habitat use, and low percentage of co-occurrence in puma (scats analysis) to include an analysis of trophic niche
shared sites, we believe this is the mechanism that best explains overlap between those two felids, and then, analyze the temporal
the coexistence of jaguars and pumas in ECBR. Of course, this overlap of the felids and their main prey. This last analysis is
statement should be taken with caution until the diet of these essential, because it would help to corroborate the coexistence
two felids can be analyzed in a future study. Jaguars showed a of the jaguar and puma in the ECBR.
strong preference for DF, used three other habitats sparingly,
and were absent from the MCF. Pumas preferred OPF but used ACKNOWLEDGEMENTS
the four other types of habitats (albeit some sparingly). Because
of the ECBR’s variety of habitat types, high heterogeneity, and We thank the Programa para la Conservación de Especies
low disturbance by humans (Steinberg et al. 2014), jaguars and en Riesgo de la Comisión Nacional de Áreas Naturales Protegidas
pumas are able to avoid each other and coexist. Other authors (CONANP); the owner of the lands, and volunteers of the wildlife
have suggested that in heterogeneous landscapes two sympatric laboratory of the Faculty of Veterinary Medicine and Zootechnics
carnivores can use different habitat types to coexist and it is of the Autonomous University of Nuevo Leon, Mexico. We also
known that pumas use a wider range of habitat than jaguars thank the Autonomous University of Tamaulipas for funding
(Emmons 1987, Aranda and Sánchez-Cordero 1996, Johnson et the project UAT/PFI2015-15, and to the Program for Profes-
al. 1996, Scognamillo et al. 2003, Sollmann et al. 2012). sional Development for Higher Education (PRODEP) through
Additionally, Elbroch and Kusler (2018) analyzed whether the project UAT-PTC-221/511-6/17-8212. We also thank to two
pumas are dominant, subordinate, or equal to other apex preda­ anonymous reviewers for their comments and to R.J. Smith for
tors, and conclude that jaguars are the dominant species over copyediting English version.
pumas (60%). Generally, pumas tend to change their activity
pattern, habitat, and diet to avoid competing with the jaguar. LITERATURE CITED
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SEMARNAT (2010) Norma Oficial Mexicana NOM-059-SEMAR- Competing Interests: The authors have declared that no
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biblioteca.semarnat.gob.mx/janium/Documentos/Ciga/ © 2021 Sociedade Brasileira de Zoologia. Published by Pensoft
agenda/DOFsr/DO2454.pdf Publishers at https://zoologia.pensoft.net

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