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Abundance and activity patterns of medium-sized felids (felidae, carnivora) in Southeastern Mexico.

In terrestrial ecosystems, apex predators have a significant influence on structure and functionality through a top-down control process (Steneck, 2005; Ritchie and Johnson, 2009). However, medium-size predators or mesopredators also contribute to the dynamics of ecosystems through diverse interactions. Both groups may affect other species in two ways: 1) lethal encounters may directly affect population size or 2) apex predators may control mesopredators through intraguild interactions (Ritchie and Johnson, 2009; Lourenco et al., 2014). In response to these interactions, species might change habitat use or alter foraging behavior and activity to diminish lethal encounters with the dominant species (Elmhagen and Rushton, 2007; Ritchie and Johnson, 2009; Lourenco et al., 2014).

In the neotropics, there are two apex predators: jaguar (Panthera onca, 37-158 kg) and puma (Puma concolor, 35-71 kg). Both species have suffered major declines due to habitat loss, overexploitation, and hunting by humans. Because of this, in some original areas of distribution, these predators are no longer present (Salom-Perez et al., 2007). There are eight medium-sized felids (species larger than 1 kg) in this region and the dominant species is the ocelot (Leopardus pardalis, 11-16 kg). This species is the most-studied by wildlife biologists compared to felids of similar size. Other species such as the margay (Leopardus wiedii, 3-6 kg), the jaguarundi (Puma yagouaroundi, 3-8 kg), Geoffroy's cat (Leopardus geoffroyi, 2-8 kg), and the oncilla (Leopardus tigrinus, 1.5-3.5 kg) are little-studied due to their cryptic behavior (Cuellar et al., 2006; de Oliveira et al., 2010; de Oliveira and Pereira, 2014).

Within the assemblage of felids, L. wiedii is the most arboreal of the felids in the neotropics. Its present distribution ranges from Mexico to the north of Argentina and Paraguay (de Oliveira, 1998). This species eats arboreal mice, squirrels, birds, amphibians, and reptiles (de Oliveira, 1998; Sunquist and Sunquist, 2002; Bianchi et al., 2011) and sleeps and rests primarily in trees; consequently its presence depends on dense vegetation (de Oliveira, 1998; Sunquist and Sunquist, 2002; but see Di Bitetti et al., 2010).

Puma yagouaroundi is largely sympatric with L. wiedii and L. pardalis. It is distributed from the south of the United States to the center of Argentina. It is mediumsized and lives in a variety of vegetation types, although it prefers the edges or semiopen areas surrounding tropical forests, scrubs, or chaparrals (de Oliveira, 1998; Sunquist and Sunquist, 2002). It has diurnal habits and consumes a variety of prey such as mice, birds, reptiles, and arthropods (Sunquist and Sunquist, 2002). Like L. wiedii it is a little-studied species (Maffei et al., 2007; Bianchi et al., 2011; Charre-Medellin et al., 2012). Members of this species are difficult to identify at an individual level as they do not have a spot pattern like L. wiedii or L. pardalis, and it is therefore difficult to estimate their population size (de Oliveira, 1998; Maffei et al., 2007; Caso et al., 2008).

Population size of L. pardalis varies across its geographic distribution (Di Bitetti et al., 2008; de Oliveira et al., 2010). In some regions L. pardalis is considered by researchers to be abundant compared to other medium-sized felids (Di Bitetti et al., 2008). Leopardus wiedii and L. tigrinus are considered more abundant where L. pardalis is scarce or absent (Vanderhoff et al., 2011; Carvajal-Villarreal et al., 2012; Oliveira-Santos et al., 2012). In contrast, in other areas where L. pardalis is more abundant, these species are less abundant (Di Bitetti et al., 2010). Also it has been suggested by Oliveira-Santos et al. (2012) that these species might alter their activity pattern in areas where L. pardalis or other large felids occur together. This temporal segregation could be an important mechanism that allows for coexistence among felids (Di Bitetti et al., 2010).

Five out of the six felid species in Mexico inhabit the southeastern region of the country: two large-sized species, P. concolor and P. onca; and three medium-sized species, L. wiedii, L. pardalis, and P. yagouaroundi. Wildlife biologists do not know population sizes of medium-sized felids in those regions where they coexist. However, researchers expect population sizes of L. wiedii and P. yagouaroundi to be low (Caso et al., 2008; Payan et al., 2008), particularly in regions where L. pardalis is abundant (Cuellar et al., 2006; de Oliveira et al., 2010). Our objective for this study was to compare the abundance of medium-sized felids and their activity patterns. We only analyzed medium-size felids due to taxonomic and size similarity. Activity patterns would suggest a strategy of reducing interference competition and allowing for coexistence. Knowledge of these factors is crucial to comprehending the factors that enable coexistence between mesopredators (Ritchie and Johnson, 2009; Oliveira-Santos et al., 2012).

MATERIALS AND METHODS--Study Area--The study site was located in the Los Chimalapas region (17[degrees]9'13"N, 94[degrees]21'13.6"W), in the state of Oaxaca, southeastern Mexico. This is part of the Selva Zoque, a region prioritized for conservation by the states of Oaxaca, Veracruz, and Chiapas (Fig. 1). The vegetation type is tropical rainforest. The climate is warm-humid with an average annual temperature of 22-26[degrees]C, and an average annual precipitation of 2,000-2,500 mm (Trejo, 2004).

Field Sampling--We installed a total of 29 permanent sampling stations from March 2011 to June 2013. We placed unbaited camera traps at a height of 30 cm above the ground. Seven sampling stations included two cameras to record both sides of organisms, for individual recognition. Due to topographical conditions and the varying home ranges of each species, the distance interval between traps ranged from 0.5-1.5 km with a total area of 22 [km.sup.2] (Fig. 1). The traps were active 24 h and programmed with a 0.3-1-min delay. We used the Wildgame IR4 4-megapixel digital game-scouting camera (Wildgame Innovations, Los Angeles, California). We used this model for the first 10-12 months of sampling. We changed traps when they were damaged. We substituted the damaged traps (100%) with the ScoutGuard SG550/SG550V (HCO Outdoors Products, Norcross, Georgia), and Bushnell Trophy Cam models (Bushnell Outdoor Products, Overland Park, Kansas). Both models remained active 14-16 months. We deposited photographs in the Coleccion de Referencia de Mamiferos del Laboratorio de Ecologia Animal of the Centro Interdisciplinario de Investigation para el Desarrollo Integral Regional, Unidad Oaxaca, Instituto Politecnico Nacional.

Data Analysis--In order to ensure that all events were independent and to avoid pseudoreplication (Tobler et al., 2008), we considered all photographs taken by each sampling station within a 1-h span as a single record. We calculated relative abundance as the number of single records of felids in 100 camera-days. In order to estimate population size and density, we identified each individual of L. wiedii and L. pardalis according to spot patterns (Trolle and Kery, 2003; Maffei et al., 2005). We determined if the population was statistically open or closed with the program CloseTest (Stanley and Richards, 2005). We estimated abundance using the Corman-Jolly-Seber probabilistic model (Lebreton et al., 1992; Santos-Moreno et al., 2007; Pdrez-Irineo and Santo-Moreno, 2014). We used the program MARK version 8.0 (White and Burnham, 1999) for the construction and analysis of the models.

The Corman-Jolly-Seber model estimates only two parameters: survival probability ([PSI]) and capture probability (p). Both parameters can vary or remain constant over time, so there are four candidate models: 1) both parameters constant ([PSI]p); 2) constant [PSI] and p varying through time (expressed in years: 2011, 2012, and 2013; [[PSI]p.sub.t]); 3) [PSI] varying over time and constant p ([[PSI].sub.t]p); and 4) both [PSI] and p vary over time ([[PSI].sub.t][p.sub.t]; Lebreton et al., 1992; Table 1). The best model was selected using the quasi-Akaike information criterion (Burnham and Anderson, 2002).

Once we selected the final model, we estimated population size (N) as the number of identified organisms divided by the probability of capture (Lindenmayer et al., 1998). Population size was extrapolated for an area of 100 [km.sup.2] in order to make comparisons between species. We calculated the effective area in accordance with Karanth and Nichols (1998), and used the mean maximum distance traveled by the individuals on two or more occasions. As the distance between traps is short and might result in dependence between records, we used the Moran index (I) to evaluate spatial autocorrelation between camera trap records (Sokal and Oden, 1978). We carried out the tests with the program ArcGis version 9.3 (ESRI, Redlands, California).

[FIGURE 1 OMITTED]

In order to describe activity patterns, we divided the 24-h period into hour-long segments, and classified each independent record within those intervals. Daytime was defined as lasting from 0600-2000h and night from 2000-0600h. We evaluated the significance of the difference of activity patterns between species using the Mardia-Watson-Wheeler (W) test (Zar, 1999). We carried out the tests with the program Oriana version 4 (Kovach Computing Services, Anglesey, United Kingdom). The level of significance of all the tests was P [less than or equal to] 0.05.

RESULTS--In 8,529 trap-days, we obtained 78 records of L. wiedii, 112 of L. pardalis, and 7 of P. yagouaroundi. Additionally, P. concolor (n = 42 records) and P. onca (n = 44) were recorded by the traps. Leopardus pardalis showed higher relative abundance (1.31 records/100 trap-days) in comparison with other felids (Table 2). We did not analyze P. yagouaroundi due to the low quantity of data. All records of this species were taken during the day. Of the total L. wiedii records, we used 40 to identify 11 individuals and discarded 38 records due to poor photographic quality. Of these 11 identified individuals of L. wiedii, seven were female, two male, and two of indeterminate sex. A total of 45% of these individuals (n = 5) remained in the zone for 1 month and the mean residence time was 5.7 [+ or -] 1.59 months. One female of L. wiedii had the longest residence time (14 months). Of the 112 records of L. pardalis, we used 59 records to identify nine individuals. Three individuals were female, five were male, and one undetermined. We observed five of nine ocelots (55%) during a single month, and the mean residence time was 7.44 [+ or -] 2.8 months.

The camera-trap records were independent for each year ([I.sub.2011] = 0.015, P = 0.84; [I.sub.2012] = 0.125, P = 0.64; [I.sub.2013] = -0.012, P = 0.65) and for all years combined (I = 0.095, P = 0.66). For L. pardalis and L. wiedii, the test results indicated a demographically open population ([chi square]l. wredi = 31.07, df = 13, P = 0.00; [chi square]L, pardalis = 223.47, df = 20, P = 0.00), and according to the best model (Table 1), the estimated abundance for L. wiedii was 36 individuals and the density was 68 individuals/100 [km.sup.2] (Table 2). According to the best model (Table 2), estimated abundance for L. pardalis was 20.13, and density was 22 individuals/100 [km.sup.2] (Table 2).

For L. wiedii, 80% of all records were at night, with peak activity from 0100-0200h, whereas 50% of records of L. pardalis were at night, with peak activity from 01000600h (Fig. 2). The activity patterns of L. wiedii and L. pardalis were significantly different (W = 17.43, P < 0.05).

DISCUSSION--The assemblage of felids at Los Chimalapas includes three medium-sized and two large-sized species, all recorded in this study. We obtained a number of records suitable for estimating population densities of L. pardalis and L. wiedii. Even the most conservative density estimations of L. wiedii (68 individuals/100 [km.sup.2]; Table 2) were still greater than the density estimated for L. pardalis in Los Chimalapas (22 individuals/100 [km.sup.2]; Table 2). Leopardus pardalis had a medium abundance in this region in comparison with other regions of South America where density estimates up to 160 individuals/ 100 [km.sup.2] have been reported (Di Bitetti et al., 2008).

In contrast to L. pardalis, few density estimates exist for L. wiedii: 12.14 individuals/100 [km.sup.2] at Sierra Nanchititla, central Mexico (Lopez, 2010) and 19 individuals/100 [km.sup.2] in the tropical dry forest in Bolivia (Cuellar et al., 2006). In the region of Misiones, Argentina, L. wiedii has fewer records, even fewer than L. tigrinus, which is a smaller species (Di Bitetti et al., 2010). In other regions, researchers have recorded L. wiedii in greater numbers and this has been attributed to the absence of L. pardalis (Vanderhoff et al., 2011; Carvajal-Villarreal et al., 2012). However, this pattern must be considered with caution, because the rate of photographic records does not always accurately reflect abundance of species (Jannelle et al., 2002), and therefore the low proportion of records does not necessarily indicate low abundance, especially in dense forest. In our study, L. wiedii was present in lower relative abundance, but we identified more individuals of L. wiedii than L. pardalis.

[FIGURE 2 OMITTED]

A possible explanation of the relationship between the densities of these species is the "ocelot effect" (de Oliveira et al., 2010). Under the ocelot effect small felids have a lower density in regions where L. pardalis is abundant and only reach high abundance in regions where the ocelot is absent or scarce. That is, when L. pardalis is the principal mesopredator, it negatively influences the populations of several felids and affects the structure of the assemblage (de Oliveira et al., 2010; de Oliveira and Pereira, 2014). The effect diminishes in cases where predator abundance is low, and other smaller species may use more resources with a low risk of negative interactions (Steneck, 2005; Ritchie and Johnson, 2009; de Oliveira et al., 2010). However, the prediction of the ocelot effect was not supported in the region of Chimalapas: the density of L. wiedii was greater than that of ocelots. Puma yagouaroundi was relatively rare, but likely due to this species' preference for the edge of forests and open areas (Sunquist and Sunquist, 2002; Caso et al., 2008). In contrast, L. pardalis frequents vegetation-dense zones (Sunquist and Sunquist, 2002). We placed camera traps inside the vegetation and maybe this was the reason that P. yagouaroundi was recorded so infrequently.

Beside intraguild predation, the relatively large population density of medium-sized felids may be explained by factors such as environment quality. The arboreal structure and dense vegetation provide a wide availability of refuge and prey. The region of Los Chimalapas is well preserved and has low human activity; it is a heterogeneous region, with steep topography and dense forest (Salas et al., 2001; Martinez, 2012). As was mentioned for L. pardalis (Perez-Irineo and Santos-Moreno, 2014), the quality of the environment and the availability of prey might affect population size; therefore a bottom-up control process might determine felid population patterns.

Both species, L. pardalis and L. wiedii, are primarily nocturnal (de Oliveira, 1998; Sunquist and Sunquist, 2002), but in this study L. pardalis had diurnal and nocturnal activity with the same frequency (50%), and differences in activity pattern between species were significant. Activity patterns of felid species may be the result of negative interactions (de Oliveira et al., 2010; Oliveira-Santos et al., 2012). However, they might also reflect a response to behavioral differences and prey preferences.

The lack of knowledge about mesopredator density and their interactions is a critical problem to understanding the patterns of abundance. This study showed that the prediction of the ocelot effect was not supported in the region of Los Chimalapas. There are possibly other explanations for observed density patterns of medium-sized felids than intraguild predation (difference in habitat selection, behavioral or bottom-up control process).

Researchers previously believed it to be difficult to find viable L. wiedii populations outside of the Amazonian region (Payan et al., 2008), but this study provides evidence that in the southeastern region of Mexico there is a considerable population of L. wiedii coexisting with L. pardalis. Both species are a prioritized conservation species in Mexico (Valenzuela and Vazquez, 2007), are listed as Endangered (SEMARNAT, 2010) and L. wiedii is cataloged as Near Threatened at an international level (Payan et al., 2008). Puma yagouaroundi and L. wiedii are poorly studied species (Downey, 1994; Bianchi et al., 2011; Carvajal-Villarreal et al., 2012; Valenzuela-Gahan et al., 2013), and both coexist with L. pardalis in southeast Mexico. There is no formal governmental conservation scheme in place in the region of Los Chimalapas, although there are voluntary community initiatives that contribute to conservation of the tropical forest and the presence of felids. The presence of these predators may ensure the health of these communities of vertebrates in tropical environments.

The authors thank the San Antonio Nuevo Paraiso community in Mexico for the facilities granted, as well as the people who collaborated on fieldwork; IDEA WILD for donated materials; Consejo Nacional de Ciencia y Tecnologia of Mexico for a scholarship provided to the first author; and Instituto Politecnico Nacional of Mexico for funding (Projects SIP20110395, SIP20120962, and SIP-20131154 to A. Santos-Moreno). We thank anonymous reviewers for their suggestions on the manuscript.

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Submitted 5 January 2015.

Acceptance recommended by Associate Editor, Jennifer K. Frey, 17 January 2016.

Gabriela Perez-Irineo *, Antonio Santos-Moreno

Laboratorio de Ecologia Animal, Centro Interdisciplinario de Investigaciin para el Desarrollo Integral Regional, Unidad Oaxaca, Instituto Politicnico Nacional, Hornos 1003, Colonia La Noche Buena, Santa Cruz Xoxocotlan, Oaxaca, Codigo Postal 71230, Mixico

* Correspondent: gabyirineo@yahoo.com.mx
Table 1--Corman-Jolly-Seber capture-recapture models for Leopardus
wiedii and Leopardus pardalis in the region of Chimalapas,
southeastern Mexico, during 2011-2013. QAICc = quasi-Akaike
information criterion, [DELTA]QAICc = difference of QAICc values
between the best and the respective model. QAICc weight = relative
contribution of each model in respect to the sum of all of the
models. The four candidate models were built according to whether one
or both parameters ([PSI] and p) vary or remain constant over time.
For example, the best model ([[PSI].sub.t]p) indicates that the
survival probability ([PSI]) varies over time: [[PSI].sub.2011],
[[PSI].sub.2012] and [[PSI].sub.2013]. In contrast capture
probability (p) is constant, so there are four parameters.

Species      Model   QAICc    [DELTA]QAICc   QAICc    No. of
                                             weight   parameters

Leopardus    Utp     92.9     0              0.484    4
  wiedii     Up      93.4     0.435          0.389    2
             Utpt    97       4.027          0.066    6
             Upt     97.1     4.123          0.061    4
Leopardus    Utp     120.71   0              0.751    4
  pardalis   Utpt    123.8    3.103          0.159    6
             Up      125.3    4.629          0.074    2
             Upt     128.4    7.705          0.015    4

Table 2--Number of records and density of felids at Los Chimalapas,
southeastern Mexico, 2011-2013.

                          Puma           Leopardus       Leopardus
                          yagouaroundi   wiedii          pardalis

No. of records            7              78              112
Relative abundance (a)    0.082          0.914           1.313
Individuals               --             11              9
Abundance [+ or -] SE     --             36 [+ or -]     20 [+ or -]
                                           0.06 (b)        0.08 (c)
Density (CI) (d)          --             68 (57-79)      22 (17-32)
Total area ([km.sup.2])                  53 (e)          89 (f)
Capture probability                      0.30 [+ or -]   0.44 [+ or -]
  [+ or -] SE                              0.06            0.07

(a) The relative abundance was number of records in 100 trap-days.

(b) The estimated abundance of L. wiedii was based on the best model
([[PSI].sub.t]p) of Corman-Jolly-Seber capture-recapture models.

(c) The estimated abundance of L. pardalis was based on the best
model ([[PSI].sub.t]p).

(d) The unit for density was individuals/100 [km.sup.2]; CI = 95%
confidence interval.

(e) The buffer used for the calculation of the total area was mean
maximum distance traveled = 1.4 km (SD = 0.1).

(f) The buffer used for the calculation of the total area was mean
maximum distance traveled = 2.6 km (SD = 0.8).
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Article Details
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Author:Perez-Irineo, Gabriela; Santos-Moreno, Antonio
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Mar 1, 2016
Words:4584
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