SciELO - Scientific Electronic Library Online

 
vol.12 número3Mammal species richness and new records in protected natural areas of the northern part of the metropolitan area of the Valley of MéxicoRelationship between age-sex classes and prevalence of Giardia spp. and Blastocistys spp. in black and gold howler monkeys inhabiting fragmented forests índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • No hay artículos similaresSimilares en SciELO

Compartir


Therya

versión On-line ISSN 2007-3364

Therya vol.12 no.3 La Paz sep. 2021  Epub 28-Mar-2022

https://doi.org/10.12933/therya-21-1128 

Articles

Spatial ecological interactions between coyote and gray fox in a temperate forest

César R. Rodríguez-Luna1 

Jorge Servin2  * 

David Valenzuela-Galván3 

Rurik List4 

1 Doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana. Calzada Del Hueso 1100, CP. 04960, Ciudad de México, México. Email: crodriguezluna@gmail.com (CRR-L).

2 Departamento El Hombre y su Ambiente, Universidad Autónoma Metropolita-Unidad Xochimilco. Calzada Del Hueso 1100, CP. 04960, Ciudad de México, México. Email: jservin@correo.xoc.uam.mx (JS).

3 Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos. Av. Universidad 1001, CP. 62209, Morelos, México. Email: dvalen@uaem.mx (DV-G).

4 Departamento de Ciencias Ambientales, Universidad Autónoma Metropolitana-Unidad Lerma. Av. Las Garzas 10, CP. 52005, Estado de México, México. Email: r.list@correo.ler.uam.mx (RL).


Abstract:

Coyotes (Canis latrans) and gray foxes (Urocyon cinereoargenteus) are abundant and widely distributed in México, with no information currently available about their spatial interactions in the country. Our objectives were to evaluate the habitat use of these species and the environmental interactions between them throughout the overlapping areas of their home ranges in temperate forests of Durango, México. We expected that their coexistence would be facilitated by the spatial segregation of their ecological niche, exhibited by the low or nil overlap between their home ranges or by differentiated habitat use. Radio-collars (VHF) were attached to nine individuals - four coyotes (two males and two females) and five gray foxes (females) - that were radio-tracked from September 2017 to August 2019. We estimated their home ranges and the size of their core areas through the minimum convex polygon and determined the extent of overlap between them. Also, we evaluated third-order habitat selection and use based on habitat availability using Manly’s habitat-selection ratios and simultaneous Bonferroni confidence intervals (95 %). The mean home range size for coyotes was larger (12.2 ± 1.74 km2) than for gray boxes (5.3 ± 0.67 km2); the interspecific mean overlap was 42 % (moderate). Of these two canids, just the gray fox showed a markedly selective habitat use. Our findings revealed a moderate overlap between the home ranges of both canids, so spatial segregation did not occur. Although a differential habitat use was observed, explaining the coexistence between these two canids in the areas where they thrive, they tend to avoid agonistic interactions.

Keywords: Biosphere reserve; Canis latrans; coexistence; Durango; habitat use; home range; overlap; radiotelemetry; segregation; Urocyon cinereoargenteus

Resumen:

El coyote (Canis latrans) y la zorra gris (Urocyon cinereoargenteus) son especies abundantes y de amplia distribución en México y con poca información acerca de sus interacciones espaciales. Nuestros objetivos fueron, evaluar sus interacciones ecológicas espaciales, a través de la superposición de sus ámbitos hogareños y del uso de hábitat en los bosques templados de Durango, México. Esperábamos que su coexistencia fuera facilitada por la segregación de su nicho ecológico a nivel espacial, exhibida por la baja o ausente superposición entre sus ámbitos hogareños y/o por un marcado uso diferenciado del hábitat. Se colocaron radio-collares (VHF) en nueve individuos, cuatro coyotes (dos machos y dos hembras) y cinco zorras grises (hembras), monitoreándolos entre septiembre de 2017 y agosto de 2019. Estimamos el tamaño de ámbito hogareño y zona núcleo de cada individuo mediante el método del mínimo polígono convexo y determinamos la proporción del área de superposición entre ellos. Además, evaluamos el uso y selección de hábitat de tercer orden con respecto a su disponibilidad mediante el coeficiente de selección de hábitat de Manly e intervalos de confianza de Bonferroni (95 %). El tamaño promedio del ámbito hogareño fue mayor para coyotes (12.2 ± 1.74 km2), que para las zorras grises (5.3 ± 0.67 km2); mientras que, el promedio de la superposición interespecífica fue de 42 % (intermedio). De los dos cánidos, sólo la zorra gris presentó un marcado uso selectivo del hábitat. Nuestros resultados mostraron que los ámbitos hogareños de ambos cánidos presentaron una superposición intermedia, por lo que no se presentó segregación espacial. Aunque si existió un uso diferencial del hábitat, que explica la coexistencia entre estos dos cánidos en los sitios donde ocurren, ya que tienden a evitar interacciones antagónicas.

Introduction

The ecological interactions between sympatric species through competition (interference or exploitation) are key phenomena that contribute to shaping the structure of ecological communities, as they can influence the abundance, distribution, habitat selection, and behavior of species within communities (Case and Gilpin 1974; Holt and Polis 1997; Caro and Stoner 2003; Hunter and Caro 2008).

Interference competition is widely documented for mammals of the order Carnivora, being considered among the main factors that shape intraguild relationships between predators (Polis et al. 1989; Palomares and Caro 1999; Linell and Strand 2000; Donadio and Buskirk 2006; Palomares et al. 2016). In fact, this type of competition between carnivores is generally higher when the species involved are morphologically similar and share similar diets (Morin 1999). The strategy of species to achieve coexistence consists of minimizing competition through niche segregation in one or several dimensions, mainly spatial, trophic, or temporal (MacArthur and Levins 1967; Pianka 1969; Pianka 1973; Schoener 1974). Within this guild, the potential for competition between sympatric species that use similar resources is largely determined by the spatial overlap between them (Kitchen et al. 1999; Palomares and Caro 1999; Grassel et al. 2015; Palomares et al. 2016). To minimize interference competition, subordinate species display a range of ecological strategies: avoidance of encounters with individuals of dominant species, separation of their home ranges, and differences in habitat use (Case and Gilpin 1974; Palomares and Caro 1999; Linell and Strand 2000; Hampton 2004; Rosenheim 2004; Donadio and Buskirk 2006; Berger and Gese 2007; Hunter and Caro 2008; Chiang et al. 2012; Viota et al. 2012; Soto and Palomares 2015; Xia et al. 2015; Gompper et al. 2016; Palomares et al. 2016).

The quantification of the size and overlap of the home ranges of carnivores, as well as the description of habitat use and selection, are essential for understanding the dynamics of ecological communities, as well as for species conservation and management (Bu et al. 2016). However, these complex interactions between sympatric species are generally poorly known in the vast majority of the systems where they thrive (Melville et al. 2015; Gompper et al. 2016).

In North America, the coyote (Canis latrans) and the gray fox (Urocyon cinereoargenteus) are mesocarnivorous species that are sympatric over large portions of their distribution ranges (Bekoff 1977; Fritzell and Haroldson 1982; Fuller and Cypher 2004; Servin et al. 2014a; Servin and Chacón 2014). The spatial interactions and the coexistence process between coyotes and various species of foxes in the Americas have been extensively studied in northern areas of their geographic range (United States of America and Canada). Research on spatial dynamics between coyotes and red foxes (Vulpes vulpes) has shown marked spatial segregation and differentiated use of the local habitat between these species (Voigt and Earle 1983; Sargeant et al. 1987; Theberge and Wedeles 1989; Harrison et al. 1989; Sargeant and Allen 1989; Gese et al. 1996; Gosselink et al. 2003; Mueller et al. 2018). In turn, research on the spatial dimension between coyotes and kit foxes (Vulpes macrotis) has shown the absence of spatial segregation; instead, a differential habitat use has been observed (White et al. 1994; White et al. 1995; Nelson et al. 2007; Moehrenschlager et al. 2007; Kozlowski et al. 2008; Kozlowski et al. 2012; Andrade-Ponce et al. 2020). Most information on spatial interactions between coyotes and gray foxes has been recorded in the United States of America, mainly in coastal shrubland and xeric shrubland areas at low altitudes (<1000 m asl). Some studies reported no spatial segregation between the two species (Neale and Sacks 2001; Chamberlain and Leopold 2005), while others evidenced that gray foxes avoid spatial coexistence with coyotes to reduce the risk of predation (Fedriani et al. 2000; Farias et al. 2012). This topic has been scarcely studied in areas within their distribution range in México, and the details about the spatial dynamics between these canid species in their natural distribution range in the country remain unknown.

For this reason, our objective was to evaluate the spatial ecological interactions between coyotes and gray foxes by analyzing the spatial segregation of the ecological niche under natural conditions in a temperate forest of the Sierra Madre Occidental, state of Durango, México. Our specific objectives were: 1) estimate the size and spatial overlap between the home ranges of both species and 2) evaluate habitat selection and use patterns to determine interspecific variations.

Our assumption was that the coexistence of these two species would be facilitated by the spatial segregation of their niches, exhibited by either a low or nil overlap of their home ranges or a pattern of differentiated habitat use. This is a case of an asymmetric interaction where coyotes display aggressive behavior against canids and other smaller species, which are displaced and even killed by coyotes, as reported for various fox species in North America (Sargeant and Allen 1989; Palomares and Caro 1999; Moehrenschlager and Sovada 2004; Moehrenschlager et al. 2007). Thus, the gray fox (subordinate species) would be actively avoiding coyotes (dominant species) to reduce the risk of predation (Polis et al. 1989; Palomares and Caro 1999; Fedriani et al. 2000; Donadio and Buskirk 2006; Temple et al. 2010; Farias et al. 2012).

Materials and Methods

Study area. This study was conducted in the buffer zone of “La Michilía” Biosphere Reserve (RBM), located in the municipality of Suchil, Durango, México, between coordinates 23° 21’to 23° 28’ N and -104° 09’ to -104° 21’ W (Figure 1). Physiographically, RBM is located in the transition zone between the Sierra Madre Occidental and the northern highlands of México (Halffter 1978); besides, it covers part of the transition zone between the Nearctic and Neotropical biogeographic regions (Löwenberg-Neto 2014; Morrone 2014; Cuervo-Robayo et al. 2020). Altitude in the study area ranges between 2,000 and 2,985 masl (Gadsden and Reyes-Castillo 1991). To the north of the RBM, the climate is temperate and semi-dry (BS1k); in the rest of the zone, the dominant climate is temperate sub-humid (CW; Garcia 2004). The mean annual temperature is 12.6 °C, fluctuating between 2 °C (winter) and 22 °C (summer); the mean annual precipitation fluctuates between 600 and 900 mm (INEGI 2017).

The main vegetation types are conifer forest (Pinus spp.) and oak forest (Quercus spp.); also present are natural grassland (Bouteloua spp.) and xeric shrubland (Arctostaphylos pungens, Acacia schaffneri). There are also transition zones between these types of vegetation, where the dominant species vary according to altitude, geomorphology, and microclimatic conditions, resulting in 22 different types of vegetation (González-Elizondo et al. 1993; Servín et al. 2014b).

Figure 1 Geographic location of the study area in the buffer zone of La Michilía Biosphere Reserve (RBM), Durango, México. Home ranges of radio-collared coyotes (dotted red lines) and gray foxes (solid blue lines), derived from the minimum convex polygon (95 %), and the overlap between them, as well as the habitat types in the study area: Sv, disturbed vegetation (purple); QF, oak forest (light blue); MF, mixed forests (green); F-MS, forests with manzanita shrubland (pale pink); G, grassland areas (pale yellow). Areas in dark blue represent water bodies; the solid black line marks the border of the RBM and the dotted black line, the core zone of the RBM; gray lines are level curves (15 m). 

Capture and Marking. We used Tomahawk® live traps and jaw traps (Victor® Soft Catch No. 3) to capture five gray foxes (females) and five adult coyotes (two females, three males), respectively. The ten individuals captured were sedated by intramuscular injection with a mixture of xylazine (xylazine hydrochloride) and ketamine (ketamine hydrochloride). The composite dose to induce anesthesia was 4 mg/kg ketamine plus 2 mg/kg xylazine for coyotes and 3 mg/kg ketamine plus 20 mg/kg xylazine for gray foxes (Servin and Huxley 1992; Kreeger and Arnemo 2018).

While individuals were sedated, we recorded morphometrics, weight, and sex; age (pup, juvenile, and adult) was determined based on tooth wear. In individuals with weight and measurements of adult animals, we fitted a 150 MHz VHF radio transmitter collar (Telonics®), weighing 120 g (model 200) for gray foxes and 170 g (model 300) for coyotes. The net weight of these radio collars accounted for 1.49 % of the mean weight of the coyotes captured (W = 11,400 ± 1418 g) and 3.88 % of the mean weight of gray foxes captured (W = 3,094 ± 205 g). After the radio collar was fitted, each individual was released and at the capture site on the same day.

The handling and physical and chemical containment of individuals were performed according to the guidelines recommended by the American Society of Mammalogy (Sikes et al. 2016), under the scientific research collection license number SGPA/DGVS/12685/18 granted to Jorge Servin, issued by the Ministry of Environment and Natural Resources of México.

Radiotracking and Location Error. We gathered radiotelemetry data between September 2017 and August 2019 (Table 1). We located individual animals at any time of the day or night using portable receivers (Telonics® Mod. TR-2) with “H”-type handheld antennas and fixed eight-element antennas known as zero-point systems (Wildlife Materials Inc.®). Animals fitted with radio collars were field-tracked using the “triangulation” method (Mech 1983). This method consists of determining the location involving at least two directions (bearings or azimuths) using a compass from two different sites of known location separated from one another by at least one kilometer. A straight line was projected from each site to the bearings obtained so that the site where these lines crossed marked the location of the animal at that time. For the laboratory analysis of these measurements, we considered only those pairs of readings that were taken within 5 minutes and with a difference greater than 20° and less than 160°. To note, readings with differences less than 20° or greater than 160° produce triangles with very sharp vertices, which significantly increase location errors (White and Garrot 1990). Prior to the start of the monitoring period for radio-fitted animals, we estimated the location error using reference transmitters placed at known sites, yielding an error of ± 3° (White and Garrot 1990).

Home Range and Overlap. Using the location data recorded in the field, we constructed an Excel® database, which was loaded into the LOAS® program Location of a Signal, version 4.0.3.8 (ESS 2010a); this returned a cloud of points in space and a database containing the georeferences of the locations of each radio-collared individual. With this database, we used the program Biotas® version 2.0a 3.8 (ESS 2010b) to calculate the size of the home range of each radio-collared individual, using the minimum convex polygon method set at 95 % (MPC; Mech 1983; White and Garrot 1990), while 50 % of sites were used to determine the core zone (i. e., the area with a high priority of use; Powell 2000). We used the MPC for its simplicity (White and Garrot 1990) and to compare our results versus other studies addressing the species studied. To estimate the space shared between radio-collared animals, we measured the overlap of home ranges between pairs of individuals and then calculated the average of this overlap (Millspaugh and Marzluff 2001).

We compared the size of the home ranges between the two species through a Student’s t-test for independent samples; in the case of coyotes, we compared the size of the home ranges between sexes through a Student’s t-test for a single sample (Sokal and Rohlf 1987).

Habitat Use and Selection. We used a vegetation map of the RBM and its area of influence (1:50,000 scale) for the classification and assignment of habitat types according to the physiognomically dominant vegetation (sensuGonzález-Elizondo et al. 1993), which was digitized by the Laboratory of Wildlife Ecology and Conservation at Universidad Autónoma Metropolitana, campus Xochimilco. This map grouped habitat types into five categories (Figure 1): disturbed vegetation and agricultural areas (Sv); oak forest (QF), dominated by Quercus spp.; mixed forests (MF), with Pinus and Quercus as dominant or subordinate species; forests (pine, oak, or mixed) including patches of A. pungens shrubland (F-MS); and grasslands (G), areas where Bouteloua spp. occur as dominant or subordinate species.

The locations of the radio-collared individuals of both species were superimposed to the resulting map to quantify the frequency with which each individual was located in each habitat type within the RBM. We calculated the habitat selection coefficient by species, individual, and habitat type, as the ratio between observed habitat use and habitat availability (Manly et al. 2004). The observed habitat use was determined from the radio-location points recorded for each individual by habitat type. Habitat availability was derived by multiplying the number of radio-location points of each individual in a particular habitat type by the observed proportion of that habitat type within its home range obtained through the MPC (Aebischer et al. 1993; Sankar et al. 2013). This comparison is analog to Johnson’s third-order selection (Johnson 1980). For each species, we calculated the habitat selection coefficient for the j-th individual and the i-th habitat type using the equation: ŵ ij = u ij / (π i u +j ), where ŵ ij is the selection coefficient of individual j in habitat i; u ij is the number of radiolocation points of individual j in habitat i; π i is the relative availability of habitat i; and u +j is the total number of individual radio location points of individual j (Manly et al. 2004). We calculated a measure of the selection made by individuals of a given species as a group (taking into account the variation in the selection of habitats of each individual) with the following equation: ŵ i = u i+ / (π i u ++ ), where ŵ i is the selection coefficient for habitat i; u i+ is the total number of radiolocation points in habitat i; and u ++ is the total number of radiolocation points for all individuals (Manly et al. 2004). Under the assumption that individual j uses habitat type i randomly, the average value of the habitat selection coefficient is ŵ = 1 (use according to availability); thus, coefficients with values ŵ > 1 indicate a higher-than-expected use (i.e., preference), while ŵ values < 1 indicate lower-than-expected use (i. e., avoidance; Manly et al. 2004). To determine whether a value of habitat selection coefficient (ŵ i ) was significantly different from 1, we generated and used the 95 % Bonferroni confidence intervals (sensuManly et al. 2004). We used a G-test or two-step log-likelihood ratio to test the null hypothesis that habitat was used according to habitat availability (Sokal and Rohlf 1987). First, we performed the G-test for each individual; afterward, we added the values of the test statistics for all individuals of a given species to test the overall habitat selection of individuals (White and Garrot 1990; Manly et al. 2004).

We calculated the habitat selection coefficient with the adehabitatHS package (Calenge 2006) for R version 4.0.1 (R Core Team 2019). All statistical analyses were performed with this software, considering a significance level α = 0.05. For those parameters that require so, we report the mean ± standard deviation.

Table 1 Home range size (MPC 95 %) and locations (Loc.) of four coyotes and five gray foxes radio-collared in 2017-2019 in the buffer zone of La Michilía Biosphere Reserve (RBM), Durango, México. 

Species Sex Individual Follow-up   Loc. Home Range (km2) Core Zone (km2)
      Period Days      
Coyote F H001 Sep 2017-Aug 2018 261 111 9.74 1.98
Coyote M M027 Sep 2017-Oct 2018 382 130 12.45 2.22
Coyote M M087 Apr 2018-Jun 2019 103 96 13.81 3.65
Coyote M M156 Sep 2017-Aug 2018 184 92 12.81 4.05
Average (SD) 232.5 (118) 107.25 (17) 12.20 (1.74) 2.97 (1.03)
Gray fox F H050 Apr 2018-Dec 2018 232 102 4.99 0.54
Gray fox F H060 Feb 2019-Aug 2019 157 67 4.40 1.63
Gray fox F H067 Apr 2018-Jan 2018 266 77 5.71 0.41
Gray fox F H077 Apr 2018-Jun 2019 429 184 6.09 1.21
Gray fox F H081 Sep 2017-Jun 2018 274 86 5.64 1.27
Average (SD)       271.6 (99) 103.2 (47) 5.37 (0.67) 1.01 (0.52)

The sex of individuals is denoted by: F for females and M for males.

Results

Although we captured and tracked ten individuals - five gray foxes and five coyotes -, a local inhabitant delivered one radio collar that we had fitted to a female coyote captured four weeks earlier, reporting that the collared coyote was found dead by gunshot. Therefore, below we report the data corresponding to nine individuals.

Home Range and Overlap. Between September 2017 and August 2019, we recorded a total of 945 radio location points, 429 corresponding to four coyotes (= 107.25 ± 17) and 516 to five gray foxes (= 103.20 ± 47; Table 1).

The average home range for coyotes was 12.20 ± 1.74 km2 (n = 4; range 9.74-13.81 km2), with a mean core zone of 2.97 ± 1.03 km2 (n = 4; range 1.98-4.05 km2); the home range of male coyotes (13.02 ± 0.70 km2; n = 3) was significantly larger (t = 8.07; d. f. = 2; P = 0.01) than the home range of the only female monitored (9.74 km2). The mean home range size for gray foxes was 5.37 ± 0.67 km2 (n = 5; range 4.40-6.09 km2), with a mean core area of 1.01 ± 0.52 km2 (n= 5; range 0.41-1.63 km2). A t-test showed that the mean home range size of coyote was significantly larger versus gray fox (t = 8.18; d. f. = 7; P = 0.001).

The mean overlap of home ranges between coyotes (intraspecific overlap) was 43.7 ± 21 % (n = 12; range 18-77 %), whereas for gray foxes, the mean overlap was 6.6 ± 5 % (n = 8; range 1-14 %). The overlap of home ranges was significantly greater between coyotes than between gray foxes (t = 4.87; d. f. = 18; P = 0.001). The mean overlap of home ranges between coyotes and gray foxes (interspecific overlap) was 42.1 ± 27 % (n = 21; range 13-98 %; Figure 1).

Habitat Use and Selection. We found that coyotes use the different habitat types according to their availability, both as a group (G = 18.36; d. f. = 13, P = 0.14) and as individuals (P > 0.05; Table 2), although the highest habitat selection coefficient was obtained for grassland areas (G; ŵ i = 1.17) and the lowest for forests with manzanita shrubland (Arctostaphilos pungens; F-MS; ŵ i = 0.77; Table 2).

On the other hand, although individual variations were observed, gray foxes showed selective habitat use as a group (G = 113.93; d. f. = 14; P < 0.001; Table 2). The gray fox preferred mixed forests (MF; ŵ i = 1.43 ± 0.17) and avoided disturbed vegetation (Sv; ŵ i = 0.17 ± 0.0), grassland areas (G; ŵ i = 0.27 ± 0.07), and forests with manzanita schrubland (F-MS; ŵ i = 0.61 ± 0.11). Separately, selection coefficient values and their confidence intervals indicated that oak forest (QF; ŵ i = 0.96; CIB 0.17-1.74) was used according to its availability (Table 2).

Table 2 G-test and habitat selection coefficients, per individual (ŵ ij ) and per group (ŵ i ), of radio-collared individuals - four coyotes and five gray foxes - in the buffer zone of La Michilía Biosphere Reserve (RBM), Durango, México. 

Species Individual G-test     Selection coefficient per individual (ŵ ij )        
    G-Value d. f. P-value Sv QF MF F-MS G
Coyote H001 5.40 3 0.145 NA 0.86 1.97 1.02 0.83
Coyote M027 4.79 4 0.309 0.96 1.11 1.20 0.48 0.90
Coyote M087 3.56 3 0.314 NA 0.76 0.89 1.13 1.65
Coyote M156 4.62 3 0.202 NA 1.09 0.95 0.60 1.76
By group 18.36 13 0.144
ŵ i ± SD 0.96 ± 0.0 0.94 ± 0.08 1.12 ± 0.13 0.77 ± 0.15 1.17 ± 0.22
95% CI 0.96- 0.97 0.74-1.14 0.77-1.46 0.38-1.17 0.60-1.75
Gray fox H050 47.22 3 < 0.001 NA 0.59 4.53 0.51 0.99
Gray fox H060 7.64 3 0.054 NA 0.24 1.35 0.97 0.61
Gray fox H067 15.23 3 0.002 NA 1.87 1.14 1.23 0.19
Gray fox H077 37.92 3 < 0.001 0.17 1.36 1.41 NA 0.21
Gray fox H081 5.93 2 0.301 NA NA 1.18 0.47 0.20
By group 113.9 14 < 0.001
ŵ i ± SD 0.17 ± 0.0 0.82 ± 0.29 1.43 ± 0.17 0.61 ± 0.11 0.27 ± 0.07
  95% CI       0.16-0.17 0.19-1.57 1.01-1.86 0.33-0.89 0.10-0.44

Habitat types are denoted by: Sv, disturbed vegetation; QF, oak forest; MF, mixed forests; F-MS, forests (pine, oak or pine-oak) and manzanita shrubland; G, grassland areas.

The sex of individuals is denoted by F for females and M for males.

SD denotes standard deviation; d. f., degrees of freedom; 95% CI, Bonferroni 95% confidence intervals.

Discussion

In a previous work carried out in the study area, Servin (2000) radio-tracked fifteen coyotes (eight males and seven females) over two years, reporting a mean home range size of C = 11.8 ± 2.71 km2 for coyotes in general, CM = 13.1 ± 2.5 km2 for males, and CH = 9.9 ± 3.3 km2 for females. These values are similar to the ones obtained in the present study. The home range size of coyotes is a highly dynamic variable influenced by climate, prey availability, and habitats suitable for reproduction, as well as by population density and mortality rate (Danner and Smith 1980; Laundré and Keller 1984; Gese et al. 1988; Servín and Huxley 1995; Servín et al. 2014b). While the home range size of a species varies geographically (Holzman et al. 1992; Chamberlain et al. 2000), our results indicate that home range size in the study area lies within the range of values reported for coyotes in different habitats across its range (Bekoff 1977; Andelt and Gipson 1979; Young et al. 2006), consistent with most of the studies carried out in temperate zones of North America (11.6-35.8 km2; Servín and Huxley 1995; Servín 2000).

In the case of gray fox females, the mean home range size reported here was 5.37 ± 0.67 km2, an area 2.4 times larger than the one reported for females by Servin et al. (2014b), which was 2.24 km2, in the same study area between 1991-1993. In this regard, some studies have reported that gray fox females tend to display a larger home range than males (Trapp and Hallberg 1975; Servín et al. 2014b) and that the home range size of this species may vary depending on habitat quality and resource availability (Fuller and Cypher 2004). Our results fall within the range of variation reported elsewhere for this species (Fritzell and Haroldson 1982; Fuller and Cypher 2004; Macdonald and Sillero-Zubiri 2004).

In the study area, the average spatial overlap between the home ranges of coyotes and gray foxes was moderate (42.1 %). However, one-third of the interspecific pairs (diads) analyzed (n = 21) to derive this data showed high overlap values (> 60 %), as reported in other studies (Neale and Sacks 2001; Chamberlain and Leopold 2005). Our results suggested that, since there are no apparent patterns of spatial avoidance of the gray fox toward the coyote through spatial segregation of the ecological niche, the spatial dynamics between these species is not fully explained by interference competition, as reported for these canid species in other areas where they display a sympatric distribution (Fedriani et al. 2000; Farias et al. 2012).

Our results also suggest that the spatial coexistence dynamics between coyotes and gray foxes in the study area is governed by space-use mechanisms at a fine scale (Lonsinger et al. 2017) mediated by differential habitat use. The gray fox used oak forest (QF) according to its availability and showed preferences for mixed forests (MF), as already reported for this species in the study area (Servín et al. 2014b), as well as in other areas over its geographic range (Haroldson and Fritzell 1984; Chamberlain and Leopold 2000). These forests offer vast areas that provide protection and shelter for gray foxes (Servín et al. 2014b), being an important element within the home range of this species (Fritzell and Haroldson 1982). The complex architecture of mixed oak-pine and pine-oak forests in the study area provide natural structures that can be used as resting sites and shelters; at the same time, these forests serve as escape routes and, therefore, are useful to avoid the risk of predation, as gray foxes are able to climb trees and even jump between tree branches (Fritzell and Haroldson 1982; Fuller and Cypher 2004). In addition, foxes can use the tree stratum as a foraging zone, as its branches are habitats for potential prey that are part of their diet, such as passerine birds, squirrels (Sciurus nayaritensis, Tamias bulleri, and T. durangae), small rodents (Peromyscus spp. and Reithrodontomys spp.), lacertids (Sceloporus spp.). and insects. On the other hand, gray foxes avoided disturbed vegetation (Sv) and grassland areas (G). It has been shown that the risk of predation by coyotes can influence resource use by gray foxes (Fedriani et al. 2000; Chamberlain and Leopold 2005). Thus, foxes are likely to be avoiding these open areas as these are devoid of shelters, hence offering lower evasion opportunities against the potential chase by coyotes (which use these habitats according to their availability) to avoid intraguild predation (Temple et al. 2010).

In the case of coyotes, although no apparent preference for or avoidance of any particular habitat type was observed, a certain trend towards the preferential use of pasture areas (G) was noted since it attained the highest habitat selection coefficient (ŵ i = 1.17). This trend of preferential use is consistent with data reported for coyotes in the RBM, as this species forage and catch their main prey (rodents and lagomorphs) preferentially in areas with open vegetation, such as grasslands (P; Servin and Huxley 1991; Servin et al. 2003). These open vegetation areas in the RBM are also home to the checker bark juniper or táscate (Juniperus deppeana) with varying abundances in different areas (González-Elizondo et al. 1993). Juniper fruits are an important element in the diet of coyotes, being the plant food most frequently consumed by coyotes in the study area (Delibes et al. 1989; Servin and Huxley 1991); this food category is actively sought and consumed by coyotes in open and grassland areas.

An aspect worth highlighting is the role of forests with manzanita shrubland (F-MS) in habitat selection and use by both species. On the one hand, coyotes used this habitat as expected, while gray foxes avoided it. One potential explanation lies in the different frequency of consumption of manzanita fruit by both species. These fruits represent a food resource highly consumed by coyotes, especially in the dry season (February-May; Servin and Huxley 1991), while it is consumed to a lesser extent by gray foxes (Delibes et al. 1989).

In the present study, we showed that the home ranges of coyotes and female gray foxes showed a moderate interspecific overlap, so no spatial segregation occurred. However, differential use of habitat was observed, which explains the coexistence of these canids in the same area because their antagonistic behavioral interactions decrease through a trend towards the differential use of resources (MacArthur and Levins 1967; Tilman 1982; Holt 2001). Our results are consistent with the theoretical hypothesis on intraguild predation (Holt and Polis 1997; Polis et al. 1989), which suggests that the coexistence between species in the same guild sharing basic resources requires that the subordinated species (gray fox) be better at exploiting the resources shared with the dominant species (coyote).

Acknowledgments

To the authorities of Ejido San Juan de Michis and Anexo La Peña, Durango, México. To M. Villa and P. Villa, for the permits granted to carry out the work. To INECOL A. C. and CONANP, for providing us with the facilities of the Biological Station “Piedra Herrada”, and to J. Medina, for the constant support provided. To E. Chacón, for logistical support, and to D. Carreón, for participating in the project. The UAM-X Wildlife Ecology and Conservation Laboratory provided equipment and funding. VISILMEX A. C. and the UAEM Biodiversity and Conservation Research Center provided support with equipment, infrastructure, inputs, and off-road vehicles. This article resulted from the thesis work of the first author (CRRL) to obtain the Ph. D. degree that is part of the Doctorate Program in Biological and Health Sciences of Universidad Autónoma Metropolitana. Thanks also to CONACyT for the postgraduate scholarship # 293353. This research study was conducted under the scientific research collection license number SGPA/DGVS/12685/18 granted to Jorge Servin, issued by the Ministry of Environment and Natural Resources of México. Anonymous reviewers and the Associate Editor contributed to improving the present work. María Elena Sánchez-Salazar translated the manuscript into English.

Literature cited

Aebischer, N. J., P. A. Robertson, and R. E. Kenward. 1993. Compositional analysis of habitat use from animal radio tracking data. Ecology 74:1313-1325. [ Links ]

Andelt, W. F., and P. S. Gipson. 1979. Home range, activity, and daily movements of coyotes. The Journal of Wildlife Management 43:944-951. [ Links ]

Andrade-Ponce, G. P., S. Gallina, B. Gómez-Valencia, and A. Lira-Noriega. 2020. Coexistencia de Vulpes macrotis y Canis latrans (Carnivora: Canidae) en la Reserva de la Biosfera de Mapimí, México. Revista Mexicana de Biodiversidad 91:1-17. [ Links ]

Bekoff, M. 1977. Canis latrans. Mammalian species 79:1-9. [ Links ]

Berger, K. M., and E. M. Gese. 2007. Does interference competition with wolves limit the distribution and abundance of coyotes? Journal of Animal Ecology 76:1075-1085. [ Links ]

Bu, H., F. Wang, W. J. McShea, Z. Lu, D. Wang, and S. Li. 2016. Spatial co-occurrence and activity patterns of mesocarnivores in the temperate forests of Southwest China. PLoS ONE 11:e0164271. [ Links ]

Calenge, C. 2006. The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecological Modelling 197:516-519. [ Links ]

Caro, T. M., and C. J. Stoner. 2003. The potential for interspecific competition among African carnivores. Biological Conservation 110:67-75. [ Links ]

Case, T. J., and M. E. Gilpin. 1974. Interference competition and niche theory. Proceedings of the National Academy of Sciences 71:3073-3077. [ Links ]

Chamberlain, M. J., and B. D. Leopold. 2000. Spatial use patterns, seasonal habitat selection, and interactions among adult gray foxes in Mississippi. The Journal of Wildlife Management 64:742-751. [ Links ]

Chamberlain, M. J. , and B. D. Leopold . 2005. Overlap in space use among bobcats (Lynx rufus), coyotes (Canis latrans) and gray foxes (Urocyon cinereoargenteus). The American Midland Naturalist 153:171-179. [ Links ]

Chamberlain, M. J. , C. D. Lovell, and B. D. Leopold. 2000. Spatial-use patterns, movements, and interactions among adult coyotes in central Mississippi. Canadian Journal of Zoology 78:2087-2095. [ Links ]

Chiang, P. J., K. J. C. Pei, M. R. Vaughan, and C. F. Li. 2012. Niche relationships of carnivores in a subtropical primary forest in southern Taiwan. Zoological Studies 51:500-511. [ Links ]

Cuervo-Robayo, A. P., C. Ureta, M. A. Gómez-Albores, A. K. Meneses-Mosquera, O. Téllez-Valdés, and E. Martínez-Meyer. 2020. One hundred years of climate change in Mexico. PLoS ONE 15:e0209808. [ Links ]

Danner, D. A., and N. S. Smith. 1980. Coyote home range, movement, and relative abundance near a cattle feedyard. The Journal of Wildlife Management 44:484-487. [ Links ]

Delibes, M., L. Hernández, and F. Hiraldo. 1989. Comparative food habits of three carnivores in western Sierra Madre, Mexico. Zeitschrift für Säugetierkunde 54:107-110. [ Links ]

Donadio, E., and S. W. Buskirk. 2006. Diet, morphology, and interspecific killing in Carnivora. The American Naturalist 167:524-536. [ Links ]

ESS. 2010a. LOAS: Location of a signal. Ver. 4.0.3.8. Ecological Software Solutions. Santa Barbara, U.S.A. [ Links ]

ESS. 2010b. Biotas. Ver. 2.0a 3.8. Ecological Software Solutions. Santa Barbara, U.S.A. [ Links ]

Farías, V., T. K. Fuller, and R. M. Sauvajot. 2012. Activity and distribution of gray foxes (Urocyon cinereoargenteus) in southern California. The Southwestern Naturalist 57:176-181. [ Links ]

Fedriani, J. M., T. K. Fuller, R. M. Sauvajot, and E. C. York. 2000. Competition and intraguild predation among three sympatric carnivores. Oecologia 125:258-270. [ Links ]

Fritzell, E. K., and K. J. Haroldson. 1982. Urocyon cinereoargenteus. Mammalian Species 189:1-8. [ Links ]

Fuller, T. K., and B. L. Cypher. 2004. Gray fox (Urocyon cinereoargenteus). Pp. 92-96, in Canids: foxes, wolves, jackals, and dogs. Status survey and conservation action plan (Sillero-Zubiri, C., M. Hoffman, and D. W. Macdonald, eds.). IUCN/SSC Canid Specialist Group. Gland, Switzerland. [ Links ]

Gadsden, H., and P. Reyes-Castillo. 1991. Caracteres del ambiente físico y biológico de la Reserva de la Biosfera “La Michilía”, Durango, México. Folia Entomológica Mexicana 81:1-19. [ Links ]

García, E. 2004. Modificaciones al sistema de clasificación climática de Köppen (para adaptarlo a las condiciones particulares de la República Mexicana), 5a ed. Publicación del Instituto de Geografía-Universidad Nacional Autónoma de México. Ciudad de México, México. [ Links ]

Gese, E. M., O. J. Rongstad, and W. R. Mytton. 1988. Home range and habitat use of coyotes in southeastern Colorado. The Journal of Wildlife Management 52:640-646. [ Links ]

Gese, E. M. , T. E. Stotts, and S. Grothe. 1996. Interactions between coyotes and red foxes in Yellowstone National Park, Wyoming. Journal of Mammalogy 77:377-382. [ Links ]

Gompper, M. E., D. B. Lesmeister, J. C. Ray, J. R. Malcolm, and R. Kays. 2016. Differential habitat use or intraguild interactions: what structures a carnivore community? PLoS ONE 11:e0146055. [ Links ]

González-Elizondo, S., M. González-Elizondo, and A. Cortés-Ortiz. 1993. Vegetación de la Reserva de la Biosfera La Michilía, Durango, México. Acta Botánica Mexicana 22:1-104. [ Links ]

Gosselink, T. E., T. R. Van Deelen, R. E. Warner, and M. G. Joselyn. 2003. Temporal habitat partitioning and spatial use of coyotes and red foxes in east-central Illinois. The Journal of Wildlife Management 67:90-103. [ Links ]

Grassel, S. M., J. L. Rachlow, and C. J. Williams. 2015. Spatial interactions between sympatric carnivores: asymmetric avoidance of an intraguild predator. Ecology and Evolution 5:2762-2773. [ Links ]

Halffter, G. 1978. Las Reservas de la Biosfera en el estado de Durango: una nueva política de conservación y estudio de los recursos bióticos. Pp. 17-43, in Reservas de la biosfera en el estado de Durango (Halffter, G., ed.). Instituto de Ecología A. C. Veracruz, México. [ Links ]

Hampton, S. E. 2004. Habitat overlap of enemies: temporal patterns and the role of spatial complexity. Oecologia 138:475-484. [ Links ]

Haroldson, K. J., and E. K. Fritzell. 1984. Home ranges, activity, and habitat use by gray foxes in an oak-hickory forest. The Journal of Wildlife Management 48:222-227. [ Links ]

Harrison, D. J., J. A. Bissonette, and J. A. Sherburne. 1989. Spatial relationships between coyotes and red foxes in Eastern Maine. The Journal of Wildlife Management 53:181-185. [ Links ]

Holt, R. D., and G. A. Polis. 1997. A theoretical framework for intraguild predation. The American Naturalist 149:745-764. [ Links ]

Holt, R. D. 2001. Species coexistence. Encyclopedia of biodiversity 5:413-426. [ Links ]

Holzman, S., M. J. Conroy, and J. Pickering. 1992. Home range, movements, and habitat use of coyotes in southcentral Georgia. The Journal of Wildlife Management 56:139-146. [ Links ]

Hunter, J., and T. Caro. 2008. Interspecific competition and predation in American carnivore families. Ethology Ecology and Evolution 20:295-324. [ Links ]

Instituto Nacional de Estadística y Geografía (INEGI). 2017. Anuario estadístico y geográfico de Durango 2017. Instituto Nacional de Estadística y Geografía. Aguascalientes, México. [ Links ]

Johnson, D. H. 1980. The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65-71. [ Links ]

Kitchen, A. M., E.M. Gese, and E. R. Schauster. 1999. Resource partitioning between coyotes and swift foxes: space, time, and diet. Canadian Journal of Zoology 77:1645-1656. [ Links ]

Kozlowski, A. J., E. M. Gese, and W. M. Arjo. 2008. Niche overlap and resource partitioning between sympatric kit foxes and coyotes in the Great Basin Desert of Western Utah. The American Midland Naturalist 160:191-208. [ Links ]

Kozlowski, A. J. , E. M. Gese, and W. M. Arjo . 2012. Effects of intraguild predation: evaluating resource competition between two canid species with apparent niche separation. International Journal of Ecology 2012:1-12. [ Links ]

Kreeger, T., and J. Arnemo. 2018. Handbook of wildlife chemical immobilization. 5th ed. Published by authors. Laramie, U.S.A. [ Links ]

Laundré, J. W., and B. L. Keller. 1984. Home-range size of coyotes: a critical review. The Journal of Wildlife Management 48:127-139. [ Links ]

Linnell, J. D., and O. Strand. 2000. Interference interactions, coexistence and conservation of mammalian carnivores. Diversity and Distributions 6:169-176. [ Links ]

Lonsinger, R. C., E. M. Gese, L. L. Bailey, and L. P. Waits. 2017. The roles of habitat and intraguild predation by coyotes on the spatial dynamics of kit foxes. Ecosphere 8:e01749. [ Links ]

Löwenberg-Neto, P. 2014. Neotropical region: a shapefile of Morrone’s (2014) biogeographical regionalisation. Zootaxa 3802:300-300. [ Links ]

MacArthur, R., and R. Levins. 1967. The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist 101:377-385. [ Links ]

Macdonald, D. W., and C. Sillero-Zubiri. 2004. Dramatis personae. Wild canids-an introduction and dramatis personae. Pp. 27-28, in Biology and conservation of wild canids (Macdonald, D. W. , and C. Sillero-Zubiri, eds.). Oxford University Press. New York, U.S.A. [ Links ]

Manly, B. F. J., L. L. McDonald, D. L. Thomas, T. L. McDonald, and W. P. Erickson. 2004. Resource selection by animals: statistical design and analysis for field studies. 2nd ed. Kluwer Academic Publishers. London, England. [ Links ]

Mech, L. D. 1983. Handbook of animal radio-tracking. University of Minnesota Press. Minneapolis, U.S.A. [ Links ]

Melville, H. I. A. S., W. C. Conway, M. L. Morrison, C. E. Comer, and J. B. Hardin. 2015. Home-range interactions of three sympatric mesopredators in east Texas. Canadian Journal of Zoology 93:547-557. [ Links ]

Millspaugh, J. J., and J. M. Marzluff. 2001. Radio tracking and animal populations. Academic Press. San Diego, U.S.A. [ Links ]

Moehrenschlager, A., and M. A. Sovada. 2004. Swift fox (Vulpes velox). Pp. 109-116, in Canids: foxes, wolves, jackals, and dogs. Status survey and conservation action plan (Sillero-Zubiri, C. , M. Hoffman, and D. W. Macdonald, eds.). IUCN/SSC Canid Specialist Group. Gland, Switzerland. [ Links ]

Moehrenschlager, A. , R. List, and D. W. Macdonald. 2007. Escaping intraguild predation: Mexican kit foxes survive while coyotes and golden eagles kill Canadian swift foxes. Journal of Mammalogy 88:1029-1039. [ Links ]

Morin, P. 1999. Community Ecology. Blackwell Science. Malden, U.S.A. [ Links ]

Morrone, J. J. 2014. Biogeographical regionalisation of the Neotropical region. Zootaxa 3782:1-110. [ Links ]

Mueller, M. A., D. Drake, and M. L. Allen. 2018. Coexistence of coyotes (Canis latrans) and red foxes (Vulpes vulpes) in an urban landscape. PLoS ONE 13:e0190971. [ Links ]

Neale, J. C. C., and B. N. Sacks. 2001. Food habits and space use of gray foxes in relation to sympatric coyotes and bobcats. Canadian Journal of Zoology 79:1794-1800. [ Links ]

Nelson, J. L., B. L. Cypher, C. D. Bjurlin, and S. Creel. 2007. Effects of habitat on competition between kit foxes and coyotes. The Journal of Wildlife Management 71:1467-1475. [ Links ]

Palomares, F., and T. M. Caro. 1999. Interspecific killing among mammalian carnivores. The American Naturalist 153:492-508. [ Links ]

Palomares, F. , N. Fernández, S. Roques, C. Chávez, L. Silveira, C. Keller, and B. Adrados. 2016. Fine-scale habitat segregation between two ecologically similar top predators. Plos One 11:e0155626. [ Links ]

Pianka, E. R. 1969. Sympatry of desert lizards (Ctenotus) in Western Australia. Ecology 50:1012-1030. [ Links ]

Pianka, E. R. 1973. The structure of lizard communities. Annual Review of Ecology and Systematics 4:53-74. [ Links ]

Polis, G. A., C. A. Myers, and R. D. Holt. 1989. The ecology and evolution of intraguild predation: potential competitors that eat each other. Annual Review of Ecology and Systematics 20:297-330. [ Links ]

Powell, R. A. 2000. Animal home ranges and territories and home range estimators. Pp. 65-110, in Research techniques in animal ecology-controversies and consequences (Boitani, L., and T. K. Fuller, eds.). Columbia University Press. New York, U.S.A. [ Links ]

R Core Team. 2019. R: A language and environment for statistical computing v4.0.1. R Foundation for Statistical Computing. Vienna, Austria. [ Links ]

Rosenheim, J. A. 2004. Top predators constrain the habitat selection games played by intermediate predators and their prey. Israel Journal of Zoology 50:129-138. [ Links ]

Sankar, K., H. A. Pabla, C. K. Patil, P. Nigam, Q. Qureshi, B. Navaneethan, M. Manjreaker, P. S. Virkar, and K. Mondal. 2013. Home range, habitat use and food habits of re-introduced gaur (Bos gaurus gaurus) in Bandhavgarh Tiger Reserve, Central India. Tropical Conservation Science 6:50-69. [ Links ]

Sargeant, A. B., S. H. Allen and J. O. Hastings. 1987. Spatial relations between sympatric coyotes and red foxes in North Dakota. The Journal of Wildlife Management 51:285-293. [ Links ]

Sargeant, A. B. , and S. H. Allen. 1989. Observed interactions between coyotes and red foxes. Journal of Mammalogy 70:631-633. [ Links ]

Schoener, T. W. 1974. Resource partitioning in ecological communities. Science 185:27-39. [ Links ]

Servín, J. 2000. Ecología conductual del coyote en el sureste de Durango. Tesis de Doctorado. Universidad Nacional Autónoma de México. [ Links ]

Servín, J., and C. Huxley. 1991. La dieta del coyote en un bosque de encino-pino de la Sierra Madre Occidental de Durango, México. Acta Zoológica Mexicana 44:1-26. [ Links ]

Servín, J. , and C. Huxley. 1992. Immobilization of wild carnivores using the ketamine and xylazine mixture. Veterinaria México 23:195-139. [ Links ]

Servín, J. , and C. Huxley. 1995. Coyote home range size in Durango, Mexico. Zeitschrift für Säugetierkunde 60:119-120. [ Links ]

Servín, J. , and E. Chacón . 2014. Gray fox. Pp. 514-515, in Mammals of México (Ceballos, G., ed.). Johns Hopkins University Press. Baltimore, U.S.A. [ Links ]

Servín, J. , E. Chacón, and R. List . 2014a. Coyote. Pp. 510-511, in Mammals of México (Ceballos, G., ed.). Johns Hopkins University Press. Baltimore, U.S.A. [ Links ]

Servín, J. , A. Bejarano, N. Alonso-Pérez, and E. Chacón. 2014b. El tamaño del ámbito hogareño y el uso de hábitat de la zorra gris (Urocyon cinereoargenteus) en un bosque templado de Durango, México. Therya 5:257-269. [ Links ]

Servín, J. , V. Sánchez-Cordero, and S. Gallina. 2003. Daily travel distances of coyotes (Canis latrans) in a temperate forest of Durango, Mexico. Journal of Mammalogy 84:547-552. [ Links ]

Sikes, R. S. 2016. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97:663-688. [ Links ]

Sokal, R. R., and F. J. Rohlf. 1987. Introduction to Biostatistics. Second edition. W. H. Freeman and Co. San Francisco, U.S.A. [ Links ]

Soto, C., and F. Palomares. 2015. Coexistence of sympatric carnivores in relatively homogeneous Mediterranean landscapes: functional importance of habitat segregation at the fine-scale level. Oecologia 179:223-235. [ Links ]

Temple, D. L., M. J. Chamberlain, and L. M. Conner. 2010. Spatial ecology, survival and cause-specific mortality of gray foxes (Urocyon cinereoargenteus) in a longleaf pine ecosystem. The American Midland Naturalist 163:413-422. [ Links ]

Theberge, J. B., and C. H. R. Wedeles. 1989. Prey selection and habitat partitioning in sympatric coyote and red fox populations, southwest Yukon. Canadian Journal of Zoology 67:1285-1290. [ Links ]

Tilman, D. 1982. Resource competition and community structure. Princeton University Press. Princeton, U.S.A. [ Links ]

Trapp, G. R., and D. L. Hallberg. 1975. Ecology of the gray fox (Urocyon cinereoargenteus): a review. Pp. 164-178, in The wild canids (Fox, M. W., ed.). Van Nostrand Reinhold. New York, U.S.A. [ Links ]

Viota, M., A. Rodríguez, J. V. López-Bao, and F. Palomares . 2012. Shift in microhabitat use as a mechanism allowing the coexistence of victim and killer carnivore predators. Open Journal of Ecology 2:115-120. [ Links ]

Voigt, D. R., and B. D. Earle. 1983. Avoidance of coyotes by red fox families. The Journal of Wildlife Management 47:852-857. [ Links ]

White, P. J., K. Ralls, and R. A. Garrott. 1994. Coyote-kit fox interactions as revealed by telemetry. Canadian Journal of Zoology 72:1831-1836. [ Links ]

White, P. J. , K. Ralls, and C. A. V. White. 1995. Overlap in habitat and food use between coyotes and San Joaquin kit foxes. The Southwestern Naturalist 40:342-349. [ Links ]

White, G. C., and R. A. Garrott. 1990. Analysis of wildlife radio-tracking data. Academic Press. New York, U.S.A. [ Links ]

Xia, J., F. Wu, W. Z. Hu, J. L. Fang, and X. J. Yang. 2015. The coexistence of seven sympatric fulvettas in Ailao Mountains, Ejia Town, Yunnan Province. Zoological Research 36:18-28. [ Links ]

Young, J. K., W. F. Andelt, P. A. Terletzky, and J. A. Shivik. 2006. A comparison of coyote ecology after 25 years: 1978 versus 2003. Canadian Journal of Zoology 84:573-582. [ Links ]

0Associated editor: Jesús Fernández

Received: February 16, 2021; Revised: May 10, 2021; Accepted: July 10, 2021

*Corresponding author: jservin@correo.xoc.uam.mx

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License