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Use of prey by sympatric bobcat (Lynx rufus) and coyote (Canis latrans) in the Izta-Popo National Park, Mexico.

Similar-sized carnivores often differ in use of available prey to facilitate coexistence (Witmer and DeCalesta, 1986; Major and Sherburne, 1987; Litvaitis and Harrison, 1989; White et al., 1995; Kitchen et al., 1999; Neale and Sacks, 2001a; Azevedo et al., 2006). Dietary studies are, thus, important for determining trophic relations among predators and prey (Chuang and Lee, 1997). Intraspecific competition can influence structure of the community (Schoener, 1974, 1982), especially between predators that are at the top of the food chain (Hairston et al., 1960; Oksanen et al., 1981). The coyote (Canis latrans) is a generalist carnivore distributed throughout Mexico and has a broad diet composed of insects, vertebrates, fruits, and vegetation (Andelt et al., 1987; Gese et al., 1988; Neale et al., 1998). In contrast, the bobcat (Lynxs rufus) is a strict carnivore that preys mainly on rodents and lagomorphs (Aranda et al., 2002) and occasionally livestock (Fritts and Sealander, 1978; Neale et al., 1998). Bobcats and coyotes are sympatric throughout most of their ranges, and, although competition may occur between the species, it has been difficult to evaluate and likely varies among areas and with availability of prey (Palomares and Caro, 1999). High densities of coyotes have been associated with low densities of bobcats (Henke and Bryant, 1999; Neale and Sacks, 2001b), which could indicate competition.

Bobcats and coyotes are sympatric in Izta-Popo National Park, which is located in the Trans-Mexican Volcanic Belt (Sierra Nevada), central Mexico. Prey for these carnivores in this national park includes the volcano rabbit (Romerolagus diazi; Cervantes and Gonzalez, 1996) and several other species of lagomorphs as well as rodents and birds (Bojorges, 2004; Granados et al., 2004). Because coyotes and bobcats are sympatric in Izta-Popo National Park, our goal was to determine prey used by each species to assess whether partitioning of the diet was a potential ecological factor facilitating coexistence. Additionally, we wanted to determine whether either species preferentially preyed on the endangered volcano rabbit and, thus, potentially contributed to the precarious status of this species.

MATERIALS AND METHODS--Our study area was located in IztaPopo National Park and Zoquiapan, Mexico (18[degrees]54'39"-19[degrees]33'00"N, 98o31,11"-98[degrees]48,10"W) which encompasses ca. 45,097 ha. The study area included the volcanoes Iztaccihuatl and Popocatepetl, which are the second and third highest elevations in Mexico at 5,280 and 5,482 m, respectively (Arriaga et al., 2000a). Climate was temperate, and the main vegetative communities were oak (Quercus) and pine (Pinus) forests. Pine forest was present at 2,500-4,000 m, and dominant species included P. hartwegii, P montezumae, P pseudostrobus, P rudis, P. leiophylla, and P teocote (Table 1; Arriaga et al., 2000a, 2000b; Hernandez and Granados, 2006).

Potential prey in the study area included white-tailed deer (Odocoileus virginianus mexicanus), common opossum (Didelphis marsupialis), nine-banded armadillo (Dasypus novemcinctus), Mexican cottontail (Sylvilagus cunicularius), eastern cottontail (S. floridanus), and volcano rabbit (R. diazi; Chapman et al., 1980; Cervantes et al., 2005). Additionally, 13 species of rodents, including Peromyscus melanotis (Castro et al., 2005b), P aztecus (Ramirez et al., 2005a), P. difficillis (Chavez and Ceballos, 2005), P maniculatus (Ramirez et al., 2005d), Reithrodontomys chrysopsis (Lira and Gaona, 2005), R. sumichrasti (Ramirez et al., 2005c), R megalotis (Sanchez and Oliva, 2005), Neotomodon alstoni (Chavez, 2005), Neotoma mexicana (Zarza and Ceballos, 2005), Liomys irroratus (Espinosa and Chavez, 2005), Dipodomys phillipsi (Oliva, 2005), Sigmodon leucotis (Ramirez et al., 2005b), and Pappogeomys merriami (Villa and Valencia, 1991), were present. Four species of insectivores also occurred on the site, including Sorex vagrans orizabae (Velazquez et al., 2001), S. saussurei (Castro, 2005), S. oreopolus ventralis (Castro, 2005a), and Cryptotis alticola (Ceballos and Carreon, 2005). Multiple species of birds, primarily Buteo jamaicensis, B. lineatus, Falco peregrinus, Cypseloides niger, Hirundo rustica, and Corvus corax, were present, including potential prey such as Dendrortyx macroura, Grallaria guatimelensis, Columbina inca, and Zenaida macroura. Some of these species were endemic to the study area (Chavez and Trigo, 1996; Chavez, 1999; Bojorges, 2004).

Other carnivores present included Urocyon cinereoargenteus nigrirostris, Bassariscus astatus astatus, Procyon lotor hernandezii, and Nasua nasua molaris (Ramirez et al., 1982; Ramirez and Mudespacher, 1987; Chavez and Trigo, 1996; Granados et al., 2004; Trites and Roy, 2005). Endemic species recorded in the study area included Romerolagus diazi, Pappogeomys merriami, Neotomodon alstoni, Reithrodontomys chrysopsis, Thomomys umbrinus volcanius, T. gambrinus peregrinus, Sorex vagrans orizabae, and Peromyscus aztecas hylocetes (Ceballos and Galindo, 1984; Chavez and Trigo, 1996; Velazquez and Romero, 1999; Velazquez et al., 2001).

We collected scats monthly during the dry (December 2004-May 2005) and wet seasons (June-November 2005). We randomly placed seven transects of different lengths in three areas of the National Park (Tlamacas, Zoquiapan, and Altzomoni). Transects were placed on semi-abandoned trails and roads that had sign of wildlife (lagomorphs, rodents, and birds). In Tlamacas (Puebla and Mexico states), we placed three transects each 4,900 m long at an elevation of 4,122 m. In Zoquiapan in the state of Puebla, we placed three transects each 1,900 m long at an elevation of 3,752 m. One transect was placed in Altzomoni, an area located between the states of Mexico and Puebla at an elevation between 3,712 and 3,983 m, and was 7,400 m in length (Table 1).

We identified scats of bobcats and coyotes by associated tracks and other sign and odor, color, and shape of scat (Aranda, 2000). We placed scats in plastic or paper bags labeled with the name of the transect, location, date, and species.

Scats were analyzed at the Animal Nutrition Laboratory of the Universidad Autonoma Metropolitana, Mexico Distrito Federal, Mexico. We washed scats through sieves of different sizes (5, 10, and 20 [mm.sup.2]) and separated skin, hair, and bones, removing traces of vegetation. We identified remains using reference guides for hairs, bones, and skulls (Glass, 1981; Monroy and Rubio, 2003). We identified larger prey (i.e., lagomorphs and larger) to species and smaller prey (e.g., rodents, insectivores, and birds) to class. We calculated frequency of occurrence and biomass of each item in scats (Ackerman et al., 1984) and used the model of Corbett (1989) to estimate biomass consumed by coyotes and the model of Ackerman et al. (1984) to estimate biomass consumed by bobcats.

We compared frequency of prey in scats using Fisher's exact test (Zar, 1996) and partitioned experiment-wise error rate by the number of comparisons to determine significant differences by species or class of prey in diets. We also used Fisher's exact test to compare the frequency of the volcano rabbit in diets to that of all other species of prey in scats. We estimated overlap of diet between coyotes and bobcats using Pianka's index (Pianka, 1973): 0 = [SIGMA] [p.sub.i] [q.sub.i]/[([SIGMA][p.sup.2.sub.i] [SIGMA] [q.sup.2.sub.i]).sup.1/2], where [p.sub.i] and [q.sub.i] represent proportions of prey in the diet of both species, respectively. Pianka's index varies between 0 (no overlap) and 1 (total overlap).

Quality of habitat was ranked for prey at each site according to the density of grasses per square meter and human activity based on a visual estimate. Density of grasses was measured with five quadrants of 5 [m.sup.2] in each site (Martinez et al., 2012). We defined human activity by the presence of traces of humans (trash, footprints, and feces). We classified habitat as excellent when density was >2 grasses/[m.sup.2] without human activity, good when 2 grasses/[m.sup.2] with human activity, fair when <2 grasses/[m.sup.2] without human activity, and poor when <2 grasses/[m.sup.2] with human activity.

Results--We collected 126 scats of bobcats and 70 scats of coyotes. Frequency of prey differed in diets of bobcats and coyotes (Fisher's exact P = 0.012); scats of bobcats contained fewer (8.6%) unidentified remains of prey than did scats of coyotes (22.2%; P = 0.003). Although only marginally different (P = 0.056), frequency of volcano rabbits was greater in scats of bobcats than in those of coyotes (15.5 versus 6.7%). Frequency of all other parts of prey was similar (experiment-wise P > 0.05). Use of prey by bobcats and coyotes showed an index of overlap of 0.94.

By class of prey, bobcats preyed primarily on lagomorphs (59%), with approximately similar use of eastern cottontails, Mexican cottontails, and volcano rabbits. Similarly, lagomorphs (62%), primarily eastern cottontails (44%; Table 2), were most frequent in diets of coyotes.

Altzomoni had the highest density of grasses (2.6 [+ or -] 2.8) and low human-activity. The site at El Papayo had the lowest density of grasses (1.4 [+ or -] 0.0) and high human-activity.

DISCUSSION--Overall, use of prey by bobcats and coyotes was extremely similar. The dietary overlap (0.94) was much greater than that in previous studies (Fedriani et al., 1999, 2000), although this result was confounded by inclusion of vegetative matter in dietary analyses of coyotes in other studies. The primary difference in use of prey between bobcats and coyotes was the presence of birds in the diet of bobcats (Table 2). Birds were absent in scats of coyotes, although low frequency of occurrence precluded statistical differences.

Dietary overlap between bobcats and coyotes was only 0.49 in central Florida (Thornton et al., 2004). Compared to our results, this was due to greater use of larger species by coyotes. Coyotes consumed a wide variety of larger prey including white-tailed deer (Odocoileus viginianus), feral pigs (Sus scrofa), and cattle (Bos taurus). In contrast, bobcats used only one of these species of large prey, white-tailed deer (Thornton et al., 2004). Similarly, diets of bobcats and coyotes in California also showed less overlap (0.69; Fedriani et al., 1999, 2000) than we observed, with diets of coyotes differing mainly by greater use of plants as food. Other studies have similarly shown varying degrees of dietary overlap between bobcats and coyotes (Huegel and Rongstad, 1986; Major and Sherburne, 1987; Kitchen et al., 1999). Most of these studies differed from ours in that they included plants as food in their analyses of the diet of coyotes. The coyote, an omnivore, would be expected to have a greater intake of fruits and other vegetation than would bobcats, an obligate carnivore.

Lagomorphs were the most common prey in the diets of bobcats and coyotes in our study, probably because they were the most available and profitable prey present in the study area (Griffiths, 1975). The average mass for the Mexican cottontail (2.0 kg) and the eastern cottontail (1.2 kg) combined offered comparable energetic handling costs for coyotes and bobcats and likely resulted in both predators obtaining more net energetic gains from these larger lagomorphs than from volcano rabbits (0.5 kg) or the similarly-sized pocket gopher (0.7 kg; Cervantes et al., 1990; Villa and Valencia, 1991). Energetic gains suggest that volcano rabbits and pocket gophers were less used as prey due to their smaller size and lower energetic value for the predator. However, bobcats consumed marginally more volcano rabbits than did coyotes (15.5 versus 6.7%; P = 0.056). Because the volcano rabbit is listed as threatened in CITES Appendix I (United Nations Environment Programme, 2012) and endangered in Mexico (Secretaria de Medio Ambiente y Recursos Naturales, 2010), intensive management of bobcats is one tool managers might consider to aid recovery of the volcano rabbit.

In terms of classes of prey used, our results were comparable with other studies in North America (Delibes and Hiraldo, 1987), e.g., lagomorphs were the most common item in diets of bobcats (59% by frequency). Studies in Mexico had similar results; in northwestern Mexico, diets of bobcats consisted of 68% lagomorphs (36% S. auduboni, 32% Lepus), and, in the Ajusco Mountain Range, their diets consisted of 69% lagomorphs (42% eastern cottontail, 15% Mexican cottontail, 12% volcano rabbit; Aranda et al., 2002). In contrast, diets of coyotes were more diverse, especially given the inclusion of plants as food. For example, along the Pacific Coast of Mexico, coyotes consumed mainly rodents and insects during the dry season and included fruits (mainly papaya and mango) during the wet season (Huegel and Rongstad, 1986; Andelt et al., 1987; Hidalgo-Mihart et al., 2001; Guerrero et al., 2004). Use of prey by coyotes in our study was similar to that in studies conducted in the Sierra del Ajusco, Mexico, where diets were comprised of 30% lagomorphs, 24% rodents, and 22% livestock (Aranda et al., 1995). The low use of lagomorphs when compared to our results was likely a consequence of higher availability of larger prey, i.e., livestock (primarily domestic sheep), in the Sierra del Ajusco. In areas where larger prey are common, they increase in the diet of coyotes. For example, white-tailed deer were the most common food of coyotes in Michigan, followed by lagomorphs (Ozoga and Harger, 1966).

In conclusion, use of prey by bobcats and coyotes was similar, and both species preyed upon the endangered volcano rabbit. Although coyotes and bobcats preyed on volcano rabbits, our study did not determine whether either species was having a harmful effect on the population of volcano rabbits; any decision to initiate control of predators would require further study.

Submitted 21 February 2013. Acceptance recommended by Associate

Editor Troy A. Ladine 13 June 2013.

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JOSE ANTONIO MARTINEZ GARCIA, GERMAN D. MENDOZA MARTINEZ,* FERNANDO X. PLATA P., OCTAVIO CESAR ROSAS ROSAS, LUIS ANTONIO TARANGO ARAMBULA, AND LOUIS C. BENDER

Universidad Autonoma Metropolitana, Unidad Xochimilco, 04960, Mexico, Distrito Federal, Mexico (JAMG, GDMM, FXPP) Colegio de Postgraduados, Carretera Mexico-Texcoco km 36.5, 56230, Estado de Mexico, Mexico (OCRR, LATA) Extension Animal Sciences and Natural Resources, New Mexico State University, Las Cruces, NM 88003 (LCB)

Correspondent: gmendoza@correo.xoc.uam. mx
Table 1-Elevation and length of transects, primary plant-associations
along transects in Izta-Popo National Park, central Mexico.

Site              Elevation (m)   Length (m)   Plant-association

Altzomoni 1 (a)    4,248-3,813      7,400      Zacaton
Tlamacas 1 (b)     3,524-3,707      4,900      Pine-Zacaton
Tlamacas 2 (b)     3,685-3,898      4,900      Pine-Zacaton
Tlamacas 3 (b)     3,621-3,957      4,900      Pine-Zacaton
Zoquiapan 1 (a)    3,418-3,445      1,900      Pine-Oyamel-Zacaton
Zoquiapan 2 (a)    3,425-3,434      1,900      Pine-Oyamel-Zacaton
Zoquiapan 3 (a)    3,406-3,457      1,900      Pine-Oyamel-Zacaton

(a) With human activity.

(b) Without human activity.

Table 2-Biomass estimated relative to number of consumed individuals
by bobcat and coyote, in the Izta-Popo National Park, Zoquiapan,
central Mexico.

Predator   Prey                       No. of      Frequency of
                                     prey items   occurrence (%)

Bobcat     Sylvilagus cunicularius       41           15.24
           Sylvilagus floridanus         62           23.05
           Romerolagus diazi             39           15.50
           Pappogeomys merrani           29           10.78
           Other rodents                 71           26.39
           Birds                          4            1.49
           Not identifified              23            8.55
Coyote     S. cunicularius               13           14.61
           S. floridanus                 28           31.46
           R. diazi                       6            6.74
           P. merrani                     7            7.87
           Other rodents                 17           19.20
           Birds                          0            0.00
           Not identifified              18           22.22

Predator   Relative biomass       Relative no. of
             consumed (%)     individuals consumed (%)

Bobcat          33.00                  13.13
                49.18                  33.73
                 7.28                  12.48
                 8.28                   9.28
                 1.32                  22.72
                 0.54                   1.28
                 0.36                   7.36
Coyote          28.75                  11.96
                61.02                  43.79
                 3.07                   5.51
                 5.49                   6.43
                 0.87                  15.71
                 0.00                   0.00
                 0.77                  16.55
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Author:Garcia, Jose Antonio Martinez; Martinez, German D. Mendoza; Plata P., Fernando X.; Rosas, Octavio Ce
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Jun 1, 2014
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