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Animal Biodiversity and Conservation 43.2 (2020) 177 Temporal changes in the diet of two sympatric carnivorous in a protected area of south–central affected by a mixed–severity fire

A. H. Zúñiga, J. R. Rau, V. Fuenzalida, A. Fuentes–Ramírez

Zúñiga, A. H., Rau, J. R., Fuenzalida, V., Fuentes–Ramírez, A., 2020. Temporal changes in the diet of two sympatric carnivorous mammals in a protected area of south–central Chile affected by a mixed–severity forest fire. Biodiversity and Conservation, 43.2: 177–186, Doi: https://doi.org/10.32800/abc.2020.43.0177

Abstract Temporal changes in the diet of two sympatric carnivorous mammals in a protected area of south–central Chile affected by a mixed–severity forest fire. Fire is a significant disruptive agent in various ecosystems around the world. It can affect the availability of resources in a given area, modulating the interaction between competing species. We studied the diet of the (Lycalopex culpaeus) and ( concolor) for two consecutive years in a protected area of southern–central Chile which was affected by a wildfire. Significant differences were observed in the dietary pattern between the two species, showing their trophic segregation. In the two years of the study, the predominant prey for cougar was an exotic species, the (Lepus europaeus), implying a simplification of its trophic spectrum with respect to that reported in other latitudes. The ecological consequences related to this scenario are discussed.

Key words: Dietary overlap, Predation, Post–fire dynamics, Microhabitat, cycles, Selectivity

Resumen Cambios temporales en la dieta de dos mamíferos carnívoros simpátridas en una zona protegida del centro y el sur de Chile afectada por un incendio forestal de intensidad desigual. El fuego es un importante agente perturbador en varios ecosistemas de todo el mundo que puede afectar a la disponibilidad de recursos en una zona determinada, regulando la interacción entre especies competidoras. Estudiamos la dieta del zorro culpeo (Lycalopex culpaeus) y el puma (Puma concolor) por dos años consecutivos en un zona protegida del centro y el sur de Chile que se vio afectada por un incendio forestal. Se observaron diferencias significativas en el régimen alimentario de ambas especies, lo que pone de manifiesto su segregación trófica. En los dos años del estudio, la presa predominante del puma fue una especie exótica: la liebre europea (Lepus europaeus), lo que sugiere una simplificación de su espectro trófico respecto a lo reportado en otras latitudes. Se analizan las consecuencias ecológicas de este hecho.

Palabras clave: Superposición alimentaria, Depredación, Dinámicas posteriores a un incendio, Microhábitat, Ciclos de roedores, Selectividad

Received: 28 XI 19; Conditional acceptance: 04 II 20; Final acceptance: 26 III 20

Alfredo H. Zúñiga, Jaime R. Rau, Laboratorio de Ecología, Departamento de Ciencias Biológicas and Biodi- versidad, Universidad de Los Lagos, Osorno, Chile.– Alfredo H. Zúñiga, Programa de Doctorado en ciencias mención conservación y manejo de Recursos Naturales, Universidad de Los Lagos, Puerto Montt, Chile.– Víctor Fuenzalida, Consultora Ambientes del Sur, Temuco, Chile.– Andrés Fuentes–Ramírez, Laboratorio de Biometría, Departamento de Ciencias Forestales, Universidad de La Frontera, Temuco, Chile and Instituto de Ecología y Biodiversidad, , Chile.

Corresponding author: Alfredo H. Zúñiga. E–mail: [email protected]

ORCID ID: A. H. Zúñiga: 0000-0002-0504-7540; J. R. Rau: 0000-0003-0444-578X; V. Fuenzalida: 0000-0003-3044-9610; A. Fuentes–Ramírez: 0000-0003-1258-7462

ISSN: 1578–665 X © [2020] Copyright belongs to the authors, who license the eISSN: 2014–928 X journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License. 178 Zúñiga et al.

Introduction Jaksic, 1979). Intense competitive dynamics can be expected where the differentiation of predator size is Physical disturbances caused by fire are one of the reduced (Gittleman, 1985). Additionally, forest fires not main modifying agents in natural ecosystems. Largely only affect the consumption of prey of both syntopic due to the combustion of mass (Bond and Kee- predators but also their dietary overlap (Pia, 2013). ley, 2005), such disturbances can alter microhabitats, This can present relevant ecological consequences, with constraints for the wild fauna (Picket and White, as noted in reports of cougar attacks on canids of 1985). The changes that forest fires cause in regard to similar size to the culpeo fox, i.e., intraguild predation the availability of resources can alter the dynamics (Mazzolli, 2009), which would affect their persistence of specie' interactions by dividing the use of resour- over time on a local scale. ces (Schoener, 1974). In such severe disturbances, The aim of this study was to determine the diet of species must find alternative mechanisms of co–use two syntopic predators, the culpeo fox and the cougar, of the resources to make their coexistence possible in a protected area of central–southern Chile that was in this new ecological context (Wiens, 1977). affected by a high–severity forest fire (Fuentes–Ramí- Carnivores are a group of special relevance in the rez et al., 2018). Knowledge of the predation patterns structuring of ecosystems due to the regulatory role of these species will help to determine their responsi- they exert over the species at lower positions of the veness in the event of a fire, helping to improve the food web (Hairston et al., 1960). However, fires can design and implementation of recovery actions for cause significant changes in prey availability interac- this ecosystem. tions, affecting the local species composition (Bouchert et al., 2014). Studies in the Northern Hemisphere (i.e., North America) concerning the response of predators Materials and methods to their prey in a context of disturbances caused by fire have found significant changes in predators’ response Study area and description of the forest fire in terms of the availability of prey (Bouchert, 2013; Cunningham et al., 2006). In contrast, in the Southern The present study was conducted at the China Hemisphere, and particularly in , the Muerta National Reserve, in the foothills zone of the effect of forest fires on the diet of syntopic predators Region of La Araucanía, in central–southern Chile is largely unknown. This is of special importance for (38º 42' 00'' S–71º 26' 00'' W). The Reserve encom- their conservation considering the low adaptability of passes 1,1170 ha (CONAF, 2014), with an irregular and the vegetation in this biogeographical area to high– rugged topography and an altitude that ranges from severity fires (Montenegro et al., 2004). Consequent 800 to 1,850 m a.s.l. The climate fluctuates between changes to the composition of local fauna (Johnston temperate to warm throughout the year, with fewer and Odum, 1956) as an outcome of the recovering than 4 months of drought (in the summer season from process in the burned areas are probable. December to March), and with ice and snow due to The remaining native forest in southern Chile is the effect of the altitude in winter and spring (Köeppen, characterized by its insularity compared to the rest 1948). The mean temperature is 19 ºC in summer and of the Neotropic region, which is reflected in a high 5 ºC in winter. The mean precipitation is 2,500 mm. The degree of endemism (Murúa, 1996). Among the pred- study area belongs to the Andean–Patagonian decidu- ators present in the native of southern Chile, ous forest included in the mountain range sub–region the most extended species are cougar (Puma concolor of La Araucanía (Gajardo, 1995). The native trees of Linnaeus 1781) and culpeo fox (Lycalopex culpaeus most note are Araucaria araucana, pumilio Molina 1782) (Iriarte and Jaksic, 2012).The cougar and N. dombeyi. In the bush stratum, Chusquea culeou, is a big , with a wide distribution in the Neotropic Maytenus disticha and Gaultheria poepiggi are of note region. It hunts a wide variety of prey, with sizes that (Luebert and Pliscoff, 2006). vary between 1 and 60 kg (Iriarte et al., 1990; Iriarte The forest fire that affected the China Muerta Na- and Jaksic, 2012). In some cases, the cougar preys tional Reserve began on March 14, 2015 and was on species linked to human settlement, like and brought under control 23 days later, on April 6.The poultry, causing socio–ecological conflicts (Polisar total surface affected by the fire, obtained through et al., 2003). In the mountainous area of southern flyovers made during the monitoring operations and Chile, the cougar presents a context–dependent with field exams, was 3,765 ha, which excludes lands mixed pattern, in which it feeds on native fauna, as at high peaks with no vegetation and rocky terrains well as exotic and domestic , such as lago- (CONAF, 2015). The levels of severity obtained were morphs and cattle (Rau and Jiménez, 2002). On the based on qualitative features, which varied between other hand, the culpeo fox (Lycalopex culpaeus) is a superficial damage of shrubs and canopy of trees, medium–sized canid with a reported preference for to carbonization of trees and disappearance of her- small mammals (Zúñiga and Fuenzalida, 2016), but it baceous and shrubby vegetation (CONAF, 2015). could prey on larger herbivores (Novaro et al., 2009), possibly competing with the cougar for some prey. Feces collection and dietary analyses This could be particularly true in central–southern Chile, since according to national records the cougar From December to May of 2017 and 2018 (sum- is smaller here (Vidal, 2015), whereas the culpeo fox mer–autumn in the Southern Hemisphere; second is larger at these higher latitudes in Chile (Fuentes and and third year post–fire, called hereafter the first and Animal Biodiversity and Conservation 43.2 (2020) 179

second year), feces were collected from the culpeo testing (Sokal and Rohlf, 1995), which demonstrates fox and cougar along the route of the study area on the selectivity of this predator for a specific prey. We the authorized trails. These trails included sites with calculated Bonferroni confidence intervals when the no burning and sites affected by the fire. The sampling comparison between the observed and expected effort included an approximate surface of 1,000 ha, frequencies was significant (Byers et al., 1984). This including burned and unburned sites. The feces of the analysis was done using the HABUSE 4.0 program, species were recognized according to morphological which made it possible to determine this predator’s criteria (Chame, 2003; Muñoz–Pedreros, 2010) and type of selectivity (i.e., refusal, neutral, or positive). photographic records in the study area (Kays and The capture frequencies considered were obtained Slauson, 2008). Later, feces were labeled and kept in in the autumn months of each of the two sampling paper bags for their analysis in the laboratory. There years, which is when the largest number of records are no recordings of other carnivores in the area. of and carnivores were obtained. In the laboratory, the samples were dried at 60 ºC and then separated manually to obtain the remains of the prey. The prey was identified by recognition of Results its cranial and dental morphological patterns in the case of rodents (Reise, 1973; Pearson, 1995), and of A total of 52 feces were collected, 36 of which corres- cuticular patterns of hairs and feathers for mammals ponded to culpeo fox (22 in 2017 and 14 in 2018) and and in general (Day, 1966). Reference collections 16 to cougar (10 in 2017 and six in 2018; table 1). In were used for the rest of the taxa. the case of the culpeo fox, 23 feces (19 in 2017 and To quantify the diet of the culpeo fox and cougar, we four in 2018) were found at unburned sites, and 13 determined the relative frequency (RF) of the prey items (four in 2017 and nine in 2018) at burned sites. Of based on the total observed (Rau, 2000). To estimate these, eight (five in 2017 and three in 2018) were in the dietary breadth of each predator, we used a trophic low severity and four were in high severity fire sites. diversity index (β; Levins, 1968); establishes the use of In the case of the cougar, six feces (four in 2017 and the resources based on the total items observed. The two in 2018) were at unburned sites, and 10 (six in standard deviation of this index was calculated using 2017 and four in 2018) were at burned sites. Of these, the jackknife method (Jaksic and Medel, 1987). To de- three (two in 2017 and one in 2018) were at sites of termine the interannual effect on diet, the standardized medium fire severity, whereas seven (four in 2017 and niche breadth index was used (Colwell and Futuyma, three in 2018) were observed at high–severity sites. 1971) to compare the two years, due to differences in A total of eight trophic items were identified through the availability of resources. feces, with five for culpeo fox and four for cougar, The trophic niche overlap was evaluated using of which only one was shared by both species. The Pianka’s (1973) index, which considers the food items European hare, Lepus europaeus, was the only lag- shared by the two species. Hutchenson's (1970) pro- omorph seen and recorded by camera traps. From cedure was used to evaluate the diversity of the two the relative consumption frequencies it can be seen predators, while pairwise comparisons were applied to that for the culpeo fox most of its dietary breadth in assess the differences between species and the sam- the first year consisted of rodents, followed by birds pling periods. In order to evaluate the effect of the prey (order Passeriformes) (fig. 1). However, in the second biomass on the dietary pattern of the two carnivores, year this pattern changed, with arthropods being the we used the trophic isocline method (Kruuk and De item of greatest frequency of consumption, reducing Kock, 1980), using the total number of prey recorded the proportion of rodents captured to almost half that in both years. This procedure is justified because it of the previous year. Diversity of prey consumed provides a more general picture of the importance of showed significant differences between the years 1 the prey biomass consumed by both predators. The and 2 (table 2). In the case of the cougar, lagomorph estimation of prey biomass was based on the weight hares represented the core of its diet (fig. 1), with measurements reported by Amaya et al. (1979), Mu- a proportion of consumption that increased in the ñoz–Pedreros and Yáñez (2009) and Norambuena second year. It is important to emphasize that in the and Riquelme (2014). Due to their low contribution in second year the richness of prey decreased notice- terms of biomass, reptiles and arthropods were not ably, with two types of prey consumed. Birds of the included in this representation. We also calculated the Order Anseriformes (Chloephaga sp.) had a similar geometrical mean of prey consumed for each species representation in both years. No statistical differences and study year (Jaksic and Braker, 1983). in the diversity of prey were detected when both years were compared (table 2). Rodent selectivity by the culpeo fox Regarding the dietary overlap between the two species, Pianka's index was b = 0.069 for the first The frequency of rodent consumption by the culpeo sampling year and b = 0.054 for the second year. fox was compared to the expected proportion of This low overlap was reinforced when the dietary rodent species, which was obtained through live breadth of the two species was compared between captures in Sherman traps (total sampling effort: the sampling years and showed to be significantly 6,960 traps/night). These capture frequencies were different (table 2). seen as the availability of prey in the environment, Regarding the effect of biomass on the con- and their respective comparisons were made by fit sumption frequency of the two predators, in the 180 Zúñiga et al.

Table 1. Dietary composition, dietary breadth and overlap for Lycalopex culpaeus and Puma concolor in the China Muerta National Reserve, sampling years 1 and 2 (2 and 3 post–fire).

Tabla 1. Composición, amplitud y superposición de la dieta de Lycalopex culpaeus y Puma concolor en la Reserva Nacional China Muerta, en los años de muestreo 1 y 2 (2 y 3 después del incendio).

Culpeo fox Cougar First year Second year First year Second year Mammals Rodents, Cricetidae Abrothrix longipilis 10 (23.25) 7 (12.72) – – Abrothrix olivaceus 7 (16.27) 1 (1.81) – – Irenomys tarsalis 3 (6.97) 1 (1.81) – – Oligoryzomys longicaudatus 7 (16.27) 10 (18.18) – – Rodents, Echymidae Myocastor coypus – – 1 (6.67) – Rodents, Lepus europaeus 3 (6.97) 3 (5.45) 9 (60) 8 (66.67) Artiodactyla Sus scrofa – – 1 (6..67) – Birds Indeterminate Passeriformes 6 (13.95) 8 (14.54) – – Indeterminate Anseriformes – – 4 (26.66) 4 (33.33) Reptiles Liolaemus sp. 3 (6.93) – – – Arthropods Indeterminate arthropods 4 (9.30) 5 (45.45) – – Number of feces 22 16 10 6 Dietary breadth (β) 6.67 + 0.58 3.56 + 3.82 2.27 + 4.52 1.12 + 0.64 Standardized niche (Bsta) 0.70 0.36 0.31 0.06

case of the cougar the consumption of hares this differences in abundance terms between sampling was over the isocline of 50 % (fig. 2), whereas the year. In the first year, a non–significant relation recently introduced wild boar Sus scrofa (Skewes was obtained between consumption and trapping et al., 2012) and birds were positioned in the inter- frequencies of the three rodent species (x2 = 3.121, mediate isoclines (between 5 and 20 %), with the p = 0.20), suggesting that prey consumption occurred representation of the aquatic rodent coypu, Myo- at random according to prey availability (table 3). castor coypus, below 1 %. In contrast, the culpeo However, in the second year this trend changed fox maintained the consumption of hares above significantly (x2 = 173.274, p < 0.0001), resulting the isocline of 20 %, the cricetid Abrothrix longipilis in a lower consumption than expected for Abrothrix between 1 and 5 %, and the rest of the species was olivaceus, but a higher consumption than expected under the isocline of 1 %.The geometrical mean of for Oligoryzomys longicaudatus, a reservoir native the weight of the culpeo fox's prey was 40.71 and rodent species and transmitter of the Hanta virus 10.38 g for the first and second year respectively, in Chile (Murúa, 1999). It should be noted that in and for the cougar it was 7,079.95 g and 5,361.64 the case of Irenomys tarsalis, this species of tree g for the same periods. rodent was not detected in the Sherman traps, A comparison of the frequencies of rodent trapping although it was in the feces, so it was not included and rodent consumption by the culpeo fox revealed in the analysis. Animal Biodiversity and Conservation 43.2 (2020) 181

80 Culpeo first year 70 Culpeo second year Cougar first year 60 Cougar second year 50

40

30 Percentage 20

10

0 Crc. Ech. Lag. Art. Pas. Ans. Lz. Arth.

Fig. 1. Percentage representation of the dietary items consumed by the culpeo fox and cougar in the study area for the two consecutive sampling years (2017–2018): Crc., Cricetidae; Ech., Echimyidae; Lag., Lagomorpha; Art., Artiodactyla; Pas., Paseriformes; Ans., Anseriformes; Lz., ; Arth., Arthropods.

Fig. 1. Porcentaje de la representación de los alimentos consumidos por el zorro culpeo y el puma en la zona de estudio durante los dos años de muestreo consecutivos (2017 y 2018): Crc., cricétidos; Ech., equimíidos; Lag., lagomorfos; Art., artiodáctilos; Pas., paseriformes; Ans., anseriformes; Lz., lacertilios; Arth., artrópodos.

Discussion In the case of the cougar, the relative absence of medium to large native species in the study area Reports from the same biogeographical area show has been compensated for by the consumption of differences in the dietary range of the culpeo fox and hares, the largest species in the study area, with the the cougar the (Rau and Jiménez, 2002; Zúñiga and exception of the introduced wild boar and sporadic Fuenzalida, 2016), revealing a simplification in the groups of cattle wandering on the Reserve. Despite local food supply. These differences could be attri- this, there are no records of cattle consumption by buted in the first term to the structural change in the cougar. Consumption of coypu (Myocastor coypus), prey assemblage in the study area due to the fire, which would reduce abundance and the incorporation of exotic species. The great capacity of canivores to move large generally exceeds the capture areas of their prey (Carbone and Gittleman, 2002), and it is Table 2. Comparison of the dietary diversity of therefore not possible to infer the place of capture of the cougar and culpeo fox throughout the two the prey through the feces detection site. However, sampling years. both species would present differences in the use of space, a situation that has been detected in the coastal Tabla 2. Comparación de la diversidad de la mountain range (Zúñiga et al., 2017 allowing them to dieta del puma y el zorro culpeo durante los use the mosaic produced by fire in a differentiated way. dos años de muestreo. Disturbances by fire in native forest are regarded to promote the occurrence of exotic species, where the lagomorphs in particular benefit from the particularities Comparisons T–value p–value of the microhabitats produced by the fire (Sokos et al., 2016), a situation that has been maintained system- Culpeo fox first year vs. second year atically through different types of disturbances in the 2.63 0.0090 Chilean territory (Jaksic et al., 2002). The presence of Cougar first year vs. second year lagomorphs in the study area would stimulate changes in the predators' feeding habits (Rubio et al., 2013), 1.40 0.1849 affecting the predation on native prey (Novaro et al., Cougar vs. culpeo fox first year 2000), and therefore on the control the carnivores 9.58 < 0.0001 exert over this group. However, the effect of the fire on the hares could show variations in abundance Cougar vs. culpeo fox second year over time (Sokos et al., 2016), which would vary the 7.70 < 0.0001 predation rate exerted on this group. 182 Zúñiga et al.

Table 3. Consumption frequency of the culpeo fox Lycalopex culpaeus in relation to observations from Sherman traps, with the signs in the brackets (–), (+) or (=) establishes the type of selection by the corresponding prey (chance, positive or negative), according to Bonferroni intervals.

Tabla 3. Frecuencia de consumo del zorro culpeo, Lycalopex culpaeus, en relación con las observaciones de las trampas Sherman; los signos entre paréntesis (–), (+) e (=) establecen el tipo de selección para la presa correspondiente (neutra, positiva o negativa), de acuerdo con los intervalos de Bonferroni.

Consumption frequency Bonferroni's Cricetid species (observed/expected) confidence intervals First year Abrothrix longipilis (0.370/0.530) (0.138–0.602) (=) Abrothrix olivaceus (0.259/0.269) (0.049–0.470) (=) Oligoryzomys longicaudatus (0.259/0.158) (0.049–0.470) (=) Irenomys tarsalis (0.111/0.040) (0.000–0.272) (=) Second year Abrothrix longipilis (0.388/0.454) (0.114–0.664) (=) Abrothrix olivaceus (0.055/0.515) (0.000–0.185) (–) Oligoryzomys longicaudatus (0.555/0.030) (0.275–0.836) (+)

which despite its size (10 kg; Muñoz–Pedreros and which determines the likelihood of their capture (Sim- Gil, 2009) presents a lower occurrence, similar to onetti, 1989; Vásquez, 1996).Thus, the greater rep- that observed in the Central Valley (Zúñiga and resentation of consumption by the two species of the Muñoz–Pedreros, 2014), showing casual consump- Abrothrix seems to follow the generalist nature tion events. In the case of the birds of the Anatidae of both rodents in terms of microhabitat use, having family, their systematic consumption in both study been found at sites with low vegetation cover (Glantz, years suggests the importance of this prey in the 1984), and to a lesser extent on O. longicaudatus, study area. This observation is evidenced in trophic a scansorial species, since their preferential spatial isoclins, where its frequency of consumption stands habits are arboreal (Murúa et al., 1986). In the case of out. Also, its intermediate size (ca. 3 kg) could be the tree mouse Irenomys tarsalis, its low consumption a significant complement to the cougar’s energy frequency could be a result of the smaller abundance requirements. Reports of consumption of this type due to the loss of trees and canopy as a result of of birds have been found in areas with presence of the fire, which constitute its main microhabitat, given wetlands (Rau and Jiménez, 2002). It is therefore of their predominantly arboreal habits (Kelt, 1993; Rau interest to determine whether in the study area the et al., 1995). Consequently, this rodent is one of the cougar would positively select these habitats, given culpeo fox’s trophic items most affected by the fire. its feeding behaviour. On the other hand, the record The consumption of lagomorphs by the culpeo fox of wild boar captured by this feline, the other exotic is less than reported in other locations (Rubio et al., species observed as prey in the study area, has only 2013; Zúñiga and Fuenzalida, 2016), which assumes recently been recorded from reports of predation by an effect of interference by the cougar, spatially re- (Skewes et al., 2012), suggesting that its stricting the culpeo fox (Zúñiga et al., 2017). consumption at present would be of very low frequen- The dietary range of both species showed a diver- cy. This is supported by observations in the study gence pattern based on the size of the captured prey. area that reveal that wild boars are concentrated in This trend is reinforced through the geometrical mean areas of lower altitude, presenting only occasional estimated for each predator. The trophic isoclines migrations of isolated individuals to areas of higher demonstrate that the cougar and the culpeo fox have altitude (Gastón León, pers. comm.). a markedly different diet habit and the importance of The dietary records obtained for the culpeo fox their prey in a biomass/consumption frequency ratio. agree partially with observations made for this canid Thus, for the cougar, the hare was found above the in this biogeographical area (Zúñiga and Fuenzalida, 50 % isocline, which reveals the relevance of this item 2016), where rodents were the main trophic category compared to larger prey, but of lower frequency in the of this species, which establishes a large differentiation scats, and therefore a lower capture rate. In contrast, with the cougar. The differences of capture between for the culpeo fox, the hare was between the 20 % and species would be explained by their use of the space, 50 % isocline, which implied an intermediate impor- Animal Biodiversity and Conservation 43.2 (2020) 183

Culpeo fox 100

90 Lag Cougar

50 Lag 50

Sus 40 40

30 50 % 30 50 %

20 20 Biomass (%) Bd Biomass (%) 20 % 20 % 10 10 Bd Abrl Myo 5 % Irn Abro 5 % 1 % Olg 1 % 0 10 20 30 40 50 60 0 10 20 30 40 50 60 Frequency Frequency

Fig. 2. Trophic isoclines for the cougar and the culpeo fox in the study area. The horizontal lines on the Y axis of the graph for culpeo fox indicate shortening for practical effects. Abrl, Abrothrix longipilis; Abro, Abrothrix olivaceus; Bd, birds; Irn, Irenomys tarsalis; Lag, lagomorphs; Myo, Myocastor coypus; Olg, Oligoryzomys longicaudatus; Sus, Sus scrofa.

Fig. 2. Isoclinas tróficas del puma y el zorro culpeo en la zona de estudio. Las líneas horizontales del eje de las Y del gráfico correspondiente al zorro culpeo indican un acortamiento a efectos prácticos. Abrl, Abrothrix longipilis; Abro, Abrothrix olivaceus; Bd, aves; Irn, Irenomys tarsalis; Lag, lagomorfos; Myo, Myocastor coypus; Olg, Oligoryzomys longicaudatus; Sus, Sus scrofa.

tance, due to its lower capture frequency, if compared sumption compared to the previous year could be to rodents as a whole. This group, despite its low the result of a disincentive of its search due to its low position in the isoclines, together would place them energy reward, which would force this canid to prioritize above the 5 % isocline, increasing their importance. the search for larger prey, as well as a physiological constraint to favor this type of consumption (Silva et Interannual variation of the carnivores' diet al., 2005). This pattern, added to the smaller number of fecal records compared to the previous year, sup- The interannual differences among carnivores are for poses the migration of individuals to habitat patches each one of the two species studied due to changes with a greater supply of resources, a fact facilitated in the availability of their prey. In the second year by the wide habitat area of this species (Salvatori et (2018), the steep drop in the Cricetidae rodent popu- al., 1999).The absence of selectivity in the predation lations resulted in a lower capture frequency, which of Cricetidae rodents in the first year is explained was a consistent decrease in the records of culpeo by the great availability of this resource, which was fox compared to the previous year. This suggests observed by the capture success in live traps, which both a modification in the dietary range and a displa- was around 20 % (A. H. Zúñiga, unpublished data). cement of this canid. The sharp decrease in rodents In contrast, in the second sampling year, where there is associated with interannual fluctuation processes was a reduction in the number of captures compared in the availability of resources, as has been reported to the previous year (1 %), there was a change in the for rodents in the Northern Hemisphere (Hansson and prey search pattern (as was the case for arthropods Henttonen, 1988). Consequently, a reconfiguration of and to a lesser extent lagomorphs), with a lower re- the culpeo fox’s dietary pattern was observed, which presentation of cricetid rodents. is demonstrated in particular by the disproportionate In the case of the cougar, the absence of statistical appearance of arthropods in the dietary range com- significance observed when the diversity of prey was pared to the previous year, greater even than that compared between the two years suggests a similar reported for the same biogeographical area (Zúñiga pattern in the use of resources during this period, and Fuenzalida, 2016).The absence of reptile con- partly by this felid being limited in the use of alternative 184 Zúñiga et al.

resources (Gelin et al., 2017). In a scenario of limited Bernardino mountains of Southern California, USA. resources, however, the cougar could migrate to other Hystrix, 23: 50–56. places in search of prey of higher energy reward, Bouchert, M. I., Farr, D. P., Rimbenieks–Negrete, M. which is part of a behavioral strategy in response to A., Pawlowski, M. N., 2014. Responses of small the seasonal decline of its prey (Pierce et al., 1999). mammals to wildfire in a Mixed Conifer Forest in the This is supported by the large habitat area that the San Bernardino Mountains, California. Bulletin of the cougar can have (Grigione et al., 2002). Under this South California Academy of Sciences, 113: 81–95. assumption, it is to be expected that the disturbance Byers, C. R., Steinhorst, R. K., Krausman, P. R., caused by fire was especially critical for the cougar 1984. Clarification of a technique of utilization– due to the shortage of prey available and given its availability data. Journal of Wildlife Management, high energy requirements, which necessitate larger 48: 1050–1053. migrations in search of prey that complement their Carbone, C., Gittleman, J., 2002. A common rule diet. This situation is in partial agreement with what for the scaling of carnivore density. Science, 295: was observed by Cunningham et al. (2006) in Medi- 2273–2276. terranean forests of the Northern Hemisphere, where Chame, M., 2003. Terrestrial feces: a mor- the absence of fecal records of one of the predators phometric summary and description. Memoriás do made it possible to infer the limitation of the habitat Instituto Oswaldo Cruz, 98: 71–94. in terms of dietary support. Colwell, R., Futuyma, J., 1971. On the measuremente One aspect to consider is the low sample size of of the niche breadth and overlap. Ecology, 52: the feces analyzed for both species, which were deter- 567–572. mined largely by the migratory action of the individuals CONAF, 2014. Plan de manejo forestal Reserva in the study area as a result of the low supply of prey, Nacional China Muerta. Documento operativo. mainly in the second year. This made its recordings Sistema Nacional de Áreas Silvestres protegidas in the study area difficult, suggesting caution when del Estado. CONAF, Santiago de Chile. interpreting the results presented here. – 2015. Plan de restauración incendio Reserva In conclusion, culpeo fox and cougar showed tro- Nacional China Muerta. CONAF, Temuco. phic differentiation with regard to the diversity of their Cunningham, S. C., Kirkendall, L., Ballard, W., 2006. prey, as a consequence of their body size differences. and abundance and diet responses Constraints of available resources as a consequence after a wildfire in Central Arizona. Western North an interannual variation would lead both species to American Naturalist, 66: 169–180. modify their dietary pattern towards prey with lower Day, M. G., 1966. Identification of hair and feather energy reward. Long–term studies in the study area remains in the gut and feces of and . could explain the variations in dietary response based Journal of Zoology, 18: 315–326. on the evolution of the ecosystem. Fuentes, E., Jaksic, F., 1979. Latitudinal size variation of Chilean : tests of alternative hypotheses. Ecology, 60: 43–47. Acknowledgements Fuentes–Ramírez, A., Barrientos, M., Almonacid, L., Aarriagada–Escamilla, C., Salas–Eljatib, C., This research was partially funded by Fondo Nacional 2018. Short–term response of soil microorgan- de Desarrollo Científico y Tecnológico FONDECYT isms, nutrients and plant recovery in fire–affected 11150487 and CONICYT–PIA Basal FB 002–2014. Araucaria araucana forests. Applied Soil Ecology, We thank the Dirección de Investigación, Universidad 131: 99–106. de La Frontera, for their support and Fabián Jaksic for Gajardo, R., 1995. 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