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INTRODUCTION

The trophic niche represents the functional status of a species based on its energetic relationships or position in the food chain (Peterson et al. 2011). The diets of different species often overlap leading to increased competition and possibly exclusion from the community (Schoener 1974a; Linnell & Strand 2000). However, diet can also be spatially or temporally partitioned among sympatric species in a given region, thereby reducing competition and favoring coexistence (Schoener 1974b; Kronfeld-Schor & Dayan 2003; Di Bitetti et al. 2009; 2010). Mammalian carnivores are ideal models to address niche-related questions due to the availability of data linking morphology to resource utilization and partitioning in multiple contexts (Davies et al. 2007). For instance, differences in activity patterns and habitat use allow the coexistence of six sympatric species from the genera Leopardus, Puma and Panthera in Argentina (Di Bitetti et al. 2010), while resource partitioning allows Lynx rufus and Leopardus pardalis to coexist in southeastern Texas (Horne et al. 2009). Furthermore, species with partially overlapping geographic distributions - especially syntopic ones - are also prone to size or morphological differences (Meiri et al. 2011). This is particularly evident in three of the six wild canid species found in Brazil, which occur sympatrically in the Cerrado - the hoary fox (Lycalopex vetulus), the crab-eating fox (Cerdocyon thous) and the maned wolf (Chrysocyon brachyurus) - and which are potential competitors due to their dietary preferences (Juarez & Marinho-Filho 2002; Hoffmann & Sillero-Zubiri 2004; Jácomo et al. 2004; Lemos et al. 2007). However, dietary overlap among these species is still poorly understood.

Although the importance of canids in the maintenance of community structure is well known, either through effects on prey populations or seed dispersal (Dalponte & Lima 1999; Rocha et al. 2004; Cheida 2005), the size and number of their populations have been markedly reduced in recent decades (Hoffmann & Sillero-Zubiri 2004). Habitat loss and fragmentation, roadkills, and harm caused by direct and indirect interactions with domestic dogs are the main anthropic effects threatening Brazilian wild canids (Hoffmann & Sillero-Zubiri 2004; Cheida et al. 2011; Lemos et al. 2011a;b; 2013; Lemos 2016). In fact, both the hoary fox and the maned wolf are considered “Vulnerable” according to Brazil’s extinction risk list (Lemos et al. 2013; Paula et al. 2013), while the crab-eating fox status is considered to be of “Least Concern” (Beisiegel et al. 2013). Nonetheless, there are still wide gaps in knowledge about the ecology of these species hindering the assessment of their extinction risk.

Given this context, an in-depth understanding of the diet and resource partitioning of sympatric wild canid species in unprotected areas (e.g. agroecosystems) would contribute to fill these gaps as well as assist in devising and implementing management and conservation strategies for them (Crawshaw Jr & Quigley 2002; Castro & Emmons 2012). Here we present the most robust assessment to date of the feeding ecology of three sympatric wild canid species living in an unprotected and altered ecotone between the Cerrado savanna and the Atlantic Forest ecosystems. We used a pool of fecal samples collected along seven years to determine how L. vetulus, C. thous and C. brachyurus utilize food resources, particularly addressing the following questions: (1) How the type and proportion of food items varies among the three species of wild canids allowing their coexistence? (2) Are differences in body size among the three species related to food niche breadth and trophic niche overlap?

MATERIAL AND METHODS

Study area

The study was conducted in an approximately 150 km2 area encompassing a group of cattle ranches within the Limoeiro region (18°33’-18°43’S, 48°07’-48°20’W), an ecotone between the Cerrado and Atlantic Forest biomes located in the municipality of Cumari, Goias state, Brazil (Fig. S1). The vegetation cover of the region was originally composed of the characteristic species of the savannah and seasonal semideciduous forest, currently altered by agricultural activities (IBGE 2004). Almost 72% of the vegetation of the area has been replaced by exotic pastures (mainly Urochloa spp.) for extensive cattle ranching, and small and medium remnants of original vegetation account for approximately 26% of the region (Lemos 2016). This region is characterized by a markedly seasonal tropical climate, with a dry season from April to September and a rainy season from October to March (Sano et al. 2008). Annual mean temperature varies from 20ºC to 22°C, and annual mean precipitation is between 1300 mm and 1600 mm (Alvares et al. 2013).

Study species

The hoary fox is a small canid (weighing 2.5-4 kg) endemic to open savanna grasslands in Brazil, which feeds mainly on insects, fruits and small vertebrates (Dalponte & Lima 1999; Dalponte & Courtenay 2004; Dalponte 2009). The crab-eating fox is a small to medium-sized canid (5-8 kg), being relatively common in the Atlantic forests of east Brazil, with an omnivorous diet that varies throughout its distribution and between seasons (Montgomery & Lubin 1978; Facure et al. 2003; Hoffmann & Sillero-Zubiri 2004). The maned wolf is the largest South American canid, weighing on average 26 kg (Jácomo et al. 2009). Its occurrence in Brazil was originally limited to the various phytophysiognomies of the Cerrado (Paula et al. 2013), with a diet composed of small to medium-sized vertebrates and fruits (Dietz 1984; Juarez & Marinho-Filho 2002; Jácomo et al. 2004; Rodrigues et al. 2007).

Data collection

We collected data from 2009 to 2015 using three complementary methods. More than 60% of fecal samples were collected from captured animals, either during the anesthetic procedures or from the traps used during live captures. We also obtained data from direct field observations, collecting samples as soon as the animals defecated, making sure not to disturb their behavior. And, there were opportunistic collections, when fecal samples were found by walking roads and trails in the study site.

We collected a total of 155 fecal samples: 65 from hoary foxes, 60 from crab-eating foxes and 30 from maned wolves. Samples collected during dry seasons throughout the seven study years represented 72% (n=47), 90% (n=54) and 86.5% (n=26) of the total number of samples for hoary foxes, crab-eating foxes and maned wolves, respectively. All fecal samples collected were identified and conserved in 70% alcohol in plastic containers. For each sample we recorded the species, sex and ID (for those already known and marked with radio collars or earrings), date and geographic coordinates of collection. The samples collected opportunistically were identified by morphological characteristics, such as shape, size and volume, odor, contents, and authors’ experience with the species studied.

Samples were washed in running water over a mesh 30 (600µm) granulometric sieve, transferred to a plastic tray for dietary item separation, and subsequently evaluated through a stereomicroscope. Items present in each sample (fur, teeth, bones, scales, seeds, shells) were separated into six food category: fruits, insects, anurans, squamates, birds or mammals, and further identified to the lowest possible taxonomic level according to specialized literature (e.g. Peláez-Campomanes & Martin 2005; Kuhlmann 2012), specialist opinions and direct comparisons with reference collections at the Cerrado Biodiversity Museum and Federal University of Uberlandia Teaching Labs. Items for which taxonomic level identification were not possible were kept in their respective food category as non-identifiable (n.i.) items for inclusion in data analyses.

Data analyses

The importance of each food category in the diets was initially expressed as an absolute frequency (AF), corresponding to the number of samples containing a given food item or category. We then calculated the frequency of occurrence (FO) based on the ratio between AF and the total number of samples. Finally, we obtained the relative frequency (RF) of each category, dividing their AF by the sum of AF for all items or categories (cf. Juarez & Marinho-Filho 2002). We compared the absolute frequency of each category in the diet of the three canid species using contingency tables and chi-square tests of independence in R Core Team (2016), further performing analyses of the residuals to interpret the results (Sharpe 2015).

We estimated the trophic niche breadth using the Levins’index, which measures how uniform is the distribution of individuals across resource categories, it is calculated as:BA=B-1/(n-1), where BA is the standardized Levins’ nichebreadth, n is the number of possible resource categories,and B is the Levins’ measure of niche breadth given by1/Ppj2, where pj represents the proportion of individualsfound in resource j, using resource category j, or thefraction of diet items from resource category j (Krebs 1999). Niche breadth was calculated for items and food categoriesand varies from 0 to 1. To facilitate interpretation andcomparison among species we considered BA=0 as verynarrow diet breadth, 0.1 < BA < 0.3 as narrow, 0.3 < BA <0.6 as medium, 0.6 < BA < 0.9 as wide, and BA=1.0 as very wide.

We evaluated the trophic niche overlap among the threespecies using Pianka’s index, obtained through pairwisecomparisons of the frequencies of items and food categoriesin each species diet. Niche overlap can be calculated usingthe formula,where Ojk is the niche overlap between species j and k,pij is the proportion of resource i in the total of resourcesutilized by species j, p_ik is the proportion of resource i inthe total of resources utilized by species k, and n is the totalnumber of resource categories. Niche overlap varies from 0 (no resources used in common) to 1 (complete overlap) (Krebs 1999). To facilitate interpretation and comparisonamong species we considered 0.1 < O_jk < 0.3 as low, 0.3< Ojk < 0.6 as medium, 0.6 < Ojk < 0.9 as high overlap,respectively and calculated the percentage of trophic nicheoverlap as P_jk = 100Pni=1 min (pij ; pik) (Krebs 1999). Data from different years were pooled for each species toincrease the robustness of all statistical analyses. To check if overlap is different than that expected by chance wedid 1 000 Monte Carlo randomizations of proportions of different food items or categories in each species’ diet tosimulate possible overlaps among the three species usingthe function niche_null_model() in the package “EcoSimR”(Gotelli et al. 2015).

A Correspondence Analysis (CA) was run to visualize dietary separation among the three canid species as in Walker et al. (2007) and Palacios et al. (2012). For this analysis, food items with relative frequency less than 5% for all species were combined in categories “other” (forexample, other insects, other fruit, other vertebrates).

RESULTS

We identified a total of 35 different types of food items across the diets of the three canid species, of which 13 were plant-based and 22 animal-based. Of these, 21 were found in fecal samples from hoary foxes, 22 from crab-eating foxes and 19 from maned wolves (Table S1). The relative frequency of animalbased items represented 86.3% of the diet for hoary foxes, 75.8% for crab-eating foxes and 63.4% for the maned wolf. Insects were the main dietary items for both hoary foxes and crab-eating foxes, accounting for 79.2% and 60% of food items, respectively. The former consumed Isoptera, Coleoptera and Orthoptera in similar proportions (each approx. 25% of the total), while the latter consumed mainly Coleoptera and Orthoptera. In contrast, fruits were the main food category for maned wolves, representing 36.6% of the items consumed. The wolf fruit (Solanum lycocarpum) was the most important dietary item, accounting for 22% of the total.

The importance of the main prey categories was different among the three canid species (χ2 =134.09, df=8, P<0.0001; Fig. 1). The hoary fox differed from the other species due to the greater consumption of insects (standardized residuals, SR=3.465) and lower consumption of fruits (SR=-2.536), birds (SR=-2.412) and mammals (SR=-2.589), while the crab-eating fox was different due to the lower consumption of birds (SR=-2.206). The maned wolf differed due to greater consumption of fruits (SR=3.093), birds (SR=6.707) and mammals (SR=3.490) and lower consumption of insects (SR=-5.422). For all species, other categories were consumed within the expected frequency (SR between -2 and 2).

Standardized niche breadth (B_A) analyses revealed low uniformity in resource utilization and narrow diet breadth for the hoary fox (B_A= 0.189, for items and 0.108, for categories) and the crab-eating fox (B_A=0.231, for items and 0.259, for categories), and medium levels for the maned wolf (B_A=0.491, for items and 0.551, for categories). These values indicate that both smaller species (especially the hoary fox) presented a less diverse diet (Table 1). Niche overlap was very high between hoary foxes and crab-eating foxes, totaling 66.1% for food items and 80.8% for food categories, it was medium between crab-eating foxes and maned wolves (36.5% , for items and 52.8%, for categories), and low between hoary foxes and maned wolves for food items (25.1% ) and medium for categories (34.1%).

The mean food niche overlap among the three canids (0.662; s2 =0.079) was marginally greater (p=0.053) than the mean simulated overlap (0.397, 2 s =0.020), for categories. And, the mean food niche overlap among the three canids (0.416; s2=0.100) was significantly greater (p=0.008) than the mean simulated overlap (0.167, s2=0.005), for itens.

Although overlap in diet among the three species was higher than random, the diets of the 3 species were clearly differentiated in the correspondence analysis, with hoary foxes consuming more termites, maned wolves consuming more wolf fruit and birds, and crab-eating foxes consuming orthopterans, scarab beetles, small mammals and fruits (Fig. 2).

DISCUSSION

This study represents the first effort to date in evaluating the diets of three sympatric canid species in an unprotected altered Neotropical landscape. Our dietary analyses indicated that hoary foxes and crab-eating foxes, species with similar body size, consumed primarily insects and presented narrow trophic niche breadths and high dietary overlap. Conversely, insects were less frequent in the diet of the maned wolf, which consisted of small vertebrates and primarily fruits (especially the wolf fruit), thereby supporting similar findings in other regions (Motta-Junior et al. 1996; Juarez & Marinho-Filho 2002; Jácomo et al. 2004; Rodrigues et al. 2007). Indeed, they actively search for wolf fruits in disturbed habitats such as secondary savannas and roadsides (Motta-Junior et al. 1996). Furthermore, the maned wolf was the only species that frequently consumed birds (relative frequency > 20%), and hence presented the widest trophic niche breadth.

The trophic niche difference associated to the consumption of termites by the hoary fox may be the key driver of their coexistence in the Brazilian Cerrado. Despite the elevated consumption of Scarabeidae and Orthoptera (occurrence frequency > 60% ), diet differences between hoary and crab-eating foxes were mostly due to the high consumption of termites by the hoary fox and high consumption of fruits and rodents by the crab-eating fox. The elevated consumption of termites by the hoary fox is a known characteristic of the species throughout its distribution (Dalponte 1997; Juarez & Marinho Filho 2002; Ferreira-Silva & Lima 2006; Lemos et al. 2011b) as termites are their primary source of protein, suggesting a primarily insectivorous diet for the species (Hoffmann & Sillero-Zubiri 2004; Tchaicka et al. 2016). In contrast, the high consumption of insects by crab-eating foxes is potentially due to two factors. First, the lower abundance of fruits in our study area, as previous studies in other habitats have shown a greater frequency of fruits in their diet (Motta-Junior et al. 1994; Facure et al. 2003; Jácomo et al. 2004; Lemos et al. 2011b). Most importantly, however, the high frequency of insects is probably related to the opportunistic feeding behavior of crab-eating foxes and the abundance of Orthoptera and Coleoptera in areas altered for cattle ranching (Ferreira-Silva & Lima 2006; Rocha et al. 2008). For instance, we found 24 Scarabeidae beetles in a single fecal sample from crab-eating foxes, highlighting their exploration of this temporally abundant resource and supporting previous findings from other environments where insects were also highly abundant (e.g., Bueno & Motta-Junior 2004; Matos Dias & Bocchiglieri 2016). Nevertheless, although we also expected greater increased competition between the hoary and crabeating foxes, the habitat and food specialization presented by the hoary fox possibly reduces their competition and facilitates their coexistence in natural and human-modified Cerrado environments (Juarez & Marinho-Filho 2002; Jácomo et al. 2004; Lemos 2007).

The more uniform consumption of food items by maned wolf may be related to the fact they have larger home ranges and travel long distances for several consecutive hours foraging (Hoffmann & Sillero-Zubiri 2004; Cheida 2005; Lemos 2016). The low overlap of trophic niches between the maned wolf and the hoary fox supports findings from a previous study conducted in pastures and unprotected woodland savannas (Juarez & Marinho-Filho 2002). However, it differs from findings from protected natural areas, where trophic niche overlap was higher for these species relative to comparisons with the crab-eating fox, probably as a result of similar habitat use patterns (Jácomo et al. 2004). However, as we found generally low trophic niche overlap values in altered unprotected areas, the higher overlap previously found in protected areas may be due to the higher fruit consumption by the hoary fox, as fruits are more diverse and abundant in the latter (FGL, pers. obs.). Since these canids are opportunistic feeders, the number of food items consumed varies depending on their availability in each area (Ferreira-Silva & Lima 2006) and may reflect the important negative consequences of landuse changes for species diversity in this biome (Klink & Machado 2005).

We identified fly larvae from the Sarcophagidae and Stratiomyidae families in fecal samples from crab-eating foxes and maned wolves, but not from hoary foxes. Their presence is associated to the decomposition of carcasses consumed by the crabeating fox (Facure & Monteiro-Filho 1996; Lemos 2007) and the maned wolf (Silveira 1999; Bueno & Motta-Junior 2004; Rodrigues et al. 2007), as their fecal samples contained birds and small mammals. Despite the absence of fly larvae in fecal samples from hoary foxes, they have been previously reported to consume carcasses of road killed animals (Lemos et al. 2011a). Despite the presence of the parasitic pathogen Trypanosoma cruzi having already been described for hoary foxes (Rocha et al. 2013), wefound for the first-time evidence of the Heteropteran species hostage of this Triatominae in a hoary fox fecal sample. The consumption of Heteropterans supports the hypothesis suggested by Rocha et al.(2013) that predator-prey interactions are important mechanisms for the maintenance and dispersal of parasites.

Despite previous studies suggesting all three of our focal species are adapted to human-modified environments (Facure & Monteiro-Filho 1996; Hoffmann & Sillero-Zubiri 2004; Rodrigues et al. 2007; Rocha et al. 2008), their forced adjustments to these conditions may result in a reduction of diet diversity and consequently increased interspecific competition, potentially leading to the exclusion of a species of a particular habitat (Begon et al. 2009).

Abreu et al. (2010) also found high dietary overlap between C. thous and L. gymnocercus, however, the authors believe that the coexistence between these species should occur through factors other than diet, such as habitat use and/or activity period. In contrast, in our area have been reported high spatial and temporal overlaps in habitat use (Lemos 2016) as well as interference competition (Lemos 2007; Lemos et al. 2011b) for C. thous and L. vetulus. Given that competition for food is a critical factor determining carnivore species coexistence (Davies et al. 2007), increased competition may alter the conservation status of these species (Hoffmann & Sillero-Zubiri 2004), especially as two of them are facing some degree of extinction risk (ICMBIO 2014).

To understand how wild species behave in humanmodified environments requires basic knowledge of diet composition and feeding ecology. Altered environments vary considerably in their ability to support wildlife populations (White et al. 1997), especially for medium and large species (Fahrig 2003; Costa et al. 2005), and this is mainly determined by the history of occupation and land use (Machado et al. 2005). The knowledge of the trophic ecology of three South American Canidae species may contribute not only to a better understanding of their ecology, but also to the elaboration of management and conservation strategies for these species, with special attention to those that are under risk of extinction and living in unprotected areas, particularly with livestock activities.

CONCLUSIONS

In this context, we suggest that for the perpetuity of the three species in cattle farm areas in the Brazilian Cerrado, it is important to maintain the supply of food, such as cultivated and wild fruits (especially maned wolf fruit) and to avoid the indiscriminate use of pesticides, since termites and small rodents are important prey for them. We also strongly urge that further studies aim at better understanding the trophic ecology of Neotropical wild canids, especially those living in unprotected landscapes, such as agroecosystems, so that future conservation and management efforts can be correctly tailored to these species and account for potential drivers of local extinction in these areas.

Supplementary materials

Acknowledgments

We thank the Cerrado Mammals Conservation Program (PCMC) for the partnership and data acquisition that made this research possible. We also thank C. Eduardo Fragoso, Stacie M. Castelda-Bickley, Hugo C. M. Costa, Leandro Abade, and Frederico Cigano Alves for sample collection, and Ivan S. Silva, Ariovaldo A. Giaretta, Julianne Milléo, Fabiana L. Rocha, Karine R. Oliveira, Lucas H. Siqueira, Élida M. Brandão and Thiago A. Rosa for contributions during identification of food items. We are grateful to the Cerrado Biodiversity Museum at the Federal University of Uberlândia (UFU) for logistical support during sample triage and lab analyses, and Fundação Parque Zoológico de São Paulo (FPZSP) for logistical support during capture campaigns. Bianca M. Kotviski received a scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) during the work.

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