High consumption of primates by pumas and ocelots in a remnant of the Brazilian Atlantic Forest

We studied the diet of the ocelot and puma during the years 2007 and 2008 at the Feliciano Miguel Abdala Reserve, in Minas Gerais, south-eastern Brazil. We collected 49 faecal samples (scats) from cats, and identified the species of cat from 23 of them by the analysis of the microstructure patterns of hairs found in their faeces: 17 scats of the puma (Puma concolor) and six of the ocelot (Leopardus pardalis). In the puma scats, we identified three species of primates (Brachyteles hypoxanthus, Alouatta guariba and Sapajus nigritus), the remains of which were found in eight of 17 collected (47.1%), representing 26.7% of items consumed. For the ocelot, we detected capuchin monkey (S. nigritus) remains in three of the six scats (50%), accounting for 18.7% of items consumed by ocelot. We were unable to identify the cat species in the remaining 26 faecal samples, but we were able to analyse the food items present. Primates were found in five of these 26 faeces (19.2%) and represented 10.2% of the items found. Although the sample size is limited, our results indicate a relatively high consumption of primates by felines. We believe that this high predation may be the result of the high local density of primates as well as the greater exposure to the risks of predation in fragmented landscapes, which tends to increase the incidence of the primates using the ground.


Introduction
Predation of primates is difficult to observe directly (Isbell, 1990).In most cases it is confirmed only by indirect means, primarily through faecal analysis (Irwin et al., 2009).However, such indirect evidence is still important for understanding the role of predation in the ecology, behaviour and conservation of primates (Isbell, 1994;Arnold et al., 2008).The development of alarm vocalisations, defence mechanisms, use of refuges and even interspecific associations are, for example, considered evolutionary characteristics influenced by predation (Isbell, 1994;Bshary and Noë 1997;Cowlishaw, 1997;Day and Elwood, 1999;Treves, 1999;Zuberbühler and Jenny, 2002;Pruetz et al., 2008).
Here we report evidence of the relatively high consumption of primates by the puma and ocelot, Leopardus pardalis (Linnaeus, 1758), in a fragment of Atlantic Forest in south-eastern Brazil, indicating the potential implications of such predation for primate populations in fragmented habitats.

Material and Methods
We collected faecal samples from cats in the Feliciano Miguel Abdala Reserve (FMAR) (19° 50'S and 41° 50'W), which belongs to Caratinga Biological Station, Minas Gerais, south-eastern Brazil, from March 2007 to May 2008.The FMAR has 957 hectares of forest, the vegetation being characterised as lower montane semi-deciduous forest (IBGE, 1995;Oliveira-Filho and Fontes, 2000).According to the Köppen classification of climate, FMAR is AW (hot and humid subtropical), with a dry season (April-September) and a rainy season (October-March).The average annual rainfall is 1091 mm and the average minimum and maximum annual temperatures are 16.7 °C and 25.4 °C, respectively (Veado, 2002).
During the fieldwork we hiked, mainly on trails and roads, throughout the study area in search of faecal samples from wild carnivores.In the field, we differentiated the faecal samples of felines through the observation of some diagnostic features such as cylindrical shape with sub-divisions, relatively sharp, rounded or tapered ends and substantial presence of hair and bones.Some faeces had a whitish colour, due to the concentration of calcium from the bones of ingested prey (Chame, 2003).These features all agree with the descriptions in the literature (Chame, 2003;Borges and Thomás, 2004) and were used to differentiate feline faecal samples from other carnivores.We also confirmed the presence of ocelot, puma and jaguarundi (P.yagouaroundi) in the area with the use of camera traps installed at the same time as the collection of faecal samples (Paschoal et al., 2012).
In the laboratory, we processed the faeces and identified the predator species by analysing the microstructural pattern of the cuticle and medullar characteristic of their hairs found in faecal samples (from self-grooming) (Quadros, 2002).We also analysed the microstructural patterns of prey hair and other undigested remains such as teeth, claws, nails and bones, which we compared directly with material deposited in the zoological museum collections of the Pontifícia Universidade Católica de Minas Gerais and Universidade Federal de Minas Gerais.From the number of prey items found, we calculated the frequency of occurrence (percentage of total faeces in which an item was found) and percentage occurrence (number of times a specific item was found as percentage of all items found) (Ackerman et al., 1984).Although the analysis of carnivore diets by frequency of occurrence is limited (Klare et al., 2011), this procedure was preferred because it is the most widely used in dietary studies of cats facilitating, therefore, the comparison of other results to the results presented here.
We considered each primate item found in a scat as representing one individual, provided that the number of teeth and/or claws (when present) did not indicate otherwise (i.e., one item/scat one prey individual).For Puma concolor we estimated the number of preyed primates also on the basis of corrected biomass.For this, the consumed biomass and number of preyed individuals were corrected according to Ackerman et al. (1984) equation (Y= 1.98 + 0.035 X, where Y= consumed biomass/scat and X= prey weight, both in kilograms).We used Paglia et al.(2012) as source for primate body weights.This correction factor produces more conservative values as it corrects for the fact that the remains of a single individual prey can be eliminated through more than one scat (Ackerman et al., 1984).For ocelot faeces and for faeces of unidentified felids, correction factors are not available and therefore were not used.

Results
We collected 49 faecal samples from cats.Through microstructural analysis of the pattern of hair, the identification of the originating predator was possible for only 23 faecal samples (17 of puma and 6 of ocelot).The faecal samples that could not be identified were grouped in a category of "unidentified cat" (Table 1).
Considering all faecal samples, identified and unidentified, Primates was the mammalian order with the second largest number of occurrences of remains in faeces, representing 16.8% of the total items found, second only to Rodentia (26.3% of items) (Table 1).The capuchin monkey, Sapajus nigritus (Goldfuss, 1809), was the primate with the highest number of occurrences (6.3% of the items), being detected in six of the faecal samples.The remains of muriqui, Brachyteles hypoxanthus (Kuhl, 1820), (Figure 1) and brown howler monkey, Alouatta guariba (Humboldt, 1812) were each found in five faecal samples.
The order Rodentia was the order most consumed by ocelots, followed by Didelphimorphia and Primates.The capuchin monkey was the only primate found in faecal samples identified as belonging to the ocelot (Table 1).Primates, on the other hand, was the order of mammals most consumed by pumas, and among these the muriqui was the most common species found: 16.6% of the items and in five of the 17 faecal samples of this cat.
Based on number of items, we estimate that 16 individuals of primates (six capuchins, five howlers and five muriquis) were consumed by cats (Table 1).Considering the corrected biomass as a basis for the estimation, we estimate that a minimum one individual of each primate species (capuchin, howler monkey and muriqui) was consumed by puma (Table 2).

Discussion
Predation on muriqui (B.hypoxanthus), brown howler monkey (A.guariba) and capuchin monkey (S. nigritus) by ocelots has been reported in FMAR by Bianchi and Mendes (2007).However, in the present study, we recorded the first instance of predation of B. hypoxanthus by puma.Although pumas and ocelots are known to prey on howler and capuchin monkeys in other areas (Brito, 2000;Ludwig et al., 2007;Miranda et al., 2005), this is the first record of puma predation on Brachyteles.Until now muriqui has only been reported as prey of jaguar (Olmos, 1994) and ocelot (Bianchi and Mendes, 2007).
The most recent publication with data on the demography of Caratinga muriquis (surveys in 2003 and2004;Strier et al., 2006), detected an increase in the mortality of newborns and infants in comparison with previous periods (Strier, 1999).Larger infants and juvenile muriquis may be more susceptible to predation than adults, because at this stage they spend a significant amount of time foraging independently (Printes et al., 1996).Lynch and Rímoli (2000) also found higher mortality rates for infant capuchin monkeys in FMAR than in other areas.Both sources (Strier et al., 2006;Lynch and Rímoli, 2000) mention predation among the potential causes of these deaths.In most cases the analysis of the faecal content does not allow accurate inferences about the age classes of the individuals (infants or adults) since relatively intact parts that could provide clues are normally not found in faeces.However, a higher proportion of underhairs in relation to guardhairs found in faeces suggest the presence of young prey (Quadros, 2002).On the basis of this, we infer that at least three infants or newborns (one each of the three primate species found in faeces) were predated in FMAR during the period of the study.Corroborating this, one of the scats had parts of a finger whose dimensions were of a young muriqui (Figure 1).
Assuming that the muriqui population in FMAR is around 300 individuals (Strier, 2010), and considering that our study spanned approximately one year, our conservative estimate of 1-5 muriquis killed/year would indicate an annual predation rate, by felids alone, of 0.3-1.7% of the local muriqui population.A similar rate would apply to capuchin monkeys if the current abundance of this primate is in fact similar to that of muriquis, as is indicated by a previous study (Almeida-Silva et al., 2005a).For brown howlers this rate might be halved, as howlers seem to be roughly twice as abundant as muriquis in FMAR (Almeida-Silva et al., 2005a).We stress, however, that these predation rates are likely underestimates not only because of the conservative nature of our estimates but also due to the fact that our sampling is far from exhaustive, both spatially and temporally.Further, other predator species, both native and domestic species, were not examined.
A study by Paschoal et al. (2012) using camera traps between 2007 and 2008 did not indicate that ocelots and pumas are present in the study area at particularly high densities.It is likely therefore that high consumption of primates in FMAR is a result of factors other than predator abundance.The abundance of primates may be one, since the local densities of muriquis and brown howler monkeys are among the highest ever recorded for the Atlantic Forest (Hirsch, 1995;Strier and Fonseca, 1996).Furthermore, the      high rates of predation of primates may also be a result of their atypical behaviour of often descending to the forest floor, which has been observed both in muriquis and brown howler monkeys at FMAR (Almeida-Silva et al., 2005b;Mourthé et al., 2007).Muriquis have been observed performing activities, such as resting, feeding, socialisation and locomotion, which are normally restricted to the arboreal stratum, on the forest floor of FMAR (Printes et al., 1996;Mourthé et al., 2007).

Total
Our findings corroborate the study of Bianchi and Mendes (2007) and suggest a high proportion of primates in the diet of cats in FMAR in relation to other Atlantic Forest areas.Both ocelots and pumas are opportunistic predators (Emmons, 1987;Delibes et al., 2011) being able to feed on abundant or vulnerable species, even if they are not the most common prey.This might be further increased in fragmented landscapes, since primates living in forest remnants need to descend to ground level frequently to get around, hence exposing themselves to attacks from terrestrial predators.As shown in Table 3, the occurrence of primates in the diet of ocelots has been recorded mainly in smaller fragments (700 to 2500 ha), including FMAR, with 957 ha (Vidolin, 2004;Moreno et al., 2006;Moreno and Giacalone, 2006;Bianchi and Mendes, 2007;Abreu et al., 2008).
Although the ocelot feeds mainly on small vertebrates (e.g.Emmons, 1987;Ludlow and Sunquist, 1987;Konency, 1989;Wang, 2002), there may be an increase in the importance of larger prey in the diet of this cat in fragmented locations or on islands where larger cats are absent or are at low densities (Moreno et al., 2006).This feature, coupled with the ocelot's tolerance to fragmented and isolated environments, which appears to be greater than that of the larger cats, suggests that ocelots may be playing a significant role in population control of medium and large mammals, including arboreal primates, at sites such as this.The diet of pumas consists mainly of mammals of medium and large size (Ackerman et al., 1984;Iriarte et al., 1990;De Azevedo, 2008), but larger prey such as the tapir, Tapirus terrestris (Linnaeus, 1758) and peccaries, Pecari tajacu (Linnaeus, 1758) and Tayassu pecari (Link, 1795) are extinct in FMAR (Veado, 2002).
It would be worthwhile to investigate whether the rate of predation on primates in FMAR indicates a likely scenario for populations of endangered primates in other isolated Atlantic Forest fragments (Hatton et al., 1984;Mittermeier et al., 2006).More than 80% of the remaining fragments of this biome are less than 50 ha in size and almost 50% of their area is within 100 m of an edge as well as being isolated from each other (Ribeiro et al., 2009).Future studies should also verify whether predation is a leading cause in the decline in the population of primates in Atlantic Forest remnants or whether other factors inherent in isolated populations with high densities (inbreeding depression, increased susceptibility to disease, intra and interspecific competition) offer even greater risks to these populations.

Table 3 .
Importance of primates in the diets of ocelots (Leopardus pardalis) and pumas (Puma concolor) in Neotropical Forests Area of coverage of the study in the Cocha Cashu Biological Station. 1

Table 2 .
Corrected biomass and number of individuals of primates preyed upon by puma.The values were corrected using the Ackermanet al.(1984) equation (See methods for details).