Vertebrate Predation and Tool-Aided Capture of Prey by Savannah Wild Capuchin Monkeys (Sapajus libidinosus)

Vertebrate predation was a vital behavior during human evolution. Some Afro-Eurasian primates, such as baboons (Papio spp.) and chimpanzees (Pan troglodytes), frequently hunt and consume vertebrate prey. Capuchin monkeys (Cebus and Sapajus) are omnivorous platyrrhines, and also hunt and consume vertebrates opportunistically. Bearded capuchin monkeys (Sapajus libidinosus) living in semi-arid savannah environments use stone tools to obtain food resources. However, only one population at Serra da Capivara National Park, Brazil, is known to use stick probes to enhance predation. I present data collected for 2 years on vertebrate predation and consumption by two groups of capuchins in this population. Recording vertebrate predation events ad libitum, I observed 72 events, at a rate of 4.6 events/100 h. The most frequent prey were lizards and snakes, followed by birds and rodents, including larger rodents such as adult rock cavies (Kerodon rupestris). The monkeys also preyed on bats, albeit rarely. Predation on vertebrates, including prey that are large relative to their body size, use of tools to aid predation, and a high degree of terrestriality in the savannah environment make robust capuchins a suitable model to understand human evolution, as well as a good comparison with Afro-Eurasian primate models.


Introduction
Predation on large vertebrates was an important behavior during human evolution (Butynski, 1982;Thompson et al., 2019). The energy obtained from consuming the meat of larger animals provided energy that allowed the maintenance of larger brains, enhanced cooperation, prolonged childhood, and shortened female interbirth intervals, among other human characteristics (Thompson et al., 2019). Other primates also hunt and consume vertebrates opportunistically. For example, olive baboons (Papio anubis) prey on at least three species of primates, ten ungulates, four rodents, three hares, one bat, four herpetofauna and six species of bird (Sommer et al., 2016;Strum, 1975). Hamadryas baboons (P. hamadryas) prey on vertebrates at a rate of 2.8 events/100 hours of observation, preying on dik dik (Madoqua kirki), hares (Lepus capensis), and Guinea fowl (Numida meleagris), among other species (Schreier et al., 2019). Yellow baboons (P. cynocephalus) hunt lizards, birds, and gazelles (Hausfater, 1976;Rhine et al., 1986). Baboons living in close forests show a much lower predation rate than those on open savannahs (Sommer et al., 2016), suggesting that the environment is an important factor in the amount of predation.
There can be sexual and age differences in the frequency and success of predation. Adult males are the most common sex-age class observed preying on vertebrates in several primate species (Butynski, 1982;Rose, 1997). For example, male chimpanzees usually hunt more frequently and successfully than females (Gilby et al., 2010;Watts & Mitani, 2002). The same pattern has been observed in a troop of olive baboons, where 93% of the predations were by adult males (Harding, 1973). Sex differences in hunting may be due to sex differences in energetic balances. Female mammals may need more stable food sources to increase their energetic intake during pregnancy and lactation (McCabe & Fedigan, 2007), and therefore be averse to more unreliable sources like hunting. In contrast, in highly sexually dimorphic species, the larger males can have more energetic costs and be more resilient to variation in energetic intake than females, and may seek prey which are challenging to catch more often than females do (Key & Ross, 1999).
In some primates, adults share highly nutritious food such as meat with immatures, and in some species, such as callitrichids, this is mainly for the nutritional gain of the recipient (Jaeggi & Gurven, 2013). Another explanation for meat sharing is the information hypothesis, which suggests the main benefits of food sharing to immatures are not nutritional, but the knowledge and experience about novel or difficult-to-process food items that they cannot access (Jaeggi & Gurven, 2013).
Afro-Eurasian primates such as baboons and chimpanzees are frequently used as models to understand the evolution of human behaviors, including predation and tool use, as they are phylogenetically closely related to humans (Rose, 1978). Platyrrhines are separated from the human lineage by 40 Myr of evolution (Lima et al., 2018). However, one group of platyrrhines shows several characteristics similar to those present during hominid evolution and can also be used as a model for human evolution. Capuchin monkeys (Sapajus and Cebus) are omnivorous primates, consuming plants, arthropods, and vertebrate prey (Fragaszy et al., 2004;Izawa, 1978). Although primarily arboreal, some savannah populations of robust capuchin monkeys (genus Sapajus) are highly terrestrial (Wright et al., 2019), and show frequent and, sometimes, highly variable tool use behavior (Falótico, Coutinho, et al., 2018a;Falótico & Ottoni, 2016;Falótico et al., 2017;Ottoni & Izar, 2008;Spagnoletti et al., 2011).
In dry forests, white-faced capuchins (Cebus capucinus) hunt several types of vertebrate prey, such as lizards, frogs, birds, squirrels, coatis, anteaters, and bats (Fedigan, 1990;Rose, 1997;Rose et al., 2003). Brown tufted capuchins (Sapajus apella) in the Amazonian forest prey on small vertebrates (Izawa, 1978), and a Sapajus group in an urban park in São Paulo (Brazil) hunted birds and shared the meat (Ferreira et al., 2002). Although vertebrate prey is a small part of the capuchin diet, it is high-quality food and rich in protein and fat (Fedigan, 1990). Robust capuchin (Sapajus) living in savannah environments could present a different prey selection, related to different prey availability or the distinctive local ecological pressure. However, there are scarce data on vertebrate predation by Sapajus living in drier environments. The few reports are of predation of an adult rock cavy, Kerodon rupestris (Filho et al., 2021), and on snakes (Falótico, Verderane, et al., 2018b;Silva et al., 2019). Sapajus avoid dangerous poisonous and constrictor snakes, but prey on non-dangerous kinds (Falótico, Verderane, et al., 2018b;Silva et al., 2019).
As in other primates, adult males are also the most common sex-age class observed preying vertebrates in capuchins (Rose, 1997). Females are expected to seek for more stable food sources to cope with reproductive cost fluctuations, being, in theory, less prone to look for unpredictable food sources such as vertebrate prey. However, there can be variations. In C. capucinus, the frequency and success of squirrel hunting by males and females differed across two sites in Costa Rica (Rose et al., 2003). At the site with smaller sex differences, simultaneous hunts of multiple squirrels were more frequent, which may have increased hunt success by females (Rose et al., 2003).
In capuchins, food sharing from adults to immatures is not only for nutritional gain, but is better explained by the information hypothesis, as a way to gain knowledge and experience about a novel or difficult-to-caught food item (Jaeggi & Gurven, 2013). Among capuchins, food sharing also happens among same-and different-sex adults (Jaeggi & Schaik, 2011). In the case of same-sex sharing, the presence of same-sex coalitions in the species was a significant predictor of the occurrences of same-sex food sharing (Jaeggi & Schaik, 2011).
Several wild populations of savanah Sapajus customarily use tools (Ottoni & Izar, 2008) and show a high degree of terrestriality (Falótico, 2011;Visalberghi et al., 2005;Wright et al., 2019), making them an additional model to Afro-Eurasian primates to understand vertebrate predation in an environment similar to that present during human evolution. The population of bearded capuchin monkeys (S. libidinosus) at Serra da Capivara National Park (SCNP) uses stick probes to enhance predation of lizards, carpenter bees, and other prey (Falótico & Ottoni, 2014), a behavior only known to be customary, so far, in this population, and that is of interest to understand the use of such tools for hunting. The probes at SCNP have a mean length of 27.9 cm and are made of tree branches and sticks (Falótico & Ottoni, 2014). Although some probes are used without modification, most (64%) are modified by the capuchins before or during the use (Falótico & Ottoni, 2014). The rate of probe tool use in SCNP is 0.27 event/h, and probes are almost only used by males (97%, Falótico & Ottoni, 2014).
I present 2 years of data on vertebrate predation and consumption by two groups of bearded capuchin monkeys in a dry savannah environment (Caatinga) in Brazil. I aim to describe the targets and frequency of predation, including events with tool use observed in these groups. I also explore differences between sex and age classes, and the occurrence of food sharing. If adult males can prey on larger prey than other age-sex classes, because they are larger, and if females require more stable resources than males do, to maintain pregnancy and lactation, I predict that adult males will have a higher predation rate than other age-sex classes. With regard to food sharing, if these capuchins follow the pattern of other capuchin populations, meat sharing will not be restricted to immatures and would support the information hypothesis for food sharing.

Data Collection
I and one field assistant followed the capuchin groups from contact (usually in the early morning, near where the monkeys stopped the day before) to dusk, or until we lost contact with the group. We tried to record all vertebrate predation events that occurred, including both when we observed a monkey capture the prey, and when we inferred capture because we saw a monkey eating a live or freshly dead vertebrate. The group was large and we could not see all individuals all the time, so our observations are ad libitum and may be biased towards more visible individuals, such as large adult males or bolder individuals.
For each event, we recorded: time and day, subject ID (and/or age and sex), type of prey (visually identifying species when possible), if a tool was used, if we observed capture, whether the prey was shared with group members, and if the sharing was passive (when the individual holding the food item allows others to pick up part of it) or active (individual holding the food item actively gives the food to others). We classified individuals as adults (> 5 years) or immatures (< 5 years, including juveniles and infants), based on body size and development for older individuals, or actual age for youngers.

Data analysis
I describe data as count of events and rate of events by contact time. I qualitatively analyse and compare the results by sex and age classes.

Results
Contact time with the two groups summed to 1711 hours (PF 1288 h, BC 423 h). We observed 78 predation events (Table I and Table SI), including 54 where we observed the monkey catch the prey, and 24 which we inferred by consumption of fresh whole prey.
The overall rate of predation was 4.6 events/100 h. PF group's rate was 4.9 events/100 h, and BC group's rate was 3.5 events/100 h. We recorded predation events in 18 of the 23 months of data collection, but we do not have sufficient data to test the seasonality of predation statistically.
We recorded the sex and age-class of the monkey in 72 predation events (in six events it was not possible to identify the sex of a juvenile). We identified 23 monkeys responsible for 49 of those events (Table SI). Most events were by adult and subadult males, followed by immature males, then adult and subadult female and immature females (Table II).
We observed passive sharing and scrounging of the carcass in nine events (12%). No active sharing was observed. The scroungers were mostly males (nine of ten individuals, 90%) and were equally immature and adults (five events each).
Lizards, including snakes, were the most common prey (54 of 78 events, 69%). The genus Tropidurus was one of the most frequent targets (Fig. 1a), and at least one endemic species from the SCNP region, T. helenae, was also preyed on. In some of the lizard predation events (four events, 7%) monkeys used probe tools to expel the prey from rock crevices (Falótico & Ottoni, 2014). Snake predation (seven events, 9%) was on non-dangerous snakes, mostly Colubridae.
Rodents were the third most preyed class (six events, 8%). Although most rodents were small, I observed an adult male hold, kill, and at least partially consume an adult rock cavy (Kerodon rupestris, Fig. 1c, d; video S1), with a body mass of around 1 kg (Lacher, 1979). In this case, we did not observe capture, but the prey was still alive when we noticed it.
Finally, I observed three events of consumption of bats (4% of events, Fig. 1b). All events took place within 20 m of rock shelter entrances, and the bats were still alive when we first saw the monkeys holding them. In two events, the first individual seen holding the prey consumed the bats. In the third event, an adult female examined the bat for approximately 4 minutes and dropped it. A juvenile male closely observing the female caught the discarded live prey and sprinted outside the researcher's view.

Discussion
Vertebrate predation is common in the bearded capuchin monkey groups I studied in a dry savannah ecosystem. The rate of predation of vertebrates by these capuchins living in savannah (4.6 events/100 h) was a similar rate to that for white-faced capuchins living in dry forest (3.66 events/100 h, Rose, 1997;4.7 events/100 h, Fedigan, 1990). Although they live in a drier environment than Cebus living in a forest, the Sapajus population did not prey on vertebrates at a higher rate, as would be expected in a drier environment, if lower food availability leads monkeys to search for food from less reliable sources, such as vertebrates. This result may also be because the drier environment provides less prey, but we do not know the prey availability in each environment to investigate. Adult males were the most common sex-age class observed preying on vertebrates, a result similar to those for other studies of capuchins and other primates (Butynski, 1982;Rose, 1997), although other groups of Cebus capuchins show no difference between males and females in the frequency of hunting for some vertebrate prey (Rose et al., 2003). I did not observe females hunting the larger rodent prey. My use of ad libitum sampling may have affected this result, as adult males are easier to spot and identify; however, I did record females hunting other vertebrate and non-vertebrate prey, indicating that the females were sampled. Adult male capuchins are 60% larger (or more) than females (Fragaszy et al., 2016) and their size may allow them to pursue and capture larger vertebrates more easily than females, as males would be better able to subdue larger prey. However, body size differences would probably not influence their hunting of small vertebrates, such as lizards, the main prey captured by capuchins in this study. Another explanation for the sex differences may be energetic balance. Although vertebrate prey is high-quality food, it is an inconsistent source. Females may not hunt as much as males if females need more stable food sources to increase their food intake during reproductive period (McCabe & Fedigan, 2007). Capuchin males are also bigger than females, and may hunt more because it provides an alternative high-energy food source required to maintain a larger body.
The prey types we observed are consistent with other studies of Sapajus (Canale et al., 2013;Fragaszy et al., 2004), showing that small lizards are common prey, usually captured on the ground when the monkeys are foraging in the leaf litter. We also observed capuchins catching bats, a rare behavior among primates (Tapanes et al., 2016). This is probably an opportunistic behavior, as the study groups live in valleys full of rock shelters and shallow caves that can increase the chance of encounters with bats.
Passive sharing of the meat was rare (12% of the events), mostly directed to males, and split equally between adults and immatures. Like previous studies on capuchins (Jaeggi & Gurven, 2013), my data support the information hypothesis about food transfer, as food sharing was not restricted to immatures. The food sharing among adult males also fits the pattern predicted when the food item is large or highly valuable and when possession is biased (Jaeggi & Schaik, 2011), and in a species with male-male coalitions such as in capuchins (Ferreira et al., 2006;Perry, 2012).
The use of probe tools to aid predation by dislodging the prey from their hiding place is a behavior observed, so far, only in this population of capuchin monkeys (Falótico & Ottoni, 2014;Ottoni & Izar, 2008). Probe tool use may enhance the chances of capturing prey, as it extends the monkeys' reach to places they cannot access with their hands, increasing the success of capturing a hidden prey. Most probe-tool use observed in predation events or attempts is aimed at small prey, such as lizards, carpenter bees, and scorpions (Falótico & Ottoni, 2014). However, I have observed the monkeys trying to dislodge larger prey, such as rock cavies (K. rupestris) from hiding places, using longer probes (maybe better described as spears, > 60 cm in length), although they were not successful (video S2). This behavior is similar to that of the Fongoli chimpanzees who use wooden spears to maim and capture bushbabies in trunk hollows (Pruetz et al., 2015;Pruetz & Bertolani, 2007). Another interesting parallel is that, like Fongoli chimpanzees, capuchin monkeys at SCNP also live in a dry savannah and are the only capuchin population known to customarily hunt vertebrates with the aid of tools.
The similarities between the capuchins we studied and the Fongoli chimpanzees may be related to the environment, which could be a necessary factor for the behavior to evolve. However, several study populations of Sapajus monkeys inhabiting similar environments have not been seen performing this behavior (Falótico, Coutinho, et al., 2018a;Ottoni & Izar, 2008), suggesting that probe use is a behavioral tradition in this study population (Haslam et al., 2018;Ottoni, 2021). Using stone tools to process encased resources is a typical behavior in Brazilian Sapajus living in the savannah biome (Ottoni & Izar, 2008). The stone tool use repertoire varies between populations and even neighboring groups in the food targets and processing style (Falótico, Coutinho, et al., 2018a;Falótico & Ottoni, 2013;Sirianni & Visalberghi, 2013). Probe tool use traditions in capuchin monkeys are much rarer than stone tool use. Although probe tool use has been occasionally or anecdotally reported in Sapajus groups (Souto et al., 2011) and individuals (Haslam & Falótico, 2015), the capuchin males at SCNP are the only known population to customarily use probes. This behavior has a learning sex bias, the females are less prone to observe and pay attention to other individuals probing with sticks (Falótico et al., 2021). The use of probes for aiding in the hunting of vertebrates, a behavior more frequently done by males, could be an additional explanation for the male bias in probe-tool use learning in the SCNP capuchin monkey population.
Predation on larger vertebrate prey (relative to their body size) with the occasional use of tools to aid predation, makes robust capuchins in this population a suitable platyrrhine model to understand the evolution of human behavior and an interesting comparison with Afro-Eurasian primate models of human evolution. This and other populations of Sapajus living in savannah environments are also highly terrestrial (Falótico, 2011;Fragaszy et al., 2004) and use stone tools (Falótico & Ottoni, 2016;Ottoni & Izar, 2008), adding to this suitability. Hunting using tools was crucial in human evolution (Domínguez-Rodrigo et al., 2005;Pickering & Dominguez-Rodrigo, 2010), although the accepted evidence of increased carnivory after the appearance of Homo erectus has been recently questioned (Barr et al., 2022). Studying primates that present similar traits which evolved independently is a promising way to understand better the evolutionary factors involved.