When foraging in their natural environments, animals need to recognize and respond to changes in food targets. This ability is especially useful when dealing with a defensive mechanism of the target food (e.g., toxicity, venom, irritants) where risk of injury represents an important cost for the forager1. Several animal species have evolved foraging strategies to minimize those potential risks involved when dealing with dangerous prey. For example, meerkats (Suricata suricatta) are able to effectively disarm scorpions to reduce the threat of injury to younger group members2. Some animals also use foraging strategies that include objects to reduce or prevent the risk of injury involved in consuming challenging food sources. Bottlenose dolphins (Tursiops sp.), for example, use detached marine sponges over their nose to nuzzle for prey in rocky sea grounds3. Primates have especially been shown to exhibit a variety of solutions as a response to dealing with the defense mechanisms of harmful target foods. White-faced capuchins (Cebus capucinus) wrap naturally-defended caterpillars and fruits in leaves before rubbing them against a substrate, which is suggested to be a means of avoiding noxious substances4. Chimpanzees (Pan troglodytes) foraging on aggressive army ant nests use nearby trees to reposition themselves off the ground, from where they can more securely dip for the ants below5. Similarly, chimpanzees are able to minimize risk to accompanying young by predating on aggressive army ants on ant trails rather than at the ant nests, even though feeding at nests yields a higher rate of energetic return6. Different solutions to minimize painful bites when preying on army ants, including stick tool use, are described for multiple chimpanzee populations throughout Africa6,7. The observed diversity suggests that hazard avoidance may be a socially influenced response8.

Animal tool use increases net gain by enabling the exploitation of inaccessible or costly to process food resources. This allows access to higher nutritional value foods9,10, an adaptive advantage in times of food scarcity11,12, competition13, or opportunistic foraging14. Tool size, weight and required transport distance influence the amount of energy expended during a given task15,16,17. To maintain the balance between cost and gain, individuals must recognize and manage energy expenditure relative to the task at hand. This requires a comprehension of the functional aspects of the food item, its physical constraints and potential risks involved.

Selectivity in the physical properties of tools has been observed amongst different primate species18,19,20 as well as corvids21. Wild chimpanzees adjust their tool selection to changing properties within one target food22,23,24. For example, with increasing ripeness of Coula edulis nuts within one fruiting season the nuts become easier to crack and chimpanzees adjust their tool selection accordingly. Neighboring chimpanzee communities that live in similar environmental conditions however react differently to changes in the target food. This indicates that responses to changing food items are socially learned22,24. Reports on wild capuchin monkeys (genera Cebus and Sapajus) suggest that they are capable of both hazard reduction and adjustment of their behaviour to match food properties4,25. When foraging for embedded larvae (S. apella) capuchins are able to distinguish between pay-off rates between two stages of the same foraging substrates26. Bearded capuchins (Sapajus libidinosus) have been observed modifying the force - although not the stone tool - throughout the sequence of cracking a single nut as a response to the state of the nut27. The same monkeys selected different stone tool sizes based on the resistance of different nut species. It is important to note that no primate studies to date have been able to determine whether a wild animal considers two states of the same food species (e.g., fresh or dry nuts, intact or partially-opened nuts) to be two different foods. Instead, these studies concentrate on animal behaviour towards the differing food targets, and we follow the same approach here.

Capuchins in Serra da Capivara National Park (SCNP) are known to exhibit a range of tool using behaviour, including different stick and stone tools for foraging, social display and self-maintenance12,28,29,30,31. They habitually use stone tools to crack open cashew (Anacardium spp.) nuts, which are native to the northeastern part of Brazil32. Cashew trees produce a pseudo-fruit in the form of an apple and a hard nut at the end of the apple which holds the reproductive seed25. The shell of unprocessed cashew nuts contains caustic Cashew Nut Shell Liquid (CNSL), a phenolic resin (similar to poison ivy or poison oak), which causes severe reactions when in contact with the skin and mucosa. We focused on capuchin processing of cashew nuts because, as cashews ripen, they appeared to change in both nut hardness and in the amount of CNSL in the nut mesocarp.

At SCNP, capuchin monkeys use stone tools to open all maturity stages of cashew nuts. Average weight of tools used by the monkeys to open cashews was greater than the average of available stones in the area, indicating a selecting behaviour32. On average, males use stone tools more frequently than females to process cashew nuts (70% of the episodes), due to the larger body size of males this is a common pattern in capuchins populations33,34,35. There is no difference in the weight, size and success of stone tool use between sexes at SCNP, however juveniles are less successful than adults in opening cashews32. Even though fresh cashew nuts are on average 25% larger than dry ones, tools are not necessary to open fresh nuts as the outer mesocarp is still soft. Some monkeys in SCNP have been observed to bite and rip open fresh cashews using their hands and teeth. However, adult group members usually used stone tools to open both fresh and dry cashew nuts, before extracting the cashew kernel with either fingers or teeth.

Our focus on tool-based processing of this potentially hazardous foraging item is of additional interest, as a different capuchin group of the same species at the Fazenda Boa Vista (FBV) site, approximately 350 km away from Serra da Capivara, specifically avoids contact with CNSL when eating cashew nuts25,36. At FBV the monkeys have never been seen using stone tools to open fresh cashews nuts. Instead they use a rubbing technique which allows them to extract the kernel using their fingers to avoid contact with the CNSL25,36. The FBV capuchins use stone tools only to process dry nuts towards the end of the fruiting season, when the toxic CNSL hardens into a more resinous material that is less likely to come into contact with the monkey’s skin.

Based on previous studies, we hypothesized that wild capuchin monkeys would adapt their tool selection when processing a food item that changes its condition over time. To test this hypothesis, we carried out field experiments with a group of wild bearded capuchins in Serra da Capivara National Park (SCNP), northeast Brazil.

As part of this study, we predicted (Table 1) that cashew nuts would increase in hardness as they dry and mature, which would require a correspondingly greater force from the monkeys to open dry nuts. We tested cashew nut hardness of different maturity stages using a standardized nut cracking device. We also expected to find that fresh cashew nuts contain more easily dispersed CSNL than dry nuts, as it is in a more liquid form in this earlier maturation stage. We therefore compared exposed CSNL between the different cashew maturation stages. The capuchins were therefore expected to use fewer strikes to open a nut when using heavier stones, and were expected to use heavier stones to open dry (harder) nuts.