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Leaves of Ficus asperifolia (actual size). Top: mature leaf, edge adorned with spines (see text for further description). Bottom: remaining lower section of leaf, with tough petiole and midrib, after consumption of the blade tip by a chimpanzee
Source publication
The manual processing of eight species of leaf was investigated in the M-group chimpanzees of Mahale Mountains National Park, Tanzania. Leaf species varied in the extent to which physical defences made consumption difficult. In all, 96 distinct techniques for leaf processing were identified, but two species with defended leaves (Ficus asperifolia a...
Contexts in source publication
Context 1
... Ficus asperifolia Miq. (Moraceae) (F. urceolaris Welw. ex Hiern) shrub or tree growing up to 5 m with medium-sized leaves (ca. 75-180 mm  25-50 mm), with rough hair on upper and lower surfaces, tough petioles, and an edge adorned with numerous spines. These form prominent teeth, which point up, out and away from the proximal end of the leaf (see Fig. 1). As the leaves mature, the spikes become more rigid and hence a more effective defence. The hairy leaf surface is also a potential deterrent to consumption. (Recorded eaten by adults or juveniles on 20.0% of field ...
Context 2
... underside of the (outer) leaf was presented to the mouth, when this could not be managed by adjusting the position of the branch the leaf itself was rotated, which required bimanual role differentiation (Elliott and Connolly 1974;Byrne et al. 2001a). The leaves were then ripped from their natural attachment often leaving behind the petiole (see Fig. 1). Frequently, this process was iterated with a series of leaves before the resulting bundle was processed further. If petioles were still attached, they were then either detached, or the leaf blade folded over with the lips to envelop the petioles as the leaves were swallowed. Bundles of older leaves were treated the same way -detached ...
Citations
... mulatta; Macfarlane & Graziano, 2009) and more recently in capuchin monkeys (Sapajus libidinosus and Sapajus spp.; Jones & Fragaszy, 2020). Besides, as pointed out by Jones and Fragaszy (2020), descriptions of this grasping ability have been also reported in great apes such as gorillas (Byrne et al., 2001) and chimpanzees (Boesch & Boesch, 1993;Corp & Byrne, 2002;Marzke et al., 2015), although it was not specifically identified as a compound grip. Our systematic observations confirmed and expanded the first description reported by Dunbar (1977). ...
We assessed whether wild geladas, highly specialized terrestrial grass eaters, are lateralized for bimanual grass‐plucking behavior. According to the literature, we expected that complex motor movements in grass feeding would favor the emergence of a population‐level hand bias in these primates. In addition, we described geladas' manual behavior based on systematic observations of several individuals. Our study group included 28 individuals belonging to a population of free‐ranging geladas frequenting the Kundi plateau, Ethiopia. We filmed monkeys while feeding on grass, and hand preference and performance were coded. Geladas performed more plucking movements per second with their left hand (LH) compared to the right one and preferred their LH both to start and finish collection bouts. Also, the rhythmic movements of each hand had a significant tendency toward isochrony. Finally, geladas used forceful pad‐to‐pad precision grips, in‐hand movements, and compound grips to pluck and collect grass blades, considered the most advanced manual skills in primate species. The LH's leading role suggests an advantage of the right hemisphere in regulating geladas' bimanual grass‐feeding behavior. The tactile input from the hands and/or rhythmic hand movements might contribute to explaining this pattern of laterality. Our findings highlighted the importance of adopting multiple laterality measures to investigate manual laterality. Moreover, the need to speed up the execution time of manual foraging might be a further important factor in studying the evolution of manual laterality and dexterity in primates.
... Studies from wild primate groups provide equivocal support for the need to learn hypothesis, with juvenile primates in many species adopting adult dietary profiles or become competent at adult feeding strategies well before they achieve adult body size or sexual maturity (Eulemur fulvus: Tarnaud, 2004; Gorilla spp.: Nowell & Fletcher, 2008;Watts, 1985;Lemur catta: O'Mara, 2015; Pan troglodytes: Bray, Emery Thompson, Muller, Wrangham, & Machanda, 2018;Musgrave, Lonsdorf, Morgan, & Sanz, 2021; Pongo spp.: Schuppli et al., 2016;van Adrichem, Utami, Wich, van Hooff, & Sterck, 2006; Saimiri spp.: Boinski & Fragaszy, 1989;Stone, 2006). However, in species that engage in extractive feeding, observational and comparative research has shown that improvements in food processing competency develop slowly for many embedded foods (e.g., Corp & Byrne, 2002;Krakauer, 2005;Johnson & Bock, 2004;Schuppli, Isler, & van Schaik, 2012). ...
Objectives
Capuchin monkeys ( Cebus spp. and Sapajus spp.) routinely extract food resources that are embedded in protective matrices. Features such as relative brain size, manual dexterity, and — in the case of Sapajus spp .— a robust feeding system are considered adaptations for accessing embedded foods. Compared with adults, juvenile capuchins exhibit reduced food processing efficiency when processing embedded foods. Although this reduced efficiency has been attributed to inexperience or lack of strength when processing embedded foods, little is known about how food material properties (FMPs) relate to age‐related changes in feeding efficiency.
Materials and methods
We used data collected from three groups of Sapajus libidinosus to test relationships between feeding efficiency and FMP variation when processing embedded and nonembedded foods. Feeding efficiency was defined in three ways: (i) duration, (ii) frequency, and (iii) variation in sequence of food processing behaviors.
Results
We found limited support for an effect of FMPs and age on feeding sequence durations or on processing behavior frequency. Number of unique behavioral patterns was negatively correlated with age. Embedded foods elicited longer durations, higher behavioral frequencies and more unique behaviors compared to nonembedded foods.
Discussion
Results indicate FMP variation impedes some measures of juvenile food processing efficiency. Foods with high stress‐limited indices reduced some measures of processing efficiency in juveniles. These data are consistent with prior studies of juvenile capuchin feeding competency when exploiting embedded foods and suggest skill development may be a relatively more important constraint for overall juvenile feeding efficiency than body size or strength.
... informational hypothesis has been found in great apes 9,20,21 ; food transfer seems to directly affect knowledge acquisition among immatures in the foraging context 2,8,22 . For instance, food solicitation and transfer ceases prior to weaning in chimpanzees 23,24 and immature orangutans mostly solicit items that are difficult to process by themselves 8 . ...
... Taken together, the results of our study suggest that the primary function of food transfer from parents to infants in wild Javan gibbons seems to support the information hypothesis similar to what has been found in great apes 5,21,24,68 . As suggested in other studies, food transfer can potentially facilitate the information transfer about food processing skills and knowledge on diets 6,69,70 . ...
The adaptive functions of food transfer from parents to their offspring have been explained mainly by two mutually non-exclusive hypotheses: the nutritional and informational hypotheses. In this study, we examined the functions of food transfer in wild Javan gibbons (Hylobates moloch) by testing these hypotheses from both infants’ and mothers’ perspectives. We observed 83 cases of food solicitations that resulted in 54 occasions of food transfers in three groups over a 19-month period in Gunung Halimun-Salak National Park, Indonesia. Infants initiated all solicitations directed at their mothers with one solicitation towards a father. Food solicitation rate decreased as infant age increased and ceased before weaning. As predicted by the informational hypothesis, infants solicited more food items difficult to obtain and preferred by their parents. On the contrary to the nutritional hypothesis, infants solicited low-quality items more often than high-quality items. Mothers did not change probability of food transfer according to the food characteristics or infant age. Hence, our results suggest that the primary function of food transfer from mother to infant Javan gibbons seems to be information transfer rather than nutritional aids, similarly to great apes.
... Although anthropological interest has always focused on the tools chimpanzees make and use, the manner in which they construct and employ tools is very similar to gorilla plant feeding in its structural complexity (Byrne, 2001(Byrne, , 2016. Chimpanzees, when eating certain plant foods, show similar characteristics to mountain gorillas (Byrne, Corp, & Byrne, 2001;Corp & Byrne, 2002;Stokes & Byrne, 2001), but it is in gaining access to insects that they more commonly employ elaborate, hierarchically embedded programs of actionand it is those tasks that involve tools. Both species show very strong behavioral laterality for these skilful tasks, but not in other, less complex aspects of their manual behavior. ...
Where did our intelligence come from? That is, what evolutionary drivers caused such specialization in cognition among humans? Only by adopting a comparative approach, considering the brains and cognitive skills of other animal species, can we discover how, when, and even perhaps why human intellectual skills evolved. Here we apply a process of evolutionary reconstruction to ancestors we share with other species, from the earliest primates at 74 Ma (million years ago) to the relatively recent ancestor shared with chimpanzees. Doing so highlights the importance of both social and ecological (nutritional) pressures in evolving intellect. Complex sociality was supported by increased perception, learning, and memory skills, long before the development of any ability to understand other beings as causal agents with independent minds. The latter, we argue, was driven by a need to feed more efficiently in ancestors we share with all living great apes.
... Such an ordered and coordinated flow is also present in stem-and leafprocessing behaviours by Virunga gorillas (Byrne & Byrne, 1993). A similar structural organization in the manipulative behaviours to process plant foods with physical defences has also been documented in wild chimpanzees (Pan troglodytes schweinfurthii) and long-tailed macaques (Macaca fascicularis) (Byrne & Stokes, 2001;Corp & Byrne, 2002;Tan et al., 2016). Byrne et al. (2001a, b) described the processing of thistle stem as consisting of four key stages: (1) initial procurement of the stem, (2) support of the stem, (3) detachment of stem item and (4) insertion of the stem into the mouth. ...
Although gorillas rarely use tools in the wild, their manipulative skills during plant processing may be similar to those of other tool-using great apes. Virunga mountain gorillas (Gorilla beringei beringei) are known for the complexity in their methods of thistle and nettle plant preparation in the wild. However, there are no comparable data on food processing in the population of mountain gorillas from the Bwindi Impenetrable National Park, Uganda. We investigated the manual actions and hand grips used when accessing edible parts of two hard-to-process plants defended by stinging hairs, epidermis or periderm (i.e. peel of Urera hypselodendron and pith of Mimulopsis arborescens), and one undefended plant (i.e. leaves of Momordica foetida) in 11 Bwindi wild mountain gorillas using video records ad libitum. Similar to thistle feeding by Virunga gorillas, Bwindi gorillas used the greatest number of manual actions for the most hard-to-process plant (U. hypselodendron), and the actions were ordered in several key stages and organized hierarchically. The demands of processing plant material elicited 19 different grips and variable thumb postures, of which three grips were new and 16 grips have either been previously reported or show clear similarities to grips used by other wild and captive African apes and by humans. Moreover, our study only partly supports a functional link between diet and hand morphology in mountain gorillas and suggests that the gorilla hand is best adapted to forceful grasping that is required for both manipulation and arboreal locomotion.
... Such an ordered and coordinated flow is also present in stem-and leafprocessing behaviours by Virunga gorillas (Byrne & Byrne, 1993). A similar structural organization in the manipulative behaviours to process plant foods with physical defences has also been documented in wild chimpanzees (Pan troglodytes schweinfurthii) and long-tailed macaques (Macaca fascicularis) (Byrne & Stokes, 2001;Corp & Byrne, 2002;Tan et al., 2016). Byrne et al. (2001a, b) described the processing of thistle stem as consisting of four key stages: (1) initial procurement of the stem, (2) support of the stem, (3) detachment of stem item and (4) insertion of the stem into the mouth. ...
Although gorillas rarely use tools in the wild, their manipulative skills during plant processing may be similar to those of other tool-using great apes. Virunga mountain gorillas (Gorilla beringei beringei) are known for the complexity in their methods of thistle and nettle plant preparation in the wild. However, there are no comparable data on food processing in the population of mountain gorillas from the Bwindi Impenetrable National Park, Uganda. We investigated the manual actions and hand grips used when accessing edible parts of two hard-to-process plants defended by stinging hairs, epidermis or periderm (i.e. peel of Urera hypselodendron and pith of Mimulopsis arborescens), and one undefended plant (i.e. leaves of Momordica foetida) in 11 Bwindi wild mountain gorillas using video records ad libitum. Similar to thistle feeding by Virunga gorillas, Bwindi gorillas used the greatest number of manual actions for the most hard-to-process plant (U. hypselodendron), and the actions were ordered in several key stages and organized hierarchically. The demands of processing plant material elicited 19 different grips and variable thumb postures, of which three grips were new and 16 grips have either been previously reported or show clear similarities to grips used by other wild and captive African apes and by humans. Moreover, our study only partly supports a functional link between diet and hand morphology in mountain gorillas and suggests that the gorilla hand is best adapted to forceful grasping that is required for both manipulation and arboreal locomotion. ADDITIONAL KEYWORDS: dexterity-feeding skill-gorillas-great ape-manipulative behaviour-precision grip-thumb.
... All diameters were measured to the nearest cm using a metric diameter tape. Detailed measurements of nest architecture were recorded by taking the nest to pieces and recording each step in reverse construction sequence, in order quantify all likely manipulative steps (sensu Corp & Byrne, 2002). For each building-step the type of material (grass, liana, shrub, or tree), type of manipulation (bend, <50% broken; break, >50% broken; or detach), and branch diameter (measured at the inside of the bend/break) was recorded. ...
... Such an ordered and coordinated flow is also present in stem-and leafprocessing behaviours by Virunga gorillas (Byrne & Byrne, 1993). A similar structural organization in the manipulative behaviours to process plant foods with physical defences has also been documented in wild chimpanzees (Pan troglodytes schweinfurthii) and long-tailed macaques (Macaca fascicularis) (Byrne & Stokes, 2001;Corp & Byrne, 2002;Tan et al., 2016). Byrne et al. (2001a, b) described the processing of thistle stem as consisting of four key stages: (1) initial procurement of the stem, (2) support of the stem, (3) detachment of stem item and (4) insertion of the stem into the mouth. ...
... Regardless, these subjects showed the morpho-functional capability required to perform the task. The manipulative abilities of some primates (primarily great apes, capuchin monkeys and macaques) have been studied for decades (e.g., Byrne et al., 2001;Corp & Byrne, 2002;Macfarlane & Graziano, 2009;Parker & Gibson, 1977;Torigoe, 1985Torigoe, , 1987) and compared directly with humans performing both simple tasks like reaching (Christel, 1993;Lacreuse & Fragaszy, 1997;Pouydebat et al., 2009Pouydebat et al., , 2011) and more complex routine tasks (Heldstab et al., 2016). However, as far as we know, no experiment in captivity has compared manual abilities during the same complex tool use task. ...
... Dynamic aspects of manual function have been described in humans (Braido & Zhang, 2004;Bullock & Dollar, 2011;Exner, 1992;Santello, Flanders, & Soechting, 1998) and a detailed taxonomy of the various forms of inhand movements is available (Elliot & Connolly, 1984). In contrast, inhand manipulation studies among non-human primates are scarce and have been investigated mainly in chimpanzees (Boesch & Boesch, 1993;Marzke & Wullstein, 1996;Corp & Byrne, 2002;Crast et al., 2009;Marzke, Marchant, McGrew, & Reece, 2015). Other primates such as gorillas (Gorilla sp.; Byrne et al., 2001), bonobos (Pan paniscus; , and capuchin monkeys (Crast, 2006) have been the focus of even fewer studies, and orangutans' (Pongo sp.) in-hand movements have been almost entirely ignored. ...
Objectives:
Humans are known to possess more complex manual abilities than other primates. However, the manual abilities of primates have not been fully explored, and we still do not know if the manipulative abilities we attribute to humans are unique. The aim of this study was to compare the manual function and performance developed by humans, gorillas and orangutans while performing the same experimental tool use task.
Materials and methods:
The study was conducted on 20 humans, 6 gorillas, and 7 orangutans. Each individual had to use a tool to collect food from a maze during six experimental sessions while maintaining the same unconstrained body posture condition. We quantified the different manual techniques used and the manual performance.
Results:
Each species used different techniques. Humans used bimanual grip techniques, pad-to-pad precision grasping postures, and in-hand movements involving fingertips. Gorillas used unimanual grip techniques and simple in-hand movements while orangutans used a variety of strategies (e.g., hand or mouth). With these techniques, humans performed the task better than both gorillas and orangutans (e.g., by being quicker to collect the food).
Discussion:
This study highlights other ways in which humans' manual dexterity differs from that of other species and emphasizes the distinct manipulative function of orangutans. The differences between the species could be due to the differing muscular anatomy and morphology of the hands, with hand proportion possibly placing particular biomechanical constraints on each species. The differences between gorillas and orangutans could result from their different locomotor behaviors, and we hypothesize terrestriality facilitates the development of complex manipulation.
... Although mothers and their late infants exhibited differences in their daily diet breadth (driven by fewer fibrous foods in the infant diet), a complete adult diet breadth was acquired during juvenility. This delay is unlikely to be accounted for by learning since fibrous foods, particularly young leaves and pith, are typically cognitively simple to acquire (Gibson, 1986;Milton, 1981a; but see Byrne & Byrne, 1993;Corp & Byrne, 2002). Instead, delays in dental development Smith et al., 2013), which restrict an individual's ability to efficiently chew fibrous foods, better explain both this pattern and the greater emphasis on young leaves over pith in the first year of life. ...
Objectives:
Primates have an extended period of juvenility before adulthood. Although dietary complexity plays a prominent role in hypotheses regarding the evolution of extended juvenility, the development of feeding behavior is still poorly understood. Indeed, few studies have investigated the timing and nature of feeding transitions in apes, including chimpanzees. We describe general patterns of feeding development in wild chimpanzees and evaluate predictions of the needing-to-learn hypothesis.
Materials and methods:
We analyzed 4 years of behavioral data (2010-2013) from 26 immature chimpanzees and 31 adult chimpanzees of the Kanyawara community in Kibale National Park, Uganda. Specifically, we examined milestones of nutritional independence (first consumption of solid food and cessation of suckling) as well as developmental changes in feeding time, diet composition, diet breadth, and ingestion rates.
Results:
Chimpanzees first fed on solid food at 5.1 months and, on average, suckled until 4.8 years. Daily feeding time of immature individuals reached adult levels between 4 and 6 years, while diet composition showed minor changes with age. By juvenility (5-10 years), individuals had a complete adult diet breadth. Ingestion rates for five ripe fruit species remained below adult levels until juvenility but continued to show absolute increases into adolescence.
Discussion:
Chimpanzees acquired adult-like patterns on all feeding measures by infancy or juvenility. These data are inconsistent with the needing-to-learn hypothesis; moreover, where delays exist, alternatives hypotheses make similar predictions but implicate physical constraints rather than learning as causal factors. We outline predictions for how future studies might distinguish between hypotheses for the evolution of extended juvenility.
