How does stone-tool use emerge? Introduction of stones and nuts to naïve chimpanzees in captivity

Nut-cracking behavior has been reported in several communities in West Africa but not in East and Central Africa. Furthermore, even within nut-cracking communities, there are individuals who do not acquire the skill. The present study aimed to clarify the cognitive capability required for nut-cracking behavior and the process through which the the nut-cracking behavior emerges. To examine emergence, we provided three naïve adult chimpanzees with a single opportunity to observe human models. A human tester demonstrated nut-cracking behavior using a pair of stones and then supplied stones and nuts to the chimpanzee subjects. Two out of three chimpanzees proceeded to hit a nut on an anvil stone using a hammer stone, one of whom succeeded in cracking open the nuts during the first test session. The third chimpanzee failed to crack open nuts. We used four variables (object, location, body part used, and action) to describe stone/nut manipulation in order to analyze further the patterns of object manipulation exhibited by the subjects. The analysis revealed that there were three main difficulties associated with nut-cracking behavior. (1) The chimpanzee who failed at the task never showed hitting action. (2) The chimpanzee who failed at the task manipulated nuts but rarely stones. (3) The combination of three objects was not commonly observed in the three chimpanzees. We also discuss our results with reference to the effect of enculturation in captivity and the social context of learning in the wild.     

Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools

We conducted an exploratory investigation in an area where nut-cracking by wild capuchin monkeys is common knowledge among local residents. In addition to observing male and female capuchin monkeys using stones to pound open nuts on stone "anvils," we surveyed the surrounding area and found physical evidence that monkeys cracked nuts on rock outcrops, boulders, and logs (collectively termed anvils). Anvils, which were identified by numerous shallow depressions on the upper surface, the presence of palm shells and debris, and the presence of loose stones of an appropriate size to pound nuts, were present even on the tops of mesas. The stones used to crack nuts can weigh >1 kg, and are remarkably heavy for monkeys that weigh <4 kg. The abundance of shell remains and depressions in the anvil surface at numerous anvil sites indicate that nut-cracking activity is common and long-enduring. Many of the stones found on anvils (presumably used to pound nuts) are river pebbles that are not present in the local area we surveyed (except on or near the anvils); therefore, we surmise that they were transported to the anvil sites. Ecologically and behaviorally, nut-cracking by capuchins appears to have strong parallels to nut-cracking by wild chimpanzees. The presence of abundant anvil sites, limited alternative food resources, abundance of palms, and the habit of the palms in this region to produce fruit at ground level all likely contribute to the monkeys' routine exploitation of palm nuts via cracking them with stones. This discovery provides a new reference point for discussions regarding the evolution of tool use and material culture in primates. Routine tool use to exploit keystone food resources is not restricted to living great apes and ancestral hominids.     

Nut predation and dispersal of Harland Tanoak Lithocarpus harlandii by scatter-hoarding rodents

Plants that use the propagule to co-opt animals as dispersal agents must balance the costs of seed predation with the benefits of dispersal. Successful post-dispersal germination is a key metric that reflects these costs and benefits. By tracking individual nuts with coded tin-tags over 3 years (2000–2003), this study quantified nut predation and dispersal of harland tanoak (Lithocarpus harlandii) by seed-caching rodents in a subtropical evergreen broadleaved forest in the Duiangyan Region of Sichuan Province, Southwest China. We found that tanoak seedlings established from rodent-generated caches in the primary stands over a 12-month post-dispersal period. Our results indicate that seed-caching rodents are effective dispersers of tanoak nuts, but dispersal effectiveness varies among years and stands, probably due to mast seeding of harland tanoak or community-level seed availability according to the predator satiation hypothesis. Some nut traits in tanoak species, e.g. large seed size, hard nut husk, lower tannin and mast seeding, are important characteristics for seed dispersal by scatter-hoarding rodents, compared with oak species with higher tannin content.     

Impact of human foraging on tree diversity,composition, and abundance in a tropical rainforest

Tropical forest tree communities are structured by a range of large-scale drivers including elevation, certain high-impact anthropogenic activities (e.g., deforestation), and fires. However, low-impact human activities such as foraging may also be subtly but notably altering the composition of tropical forest tree communities. The study assessed the (i) differences in species diversity, patterns of relative abundance, and pairwise beta diversity between trees with edible and inedible fruits and seeds along an elevation gradient, and (ii) impact of human foraging on the forest tree communities in Oban Division of Cross River National Park, Nigeria. Fifteen permanent 40 by 40 m plots were established along an elevational gradient (120–460 m above mean sea level). All trees of 0.1 m diameter at breast height (dbh) and above were measured, identified, and, with the aid of structured questionnaires, classified into those with edible and inedible fruits/seeds. A total of 35 edible species with density of 128 stems/hectare and basal area of 11.99 m²/hectare, and 109 inedible species with density of 364 stems/hectare and basal area of 22.42 m²/hectare were sampled. However, the evenness of edible and inedible species was similar at pooled and plot levels. For inedible species, there was a positive relationship between pairwise beta diversity and elevation, and this was driven mainly by turnover. In contrast, edible species exhibited a non-significant trend between elevation and beta diversity. Thus, the study showed that human foraging of edible fruits may have subtly influenced patterns of species diversity and community structure in this tropical forest.     

Substrate optimization in nut cracking by capuchin monkeys (Cebus apella)

We conducted an experiment to examine the effect of substrate on the nut-cracking behavior of a group of semicaptive capuchin monkeys. We wanted to determine whether tufted capuchin monkeys were selective in choosing the substrate on which they pound nuts, and whether the choice of substrate affected the outcome. Eight adult females and eight juveniles were provided with nuts in the outdoor facility. We found that 1) all adult females and three young capuchins succeeded in cracking nuts; 2) they preferred the hardest substrates (concrete and stone); 3) there is a link between the substrate and the amount of time needed to crack a nut; 4) most young capuchins used various substrates, some of which were inadequate, in a haphazard manner; and 5) there are different forms of nut cracking. We conclude that adult capuchins choose the hardest substrates, and that these substrates support efficient cracking.     

Ricinodendron rautanenii (Euphorbiaceae): Zambezian wild food plant for all seasons

Ricinodendron rautanenii provides an easily stored sweet-tasting fruit containing a nut whose seed is rich in fat, protein, and minerals. Its distribution is largely confined to the Zambezian phytogeographical region of Africa, centered on the nutrient- poor Kalahari sands of southeastern Angola and northeastern Namibia. There the estimates of annual nut production range from ca. 250 kg/ha to 800 kg/ ha. In this subhumid summer-rain climate this tree flowers in late spring and the fruits fall in autumn. A significant proportion of the nuts are still edible after having lain on the ground for a year. The nuts were traditionally a staple food for the subregion’s rural populations.     

Sooty mangabeys scavenge on nuts cracked by chimpanzees and red river hogs—An investigation of inter‐specific interactions around tropical nut trees

Carrion scavenging is a well‐studied phenomenon, but virtually nothing is known about scavenging on plant material, especially on remnants of cracked nuts. Just like meat, the insides of hard‐shelled nuts are high in energetic value, and both foods are difficult to acquire. In the Taï forest, chimpanzees (Pan troglodytes) and red river hogs (Potamochoerus porcus) crack nuts by using tools or strong jaws, respectively. In this study, previously collected non‐invasive camera trap data were used to investigate scavenging by sooty mangabeys (Cercocebus atys), two species of Guinea fowl (Agelestres meleagrides; Guttera verreauxi), and squirrels (Scrunidae spp.) on the nut remnants cracked by chimpanzees and red river hogs. We investigated how scavengers located nut remnants, by analyzing their visiting behavior in relation to known nut‐cracking events. Furthermore, since mangabeys are infrequently preyed upon by chimpanzees, we investigated whether they perceive an increase in predation risk when approaching nut remnants. In total, 190 nut‐cracking events were observed in four different areas of Taï National Park, Ivory Coast. We could confirm that mangabeys scavenged on the nuts cracked by chimpanzees and hogs and that this enabled them to access food source that would not be accessible otherwise. We furthermore found that mangabeys, but not the other species, were more likely to visit nut‐cracking sites after nut‐cracking activities than before, and discuss the potential strategies that the monkeys could have used to locate nut remnants. In addition, mangabeys showed elevated levels of vigilance at the chimpanzee nut‐cracking sites compared with other foraging sites, suggesting that they perceived elevated danger at these sites. Scavenging on remnants of cracked nuts is a hitherto understudied type of foraging behavior that could be widespread in nature and increases the complexity of community ecology in tropical rainforests.     

Physical properties of palm fruits processed with tools by wild bearded capuchins (Cebus libidinosus)

Habitually, capuchin monkeys access encased hard foods by using their canines and premolars and/or by pounding the food on hard surfaces. Instead, the wild bearded capuchins (Cebus libidinosus) of Boa Vista (Brazil) routinely crack palm fruits with tools. We measured size, weight, structure, and peak-force-at-failure of the four palm fruit species most frequently processed with tools by wild capuchin monkeys living in Boa Vista. Moreover, for each nut species we identify whether peak-force-at-failure was consistently associated with greater weight/volume, endocarp thickness, and structural complexity. The goals of this study were (a) to investigate whether these palm fruits are difficult, or impossible, to access other than with tools and (b) to collect data on the physical properties of palm fruits that are comparable to those available for the nuts cracked open with tools by wild chimpanzees. Results showed that the four nut species differ in terms of peak-force-at-failure and that peak-force-at-failure is positively associated with greater weight (and consequently volume) and apparently with structural complexity (i.e. more kernels and thus more partitions); finally for three out of four nut species shell thickness is also positively associated with greater volume. The finding that the nuts exploited by capuchins with tools have very high resistance values support the idea that tool use is indeed mandatory to crack them open. Finally, the peak-force-at-failure of the piassava nuts is similar to that reported for the very tough panda nuts cracked open by wild chimpanzees; this highlights the ecological importance of tool use for exploiting high resistance foods in this capuchin species.     

Diet of the northern bearded saki (Chiropotes satanas chiropotes): A neotropical seed predator

Data on the diet of Chiropotes satanas chiropotes, the northern bearded saki, has been collected during several years of primate field observations in the Raleighvallen-Voltzberg Reserve in Suriname. This species feeds predominantly on immature seeds and ripe fruit, mainly the former. Chiropotes is especially fond of the members of the Brazil nut family, Lecythidaceae, and other species with exceptionally hard or tough seed pods. Concomitantly, Chiropotes shows striking dental and gnathic adaptations that facilitate opening and ingesting these well-protected food items. Seed predation in the Old World colobine, Colobus satanas, has been discussed primarily as a strategy for survival in forests characterized by leaves with low nutrient content and high toxicity; however, it now appears that arboreal seed predation is a relatively widespread primate dietary strategy found among higher primate species in a variety of forest types on three continents. It is yet another way of “making a living” in a tropical rain forest.     

The evolutionary ecology of nut dispersal

A variety of nut-producing plants have mutualistic seed-dispersal interactions with animals (rodents and corvids) that scatter hoard their nuts in the soil. The goals of this review are to summarize the widespread horticultural, botanical, and ecological literature pertaining to nut dispersal inJuglans, Carya, Quercus, Fagus, Castanae, Castanopsis, Lithocarpus, Corylus, Aesculus, andPrunus; to examine the evolutionary histories of these mutualistic interactions; and to identify the traits of nut-bearing plants and nut-dispersing rodents and jays that influence the success of the mutualism. These interactions appear to have originated as early as the Paleocene, about 60 million years ago. Most nuts appear to have evolved from ancestors with wind-dispersed seeds, but the ancestral form of dispersal in almonds (Prunus spp.) was by frugivorous animals that ingested fruit. Nut-producing species have evolved a number of traits that facilitate nut dispersal by certain rodents and corvids while serving to exclude other animals that act as parasites of the mutualism. Nuts are nutritious food sources, often with high levels of lipids or proteins and a caloric value ranging from 5.7 to 153.5 kJ per propagule, 10–1000 times greater than most wind-dispersed seeds. These traits make nuts highly attractive food items for dispersers and nut predators. The course of nut development tends to reduce losses of nuts to insects, microbes, and nondispersing animals, but despite these measures predispersal and postdispersal nut mortality is generally high. Chemical defenses (e.g., tannins) in the cotyledons or the husk surrounding the nut discourage some nut predators. Masting of nuts (periodic, synchronous production of large nut crops) appears to reduce losses to insects and to increase the number of nuts dispersed by animals, and it may increase cross-pollination. Scatter hoarding by rodents and corvids removes nuts from other sources of nut predation, moves nuts away from source trees where density-dependent mortality is high (sometimes to habitats or microhabitats that favor seedling establishment), and buries nuts in the soil (which reduces rates of predation and helps to maintain nut viability). The large nutrient reserves of nuts not only attract animal dispersers but also permit seedlings to establish a large photosynthetic surface or extensive root system, making them especially competitive in low-light environments (e.g., deciduous forest) and semi-arid environments (e.g., dry mountains, Mediterranean climates). The most important postestablishment causes of seedling failure are drought, insufficient light, browsing by vertebrate herbivores, and competition with forbs and grasses. Because of the nutritional qualities of nuts and the synchronous production of large nut crops by a species throughout a region, nut trees can have pervasive impacts on other members of ecological communities. Nut-bearing trees have undergone dramatic changes in distribution during the last 16,000 years, following the glacial retreat from northern North America and Europe, and the current dispersers of nuts (i.e., squirrels, jays, and their relatives) appear to have been responsible for these movements.     

Pine nut syndrome: a simple test for genome size of 12 pine nut�Cproducing trees links the bitter aftertaste to nuts of P. armandii Zucc. ex Endl.

Genome sizes of 12 pines that produce edible nuts were investigated by flow cytometry with propidium iodide. Results were compared with the genome size and taste of 11 commercial samples of pine nuts to determine which species is the cause of a lingering bitter aftertaste (??pine nut syndrome??). Each nut sample was visually separated into two to six subsets. From a single nut, the embryo and the endosperm were measured. On the basis of nuclear DNA content, pine species could be matched with their nuts. Seven out of the 11 commercial samples contained only a single pine species: P. koraiensis Sieb.& Zucc., P. pinea L., P. armandii Zucc. ex Endl., or P. gerardiana Wall. ex Don, but the other four samples were a mix of two species. Tasting showed definitively that P. armandii is the origin of the bitter aftertaste. Nuclear DNA content can be measured using flow cytometry in less than 5?min, including the calculations. This makes it easy to identify the problem-causing nuts. With hindsight, it is now also possible to identify the species of four common edible pine nuts.     

Percussive tool use by Ta? Western chimpanzees and Fazenda Boa Vista bearded capuchin monkeys: a comparison

Percussive tool use holds special interest for scientists concerned with human origins. We summarize the findings from two field sites, Taï and Fazenda Boa Vista, where percussive tool use by chimpanzees and bearded capuchins, respectively, has been extensively investigated. We describe the ecological settings in which nut-cracking occurs and focus on four aspects of nut-cracking that have important cognitive implications, namely selection of tools, tool transport, tool modification and modulation of actions to reach the goal of cracking the nut. We comment on similarities and differences in behaviour and consider whether the observed differences reflect ecological, morphological, social and/or cognitive factors. Both species are sensitive to physical properties of tools, adjust their selection of hammers conditionally to the resistance of the nuts and to transport distance, and modulate the energy of their strikes under some conditions. However, chimpanzees transport hammers more frequently and for longer distances, take into account a higher number of combinations of variables and occasionally intentionally modify tools. A parsimonious interpretation of our findings is that morphological, ecological and social factors account for the observed differences. Confirmation of plausible cognitive differences in nut-cracking requires data not yet available.     

Human-induced rapid environmental change: A case study showing negative impact on animal culture

Changes in land use in recent decades have caused substantial biodiversity loss. Some authors suggest that animal cultures could be threatened by human pressure. The tradition of nut-cracking has been thoroughly studied since 2005 in the capuchin monkeys (S. libidinosus) of Fazenda Boa Vista (FBV). Despite being a relatively well-preserved area, the advance of intensive monocultures in the proximity of FBV, among other factors, may have affected the environmental features of the region. In this contribution we investigated the hypothesis that the tradition of nut-cracking using stone tools by bearded capuchin monkeys at FBV is threatened by the rapid transformation of the habitat. We analyzed longitudinal climatic data (mean maximum and minimum temperature and mean maximum and minimum humidity) from 2006 to 2020, and data from the periods 2006–2010 and 2015–2020 for the variables related to nut-cracking: availability of palm trees bearing fruits, ground use and consumption of palm nuts by the monkeys. We show an increase in maximum temperature and a decrease in minimum temperature and minimum humidity over the study years. There was a sharp drop in the number of fruiting palm trees per hectare between the two study periods and a decrease in the time that monkeys spent on the ground, eating palm nuts, and nut-cracking with tools. We confirmed the hypothesis that the tradition of using tools in feeding is threatened. Our results show that in less than two decades, habitat anthropization already negatively impacts animal cultures. We emphasize the importance of considering behavioral diversity in conservation criteria.     

Edible nuts of the pacific northwest

Only four kinds of native nut—hazelnut, chinquapin and two acorns—and introduced American walnut, Persian walnut and European filbert constitute the sources of edible nuts in this region.     

The potential for harvesting fruits in tropical rainforests: new data from Amazonian Peru

New data shows that edible fruit and nut production in Amazonian forests is substantially lower than most conservationists assume. Direct measures of production in Amazonian Peru show that two terra firma forest types produced significantly less edible fruit than an alluvial soil forest. Swamp forest produced more edible fruit than any other forest type measured. Palms produce 60% of edible fruit productivity, averaged over three forest types, but the most preferred palm fruits are difficult to harvest because they are borne too high for easy access by collectors. Forest fruit collection in Amazonia is less productive in the short-term than all other food-producing activities except for hunting and cattle ranching. Technological, social and political changes are essential so that sustainable but intrinsically low-yielding extractive activities like fruit collecting become more attractive to Amazonians.     

Kinematics and energetics of nut-cracking in wild capuchin monkeys (Cebus libidinosus) in Piauí, Brazil

Wild bearded capuchins (Cebus libidinosus, quadrupedal, medium-sized monkeys) crack nuts using large stones. We examined the kinematics and energetics of the nut-cracking action of two adult males and two adult females. From a bipedal stance, the monkeys raised a heavy hammer stone (1.46 and 1.32 kg, from 33 to 77% of their body weight) to an average height of 0.33 m, 60% of body length. Then, they rapidly lowered the stone by flexing the lower extremities and the trunk until the stone contacted the nut. A hit consisting of an upward phase and a downward phase averaged 0.74 s in duration. The upward phase lasted 69% of hit duration. All subjects added discernable energy to the stone in the downward phase. The monkeys exhibited individualized kinematic strategies, similar to those of human weight lifters. Capuchins illustrate that human-like bipedal stance and large body size are unnecessary to break tough objects from a bipedal position. The phenomenon of bipedal nut-cracking by capuchins provides a new comparative reference point for discussions of percussive tool use and bipedality in primates.     

Fruit Ripening Signals and Cues in a Madagascan Dry Forest: Haptic Indicators Reliably Indicate Fruit Ripeness to Dichromatic Lemurs

Fruit ripeness can be indicated through changes in chromaticity, luminance, odor, hardness, and size to attract seed dispersing animals. We quantified these attributes for both ripe and unripe fruits of 31 lemur-dispersed plant species in Ankarafantsika National Park, a tropical dry forest in northwestern Madagascar. We used spectroscopy, gas-chromatography mass-spectrometry, and a modified force gauge to quantify chromaticity, luminance, odor, and hardness. We compared these traits between unripe and ripe fruits of each species to determine which traits reliably indicate fruit ripeness across species. Overall, ripe fruits were significantly heavier and softer than unripe fruits. Ripe fruits were not more chromatically-conspicuous or odiferous relative to unripe fruits, nor were ripe fruits more conspicuous in the luminance channel. Contrary to expectation, our findings indicate that, in this particular system, plant-lemur interactions may be strongly mediated by haptic traits, such as fruit hardness, which are consistent and reliable indicators of fruit ripeness. Despite the potential importance of haptic indicators of fruit ripeness, they are underrepresented in the literature on sensory ecology.     

论季雨林的水平地带性

季雨林是受制于湿度因子的经度地带性植被类型,它是随着湿度条件的下降由热带雨林向热带疏林过渡的居间类型,而不是受制于温度因子的纬度地带性植被类型,不是随着温度条件的下降由热带雨林向亚热带常绿阔叶林过渡的居间类型。我国南亚热带的榕树群系、黄桐群系,以及热带北缘的青皮群系均不应是季雨林,前二者是典型的南亚热带低地常绿阔叶林或南亚热带雨林,后者则是热带雨林的一分类群。     

Diversity and composition of tropical butterflies along an Afromontane agricultural gradient in the Jimma Highlands,Ethiopia

Afromontane landscapes are typically characterized by a mosaic of smallholder farms and the biodiversity impacts of these practices will vary in accordance to local management and landscape context. Here, we assess how tropical butterfly diversity is maintained across an agricultural landscape in the Jimma Highlands of Ethiopia. We used transect surveys to sample understory butterfly communities within degraded natural forest, semi‐managed coffee forest (SMCF), exotic timber plantations, open woodland, croplands and pasture. Surveys were conducted in 29 one‐hectare plots and repeated five times between January and June 2013. We found that natural forest supports higher butterfly diversity than all agricultural plots (measured with Hill's numbers). SMCF and timber plantations retain relatively high abundance and diversity, but these metrics drop off sharply in open woodland, cropland and pasture. SMCF and timber plantations share the majority of their species with natural forest and support an equivalent abundance of forest‐dependent species, with no increase in widespread species. There was some incongruence in the responses of families and sub‐families, notably that Lycaenidae are strongly associated with open woodland and pasture. Adult butterflies clearly utilize forested agricultural practices such as SMCF and timber plantations, but species diversity declines steeply with distance from natural forest suggesting that earlier life‐stages may depend on host plants and/or microclimatic conditions that are lost under agricultural management. From a management perspective, the protection of natural forest remains a priority for tropical butterfly conservation, but understanding functioning of the wider landscape mosaic is important as SMCF and timber plantations may act as habitat corridors that facilitate movement between forest fragments.     

Oil Palm Use by Adjacent Communities of Chimpanzees at Bossou and Nimba Mountains,West Africa

We investigated oil palm (Elaeis guineensis) use for feeding in 3 chimpanzee communities: Bossou and Seringbara in Guinea and Yealé in Côte d'Ivoire. Bossou was used as the benchmark for comparison. Bossou chimpanzees (Pan troglodytes verus) exhibit a wide range of oil palm targeted behaviors. We used direct observations of their two tool use, i.e., nut-cracking and pestle pounding, to establish strict and reliable criteria to ascertain the presence of comparable behaviors at the two adjacent Nimba sites. Based on monthly surveys of oil palms across the three sites, significant differences in patterns of use emerged. Bossou chimpanzees demonstrated the greatest frequency of oil palm use, while Seringbara chimpanzees, 6 km away, failed to exhibit any use and Yealé chimpanzees, 12 km away, showed all uses comparable to Bossou chimpanzees except pestle pounding and mature leaf pith-feeding. We examined the density and distribution of oil palms, tool availability for nut-cracking and pestle pounding, fruit, flower and nut availability, competition with sympatric species for fruit and nuts and the diversity of fruit species in the diet across the 3 sites. We found no clear difference in proximate environmental variables underlying observed variations in oil palm use among the 3 sites, yielding the conclusion that the differences are cultural. Assuming individual interchange between communities and the involvement of social learning in the intracommunity transmission and maintenance of oil palm uses, the result raises interesting questions about diffusion of behavior between neighboring chimpanzee communities.