Exploitation of underground bee nests by three sympatric consumers in Loango National Park,Gabon

Honey represents a highly nutritious resource for animals, but is difficult to obtain given bees' defensive strategies. We investigated exploitation of the underground nests of stingless bees (Meliplebeia lendliana) by three sympatric consumers in Loango National Park, Gabon: the central African chimpanzee (Pan troglodytes troglodytes), forest elephant (Loxodonta cyclotis) and honey badger (Mellivora capensis). Given the differences in their respective morphological traits and sensory abilities, we hypothesized that chimpanzees would be more limited in digging out the bee nests, compared to the other two competitors, and would show behavioral strategies to overcome such constraints. Our dataset comprised camera trap footage recorded over 60 mo at 100 different bee nests. Chimpanzees visited the nests more often than the other consumers, showing a frequency of extraction success comparable to that observed in honey badgers, the most efficient digger. Both chimpanzees and honey badgers increased their extractive attempts across the dry season, whereas elephants did not. The soil hardness was greater during the dry season than the wet season and, possibly in order to compensate for this, chimpanzees showed a tendency toward digging at nests found in relatively softer soil. They also seemed to be inhibited by indirect cues left by other consumers, possibly as a risk‐avoidance strategy. Overall, chimpanzees and honey badgers extracted the underground nests of stingless bees with similar frequencies, whilst forest elephants did so only occasionally. Moreover, chimpanzees can use tools and other behavioral strategies to overcome the physical limitations that may constrain their exploitation of this resource.     

Flexible and Persistent Tool-using Strategies in Honey-gathering by Wild Chimpanzees

Several populations of wild chimpanzees use tools to raid bee nests, but preliminary observations of chimpanzees in the Congo Basin indicate that they may have developed sophisticated technical solutions to gather honey that differ from those of apes in other regions. Despite the lack of habituated groups within the range of the central subspecies, there have been several reports of different types of tools used by chimpanzees to open beehives and gather honey. Researchers have observed some of these behaviors (honey dipping) in populations of western and eastern chimpanzees, whereas others (hive pounding) may be limited to this region. Toward evaluating hypotheses of regional tool using patterns, we provide the first repeated direct observations and systematic documentation of tool use in honey-gathering by a population of Pan troglodytes troglodytes. Between 2002 and 2006, we observed 40 episodes of tool use in honey-gathering by chimpanzees in the Goualougo Triangle, Republic of Congo. Pounding was the most common and successful strategy to open beehives. Chimpanzees at this site used several tools in a single tool-using episode and could also attribute multiple functions to a single tool. They exhibited flexibility in responses toward progress in opening a hive and hierarchical structuring of tool sequences. Our results support suggestions of regional tool using traditions in honey-gathering, which could be shaped by variation in bee ecology across the chimpanzee range. Further, we suggest that these chimpanzees may have an enhanced propensity to use tool sets that could be related to other aspects of their tool repertoire. Clearly, there is still much to be learned about the behavioral diversity of chimpanzees residing within the Congo Basin.     

Chimpanzee tool technology in the Goualougo Triangle, Republic of Congo

With the exception of humans, chimpanzees show the most diverse and complex tool-using repertoires of all extant species. Specific tool repertoires differ between wild chimpanzee populations, but no apparent genetic or environmental factors have emerged as definitive forces shaping variation between populations. However, identification of such patterns has likely been hindered by a lack of information from chimpanzee taxa residing in central Africa. We report our observations of the technological system of chimpanzees in the Goualougo Triangle, located in the Republic of Congo, which is the first study to compile a complete tool repertoire from the Lower Guinean subspecies of chimpanzee (Pan troglodytes troglodytes). Between 1999 and 2006, we documented the tool use of chimpanzees by direct observations, remote video monitoring, and collections of tool assemblages. We observed 22 different types of tool behavior, almost half of which were habitual (shown repeatedly by several individuals) or customary (shown by most members of at least one age-sex class). Several behaviors considered universals among chimpanzees were confirmed in this population, but we also report the first observations of known individuals using tools to perforate termite nests, puncture termite nests, pound for honey, and use leafy twigs for rain cover. Tool behavior in this chimpanzee population ranged from simple tasks to hierarchical sequences. We report three different tool sets and a high degree of tool-material selectivity for particular tasks, which are otherwise rare in wild chimpanzees. Chimpanzees in the Goualougo Triangle are shown to have one of the largest and most complex tool repertoires reported in wild chimpanzee populations. We highlight new insights from this chimpanzee population to our understanding of ape technological systems and evolutionary models of tool-using behavior.     

Chimpanzees in Bwindi-Impenetrable National Park, Uganda, use different tools to obtain different types of honey

Evidence of tool use for foraging for honey by chimpanzees in Bwindi-Impenetrable National Park, Uganda, is reported. These are the first records of tool use by chimpanzees in this region of the Albertine Rift. Tools of two types were found at sites of bee activity. Chimpanzees apparently use small stick tools to forage for the honey of a stingless bee [Meliponula bocandei (Trigonidae)] that nests in tree cavities and also in subterranean holes. They use significantly larger, thicker tools to assist in foraging for honey of African honeybees (Apis mellifera).     

Use of tool sets by chimpanzees for multiple purposes in Moukalaba-Doudou National Park,Gabon

We report our recent findings on the use of tool sets by chimpanzees in Moukalaba-Doudou National Park, Gabon. Direct observations and evidences left by chimpanzees showed that chimpanzees used sticks as pounders, enlargers, and collectors to extract honey from beehives of stingless bees (Meliponula sp.), which may correspond to those previously found in the same site for fishing termites and to those found in Loango National Park, Gabon. However, we observed chimpanzees using a similar set of tools for hunting a medium-sized mammal (possibly mongoose) that hid inside a log. This is the first report of hunting with tools by a chimpanzee population in Central Africa. Chimpanzees may recognize the multiple functions and applicability of tools (extracting honey and driving prey), although it is still a preliminary speculation. Our findings may provide us a new insight on the chimpanzee’s flexibility of tool use and cognitive abilities of complex food gathering.     

Tool-use to obtain honey by chimpanzees at Bulindi: new record from Uganda

Honey-gathering from bee nests has been recorded at chimpanzee (Pan troglodytes) study sites across tropical Africa. Different populations employ different strategies, ranging from simple ‘smash-and grab’ raids to use of sophisticated tool-sets, i.e., two or more types of tool used sequentially in a single task. In this paper I present evidence of tool-use, and the probable use of a tool-set, for honey-gathering by unhabituated chimpanzees at Bulindi, a forest–farm mosaic south of the Budongo Forest in Uganda. Between June and December 2007, 44 stick tools were found in association with 16 holes dug in the ground, corresponding to the period when stingless bees (Meliponula sp.) appeared in chimpanzee dung. In 11 cases the confirmed target was a Meliponula ground nest. Two potential tool types were distinguished: digging sticks encrusted with soil, and more slender and/or flexible sticks largely devoid of soil that may have functioned to probe the bees’ narrow entry tubes. Reports of chimpanzees using tools to dig for honey have been largely confined to Central Africa. Honey-digging has not previously been reported for Ugandan chimpanzees. Similarly, use of a tool-set to obtain honey has thus far been described for wild chimpanzee populations only in Central Africa. Evidence strongly suggests that Bulindi chimpanzees also use sticks in predation on carpenter bee (Xylocopa sp.) nests, perhaps as probes to locate honey or to disable adult bees. These preliminary findings from Bulindi add to our understanding of chimpanzee technological and cultural variation. However, unprotected forests at Bulindi and elsewhere in the region are currently severely threatened by commercial logging and clearance for farming. Populations with potentially unique behavioral and technological repertoires are being lost.     

Chimpanzees prey on army ants with specialized tool set

Several populations of chimpanzees have been reported to prey upon Dorylus army ants. The most common tool‐using technique to gather these ants is with “dipping” probes, which vary in length with regard to aggressiveness and lifestyle of the prey species. We report the use of a tool set in army ant predation by chimpanzees in the Goualougo Triangle, Republic of Congo. We recovered 1,060 tools used in this context and collected 25 video recordings of chimpanzee tool‐using behavior at ant nests. Two different types of tools were distinguished based on their form and function. The chimpanzees use a woody sapling to perforate the ant nest, and then a herb stem as a dipping tool to harvest the ants. All of the species of ants preyed upon in Goualougo are present and consumed by chimpanzees at other sites, but there are no other reports of such a regular or widespread use of more than one type of tool to prey upon Dorylus ants. Furthermore, this tool set differs from other types of tool combinations used by chimpanzees at this site for preying upon termites or gathering honey. Therefore, we conclude that these chimpanzees have developed a specialized method for preying upon army ants, which involves the use of an additional tool for opening nests. Further research is needed to determine which specific ecological and social factors may have shaped the emergence and maintenance of this technology. Am. J. Primatol. 72:17–24, 2010. © 2009 Wiley‐Liss, Inc.     

Tool use by wild cebus monkeys at Santa Rosa National Park,Costa Rica

Although wild cebus monkeys have been observed to use tools, this behavior has been reported only rarely. No one has systematically examined tool use in wildCebus, and it is not known how prevalent tool use is in the species' natural repertoire. During 300 hr of observation on 21 wild capuchins (Cebus capucinus imitator) at Santa Rosa National Park in Costa Rica, 31 incidents of tool use, including eight different types of tool-use behavior, were observed. These observations indicate that tool use is a notable behavior pattern in this troop. Considering these incidents of tool use in conjunction with other reports on complex food-getting and preparation behavior byCebus suggests that tool use is a manifestation ofCebus' high behavioral adaptability. Since onlyCebus and the great apes (especially chimpanzees) have been observed to show such a diverse tool-use repertoire, to use tools so frequently, or to show such complex food-getting behavior in the wild, these observations also support the notion thatCebus and the great apes have followed a parallel evolutionary development of tool-using capacity.     

Tool-set for termite-fishing and honey extraction by wild chimpanzees in the Lossi Forest, Congo

The use of perforating sticks and flexible stalks in combination for termite fishing and a complex tool-set of three components used sequentially (stout chiel, bodkin, and dip-stick) to penetrate melipone and ground-dwelling bee hives byPan troglodytes troglodytes are documented or, inferred from circumstantial evidence. Functionally, termite extraction tools were similar to other locations in west and central Africa, but the plants and the number of raw material species used were different. Tools varied in the degree of modification (fraying ends). Chimpanzees in the Lossi forest seem to be able to use the tools not in a stereotyped fashion, but in a flexible, insightful way. The extraction of Melipone honey using large pieces of wood as pounding tools has rarely been recorded elsewhere. The most impressive technological solution to the honey-getting problem by wild chimpanzees was shown by this study. This is the only known, use of a tool-set of three components in sequence to extract honey by wild chimpanzees.     

Pestle-pounding behavior of wild chimpanzees at Bossou,Guinea: A newly observed tool-using behavior

A new type of tool-using behavior was observed in a group of wild chimpanzees (Pan troglodytes verus) at Bossou, Guinea. The chimpanzees used the leaf-petiole of oil-palm trees (Elaeis guineensis) as a pounding tool to deepen a hole in the oil-palm crown which appeared after the chimpanzees had pulled out the central young shoots. Finally, the chimpanzees extracted and ate the apical meristem or apical bud of the oil-palm tree which is edible but inaccessible without such tool use. The motor pattern which the chimpanzees employed is similar to that used for termite-nest digging but it is more exaggerated and requires great force. The behavior is reminiscent of pestlepounding. The chimpanzees exploit substantial amounts of food with this tool-using skill, compensating for insufficient fruit foods in the primary forest. This tool-using behavior was first observed in 1990 and, to date, almost half of the group members have been confirmed to use the pestle tool. It appears that this tool-using behavior was invented recently and has since spread widely throughout the group as a habitual one.     

Tool use in wild spider monkeys (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>)

Tool use has been observed in a variety of primate species, including both New and Old World monkeys. However, such reports mainly address the most prodigious tool users and frequently limit discussions of tool-using behavior to a foraging framework. Here, we present observations of novel and spontaneous tool use in wild black-handed spider monkeys (Ateles geoffroyi), where female spider monkeys used detached sticks in a self-directed manner. We introduce factors to explain Ateles tool-using abilities and limitations, and encourage the synthesis of relevant research in order to gain insight into the cognitive abilities of spider monkeys and the evolution of tool-using behaviors in primates.     

Fluid dipping technology of chimpanzees in Comoé National Park,Ivory Coast

Over a 6 month period during the dry season, from the end of October 2014 to the beginning of May 2015, we studied tool use behavior of previously unstudied and non‐habituated savanna chimpanzees (Pan troglodytes verus) living in the Comoé National Park, Ivory Coast (CI). We analyzed all the stick tools and leaf‐sponges found that the chimpanzees used to forage for ants, termites, honey, and water. We found a particular behavior to be widespread across different chimpanzee communities in the park, namely, dipping for water from tree holes using sticks with especially long brush‐tip modifications, using camera traps, we recorded adults, juveniles, and infants of three communities displaying this behavior. We compared water dipping and honey dipping tools used by Comoé chimpanzees and found significant differences in the total length, diameter, and brush length of the different types of fluid‐dipping tools used. We found that water dipping tools had consistently longer and thicker brush‐tips than honey dipping tools. Although this behavior was observed only during the late dry season, the chimpanzees always had alternative water sources available, like pools and rivers, in which they drank without the use of a tool. It remains unclear whether the use of a tool increases efficient access to water. This is the first time that water dipping behavior with sticks has been found as a widespread and well‐established behavior across different age and sex classes and communities, suggesting the possibility of cultural transmission. It is crucial that we conserve this population of chimpanzees, not only because they may represent the second largest population in the country, but also because of their unique behavioral repertoire.     

Subsistence Technology of Nigerian Chimpanzees

A trademark of Homo sapiens is the enormous variation in behavioral patterns across populations. Insight into the development of human cultures can be aided by studies on communities of Pan across Africa that display unique combinations of social behavior and elementary technology. Only cross-population comparisons can reveal whether the diversity reflects differential genetics, environmental constraints, or is a cultural variant. However, the recently recognized and most endangered subspecies, Pan troglodytes vellerosus, remains completely unstudied in this respect. We report first evidence from a new long-term study of Nigerian chimpanzees at Gashaka. Their dietary composition is highly varied and they have to cope with high concentrations of antifeedant defenses of plants against consumption. Gashaka chimpanzees use a varied tool kit for extractive foraging. For example, they harvest insects throughout the year, via digging sticks and probes, to obtain honey from stingless-bee and honeybee nests, dipping wands to prey on army ants, and fishing rods to eat arboreal ants. Tools appeared to be custom-made with a considerable degree of standardization in length, diameter, and preferential use of distal ends. Moreover, compared to the rainy season, tools were longer during the dry season when insects retreat further into their nests. Many of the expressions of subsistence technology seem to be environmentally constrained. Most notably, the absence of termite-eating could reflect a low abundance of mounds. Other traits may represent cultural variation. For example, the chimpanzees did not hammer open 2 types of hard-shelled nuts with tools, unlike what occurs elsewhere in West Africa. The prevalence of elementary technology may indicate that the material culture of Gashaka chimpanzees is most related to core cultural tendencies of Central African populations.     

Archaeological Analysis Does Not Support Intentionality in the Production of Brushed Ends on Chimpanzee Termiting Tools

Some chimpanzees use 2 types of tools to extract underground termites for consumption. Chimpanzees insert thin, flexible probes into tunnels or holes in termite mounds (fishing), and sometimes use stouter, rigid sticks to first puncture the holes and also possibly to fish. Many puncturing sticks have distinctive “brushed” ends. Researchers have hypothesized that chimpanzees create the brushed ends intentionally to increase their affixibility to biting termites (Sugiyama, 1985). The results of our archaeological analysis of a large collection of puncturing sticks used by Central African chimpanzees falsifies this hypothesis, and instead agrees with the recent behavioral observations of Sanz et al. (2004; cf. Bermejo and Illera, 1999) that brushing is a coincidental result of procuring sticks from vegetation sources. The results highlight the positive contribution of an archaeological approach to problems in chimpanzee material culture and emphasize to primatologists the value of curating artifacts.     

“Stepping-sticks” and “seat-sticks”: New types of tools used by wild chimpanzees (Pan troglodytes) in Sierra Leone

In Tenkere, Sierra Leone, a community of wild chimpanzees (Pan troglodytes verus) spent long hours eating the fruits and flowers of the Kapok (Ceiba pentandra) tree. The branches of this species are covered in sharp thorns which make movement in their high canopies problematic for the chimpanzees. In an apparent attempt to increase their mobility and to ease the discomfort of lengthy bouts of eating in these trees, some of the Tenkere chimpanzees have been observed using stick tools as foot (“stepping-sticks”) and body (“seat-sticks”) protection against the painful thorns. This form of tool-using is culturally unique to the Tenkere chimpanzees, as at other sites where these apes have been observed eating parts of kapok trees, there are no published records of this tool technology. In three of the stepping-stick tool use incidents, the chimpanzee used the tool(s), held between their greater and lesser toes, in locomotion. This form of tool use is the first recorded case of habitually used tools that can be justifiably categorized as being “worn” by any known wild population of Pan troglodytes. Am J Primatol 41:45–52, 1997. © 1997 Wiley-Liss, Inc.     

A novel form of spontaneous tool use displayed by several captive greater vasa parrots (Coracopsis vasa)

Parrots are frequently cited for their sophisticated problem-solving abilities, but cases of habitual tool use among psittacines are scarce. We report the first evidence, to our knowledge, of tool use by greater vasa parrots (Coracopsis vasa). Several members of a captive population spontaneously adopted a novel tool-using technique by using pebbles and date pits either (i) to scrape on the inner surface of seashells, subsequently licking the resulting calcium powder from the tool, or (ii) as a wedge to break off smaller pieces of the shell for ingestion. Tool use occurred most frequently just prior to the breeding season, during which time numerous instances of tool transfer were also documented. These observations provide new insights into the tool-using capabilities of parrots and highlight the greater vasa parrot as a species of interest for studies of physical cognition.     

PVC nest boxes are less at risk of occupancy by feral honey bees than timber nest boxes and natural hollows

Feral European Honey Bee (Apis mellifera) has been identified as a potential nest competitor for Australian hollow nesting species, but few studies have investigated the impact of feral honey bee competition on Threatened species. Our study used data from Glossy Black‐cockatoo (Calyptorhynchus lathami halmaturinus) nests on Kangaroo Island, monitored and managed over an 11‐year period, and found 12% of nests became occupied by feral honey bees during that period. Our results indicate that feral honey bees were less likely to occupy nest boxes made of PVC (5%) compared with wooden nest boxes (24%) or natural hollows in Eucalyptus trees (14%). The removal of feral honey bee hives from nests is a priority for long‐term conservation of glossy black‐cockatoos on Kangaroo Island. We recommend that PVC nest boxes are chosen for future nesting habitat restoration, due to the more frequent use of wooden nest boxes by feral honey bees.     

Honey‐Making Bee Colony Abundance and Predation by Apes and Humans in a Uganda Forest Reserve1

Honey‐making bee colonies in Bwindi Impenetrable National Park were investigated with Batwa Pygmies locating 228 nests of Apis and five stingless bees (Meliponini). The relative importance of predation, food supply, nesting site, and elevation affecting abundance were studied for meliponines in particular. Nest predation and overall nest abundance had no correlation with elevation along a 1400 m gradient, nor did flowering phenology or pollen collection. Many suitable, large trees were unoccupied by bee nests. In 174 ha of forest plots, 2 Meliponula lendliana, 13 M. nebulata, 16 M. ferruginea, 16 M. bocandei, and 20 Apis mellifera adansonii nests occurred, suggesting a habitat‐wide density of 39 nests/km². Compared to other studies, Ugandan Meliponini were uncommon (0.27 colonies/ha, tropical mean = 1.9/ha), while Apis mellifera was numerous (0.12 nests/ha, tropical mean = 0.06/ha), despite park policy allowing humans to exploit Apis. Meliponine colony mortality from predators averaged 12 percent/yr and those near ground were most affected. Tool‐using humans and chimpanzees caused 82 percent of stingless bee nest predation. Selective factors affecting nest heights and habit may include auditory hunting by predators for buzzing bees, and indirect mutualists such as termites that leave potential nesting cavities. Mobility and free‐nesting by honey bee colonies should enable rapid community recovery after mortality, especially in parks where human honey hunting is frequent, compared to sedentary and nest‐site‐bound Meliponini.