We have already discussed the seasonal availability of food sources which can drive an opportunistic lifestyle Tebbich et al. Others have discussed embedded or difficult to open food Parker, and the absence of competitors exploiting this niche as a promotor for tool use Orenstein, ; Kenward et al. There are no specialized extractive foragers such as woodpecker inhabiting the Tanimbar archipelago which usually would occupy this niche.
However, other species such as the Tanimbar friarbird Philemon pulmigenis have also been observed to share at least once resource with the Goffin that requires extractive foraging during the dry season personal observation , the coconut.
In turn, this may also facilitate innovations Greenberg, and has been suggested as a possible driver for the evolution of tool use in New Caledonian crows Kacelnik et al. During group foraging events in open spaces, such as on fields, individuals typically aggregate on nearby trees until a critical mass has gathered approx. Temporary large aggregations of individuals and an apparent fission-fusion structure of groups suggests that alongside the environmental complexity, the social structure of this species may represent a promising avenue for further research e.
Our preliminary observations concerning differential social structures, multiple sightings of large groups and interactions within these groups support the notion that these birds might have the possibilities to learn from conspecifics, which has been demonstrated by captive individuals in a previous study Auersperg et al.
This seems to satisfy the criteria that have been proposed necessary in order for innovations to be transmitted and maintained within a population, such as spatial proximity, a potential for social learning and reduced intraspecific competition Fox et al.
As mentioned earlier, data from controlled studies in captivity have shown that Goffins use objects as tools and socially transmit their tool using skills to other individuals Auersperg et al. Therefore, limitations with regards to cognitive and morphological constraints for flexible tool use do not seem to play a major role Hunt et al.
Thus, we conclude that the ecological framework in which this species evolved would satisfy various criteria that have been argued to underlie tool use in wild individuals e. We are also aware that we cannot fully exclude that our total observation time in their original habitat on Tanimbar ca. Challenges surrounding field observations of rare behaviours are exemplified in investigations of the percussive tool use of black palm cockatoos Probosciger aterrimus , a behaviour which is well documented in the literature but also can be recorded only once per hours of observation time Heinsohn et al.
Here, male cockatoos use sticks for drumming on trees with hollows, which has been suggested to advertise nest quality over large distances Heinsohn et al. However, tools for social display are only required for very distinctive purposes that occur infrequently attracting a mate, deterring an intruder and only during specific seasons e.
Birds, such as the New Caledonian crow or the woodpecker finch, that use tools habitually for foraging purposes rather than for display show a much higher percentage of tool related behaviours within overall observation times daily observations in New Caledonian crows; Hunt, However, other species such as nuthatches express tool using behaviour more rarely or seasonally Morse, ; Gray et al.
At this point it is important to note that despite careful awareness and consideration, a potential bias regarding the number of observations in different habitats can never be fully excluded. Birds are more conspicuous in open areas which provide easier access to food that does not require extractive foraging with exception of the coconuts and are better concealed in the dense tropical forest habitat.
Predation in the dense forest may also be lower than in open areas which, together with the afore mentioned hypothesis of tool use evolving as a result of reduced predation risk, might suggest potential occurrences of tool use to develop predominantly in the forest habitat. During our pilot expedition in Mioduszewska et al. While the snipping of smaller branches and leaves is quite common and may be part of the play repertoire, dropping of larger branches have only been observed in this context.
This may occur as a stereotyped release of agitation in association with the effect of deterring ground predators. However, it will have to remain speculative until further systematic investigations can be made.
Hence, innovative problem solving may be facilitated when moving into novel environments Alcock, More recently a population that has been introduced and successfully established itself in Singapore, is facing potentially very different environmental and anthropogenic challenges. A comparative approach of studying these two populations might provide interesting insights regarding behavioural innovations and adaptations to human induced changes.
Nevertheless, the necessity for doing so may be limited. The bill of birds has been subject to evolutionary pressures determining its morphology e.
It may be used to dig up embedded material such as roots by shovelling soil as elaborated earlier. Tree bark can be levered to reach insects or sap and decaying wood can also be easily manipulated with the strong and sharp opposing mandibles. The zygodactyl feet and long digits allow for a good grip and for probing in holes as described above. These features make tool use often — but not completely — obsolete. Thus, species that may have the cognitive prerequisites to develop tool use will not do so if the morphological adaptations are adequate to succeed at solving the majority of extractive foraging problems in their natural habitat.
Nevertheless, they possess a beak which makes them well adapted for extractive foraging. We suggest that the described socio-ecological and morphological characteristics support their generalist lifestyle and have promoted behavioural flexibility to meet novel environmental challenges including new extractive foraging problems but without an imminent need for using tools. We are grateful to the Indonesian Government for granting and supporting our research.
Lilipory and Cardolin Lattuputy who supported our scanning efforts in the forest. We would like to express our deep gratitude to Wilhelmus, Vera and Kletus Samangun for their help hosting us in the Lorulun fields, Alowisius Sakliresi, Petrus Sainyakit, Atanasius Sainyakit and Yakobus Sainyakit for invaluable help in the Lorulun forest and fields, to Leo Samangun for his kind involvement in our local outreach work, as well as the people of Lorulun for hearty receiving us to their community.
We are very grateful to the editor and two anonymous reviewers for their helpful comments and suggestions how to improve the manuscript. Alcock , J. The evolution of the use of tools by feeding animals.
Auersperg , A. Exploration technique and technical innovations in corvids and parrots. Elsevier , p. Navigating a tool end in a specific direction: stick-tool use in kea Nestor notabilis. Tool making cockatoos adjust the lengths but not the widths of their tools to function.
Unrewarded object combinations in captive parrots. Object permanence in the Goffin cockatoo Cacatua goffini. Combinatory actions during object play in psittaciformes Diopsittaca nobilis , Pionites melanocephala , Cacatua goffini and corvids Corvus corax , C. Social transmission of tool use and tool manufacture in Goffin cockatoos Cacatua goffini.
B Biol. Flexibility in problem solving and tool use of kea and New Caledonian crows in a multi access box paradigm. Biro , D.
Tool use as adaptation. Brejaart , R. Diet and feeding behaviour of the kea Nestor notabilis. Cahyadin , Y. Call , J. Three ingredients for becoming a creative tool user. Sanz , C. Cambridge University Press , Cambridge , p. Crain , B. A tool for every job: assessing the need for a universal definition of tool use.
Darwin , C. On the origin of species by means of natural selection, or, the preservation of favoured races in the struggle for life , 1st edn. On the tendency of species to form varieties; and on the perpetuation of varieties and species by natural means of selection. Diamond , J. Kea, bird of paradox. The evolution and behavior of a New Zealand parrot, Vol. University of California Press.
Diquelou , M. The role of motor diversity in foraging innovations: a cross-species comparison in urban birds behavioral ecology. Emery , N. Cognitive ornithology: the evolution of avian intelligence.
Forshaw , J. Parrots of the world , 3rd rev. Fox , E. Intra-and interpopulational differences in orangutan Pongo pygmaeus activity and diet: implications for the invention of tool use. Fragaszy , D. Study Behav. Gray , M. Tool usage by juvenile Sitta pusilla brown-headed nuthatch. Greenberg , R. The role of neophobia and neophilia in the development of innovative behaviour of birds. Reader , S.
Oxford University Press , p. Ecological aspects of neophobia and neophilia in birds. However, we did not measure the availability of raw material on the island and therefore can not adequately test the hypothesis that the daily removal of tools from the study area significantly affected the availability of optimal tools and led to differences in tool characteristics of the selected tools between the two experiments of our study.
The habitats of some Australopithecus as well as Paranthropus and Homo sites have been reconstructed as ranging from closed woodlands to shrublands, which, based on analogy with similar modern habitats, probably held an abundance of USOs [ 62 , 67 ]. Fallback foods are often critical for organisms when entering new environments, especially seasonal ones [ 3 ]. Thus, it is not unlikely that USOs served as such fallback resources in the increasingly seasonal habitats occupied by hominins as the Pliocene and Pleistocene progressed.
However, in such dry environments, the soil hardness may have been a significant obstacle for hungry hominins to have overcome. For example, the extreme hardness of the soil in the savanna woodland of Ugalla during the dry season may be one factor that prevents the chimpanzees from obtaining USOs during this part of the year [ 31 ].
Even sticks may not be sufficiently sturdy enough to breach densely compacted sediment under such conditions. Bearded capuchins living in another dry and seasonal environment use stones rather than plant tools in the excavation of underground food, even if they readily use sticks for tasks other than excavation [ 34 ]. Before fire was used to harden excavating sticks, plant tools may have been inefficient to use for breaking the very hard soil of arid environments during the dry season.
If early hominins obtained USOs during this season, they may have obtained them either from locations where the soil was sandy or from water [ 28 , 68 ], but if the soil was hard they may have required either sturdy bone or sharp stone tools for excavation. Zihlman et al. In addition, modern human hunter-gatherers have been observed using stones as excavating tools reviewed in [ 70 ]. However, it seems reasonable to conjecture that at least some Pliocene and Pleistocene hominins, who—in addition to their archaeologically documented tool-making and—using capabilities e.
Captivity produces uncommon environmental and social conditions for animals, such as increased contact between individuals and lack of predation [ 78 ]. We observed several social behaviors in the context of underground food excavation in our study. The chimpanzees saw each other excavating, and sometimes excavated socially even the same holes and shared the excavated food.
Thus, in the scenario of using USOs as fallback foods, similar social behaviors would have provided adaptive benefits for early hominin individuals excavating in groups, such as protection from predators and opportunities for tool learning by immature individuals. The hypothesized abundance of USOs in hominin habitats would have prevented intergroup food competition.
Both wild bearded capuchins and chimpanzees have been reported to reuse USO excavating sites [ 31 , 34 ] and thus such sites may provide excavation opportunities for inexperienced individuals [ 79 ], especially if tools left at the excavation sites would be reused as it was the case in our study.
Further, the majority of individuals in our study succeeded in excavating with tools. Interestingly, we found that other behaviors besides digging were involved in the tool-assisted excavation of underground food: probing, perforating, pounding, shoveling and enlarging. As such, the excavation of artificially buried food and presumably the excavation of USOs does not involve a single tool behavior but rather a repertoire.
This would suggest that USO excavation by wild chimpanzees may be similar in complexity to other underground food source extractive tasks such as foraging for underground honey bee nests [ 54 ] or termites [ 55 ]. In the context of underground food excavation, the chimpanzees in our study selected tools for the task, reused some tools more frequently than others and transported tools.
These behaviors have already been reported for chimpanzees in other contexts, considered complex, such as foraging for termites [ 55 ], honey [ 56 ] and nut kernels [ 43 ].
Here we show that they also occurred in a context analogous to the excavation of wild USOs, further suggesting that USO excavation by wild chimpanzees may be a complex task. However, captive primates may exhibit a higher frequency and diversity of tools use than their wild counterparts captivity bias effect, [ 69 ] and thus direct observations of wild chimpanzees excavating USOs are needed to confirm this hypothesis.
Our results highlight the importance of conducting experiments with captive primate populations to enable us to better understand the behavior of their non-habituated, unobservable wild conspecifics that can only be indirectly studied using archaeological methods sensu [ 80 ] and to explore the implications of such behaviors for human evolution.
Eight reuse events are not included in the table because the individuals that reused the tools could not be identified. We thank the Kristiansand Zoo for their support and help in this study, in particular to Hege Aas, Hildegunn Johannesen and Mathias Henriksen, as well as the rest of zoo keepers. We are very grateful to William C.
McGrew for his many useful comments on the manuscript and to Trond Reitan and Axel Hernandez-Aguilar for advise on data analysis. We also thank Helene Lampe and Karl I. Ugland for comments on parts of this manuscript. We are grateful to Alejandra Pascual-Garrido and anonymous reviewers for their insights that greatly improved this manuscript.
Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract It is hypothesized that tool-assisted excavation of plant underground storage organs USOs played an adaptive role in hominin evolution and was also once considered a uniquely human behavior.
Materials and methods Study subjects Our study was conducted on a colony of chimpanzees Pan troglodytes housed at the Kristiansand Zoo in Kristiansand, Norway. Download: PPT. Experimental setting and design Experiment 1. Fig 2. Sample of the tools provided to the chimpanzees sticks and bark in Experiment 1. Experiment 1 included three conditions. Experiment 2. Experiment 2 included two conditions. Data collection Experiment 1. Data analysis Statistical analyses were carried out using R version 2.
In order to study tool selection by the chimpanzees, we conducted the following analyses. Results Description of excavating behaviors Experiment 1 Nine out of the 10 chimpanzees were observed to excavate manually all individuals except the infant , with seven of them 3 females and 4 males using tools to do so. Fig 3. Tool use behaviors that emerged during the excavation of underground food. Fig 4. Plot of the proportions of each excavating behavior performed during each experimental condition.
Table 1. Number of events of each excavating behavior performed by each individual during the Loose Soil Condition of Experiment 1. Table 2. Number of events of each excavating behavior performed by each individual during the Compacted Clay Condition of Experiment 1. Other behaviors observed in the context of excavation Experiments 1 and 2 During the conditions when the holes were covered in both experiments, the chimpanzees revisited the holes and excavated the partially filled holes and the soil below the level where the fruits had been the bottom of the hole.
Excavating modalities Experiment 1 and 2 Eight out of nine chimpanzees all except the adult female Dixi, S1 Table were observed excavating manually and seven excavated with tools. Table 3. Total individual bout counts and total bout durations in seconds of the manual and tool excavating bouts.
Table 4. Table 6. Number of tools reused and number of reuse events per individual during Experiment 1. Discussion All but one adult female chimpanzee succeeded in excavating underground food in at least one of the experiments conducted, and the majority of the chimpanzees also did so with tools seven out of ten and seven out of nine in Experiments 1 and 2, respectively. Supporting information.
S1 Table. Demographic data of the individuals included in the experiments. S2 Table. Ethogram of tool use behaviors involved in excavation. S3 Table. Ethogram of manual techniques observed during Experiment 2.
S4 Table. Number of tool-excavation events performed by each individual during the Compacted Soil Condition of Experiment 2.
S5 Table. Dimensions of the selected and selected-non-provided tools used per individual during Experiment 1. S6 Table. Number of times each tool was reused and individual count of reuse events. S1 Appendix. Model structures and estimates. Acknowledgments We thank the Kristiansand Zoo for their support and help in this study, in particular to Hege Aas, Hildegunn Johannesen and Mathias Henriksen, as well as the rest of zoo keepers. References 1.
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