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Primates

, Volume 59, Issue 2, pp 173–183 | Cite as

Extractive foraging and tool-aided behaviors in the wild Nicobar long-tailed macaque (Macaca fascicularis umbrosus)

  • Arijit Pal
  • Honnavalli N. Kumara
  • Partha Sarathi Mishra
  • Avadhoot D. Velankar
  • Mewa Singh
Original Article

Abstract

Macaques possess a repertoire of extractive foraging techniques that range from complex manipulation to tool-aided behaviors, to access food items that increase their foraging efficiency substantially. However, the complexity and composition of such techniques vary considerably between species and even between populations. In the present study, we report seven such complex manipulative behaviors that include six extractive foraging behaviors, and teeth flossing, in a population of Nicobar long-tailed macaques. The apparent purpose of these behaviors was an extraction of encased food, processing food, foraging hidden invertebrates, and dental flossing. Among these behaviors, three behaviors viz. wrapping, wiping, and teeth-flossing were tool-aided behaviors, where macaques used both natural and synthetic materials as tools. Occasionally macaques also modified those tools prior to their use. The substrate use patterns of leaf rubbing and teeth flossing were similar to that observed in other macaques. The spontaneous tool modification to perform wrapping was a first time observation. These observations suggest that Nicobar long-tailed macaques have a high level of sensorimotor intelligence which helps to evolve such innovative foraging solutions.

Keywords

Bush beating Flossing Husking Substrate use Wiping Wrapping 

Introduction

Animals employ different foraging techniques, with spatial and temporal variability, to access food resources in heterogeneous environments (King 1986). Some of the food items are encased or embedded in a matrix and are not visible to the naked eye which makes it difficult for an animal to acquire them. To counter such difficulties and to maximize their foraging efficiency, animals develop various extractive foraging techniques using distinct manipulative skills (Parker and Gibson 1977). Extractive foraging has been reported across animal taxa, from birds to mammals, and it involves innovative techniques ranging from dexterous manipulation to tool use. Egyptian vulture (Neophron percnopterus) uses a stone as a tool to break the outer shell of the ostrich egg (Goodall and Goodall 1966), and New Caledonian crow (Corvus moneduloides) manufactures tools from dry grass to extract lizards from crevices (Troscianko et al. 2008). Various taxonomic groups of mammals, from rodents (giant kangaroo rat, Dipodomys ingens; Ewer 1968) to great apes (chimpanzee, Pan troglodytes; Watts 2008), employ diverse extractive foraging techniques. Among them, some techniques require a high degree of sensorimotor intelligence and manipulation (Melin et al. 2014). For example, where pigs (Sciurus sp.) use dexterous manipulation to break a nutshell, chimpanzees use stone tools to perform the same task (Ewer 1968; Sugiyama and Koman 1979). Similarly, the stone tools are used by sea otter (Enhydra lutris) to crack exoskeletons of mussels, crabs, and urchins by pounding them over a stone (Hall and Schaller 1964), and long-tailed macaques (Macaca fascicularis) break oyster, gastropods, and swimming crabs by cracking them with stones (Malaivijitnond et al. 2007).

As expected, primates possess a repertoire of wide and diverse foraging techniques. However, the diversity of extractive foraging behavior largely varies between taxonomic groups (King 1986; Yamakoshi 2004). For example, baboons (Papio sp.) and macaques (Macaca sp.) dig out soil for underground bulbs and tubers using their hands (Dunba 1977; Wheatley 1988), whereas capuchins (Sapajus sp.) perform the task with the help of tools (Moura and Lee 2004). Though all primate species use their hands, mouth, or feet in context-specific extractive foraging, the extractive foraging using tools has been observed only in capuchins (Moura and Lee 2004), great apes (Watts 2008), and macaques (Chiang 1967; Malaivijitnond et al. 2007; Tan et al. 2016).

Having a high level of sensorimotor intelligence, macaques show a variety of extractive foraging techniques distributed from the use of manual dexterity to tool-aided foraging behaviors (Wheatley 1988; Malaivijitnond et al. 2007; Tan et al. 2016). Food preparation by removing inedible parts of food items is widely seen in different macaque species and populations (Yamakoshi 2004). A Japanese macaque (M. fuscata) population of Koshima washed sweet potatoes in water (Kawamura 1959) and Balinese long-tailed macaques (M. fascicularis fascicularis) were seen to clean clayish cassava root in ditches (Wheatley 1988). Bonnet macaques (M. radiata; Kuruvilla 1980) and Japanese macaques (Yamakoshi 2004) were also seen to remove bitter pulp of food by rubbing it against a tree bark. In rainforests of the Western Ghats, lion-tailed macaques (M. silenus) used the leaf to remove caterpillar hair before ingesting it (Hohmann 1988), while long-tailed macaques (M. f. fascicularis) of Singapore were seen to remove ants from fruits by rubbing the fruit with dry leaves (Chiang 1967). Long-tailed macaques of Nom Sao Island removed glochidia from Opuntia cacti by using sand, rock, and water in a series of manipulative techniques (Tan et al. 2016). Some populations of Burmese long-tailed macaques (M. f. aurea) along the Andaman Sea coast of southern Thailand (Malaivijitnond et al. 2007; Gumert et al. 2009, 2011; Tan et al. 2015), and one population of hybrids (M. f. fascicularis × M. f. aurea) on Koram Island in the Gulf of Thailand (Tan 2017), use tools habitually to crack gastropods in the coastal environments.

The Nicobar long-tailed macaque is endemic to three islands viz. Great Nicobar, Little Nicobar, and Katchal in the Andaman and Nicobar archipelago of India (Umapathy et al. 2003). Since, other long-tailed macaques show a diverse and complex repertoire of extractive foraging techniques, specifically in the island systems with high variations in environments and distribution of food resources, we expected a variety of extractive foraging methods in the Nicobar long-tailed macaque. Here we report a detailed account of the substrate use and the tool-aided extractive foraging and other related behaviors recorded in a wild Nicobar long-tailed macaque group in the Great Nicobar Island. The observations might help in understanding the adaptive capability of this widespread species occupying a large variety of habitat types.

Materials and methods

Study site

We conducted the present study in the Great Nicobar Biosphere Reserve of the Great Nicobar Island (895.48 km2) which lies between 93°38ʹ05.6″–93°57ʹ13.7″E and 6°44ʹ7.8″–7°13ʹ46.6″ N in the Bay of Bengal. Being a tropical island, the Great Nicobar receives 4200 mm of rainfall with temperature ranging between 22 and 32 °C. Vegetation of the island consists of moist evergreen forest, coastal mangroves, coastal littoral forest, and freshwater swamps with commercial plantations of coconut and betel nut (Velankar et al. 2016).

Study subjects

We selected a group of Nicobar long-tailed macaques with 20 individuals (group name TR) at Campbell Bay, a coastal village in the Great Nicobar Island. The group ranged over the village and part of a nearby forest. The group demography varied from 3–2 adult males, 3–2 adolescent males, 8–7 adult females, 3–0 juveniles, and 3–0 infants during the study period.

Methods

Data on extractive foraging by the TR group was collected over 1660 h of observation between December 2013 and April 2015, as part of a larger study on their ecology and behavior carried out between August 2013 and December 2015. Three observers conducted dawn (0600 h) to dusk (1830 h) follows of the TR group, during which they collected behavioral data using focal and scan sampling, supplemented with all-occurrence sampling for extractive foraging events. In focal animal sampling, one individual was randomly selected and followed for 10 min at a time and data on each activity along with foraging and manipulative behaviors was recorded with time (seconds) in a predesigned data sheet. Group scan sampling was conducted on all the visible individuals of the TR group for 5 min at 30-min intervals to collect data on major behavioral states viz. feeding (ingestion of food), foraging (searching and extracting food), moving (moment on trees and ground), resting (sleeping and sitting), socializing (grooming, play, aggressive, and affiliative interactions), and social association (proximity between individuals). Depending on the feasibility, some events of extractive foraging were recorded on video using a Sony HSC 200 V camera to understand the mode of operations as well as for documentary evidence. In each extractive foraging event, we recorded the age-sex class of the subject viz. adult male, subadult male, adult female, juvenile, and infant. In total, we recorded extractive foraging events from 15 individuals that included three adult males, three subadult males, seven adult females, and two juveniles.

Results

Description of behaviors

We observed seven complex manipulative behaviors that included six extractive foraging and a tool-aided teeth flossing behaviors. These behaviors were grouped into four categories based on their apparent purposes, behavioral components, and materials used (Table 1). Of these behaviors, we classified “wrapping”, “wiping”, and “teeth-flossing” as tool-aided behaviors where macaques used both natural and synthetic materials like leaves, twigs, plant parts, feathers, wire, thread, and cloth. Occasionally, some individuals modified these materials prior to use by splitting, ripping, and removing them from matrixes, and we describe these behaviors as tool modification.
Table 1

Extractive foraging behaviors by individuals of different age-sex classes of the TR group

Category

Behavior

Purpose

Mode of operation

Substrate

Cases per age-sex classes

Total cases

Adult male (N = 3)

Subadult male (N = 3)

Adult female (N = 7)

Juvenile (N = 2)

No. of cases

Individual involved (%)

No. of cases

Individual involved (%)

No. of cases

Individual involved (%)

No. of cases

Individual involved (%)

No. of cases

Individual involved (%)

Coconut processing

Husking

Raw coconut feeding

Peel

22

3 (100%)

16

3 (100%)

42

7 (100%)

3

2 (100%)

83

15 (100%)

Coconut pounding

Coconut shell breaking

Pound

Earth, log, rock

15

3 (100%)

9

3 (100%)

12

4 (57%)

1

1(50%)

37

11 (73%)

Food washing

Tool-aided food rubbing

Cleaning food item

Wrap, rub, bite

Leaf, twig, paper, polythene

12

2 (67%)

27

3 (100%)

17

2 (29%)

0

0 (100%)

56

7 (47%)

Food rubbing by hand

Cleaning food item

Rub

7

2 (67%)

16

3 (100%)

19

6 (86%)

3

1 (50%)

45

12 (80%)

Washing

Cleaning food item

Wash

Water

0

0 (0%)

3

2 (67%)

2

1 (14%)

1

1 (50%)

6

4 (27%)

Flossing

Teeth flossing

Cleaning teeth (?)

Floss

Grass, wire, coir, plant fiber

3

1 (33%)

12

3 (100%)

10

5 (71%)

0

0 (0%)

25

9 (60%)

Invertebrate foraging

Bush beating

Invertebrate foraging

Beat

9

3 (100%)

4

2 (67%)

4

2 (29%)

0

0 (0%)

17

7 (47%)

Coconut processing

In the tropical Andaman and Nicobar archipelago, coconut (Cocos nucifera) is abundant as it is cultivated by the islanders as an economic crop. As a result of the non-seasonal continuous fruiting and a long development period, there are always coconuts of different maturity stages available in the trees and those fallen on the ground. Nicobar long-tailed macaques feed on coconut regularly. The macaques were observed to feed on the endosperm of coconut and to also drink coconut water. However, all the edible parts of a coconut are encased in a multilayered matrix. The macaques were observed to extract these edible parts by employing complex manipulative processes that are described here (Figs. 1, 2).
Fig. 1

Tender coconut husking by an adult Nicobar long-tailed macaque male. a Individual started husking a mature coconut by biting one terminal part of it, b pulling the ripped husk with their teeth while holding the coconut on the ground with their hands, c, d repeatedly husking the coconut with their teeth while holding it on the ground with both hands and legs

Fig. 2

Different stages of coconut processing by Nicobar long-tailed macaques. a Tender coconut husking by an adult male, b drinking coconut water after partially removing of husk, c eating endosperm, d coconut attached with stalk after in situ processing, e, f husking mature dry coconut, g biting complete dehusked coconut to crack the shell, and h eating endosperm from cracked coconut shell

Husking

Macaques were observed to use husking to extract endosperm and water by removing the outer fibrous covering (exocarp and mesocarp) of the coconut fruit. Macaques either plucked the coconut or used it directly while it was still attached to a tree. They used two different strategies to pluck the coconuts: detaching the coconut with their teeth while holding it with hands, or twisting it along its horizontal axis using hands. The plucked coconut was carried to a suitable place such as midrib of a leaf of the tree, branches of another tree, a concrete wall, or it was dropped to the ground. However, an unplucked coconut which was still attached to a tree was processed in situ. In either case, the animal removed the outer fibrous layer using teeth. An individual bit on either terminal of the coconut and tore out a portion of the fibrous covering by pulling the coconut head backward while holding it on the substrate. While husking, both hands and legs were used either alternatively or simultaneously to hold the coconut firmly on the substrate. They repetitively removed the husk until an access was made to the edible part. For a tender coconut, once the fibrous covering was removed, endosperm was exposed as a result of the absence of hard inner shell (endocarp). Hence, after partial removal of the husk, macaques accessed the endosperm and water. However, in the case of a matured coconut, they had to completely remove the husk because the endosperm is encased in a tough outer shell which also has to be broken. A total of 83 husking events were recorded and all individuals were observed to perform these behaviors; adult males, subadult males, adult females, and juveniles engaged in 22, 16, 42, and 3 events, respectively (Table 1).

Coconut pounding

Pounding was employed by macaques to crack the hard inner shell of a matured coconut to access the endosperm. After completely removing the exocarp and mesocarp by husking, macaques pounded the dehusked coconut to break the shell. Macaques lifted the coconut and pounded it repeatedly using either one or both hands on a substrate until a fissure was formed on the shell (Supplementary video 1). Then, they used their canines over the fissure to crack open the shell. A total of 37 coconut pounding events were recorded; adult males, subadult males, females, and a juvenile performed 15, 9, 12, and 1 events, respectively.

Food washing

Food washing included three techniques where macaques removed the non-edible particles like hair, thorn, mud, soil, and sand from the food items by using various substrates and materials.

Tool-aided food rubbing

The tool-aided food rubbing behavior was seen with two sequences, i.e., wrapping and wiping.

Wrapping: If a food item was covered with thorns, hairs, or mud, macaques procured materials such as leaves, branches, paper, cloth, or polythene sheets from the vicinity. They wrapped these materials over the food items. In addition to the readily available material, macaques also procured and processed these materials from the nearby plants either by breaking the twig with bunches of leaves or by bending a leafy branch using both hands and detaching it using their teeth. They also wrapped a leafy branch or broad leaves over the food items without detaching them from the stalk (Fig. 3).
Fig. 3

A subadult male modifying a tool by cutting it from a plant to perform wrapping over a dehusked coconut. a, b Individual detaching a twig from a plant with their teeth while kept a dehusked coconut in front; c using hands to completely detach the twig from the stalk and d wrapping the twig over the dehusked coconut

Wiping: After wrapping those materials over the food items, the macaques often wiped the food with the help of hands. Then they bit or ate over the wrapped portion of a food item (Supplementary videos 2 and 3).

These tool-aided food rubbing techniques were observed for food items such as husked coconut, cashew nut (Anacardium occidentale), Indian bael (Aegle marmelos), Pandanus fruit, or closed plastic containers with food. Except for juveniles, all other age-sex classes were observed to perform the tool-aided food rubbing behavior (N = 56). Adult males, subadult males, and adult females were observed to perform the tool-aided food rubbing 12, 27, and 17 times, respectively.

Food rubbing by hand

Macaques were observed to clean the small seeds, fruits, and the edible vegetative parts which could fit in their palms before ingestion. The food item was kept between the two palms and they moved the hands repeatedly in opposing directions, thus rubbing the food item in the process before ingesting it (Supplementary video 4). A total of 45 food rubbing events with their hands were observed; the adult males, subadult males, adult females, and juveniles performed 7, 16, 19, and 3 times, respectively.

Washing

The macaques were observed to wash food items while foraging in puddles, water holes, and freshwater swamps. Food items including tubers and fruits were extracted from the muck and washed in a water body. After extraction, the food items were dipped and rinsed by holding them in a hand while swaying it on the water surface to remove the mud. A total of 6 events were performed by subadult males, adult females and juveniles 3, 2, and 1 times, respectively. Adult males were not observed to perform this behavior.

Teeth flossing

Macaques were observed to take a grass blade, a Casuarina needle, a feather, a nylon thread, or a metal wire and perform teeth flossing (Fig. 4). A macaque put one of these objects between its teeth and closed its mouth such that either of the tips of the object was exposed. The exposed tip was then held by a hand and pulled out (Supplementary video 5). This behavior was repeated several times and was performed while the macaques were resting after a foraging session. Except for juveniles, all other age-sex classes performed teeth flossing. A total of 25 teeth flossing events were recorded; adult males, subadult males, and adult females performed 3, 12, and 10 events, respectively.
Fig. 4

An adult female flossing her teeth with a metal wire

Bush beating

Bush beating was employed by the macaques to forage on invertebrates from the bushy open scrub vegetation. Macaques were seen to forage on invertebrates like grasshoppers, moths, and other insects from the ground vegetation that comprised grasslands with small scattered bush patches. Macaques beat the bush using their hands. The flushed invertebrates were caught on the ground or from the air. Sometimes when the grasshoppers escaped and relocated to other bushes, macaques followed them and again flushed them out by beating the bush. We recorded 9, 4, and 4 such events by adult males, subadult males, and adult females, respectively.

A total of 269 events of complex manipulative behaviors were recorded during the study. Among age-sex classes, subadult males and females were observed to perform all seven behaviors, while juveniles were not seen performing food rubbing, bush beating, and teeth flossing (Table 1).

Discussion

The present study is a detailed report on extractive foraging and tool-aided behaviors in the Nicobar long-tailed macaque which is confined to three remote islands of the Nicobar group of islands of India. The extractive foraging techniques employed by the Nicobar long-tailed macaque included manipulative methods like husking and coconut pounding to access water and endosperm from the multilayered matrix of coconut, bush beating to forage on invertebrates from bushes, and tool-aided food rubbing to make the food items ingestible by removing inedible parts like mud, dirt, thorn, or hair. Another interesting tool use behavior of Nicobar long-tailed macaques was teeth flossing by putting thin objects between teeth. The variety of extractive techniques, some of which required prior knowledge about a hidden resource and a tentative plan to access it, indicate a high level of sensorimotor intelligence in this species.

Macaques are known to engage in various extractive foraging techniques (King 1986; Yamakoshi 2004) that involve manipulation, simple tool use, and complex tool manufacturing (Sinha 1997). One of the most widely available fruit in habitats of a large number of macaque species is the coconut. However, coconut eating varies between species and populations. For example, the black macaque (M. nigra; O’Brien and Kinnaird 1997) and the Tonkean macaque (M. tonkeana; Erwin and Southwick 1992) were not seen to feed on the coconut, while only one group of the moor macaque (M. maurus; Supriatna et al. 1992) fed on this fruit on the Sulawesi Islands. Even the trained “coconut harvester” pigtail macaque (M. nemestrina) showed little interest in coconut eating (Bertrand 1966). However, apart from the Nicobar long-tailed macaque (Umapathy et al. 2003), rhesus macaque (M. mulatta) in Cayo Santiago (Hauser and Marier 1993) and Bangladesh (Jaman and Huffman 2013) and M. f. fascicularis in Bali (Wheatley 1988) are known to feed on the coconut. Balinese M. f. fascicularis were reported to drink coconut water after husking the outer fibrous cover and to eat endosperm after scooping it with their hands, though they were not observed to break the coconut shell by pounding it on a hard surface. There was a historical record (by J. Berard in 1938) of pounding hard endoderm shell by two individuals of rhesus macaques in Cayo Santiago (Visalberghi and Fragaszy 1990), and recently a single male was observed to break a coconut shell by underhand vertical throw in the same population (Comins et al. 2011). So far, the present study is the first detailed description of coconut extracting techniques which may help us to further understand the diversity of complex manipulative behaviors to access encased food items in Nicobar long-tailed macaques.

Various techniques are used by different species of macaques for cleaning and removing the non-edible parts from food items (Yamakoshi 2004). These techniques include leaf washing and leaf rubbing to remove the dirt or non-edible parts, e.g., a leaf is used to remove the hairs from a caterpillar by M. f. fascicularis (Chiang 1967; Wheatley 1988) and M. silenus (Hohmann 1988); Opuntia fruit was observed to be rubbed on sand or a rock to remove the irritant hairs by M. f. fascicularis (Tan et al. 2016); fruits are rubbed on tree bark to remove dirt by bonnet macaques (Kuruvilla 1980). Similarly, Japanese macaques rubbed fruit on tree bark to remove the bitter pulp of the fruits (Yamakoshi 2004), and one individual was observed to roll a frog on a tree trunk before ingesting it (Suzuki 1965). Tool-aided food rubbing, food rubbing by hand, and food washing observed in the Nicobar long-tailed macaque have also been observed in M. f. fascicularis (Chiang 1967; Wheatley 1988). In Singapore and Bali, these macaques were seen to roll fruits and seeds over the ground with an open palm and also rubbing them with leaves after putting them between their palms. However, Nicobar long-tailed macaques use both natural and synthetic materials to wrap and rub over the food items. The technical components of tool-aided food rubbing are similar to the leaf washing and leaf rubbing behavior seen in M. f. fascicularis of Singapore and Bali (Chiang 1967; Wheatley 1988). Nicobar long-tailed macaques were also observed to process the material by breaking the branches of plants or twigs or ripping readily available materials for rubbing the food items. To our knowledge, this is the first spontaneous and idiosyncratic material processing behavior seen in a wild long-tailed macaque.

Food washing was first observed in a female Japanese macaque, which washed sweet potatoes in water (Kawamura 1959), and later this behavior got propagated within a provisioned group (Kawai 1965). Wheatley (1988) reported washing clayish fruit and digging up sweet potato and cassava root in a stream and a ditch respectively by M. f. fascicularis. Similarly, the Nicobar long-tailed macaque was observed to wash tubers and fruits in water after digging them from the muck of puddles. The food washing technique is discussed as an extractive foraging technique for its immense contribution to the understanding of the material culture in primates (Kawamura 1959; Izawa 1982; Wheatley 1988).

The Nicobar long-tailed macaques kept a food item on its palm and rubbed it by hand to clean it before ingestion, which is similar to the behavior performed by bonnet macaques (Kuruvilla 1980), lion-tailed macaques (Hohmann 1988), and Balinese long-tailed macaques (Wheatley 1988). Nevertheless, the type of food items and the mode of operations are identical to the previous records on other species and subspecies. The apparent purpose and mode of operation of all three food processing behaviors recorded in Nicobar long-tailed macaques were also observed in other macaques; however, the complexity and composition of those manipulation techniques vary between species, subspecies, and even populations.

The teeth flossing is a tool-aided behavior recorded only in two species of macaques, i.e., Japanese macaques (Leca et al. 2010) and Thai long-tailed macaques (Watanabe et al. 2007). An adult female of Japanese macaques was observed to floss her teeth with her own fur, and that of a neighboring individual (Leca et al. 2010), by “stretching with mouth”, “stretching with hand”, and “plucking” techniques to floss. The free-ranging M. f. fascicularis of Lopburi, Thailand used human hair and coconut shell fiber to floss their teeth (Watanabe et al. 2007). Although the use of human or animal hair was not observed in the Nicobar long-tailed macaque, the materials used were similar in physical characteristics to the flossing materials used by the other macaques. Nicobar long-tailed macaques used only one hand to floss their teeth, which is dexterously analogous to “stretching by hand” in the Japanese macaque (Leca et al. 2010) and M. f. fascicularis (Watanabe et al. 2007).

Invertebrates are one of the major faunal components in the diet of many of the macaque species (Menard 2004). Apart from manual dexterity, olfactory, and auditory cues, macaques also need prior information on hiding places of invertebrates which indicates intelligence to find the hidden invertebrates (King 1986). Apart from manually exploring, the Nicobar long-tailed macaque utilized the bush beating technique to catch the hidden invertebrates. Therefore, the bush beating technique implies that these macaques have a conceptual understanding of hiding places of invertebrates. Melin et al. (2014) suggested that the dependency on insectivory is one of the primary factors acting on shaping the evolution of dexterity in primates. They argued that the evolution of primarily specialist feeding diet like insectivory increased spatiotemporal intelligence, cognitive mapping, and sensorimotor intelligence, which help in acquiring the information on where, when, and how to find insects.

The two components of extractive foraging, i.e., finding and extracting food items, are independent acts (King 1986). In the first case, an animal should have the ability to consider the temporary absence of the stimuli to locate a hidden food source, while the other case requires skills to remember and plan the process and to react to multiple variables simultaneously (Menzel and Wyers 1981). Nicobar long-tailed macaques perform various extractive foraging techniques like husking, coconut pounding, tool-aided food rubbing, washing, and bush beating to extract the inaccessible food items. Therefore, the performing ability of these tool-aided extractive foraging techniques implies that the Nicobar long-tailed macaque has complex manipulative skills with advanced sensorimotor intelligence (van Schaik et al. 1999). The present study sets the stage for further exploration about the spread of the complex foraging techniques among the group members and a possible cultural transmission of behaviors across generations.

Notes

Acknowledgements

The present research was supported by the Department of Science and Technology, Government of India (Grant no. SR/SO/AS-49/2011) to HNK and INSPIRE fellowship, Department of Science and Technology, Government of India (Grant no. A.20020/11/97-IFD.DT.31.03.2010) to A. Pal. We thank Principal Chief Conservator of Forests, Port Blair, Andaman and Nicobar islands for permitting us to carry out the field work (Permit no. CWLW/WL/134/566). We thank the local people of Campbell Bay for being helpful throughout the study. MS and PSM thank SERB for the award of a J.C. Bose Fellowship during which this article was prepared. We also acknowledge the anonymous reviewers and the handling editor whose comments helped enhance the quality of this article.

Compliance with ethical standards

Ethical approval

This study was approved by the Ethical Committee for Animal Research of Sálim Ali Centre for Ornithology and Natural History, Coimbatore. It also adhered to the guidelines and principles of the Ministry of Environment, Forest and Climate Change, Government of India. Further, permission to carry out this study was granted by the Andaman and Nicobar Forest Department (Permit no. CWLW/WL/134/566).

Supplementary material

Video 1 An adult male performing coconut pounding to break outer shell of a dehusked coconut (MP4 15882 kb)

Video 2 A subadult male employing tool-aided food rubbing by rubbing dry leaves over a cashew nut to remove latex (MP4 47576 kb)

Video 3 A left-hand amputee adult male modifying a tool by detaching it from tree twigs and wrapping it over dehusked coconut shell (MP4 455270 kb)

Video 4 An adult female cleaning sand from food items by employing food rubbing by hand technique (MP4 27847 kb)

Video 5 A subadult male flossing teeth with a feather (MP4 16030 kb)

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Copyright information

© Japan Monkey Centre and Springer Japan KK 2017

Authors and Affiliations

  • Arijit Pal
    • 1
    • 2
  • Honnavalli N. Kumara
    • 1
  • Partha Sarathi Mishra
    • 1
    • 3
  • Avadhoot D. Velankar
    • 1
    • 2
  • Mewa Singh
    • 4
    • 5
  1. 1.Sálim Ali Centre for Ornithology and Natural HistoryCoimbatoreIndia
  2. 2.Manipal UniversityManipalIndia
  3. 3.Bharathiar UniversityCoimbatoreIndia
  4. 4.Biopsychology Laboratory and Institution of ExcellenceUniversity of MysoreMysoreIndia
  5. 5.Organismal Biology UnitJawaharlal Nehru Centre for Advance Scientific ResearchBangaloreIndia

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