Int J Primatol (2008) 29:543–548 DOI 10.1007/s10764-007-9176-y

Fishing in Macaca fascicularis: A Rarely Observed Innovative Behavior Anne-Marie E. Stewart & Chris H. Gordon & Serge A. Wich & Philippa Schroor & Erik Meijaard

Received: 26 October 2006 / Accepted: 12 July 2007 / Published online: 1 April 2008 # Springer Science + Business Media, LLC 2007

Abstract Observations of fishing behavior in nonhuman primates are rare and isolated, and there is no prior published observation on the behavior in long-tailed macaques (Macaca fascicularis). We observed fishing behavior in 3 groups of longtailed macaques from 2 separate study sites in North Sumatra and East Kalimantan, Indonesia. We propose that the behavior is rare and fulfills the requirements for classification as innovation. Further, all of the fishing individuals were watched by other members of their group, with their actions inciting attempts at fishing by them. We consider the possibility that the behavior has the potential to become cultural within the populations. Keywords Borneo . culture . diet . fishing behavior . innovation . primates . Sumatra

Introduction Son (2003), Wheatley (1980), and Yeager (1996) described the diets of long-tailed macaques (Macaca fascicularis) in detail. They are omnivorous, but consume mainly leaves, seeds, and fruit. In fact, researchers generally believe that omnivory in macaques is imposed rather than chosen (Corlett and Lucas 1990). For instance, Berenstain (1986), reported that long-tailed macaques fed primarily on fruits until a major fire destroyed the resource; then they switched to insects, stems, leaves, and dipterocarp seeds. The studies of Ungar (1995), Wheatley (1980), and Yeager (1996) A.-M. E. Stewart (*) : C. H. Gordon : P. Schroor : E. Meijaard The Nature Conservancy, East Kalimantan Programme, Samarinda 75123, East Kalimantan, Indonesia e-mail: [email protected] S. A. Wich Great Ape Trust, 4200 SE 44th Ave, Des Moines, IA 50320, USA E. Meijaard School for Archaeology and Anthropology, the Australian National University, Canberra, ACT 0200, Australia

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on the feeding quotas of long-tailed macaques showed that the selection of fruits varies regionally by as much as 25%, whereas comparisons with sympatric primates proved that they readily select fruits over other foods (Ungar 1995; Yeager 1996). The diets of long-tailed macaques may also contain fungi, vertebrates, and invertebrates, including insects, frog eggs and crabs (Payne and Francis 1998; Son 2003). Indeed, long-tailed macaques are also referred to as crab-eating macaques. Here, we report on observations of previously unrecorded fishing behavior in longtailed macaques and speculate on the nature of the activity, thereby adding to our understanding of macaque feeding behavior and further emphasizing their ecological flexibility.

Methods We opportunistically recorded long-tailed macaque behavior while carrying out other field surveys in 2 sites in Indonesia: Ketambe River (03°41′ N, 97°39′ E), Leuser Ecosystem, Sumatra, and the Lesan conservation area (01°36′ N, 117°10′ E), a Nature Conservancy (TNC) program site in East Kalimantan. We considered the behavior to be rare, as confirmed via a literature search in the following online databases: Zoological Record (1978–current), Current Contents (1993–current), and ISI Web of Knowledge. We selected and contacted all zoologists who had studied foraging behavior in wild long-tailed macaque populations over a significant time, asking how many hours they had spent observing macaques at their respective sites, and whether they had ever observed fishing behavior. Observations We observed the macaques on 3 separate occasions, in 3 separate groups and from 2 different sites over 8 yr. Our first observation, on April 14, 1998 at 1045 h, was of a group of long-tailed macaques along the Ketambe River, North Sumatra. The river often contains areas where the water flow is very slow or where temporary pools are formed. Five females sat on rocks in one of the pools and seemed to be scanning the water. The rest of the group was in the forest, in trees and on the ground. After 3 min, 1 female with a small infant clinging to her bent closer to the water and grasped a fish. She used both hands and quickly ingested it. The fish was ca. 15 cm long, and she chewed it for 2 min before swallowing it completely. While eating the fish, she remained seated on the rock whence she caught it. The fish tail hung out of her mouth for a short time, and the infant tried unsuccessfully to grasp it. The 4 other females watched her while she ate the fish, but soon returned to staring at the water. At 1055 h, a different female reached for the water but caught nothing. It was not possible to see whether she tried to grasp a fish or something else. On April 29, 1998 at 1320 h, in another location along the Ketambe River, 3 females from a different long-tailed macaque group sat on rocks along the river’s edge, at a section where it flowed very slowly. The rest of the group were in trees along the riverbank. At 1326 h, 1 of them quickly reached into the river but caught nothing. Shortly afterwards, the second female also reached into the water, and with both hands caught a ca. 15-cm fish. In 2 min she consumed it. The 2 other females

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intently watched her, until finally the third female also reached into the water. However, she was unsuccessful, and it is unknown whether she attempted to grasp a fish or another object. The 3 females remained at the river’s edge for another few minutes, and then moved into the forest. The third observation was 1750 km to the east in the Lesan conservation area. On March 22, 2006, at 1530 h, we observed a troop of long-tailed macaques foraging along the riverbank, ca. 100 m away from us. Most of the troop remained concealed in the dense riverine vegetation, occasionally approaching the river to drink. However, 3 adult macaques (undetermined sex) moved onto the rocks in a shallower section of the river and stayed in the open for ca. 20 min. The river has a rocky substrate and one can regularly see fish from the banks. The adults were staring at the water and it appeared as though they were watching fish swimming in the shallows. Our assumptions were confirmed when, on 2 separate occasions, a macaque reached into the water and swiftly grasped a ca. 20-cm fish before retreating back into the vegetation with it in its mouth.

Discussion Despite ca. 20,000 h of observations of long-tailed macaques feeding by 16 researchers (Table 1), we are the first to note active fish catching. Son (2003) probably spent the most time observing long-tailed macaque feeding behavior in a largely aquatic environment. Though he documented a total of 14 animal species as part of their diet, he did not observe fishing. Similarly, despite 5000 h of

Table 1 Extensive studies of long-tailed macaques Source

Year Location

Fishing observed

Berenstain Bernstein (pers. Comm.) de Ruiter (pers. Comm.) Fooden (pers. comm.) Hedges (pers. comm.) Lucas and Corlett Poirier and Smith Son Southwick and Cadigan Sterck and Steenbeek Sussman and Tattersall Ungar van Noordwijk et al. van Noordwijk and van Schaik Wheatley Yeager

1986 Kutai NP, East Kalimantan 1967 Malaysia Ketambe River, Sumatra 1971 Thailand 2000 Baluran NP, Java 1998 Bukit Timah NR, Singapore 1974 Angaur Island, Micronesia 2003 Can Gio Mangroves, Vietnam 1972 West Malaysia 1997 Ketambe River, Sumatra 1981 Mauritius 1995 Ketambe River, Sumatra 1993 Ketambe River, Sumatra 2001 Ketambe River, Sumatra

No No No No No No No No No No No No No No

1500 a 5000 b 200 1000 250 1260 900 720 125 500 470 5000

1982 Kutai NP, East Kalimantan 1996 Tanjung Puting NP, Central Kalimantan

No No

1000 1500

a b

Study not conducted in a riverine setting. Hours of observation not recorded.

Hours observed

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observations in a riverine environment, van Noordwijk and van Schaik (2001), did not see fish-catching. However, Van Schaik (pers. comm.) recorded long-tailed macaques handling and smelling fish killed by fishermen, without actually consuming them. Yeager (1996) studied long-tailed macaques in Central Kalimantan for several years. Macaques occasionally reached into small shallow ponds, but never caught fish (Yeager, pers. comm.). Researchers have recorded fishing behavior in several other primate species: Japanese macaques (Macaca fuscata yakui: Watanabe 1989), chacma baboons (Papio ursinus: Hamilton and Tilson 1985), olive baboons (Papio anubis: Ransom 1981), chimpanzees (Pan troglodytes: Nash 1981) and rehabilitated orangutans (Pongo pygmaeus: Russon and Kuncoro, pers. comm.). Watanabe (1989) first recorded fish-eating among nonhuman primates in a group of Japanese macaques on Koshima Island in 1979, with adult males living on the periphery of the group being the first to exhibit the habits. The early reports described macaques stealing fish from anglers, or eating dead fish that had washed up on the beach. de Waal (2001) later recorded active fishing behavior among the Japanese macaques of the Koshima population, where they caught fish and small octopi, from rock pools. Likewise, Hamilton and Tilson (1985) recorded chacma baboons catching fish in drying Namibian desert waterholes. Russon and Kuncoro (pers. comm.) twice observed rehabilitated orangutans attempting to fish on Pulau Kaja, in Central Kalimantan. On 1 occasion, an adolescent female tried unsuccessfully to catch fish by wading waist-deep into a pond on the island and driving the fish with her outstretched hands. The second observation involved an adolescent male that, during the middle of the dry season, caught and consumed a weakened fish from a very shallow, slow-flowing river. Long-tailed macaques are comfortable in aquatic environments, with large groups sometimes wading up to their necks in the sea or into the mud, looking for crabs and razor clams (Son 2003; Meijaard, pers. obs.). Fish consumption may be just a rarely observed behavior linked to their ability to extract food from aquatic environments. However, one wonders whether the effort and skill required to catch live fish from a fast-flowing river is an opportunistic behavior driven by resource scarceness. Hamilton and Tilson (1985) suggested that situations in which monkeys can catch live fish in their habitats are probably rare. de Waal (2001), Hamilton and Tilson (1985), and Russon and Kuncoro (pers. comm.) recorded primates catching fish that were trapped in small pools or shallow water. Though our observations in Ketambe were in a slow-flowing section of river, where the macaques fished along the Lesan River, there were no such small pools in which the fish could be trapped. Small, sheltered pools form in the Lesan River during the dry season when the water level is lower, but in March, the water was fast flowing and we noted no pools. Watanabe (1989) noted that the Japanese macaques did not seem to have a particular fondness for raw fish, and attributes their consumption of fish to changes in the nutritional status of their habitat. When other food was available to them, the macaques did not eat fish. Forest fruit supplies in Lesan were probably low in March, based on our phenological observations, but it does not necessarily mean that the fishing activities were imposed by a lack of other foods. In Ketambe, fruit availability was high during the period of fishing. The fishing behavior of the long-tailed macaques may not simply be a one-off opportunistic reaction to the presence of an obtainable food source. Instead, the

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subjects may have been displaying an innovative behavior in response to a particular environmental stimulus. Individuals may use some innovative behaviors only under unusual ecological or demographic situations, and thus they occur infrequently. However, this begs the question of whether the ecological conditions in Ketambe and Lesan are now different than before, and especially why, during the 11,500 h previously spent studying macaques in Ketambe, researchers did not observe the behavior. Van Schaik et al. (2006) found that the first 4 mo of their 3-yr orangutan (Pongo abelii) study coincided with unusually low fruit availability, and their subjects showed many innovative behaviors that they used rarely if at all during the next 2.5 yr. Owing to low fruit availability in March in our Lesan site, perhaps our long-tailed macaques may also have shown increased use of innovative behaviors. As Giraldeau et al. (1994) and Sol (2003) state, innovations affect ecology, by increasing a population’s niche breadth. However, one should be cautious when labeling a certain behavior innovative or cultural. Laland and Janik (2006) argue that one should adopt a more thorough consideration of the interplay among genetics, ecology, and culture when addressing the origin of behaviors. For behavior to be described as innovative, it needs to meet certain predetermined criteria. The first is that innovations are not universal in a given species (van Schaik et al.. 2006). A nonuniversal behavior is one that is absent in some populations or present at low occurrence in all populations. The second is that individuals that do not perform the behavior do so because they lack the knowledge to perform it, and not because of some observational error (van Schaik et al. 2006). We recognize that our observations were fleeting and that researchers have not studied the populations further. We therefore suggest follow-up studies to determine whether the behavior occurs regularly in the focal areas and in neighboring populations where ecological circumstances allow. Innovation drives cultural change (de Waal 2001), and cumulative culture requires repeated innovation (Boyd and Richerson 1996; Henrich and McElreath 2003). Innovations performed more often are more likely to reach cultural status within a population, while across populations, innovations that increase comfort are less likely to become cultural than those that meet subsistence needs (van Schaik et al. 2006), such as fishing. The key to defining this as culture is to see whether the techniques are spreading and persist in the population because other individuals learned by observing the experts (van Schaik 2006). Only with continued studies and further observations of the behavior can we begin to consider whether fishing has indeed reached cultural status.

Acknowledgments We thank Carel van Schaik and Anne Russon for their input and comments on an earlier draft of the manuscript; Irwin Bernstein, Jan de Ruiter, Jack Fooden, Simon Hedges, Peter Lucas, Charles Southwick, Liesbeth Sterck, Bruce Wheatley, and Carey Yeager for additional information on macaque studies; and Bonnie Metherall for library assistance. S. A. Wich thanks the Indonesian Institute of Science (LIPI, Jakarta) for cooperation and support of and the Indonesian Nature Conservation Service (PHKA) for permission to work in Indonesia. S. A. Wich also thanks Universitas Nasional (Jakarta) for their support throughout the years and the Netherlands Foundation for the Advancement of Tropical Research (WOTRO), the Netherlands Organization for Scientific Research (NWO), and the Leuser International Foundation Programme for financial and logistical support for the research at Ketambe.

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