Anthropol. Sci. 101(2), 187-193, 1993

Elimination of External Parasites (Lice) Is the Primary Function

of Grooming in Free-ranging Japanese Macaques

ICHIROU TANAKA 1 AND HARUO TAKEFUSHI2

1 Department of Anthropology, Faculty of Science, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113, Japan. 2 Jigokudani Monkey Park, Yamanouchi-machi, Nagano, Japan.

Received November 10, 1992

•ôGH•ô Abstract•ôGS•ô Grooming behavior was studied from September 1990 to May 1992 in the provisioned troop of free-ranging Japanese macaques (•ôNH•ôMacacafuscata•ôNS•ô) at Jigokudani Monkey Park, Japan. By confiscating what macaques picked up during

grooming, we found that macaques pick up lice (•ôNH•ôPedicinus obtusus•ôNS•ôand •ôNH•ôPedicinus•ôNS•ô •ôNH•ô eurygaster•ôNS•ô) and the eggs of lice and eat them. Slow motion video replays were used to discriminate the prey of grooming. Most (98.9%) of what Japanese macaques picked up and ate during grooming were the eggs of lice. Hence, allo

- grooming has an altruistic function to eliminate the external parasites on others. In particular, grooming of infants by mothers appears to be important maternal care. On the other hand, in Japanese macaques, grooming is also -feeding behavior, and such selfish benefit may favor grooming under individual natural selection.

•ôGH•ô Key Words•ôGS•ô: Japanese macaques, grooming, lice

INTRODUCTION

The function of grooming in is unclear (Goosen,1987). Allo-grooming

in primates is obviously important as fur-cleaning behaviour, although it appears

to go beyond the functional demands of cleaning in some species (Sparks, 1967).

Though grooming plays a role in the reduction of tension (Furuya, 1957) and the

promotion of social bonding (Carpenter, 1942), Alexander (1974) suggests that

grooming have evolved primarily as a disease controlling mechanism because external parasites are removed. This hygienic function of grooming in catarrhines

has been only suggested (Sparks, 1967; Goosen, 1987) although human beings

eliminate human lice (Pediculus humanus) (Sugawara,1986). Old world monkeys

are the natural hosts of lice and ticks (Kuhn, 1967) and most stroke their fur and

sometimes pick up something during grooming (Sparks, 1967). Furuya (1957)

suggested that Japanese macaques (Macaca fuscata) picked up and ate lice and the

eggs of lice. Two species of lice (Pedicinus obtusus and Pedicinus eurygaster) are

parasites on Japanese macaques (Kaneko, 1971). However, discrimination of lice from dandruff is not possible by visual observation alone. We investigated grooming 188 TANAKAAND TAKEFUSHI

function in Japanese macaques by directly seizing what macaques pick up during grooming.

METHODS Free-ranging Japanese macaques (Macaca fuscata) were researched at Jigokudani Monkey Park, the Shiga Heights, Nagano Prefecture Japan from September 1990 to May 1992. The ecological condition of the study area has been described in detail by Wada and Ichiki (1980). Sightseers are not permitted to feed the monkeys. Confiscation of What Japanese Macaques Pick up during Grooming Our first attempts to seize what Japanese macaques pick up during grooming resulted in failure, since the adult monkeys grimaced and threatened us. We were only able to obtain one imago on September 8 1990. On October 14 1990, a Japanese macaque mother named Tomoetake robbed her 1-year-old daughter of what the daughter had picked up while grooming and ate it. The daughter, however, remained calm, gazed at her mother's handling of the object for three seconds, and resumed grooming. Thus, we decided to follow suit. We selected two juveniles whom we could touch and accustomed them to the presence of our hands near the grooming site for several months. If these juveniles continued grooming under this condition, we attempted to remove what macaques pick up during grooming with a both-sided adhesive tape on our thumbs. During and after our intervention, these two juvenile macaques remained calm and continued grooming. Sampling Procedure We observed the monkeys using the focal- sampling (continuous record ing)method (Martin and Bateson,1986) for grooming dyads. To record the details of grooming behaviour, we used 8mm video cameras (SONY CCD-TR75, CCD- TR705, and CCD-TR900) with an external color LCD 4-inch monitor (SONY MGV-41), which permitted us to turn our eyes away from the eyes of macaques. Thus monkeys did not mind our observing their behaviour close by. During picking up something, Japanese macaques first grip something on hair with their first finger and thumb, second draw hair through the forefinger and thumb, third bring the object to the mouth, and fourthly eat it in sequence. Monkeys often repeat the first and the second until the object leaves the hair. During the video playback of grooming, we recorded when the groomer's fingertips came in contact with an object to be picked up and when that process was completed. Then we computed the duration of this behavioral sequence. If a temporal length included more than 1 second discontinuity of grooming, we excluded this lenght from the analysis of duration. We also calculated intervals from the end of one behavioral sequence to the start of the next. If an interval included more than 1 second discontinuity of grooming, we also excluded this interval from analysis. We Hygienic Function of Grooming 189

investigated 4475 behavioral sequences in which some object was removed during grooming by video observation on 157 grooming pairs (from 59 groomer) using database management software (IBM query & database managers in operating system/2 extended eidtion version 1.2) on IBM 8555-F61.

RESULTS

From 1990 to 1992, we succeeded seven times in seizing what Japanese macaques pick up during grooming (Table 1). One was a louse imago (Pedicinus species) (Fig. 1) and the other six were the eggs of lice. All the eggs were attached to a single hair with cement. This glue was situated below the egg and surrounded the hair of macaques like American doughnuts (Fig. 2).

Besides video observation, on September 27 1988, we observed that an adult female named Dokudami picked up a tick (Haemaphysalis longicornis) from her infant. She crushed the tick to death against a rock, then she wiped the fluid of the tick off her right hand by rubbing her hand over the rock. She killed but did not eat the tick. Thus, the handling of the tick differed from that of lice and lice eggs, because Japanese macaques ate all the eggs and imagoes of lice (see below).

We observed that the macaques ate what they had picked up during grooming

4475 times. As to the prey of grooming, video replays could discriminate imagoes from eggs: if macaques picked up an egg, the ring adhesive on the hair forced the monkeys to comb the egg along the hair with the nail of their first finger and the tip of their thumb; if macaques picked up an imago, they only picked up the insect free from fur. When lice were removed by mouth, macaques only licked off imagoes free from fur; they scraped lice eggs from hairs with teeth. Therefore, video analysis revealed that most (98.9%) of what Japanese macaques pick up during grooming were the eggs of lice: Japanese macaques picked up 4411 lice eggs, 48 lice imagoes, and 16 undistinguishable objects. It took 4.86•}0.07 sec (mean•}SEM, N=4345) to handle a louse (an egg or imago). The average interval between the end of one behavioral sequence and the start of the next is 11.0•}0.2 (SEM) sec (N=3331). if monkeys found imagoes, macaques often smacked their lips. Moreover, before eating lice imagoes, juvenile monkeys sometimes let loose their white insect prey on their black palms and gazed at the struggling louse for several seconds; this behavior enabled us to obtain our first sample (see Table 1). 190 TANAKA AND TAKEFUSHI

Fig 1. A louse imago which we robbed of a Japanese macaque in grooming (photographed by So-Ichi Imai). Its body length was 2.2mm. Hygienic Function of Grooming 191

Fig 2. The attachment of a louse egg on a macaque hair (photographed by Shin-Ichi Hayama). a: the egg of louse. b: the ring of cement. c: a macaque hair. The length of the egg was 0.6mm. 192 TANAKA AND TAKEFUSHI

Table 1. Confiscations of what Japanese macaques picked up in grooming.

a An egg was seized in self-grooming.

DISCUSSION We succeeded in seizing what Japanese macaques pick up during grooming seven times. One was an imago of louse (Pedicinus species) and the other six were the eggs of lice. Although a rare occurrence, a Japanese macaque also picked up and removed a tick, the other external parasite. These samples revealed that one of the functions of grooming is the elimination of external parasites. The suggested hygienic function of grooming (Sparks, 1967; Goosen, 1987) came true. Ehardt (1988) showed that Sooty mangabey (Cercocebus atys) adult females concentrated grooming on their offspring. Thus, grooming of infants by their mothers appears to be an important maternal care in monkeys, since the young appear to be vulnerable to blood-sucking . Juvenile Japanese macaques often scraped lice eggs from hairs with lower incisors like the toothcomb of prosimians that have narrow mazzles with four elongated lower incisors and two canines (Napier and Napier, 1985). These thin incisors appear to be suited for a dental comb, because small teeth can be used to scrape lice eggs from hairs precisely (Buettner-Janusch and Andrew, 1962). Juvenile macaques have also little incisors. Therefore, juveniles appear to be able to take off the eggs of lice accurately. As the teeth grow, this becomes inaccurate. Thus, adult macaques appear to use mainly the first fingers and their thumbs. Grooming in Japanese macaques is also insect-feeding behaviour because monkeys eat chiefly the eggs and rarely the imagoes of lice. In grooming, hence, stroking fur is searching for lice; picking up is the handling of lice. Since most of prey cannot run away, macaques appear to be able to forage the eggs of lice easily in spite of small size. Because during grooming macaques can obtain insects, protein-rich food, grooming may have a selfish benefit. This might favor grooming under individual natural selection, although grooming also may have an altruistic function as the elimination of external parasites on others. HygienicFunction of Grooming 193

Delousing plays a role in social interaction among human gatherer-hunters who suffer from human lice (Sugawara, 1986). Secondary and social functions were added to the primary hygienic function of grooming in monkeys (see Introduction). This similarity requires the further study of grooming.

ACKNOWLEDGEMENTS We would like to thank Dr. Kenichi Aoki, Professor Toshisada Nishida, Dr. Tomo'o Enomoto, Professor Hideo Nigi, Mr. Eishi Tokida, Dr. Shin-Ichi Hayama, and anonymous reviewers for helpful advice; Mr. Sougo Hara for permission to study at Jigokudani Monkey Park; and Mr. Shigenori Nishizawa, Mr. Toshio Hagiwara, Mrs. Miyuki Miyazawa, and the other staff of Jigokudani Monkey Park for their assistance. This study was supported in part by a Grant-in-Aid from the Japanese Ministry of Education, Science and Culture.

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