Primates DOI 10.1007/s10329-008-0126-x
ORIGINAL ARTICLE
Prevalence of muzzle-rubbing and hand-rubbing behavior in wild chimpanzees in Mahale Mountains National Park, Tanzania Nadia Corp Æ Hitoshige Hayaki Æ Takahisa Matsusaka Æ Shiho Fujita Æ Kazuhiko Hosaka Æ Nobuyuki Kutsukake Æ Michio Nakamura Æ Miho Nakamura Æ Hitonaru Nishie Æ Masaki Shimada Æ Koichiro Zamma Æ William Wallauer Æ Toshisada Nishida
Received: 25 June 2008 / Accepted: 22 December 2008 Ó Japan Monkey Centre and Springer 2009
Abstract In 1998, four chimpanzees in the Mahale Mountains National Park, Tanzania, were observed wiping their mouths with non-detached leaves or stalks of grass, or rubbing their mouths with a tree trunk or branch, especially while eating lemons. The number of mouth-wiping/rubbing individuals increased to 18 in 1999. By 2005, 29 chimpanzees were documented wiping/rubbing their muzzles in this way. N. Corp Staffordshire University, Staffordshire, UK H. Hayaki Kobe Gakuin University, Kobe, Japan S. Fujita Yamaguchi University, Yamaguchi, Japan K. Hosaka Kamakura Women’s University, Kamakura, Japan N. Kutsukake The Graduate University for Advanced Studies, Hayama, Japan Michio Nakamura H. Nishie Kyoto University, Kyoto, Japan Miho Nakamura ANC Production, Tokyo, Japan M. Shimada The University of Shiga Prefecture, Hikone, Japan K. Zamma Great Ape Research Institute, Okayama, Japan W. Wallauer Jane Goodall Institute, Kigoma, Tanzania T. Matsusaka T. Nishida (&) Japan Monkey Centre, Kanrin, Inuyama, Aichi, Japan e-mail:
[email protected]
Although it is difficult to determine whether the chimpanzees acquired this behavior as a result of trial and error or social learning, the fact that chimpanzees at other sites perform this behavior with detached leaves or leafy twigs much more often than with intact items suggests the possibility that cleaning with intact plant parts at Mahale spread via social learning. Keywords Chimpanzee Leaf napkin Mahale Mountains National Park Muzzle rub Hand rub Social learning
Introduction Local variation in chimpanzee behavior has recently attracted much attention (e.g., McGrew 1998; de Waal 2001; Whiten et al. 2003). Use of detached plant items to wipe parts of the body (e.g., ‘‘leaf napkin’’) is one such behavior. It is a frequently observed behavior of chimpanzees at Gombe (Goodall 1986), Taı¨, and Kibale, but is only rarely observed at Budongo, Bossou, and Mahale Mountains National Park, Tanzania (Nishida 1994; Whiten et al. 1999). During the dry season of 1998, we noticed four chimpanzees in the M group wiping lemon juice from their lips and chins by use of twigs and leaves. This behavior, termed ‘‘muzzle rubbing’’ (Nishida et al. 1999), differed from the pattern described above because they did not detach the item from the plant substrate, but instead used the intact plant. One chimpanzee was also observed wiping his hands, in addition to his face. In 1999, however, 18 and 12 chimpanzees were observed wiping their faces and/or hands, respectively. It is difficult to interpret this phenomenon in the natural habitat and whether it spreads via social learning or reflects individual learning. However, the rapid spread of standardized object manipulation in the wild (e.g., Goodall 1973; Kummer and Goodall
123
Primates
1985; Boesch 1995; Matsusaka et al. 2006; Nishida et al. 2009) seems to be rare, and we believe that our observations provide a useful source of information. Thus, to stimulate observations at other sites, we herein report the details of the behavioral patterns that we observed at Mahale.
Methods M-group chimpanzees were observed from early morning to dusk. NC investigated their feeding techniques (Corp and Byrne 2002) while TN studied the behavior of immature chimpanzees, with special focus on innovative behavior patterns, including wiping behavior. Other authors studied adult males (HH, KH), adult females (SF, MS), adult males and females (NK, KZ), and immature individuals (HN, TM, and Michio Nakamura). Miho Nakamura was engaged in video-shooting of the M group and stayed for 2–4 months in 1989, 1991, 1992, 1995, and 1999. Lemon trees (Citrus limon) grow in a patchy distribution throughout the national park in areas around the research station and where there were previously villages. Lemon trees bear ripe fruit in the dry season, mostly from July to September. M-group chimpanzees began to incorporate lemons into their diet in the early 1980s (Takahata et al. 1986). WW has studied the chimpanzees at Gombe for 10 years. After NC first noticed this wiping behavior in 1998, special attention was paid to chimpanzees eating lemons. When biting open the hard rind of lemons, the juice frequently dribbles from their mouths and lips, and can squirt into their eyes. In such cases, the juice is removed by wiping their mouths or chins with a branch, trunk, or the leaves of a tree or shrub, or with grasses. Lemon juice may also be wiped off their hands using a branch or stalk of grass. The same behavior was observed in response to the sticky liquid of Apocynaceae species such as Saba comorensis (fourteen times), Voacanga lutescens (five times), and Diplorhynchus condylocarpon (three times); juicy fruits such as ripe Ficus capensis (once) and Myrianthus arboreus (once); and other liquids such as nasal mucus (once), semen or vaginal liquid (four times), and feces or urine (four times). Carpenter ants were also once wiped away from the arm by use of detached leaves. Observations were classified according to whether the mouth or hand was wiped; we did not, however, distinguish between lemon juice and other liquids because the behavior was the same. Definitions Wiping and rubbing Here we operationally define wiping mouths with detached parts of plants (in particular, leaves) as ‘‘wiping’’ and
123
wiping mouths with still-attached parts of plants as ‘‘rubbing’’. A chimpanzee may pull a flexible leafy branch toward him with one hand and wipe the mouth with it without detaching the branch. This behavior may well be called ‘‘wiping’’ in ordinary English usage, but we call it ‘‘rubbing’’; we also call it ‘‘rubbing’’ when he moves his mouth close to the stout branch or tree trunk and rubs it against the substratum. On such occasions, he may hold the branch or the trunk of a tree with one hand, or just move the mouth to the substratum. We have never seen a chimpanzee detaching a leaf or a leafy branch to wipe his hand. The chimpanzee used detached leaves only for wiping body parts other than the hands. So here the hand was only rubbed against a stout branch, the trunk of a tree, or the ground. Bouts and actions We differentiated bouts and actions. A rubbing bout was defined as an episode of fruit eating during which an individual continued to pick and eat fruits (whether in a single tree or different trees) and rub the muzzle or hand at least once. A rubbing action was defined as a sequence (several times) of rubbing motions such as rubbing the muzzle or hand against a plant part. Study periods The entire study period from 1997 to 2005 was divided into periods I to VII (Table 1), each of which corresponded to a one-year period that was operationally defined as beginning in October and ending the following September.
Results Muzzle rubbing In study period I, four chimpanzees wiped lemon juice from their mouths on four separate occasions (Fig. 1). The occurrence of this behavior increased during period II and reached a plateau in period III. In total, 29 chimpanzees were observed rubbing their muzzles (Table 1). The increase in period II can be partly explained by a large crop of lemons in 1999, and researchers’ increased focus on the behavior. After 2000, the fruit yield was poor except in 2002 and 2005; thus, the M group rarely spent time in the camp area eating lemons, reducing the opportunity to observe the behavior. The youngest individuals for which muzzle rubbing was observed were 4 years 4 months in males and 2 years 4 months in females. Unlike that documented in other areas, mouth cleaning in M-group chimpanzees was predominantly performed by muzzle rubbing, rather than
NC, TN, NK
NK, TM, SF, TN
TN, MS, HN
TN MN, HN, TN
4
2
2 4
30
NC, TN, KZ
6
NC, HH 1
11
22
0 3
1
3
3
11
1 4
wiping (‘‘the leaf napkin,’’ Goodall 1986), which may be a type of tool use (sensu Beck 1980).
35 48
63
2 4 2 4
3 4
2 2
2
4 9
5
6 10
6
1
16
4
17
39
Hand rubbing Hand cleaning involved use of an intact plant part or the ground only, and was thus termed ‘‘hand rubbing’’, following the definition above. Hand rubbing was observed only once in period I, but on 16 occasions in period II. As with muzzle rubbing, hand rubbing reached a plateau in period III, when 15 chimpanzees displayed this behavior (Table 1). The youngest individuals for which hand rubbing was observed were 4 years 2 months in males and 4 years 5 months in females.
4
14
5
2
1
0 3
29
6
72
10
26
3
2 7
126
Wiping behavior During the study periods, wiping behavior was seen only four times. The leaf napkin strategy was used by one adult male (FN), who detached and used a large leaf of Myrianthus to wipe his mouth on two occasions. An adult female (Wx) wiped urine off her thigh soiled by her infant using large detached leaves, and a juvenile male (MC) wiped carpenter ants off his arm using detached leaves.
70 Total
2 5 VI. Oct. 2002–Sep. 2003 VII. Oct. 2003–2005
12
2 V. Oct. 2001–Sep. 2002
IV. Oct. 2000–Sep. 2001
10 III. Oct. 1999–Sep. 2000
I. Oct. 1997–Sep. 1998
4
Individual differences 35
Number of individuals that were observed to rub hand during each study period Number of new individuals that began to rub hand during each study period Number of rubbing actions Number of bouts Number of bouts
Number of rubbing actions
Number of new individuals that began to rub muzzle during each study period
Number of individuals that were observed to rub muzzle during each study period
Rubbing hand Rubbing muzzle
Study period
Table 1 Number of performers in seven study periods
Fig. 1 FN (adult male) rubs his mouth with a leafy part of a shrub (Photo by Hitoshige Hayaki in August 1998)
II. Oct. 1998–Sep. 1999
Observers
Primates
Fourteen chimpanzees showed both muzzle and hand rubbing, thirteen muzzle rubbing only, and seven hand rubbing only (Table 2). Thus, the presence or extent of muzzle rubbing did not predict the presence or extent of hand rubbing. In particular, FN, the alpha male of the group at the time, rubbed his muzzle in 13 bouts (22 actions) over the six study periods, but never rubbed his hands. Likewise, Tz, an adult female, often rubbed her muzzle, but never her hands.
123
Primates Table 2 List of individuals who rubbed muzzle and/or hand IDa
Name of Mother
Birth year
1960b
Ca
Number of bout
Hand rub Number of action 1
0
0
7 8
2 1
3 1
1961b
44
0
0
Ca
1985
CD Cr
Ca Ca
1991 1997
39
Muzzle rub
1
CT
Wx
Earliest age at which rubbing was seen
Period III III, IV VI
Number of bout
Number of action
0
0
0
0
1 0
1 0
IV
1
1
VI VI
AL
Wx
1982
17
1
1
II
1
1
Ai
Wx
1988
13
1
1
IV
0
0
At
Wx
I, III
Ft
1996
2
2
2
1963b
40
0
0
11
PM
Ft
1988
Fv
Ft
1999
7
7
0
0
II, III, IV, V
Period
1
2
IV
1
1
VI III
1
1
0
0
DE
1963b
36
1
1
II
1
1
Nk
1970
29
1
1
II
2
3
II
Op
1971b
28
0
0
1
1
III
OS
Op
1998
7
1
1
OR
Op
1991
8
0
0
Rb
Op
1986
13
0
0
Rc Pi
Rb
1998 1972b
2 28
1 0
4 0
IV
PR
Pi
1991
8
2
2
1974b
25
1
1
Jn Jd
1995
4
2
4
FN
1978b
20
13
22
Ld
1980b
19
1
1
0
0
1
7
0
0
Lz
Jn
Ld
Ak Ac
1999 1981
Ak
18
1998
VI
IV
0
0
2
8
II, IV
2
3
II
0 2
0 2
III, VI
II
0
0
II
0
0
II, III
2
3
I, II, III, IV, V, VI
0
0
III II
0
0
0
0
1
3
0
0
II, III
II
DG
1981b
17
1
1
III
1
4
I
Cy
1982b
17
2
2
II
3
4
II, III
0
0
0
0
I, II, IV
3
7
V
0
0
II, IV, V
0
0
I, II III
0 0
0 0
0
0
3
8
II, IV II
Ce
Cy
Ab Aq
Ab
1998 1982
13c
4
11
1998
3
1
2
Tz
1982
17
5
28
CL Ef
1985b 1986b
13 13
2 1
2 1
EM
0
0
DW
Ef
2000 1988
10
3
3
Pp
1990
9
0
0
1
1
Ik
1965b
0
0
0
0
II
Im
Ik
1998
0
0
0
0
Iv
Ik
1993
6
2
2
II, III
1
3
Zl
1987b
12
1
1
II
0
0
Xt
1975b
0
0
0
0
5
10
0
0
XM
Xt
Mj
123
1995 1980b
4
II, IV
3
4
0
0
II, V
II
II, III, V
Primates Table 2 continued IDa
Name of Mother
Birth year
MC
Mj
1996
Me
Mj
2001
Earliest age at which rubbing was seen
4
Total
Muzzle rub Number of bout
Hand rub Number of action
0
0
2
2
68
125
Period
VI
Number of bout
Number of action
0
0
0
0
34
62
Period
When either or both of a mother’s offspring rubbed, performances of all the family members are shown a
Two capital letters indicate males and one capital letter females
b
Estimated age
c
Observation outside of this study
Eleven males and sixteen females rubbed their muzzles only, whereas seven males and twelve females rubbed their hands only. Considering the female-biased sex ratio of M group, these data do not demonstrate a sex-based difference in rubbing behavior. Four infants rubbed their mouths, but none of them rubbed their hands. This may reflect the feeding skill of infants because their mouths are more likely to be soiled by food than are the mouths of older individuals. Five infants or juveniles and eight adults or adolescents rubbed their muzzles only. In contrast, only three infants or juveniles rubbed both their muzzles and hands, whereas eighteen adults or adolescents rubbed their hands only or both their hands and their muzzles. Thus, older individuals showed a higher tendency to rub their hands (df = 1, v2 = 4.16, P \ 0.05). Decline of rubbing behavior After 2002, the frequency of muzzle/hand rubbing seemed to decline. HN observed FN as his focal individual for 115 h between 2002 and 2004, and frequently observed him eating lemons; however, he never saw FN rubbing his muzzle or hands. In 2005, KH completed 200 h of focal observation, but never saw rubbing behavior. Concordance between mother and offspring If social learning was involved, we might expect concordance between a mother and her immature offspring. Our observations included nine pairs of mothers and immature offspring (2.5–10 years) that were observed to engage in rubbing at least once. Two of these mother–offspring pairs (Ca–Cr, Op–OR) showed the same pattern of rubbing behavior, i.e., mouth versus mouth or hand versus hand. Four pairs (Ca–CD, Wx–At, Jn–Jd, Ab–Aq) shared at least one rubbing method. However, three cases were contradictory: For example, an infant female (Rc) showed muzzle rubbing, but not hand rubbing, whereas her mother (Rb) showed hand rubbing, but not muzzle rubbing (Table 2).
Discussion Lemon trees have grown around the research station since the 1960s, after seeds discarded by TN germinated. After the grove of lemon trees appeared, M group chimpanzees suddenly began to eat the lemons in 1982, and this habit spread very quickly among them (Takahata et al. 1986). However, we never observed them muzzle or hand rubbing when eating lemon juice until 1989. Since 1989, a film crew (ANC Productions) has regularly recorded the Mgroup chimpanzees for periods of 2–4 months at a time. While the footage documents many instances of lemon eating in 1989, 1991, 1992, and 1995, there is no evidence of any associated muzzle or hand rubbing. However, in 1995, they recorded Ab rubbing the juice of a Saba fruit from her lips on to a tree trunk. During 40 years of research on the M group, TN observed muzzle rubbing on only a few (\10) occasions while chimpanzees were eating Saba or Parkia flicoidea. He also observed the leaf napkin technique on a few occasions. In addition to FN’s cases mentioned above, an adult male (NS) wiped feces from his anus using a leaf, and another adult male (DE) wiped feces from his back soiled by another male using a leafy twig. Thus, it seems that wiping with both detached and intact plant parts was already part of the behavioral repertoire of at least some of the M-group chimpanzees before its observation in the context of lemon eating. Why did these behaviors become prevalent in 1999? Was it by social learning or some other mechanism? If social learning was involved, we might expect concordance between a mother and her immature offspring. As shown above, the concordance is not always clear. However, this may be related to age differences in rubbing behavior, as mentioned above. Moreover, chimpanzees often ate in the presence of other chimpanzees, including playmates (Matsusaka and Nishida unpublished); therefore, youngsters who often peer with individuals other than their mothers when eating might learn rubbing techniques from
123
Primates
them. Emulation (Tomasello and Call 1997) might work as a mechanism for social learning. Thus, the observational evidence at Mahale is ambiguous regarding social learning. However, at Gombe, detached leaves are often used to wipe somewhat sticky substances, especially off the hands. Chimpanzees at Gombe occasionally remove the adherent latex of Saba from their lips using a branch or the main trunk of a tree, in effect scraping the latex off on the rough bark, namely with the muzzle-rubbing technique. However, they use detached leaves when cleaning non-sticky substances from the mouth. This contrasts remarkably with the Mahale chimpanzees’ method of rubbing non-sticky lemon juice off their mouths. Furthermore, chimpanzees at Gombe use detached leaves or leafy branches much more often than they use intact branches or leaves. At Gombe, and at Budongo and Kibale, this leaf-napkin strategy has become customary (Whiten et al. 1999). In conclusion, two hypotheses to explain the prevalence of muzzle rubbing appear viable. The first hypothesis is that individual learning is the major mechanism of this behavior pattern. It is probable that the high yield of lemons in 1999 stimulated the chimpanzees to eat more lemons, increasing the likelihood that chimpanzees would clean their faces or hands via trial and error. At Gombe, where there are no lemon trees, individual learning remained at a low level. There, chimpanzees use muzzle rubbing only to remove the sticky liquid of Saba fruits. However, this hypothesis cannot explain why, at Mahale, muzzle rubbing increased, but not the leaf-napkin technique. The alternative hypothesis is that social transmission, in addition to trial and error, is a major mechanism of this behavior pattern. The lemon trees at Mahale comprise a concentrated patch or grove around the camp. Thus, opportunities for social learning are plentiful. The fact that the alpha male FN was one of the first individuals to exhibit muzzle rubbing while foraging on lemons and showed the pattern most often favors the social transmission hypothesis because the alpha male might have a great influence on information transmission (Nishida 1987). Currently, the social transmission hypothesis seems more likely. We propose that although muzzle rubbing is a simple behavioral pattern, it is worth studying to clarify the nature of learning in the natural habitat. Our hope is that this paper stimulates detailed studies of similar behavioral patterns at other study sites. Acknowledgments We thank the Tanzania Commission for Science and Technology, Tanzania Wildlife Research Institute, and Tanzania National Parks for permission to conduct the field study, and
123
Mahale Mountains National Park and Mahale Mountains Wildlife Research Centre for logistical support. Field work and data analyses were financially supported by a Grant for Basic Research from the Ministry of Education, Sports, Culture, Science, and Technology, Japan (#12375003, 16255007, and 19255008), The Leakey Foundation, and the Global Environment Research Fund (F-061) of the Ministry of Environment, Japan. We thank W.C. McGrew, Y. Takahata, and an anonymous reviewer for constructive comments.
References Beck B (1980) Animal tool behavior. Garland Press, New York Boesch C (1995) Innovation in wild chimpanzees (Pan troglodytes). Int J Primatol 16:1–16 Corp N, Byrne R (2002) The ontogeny of manual skill in wild chimpanzees: evidence from feeding on the fruit of Saba florida. Behaviour 139:137–168 Goodall J (1973) Cultural elements in a chimpanzee community. In: Menzel EW (ed) Precultural primate behavior. Karger, Basel, pp 144–184 Goodall J (1986) The chimpanzees of Gombe. Harvard University Press, Cambridge Kummer H, Goodall J (1985) Conditions of innovative behavior in primates. Philos Trans Roy Soc Lond B 308:441–471 Matsusaka T, Nishie H, Shimada M, Kutsukake N, Zamma K, Nakamura M, Nishida T (2006) Tool-use for drinking water by immature chimpanzees of Mahale: prevalence of an unessential behavior. Primates 47:113–122 McGrew WC (1998) Culture in nonhuman primates? Ann Rev Anthropol 27:301–328 Nishida T (1987) Local traditions and cultural transmission. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 462–474 Nishida T (1994) Review of recent findings on Mahale chimpanzees: implications and future research directions. In: Wrangham RW, McGrew WC, de Waal FBM, Heltne PG (eds) Chimpanzee cultures. Harvard University Press, Cambridge, pp 373–396 Nishida T, Kano T, Goodall J, McGrew WC, Nakamura M (1999) Ethogram and ethnography of Mahale chimpanzees. Anthropol Sci 107:141–188 Nishida T, Matsusaka T, McGrew WC (2009) Emergence, propagation or disappearance of novel behavioral patterns in the habituated chimpanzees of Mahale: a review. Primates 50. doi: 10.1007/s10329-008-0109-y Takahata Y, Hiraiwa-Hasegawa M, Takasaki H, Nyundo R (1986) Newly acquired feeding habits among the chimpanzees of the Mahale Mountains National Park, Tanzania. Hum Evol 1:277– 284 Tomasello M, Call J (1997) Primate cognition. Oxford University Press, New York de Waal FBM (2001) The ape and the sushi master. Basic Books, New York Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C (1999) Cultures in chimpanzees. Nature 399:682–685 Whiten A, Horner V, Marshall-Pescini S (2003) Cultural panthropology. Evol Anthrop 12:92–105