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Variability in contact calls between troops of Japanese macaques: a possible case of neutral evolution of animal culture
900
Animal Behaviour, 38, 5
allows I C l b to be held in the reset state, preventing generation of the solenoid driver pulse. The remainder of the circuit simply emulates a user by electrically pressing the Start button twice. I C l a produces a 0.5-s pulse to turn on transistor TR3 via D4, closing the relay (RLA) which is connected to the three contacts of the timer Start button. It also initiates a delay pulse of 0.5 s generated by IC2a, the end of which triggers IC2b to produce a 0.5-s pulse which closes RLA again via 195 and TR3. Since each pressing of the Start button activates the sounder in the timer, it is necessary to use a crude monostable pulse generator consisting of TR2 and the components connected to its base to reset I C l a and prevent its repeated triggering. The solenoid driver pulse generated by I C l b lasts long enough to render the monostable pulse generator immune to retriggering by the sounder. The total reset to restart time for the timer is 1.0 s and should be added to the delay time preselected on the timer. The camera used is a 35 mm Olympus AF1 compact, which is particularly suitable since it has automatic film wind-on and exposure facilities. It is mounted on a tripod fitted with an aluminium bracket carrying the solenoid which presses the shutter release button. Since it is a weatherproof model, no additional protective measures are necessary to use it in the field. In the present study the camera controller is being used to provide a photographic record of the attendance pattern of rooks, Corvus fi'ugilegus L., at a rookery during daylight hours throughout the year. The requirement for data collection over a long period makes an automatic technique essential. This record is used to monitor changes in attendance pattern at the rookery over the annual cycle. Of particular interest is the pattern of attendance during the autumn (September-November). This period marks a resurgence in sexual behaviour in thc rook, and rookery attendance is used to examine one potential adaptive function of this autumn sexuality, namely nest-site selection. High levels of attendance are indicative of a temporal commitment to the nest site midway between breeding seasons. The apparatus is sited in a hide providing a view across a section of the rookery at canopy level. Seven nest sites are monitored and the rooks can be distinguished from about 15 m away. To record the attendance of rooks, the timer is set to release the shutter at half-hour intervals. A large-figure liquid crystal digital clock suspended in the field of view provides a precise record of the time of the exposure. This rather crude system of verification might be avoided by using a more expensive camera model equipped with a data-back, thereby render-
ing the clock superfluous. A 36-exposure film allows monitoring of the rookery for between 30 and 72 h depending on seasonal changes in daylength. Once exposed, the film is developed and printed as a contact sheet, and each frame examined for the presence of rooks. The camera controller is also being used to monitor the frequency of appearance of scavenging birds at a sheep carcass in the field over much longer periods. For this a Bauer C500XLM stopframe 8 mm cine camera is being used enclosed with the controller within a splashproof box. Since this camera has a remote input, a solenoid is unnecessary. The remote jack is connected to B and OV and diode D2 is removed. In addition to the two applications described here, the controller could easily be adapted to operating other recorders, dispensers or feeders with a relay attached to A, B. The described apparatus' simplicity, cheapness and adaptability make it an extremely useful alternative to commercial apparatus. RICHARD S. RUTNAGUR MARTIN D. BURNS MICHAEL H. HANSELL
Department o f Zoology, Glasgow University, Glasgow G12 8QQ, Scotland, U.K. References Martin, P. & Bateson, P. 1986. Measuring Behaviour. Cambridge: Cambridge University Press. Mudge, G. P., Aspinall, S. J. & Crooke C. H. 1987. A photographic study of seabird attendance at Moray Firth colonies outside the breeding season. Bird Study, 34, 28-36.
(Received 22 February 1989; revised 6 April 1989; MS. number: sc 494)
Variability in Contact Calls between Troops of Japanese Macaques: a Possible Case of Neutral Evolution of Animal Culture Within-species variation in the structure of primate social signals is well documented, but examples of the use of the same signal in different functional contexts are rare. Female chimpanzees, Pan troglodytes, of the eastern and western races use the same gesture (pointing to the back) in different contexts, namely as an invitation to an infant and during aggressive interactions (Goodal11986). To date, no such functional differences in the use of the same vocalization have been described, although the use
Short Communications of contact calls appears to vary between troops of Japanese macaques (Macacafuscata: Itani 1963; Green 1975a; Masataka 1989). For example, almost all grooming bouts were preceded by contact calls in the Koshima troop in Mori's (1975) study, whereas this was seldom the case in a different troop transplanted to the U.S.A. (Blount 1985). In the study described in this paper, I examined such variability further by comparing the relationship between calling and grooming in three troops of Japanese macaques, including that studied by Mori (1975). Three artificially provisioned, free-ranging troops of Japanese macaques (the Shiga A1 in Nagano Prefecture, the Choshi-kei on Shodoshima Island and the Koshima troops) were observed using both the sequential sampling method and the focal animal sampling method (Altmann 1974). Focal animals were chosen randomly among adult females and their grooming behaviour and vocalizations were recorded. I studied the Shiga A1 between October and December 1984 (200 h), between October and December 1985 (200 h) and in May 1986 (75 h); the Choshi-kei between January and February 1986 (60 h); and the Koshima b~'tween August and September 1986 (80 h). 'Girneys' and 'coos' were exclusively vocalized immediately before grooming contacts. The duration of grooming did not vary with respect to the types of preceding vocalizations (Mann-Whitney U-test, Z=0-879, N1=80, N2=10, P>0-05, two-tailed). Thus the two sounds were lumped together for the following analysis. Grooming bouts following these contact calls lasted longer than those without contact calls (Mann-Whitney U-tests; Koshima: Z=2.66, N~=46, N2=53; Shiga: Z = - 2 . 1 , N~=13, N2=47; Choshi: Z = 1.97, NI = 11, N2 = 23; P < 0-05 for each troop, two-tailed), regardless of whether the call was given by groomer or groomee (Koshima: Z=0-55, N1=42, N 2 = l l ; Shiga: U = I 8 , N l = 7 , N2=6; Choshi: U=9, N~=4, N2=7; P > 0 . 0 5 for each troop, two-tailed). The patterns of contact calling did not vary seasonally in the Shiga troop (groomer used contact call: X2=0-42, df= 1, P > 0.05; groomee used contact call: Z2= 2-84, df= 1, P > 0.05). In the Koshima troop contact calls were uttered frequently by the groomers, wherease they were uttered mostly by the groomees in the Shiga and the Choshi troops (Fig. 1). Pair-wise comparisons showed that the likelihood differed significantly between the Koshima and the Choshi troops (Z2=9'11, df=l, P<0"01) and between the Koshima and the Shiga troops (X2=5.13, df=l, P<0-05), but not between the Shiga and the Choshi troops (Z2=0.76, df= 1, P > 0.05). Similarly the probabilities with which contact calls were
901
uttered by groomees were significantly different between the Koshima and the Shiga troops (Z2=22-15, df= 1, P<0.01) and between the Koshima and the Choshi troops (Z2=5.60, d f = l , P<0'05), but not between the Shiga and the Choshi troops (Z2=0.92, df= 1, P>0.05). A comparison of my data with those of Mori (1975) revealed that contact call usage in the Koshima troop did not differ in 1975 and 1986 (Z2=0-764, df= 1, P>0.05), suggesting this pattern of vocal usage has remained constant, possibly as a result of cultural transmission. Contact calls were more often used between nonrelatives in the Koshima than in the Shiga (Fig. 1). With regard to the dominance relations of grooming participants, contact calls were directed from the subordinate to the dominant animals (Fig. 1), as found by Blount (1985). There are a number of possible explanations for the differences between the three troops in the way contact calls are used during grooming. For example, they may logically reflect differences in the way in which animal keepers care and provision monkeys in the troops (cf. Green 1975b). However, the animal keepers enter the provisioning area solely to distribute food to the monkeys in the study troops. In such circumstances grooming interactions rarely occur. Thus it is unlikely that the keepers affected the differences between troops described here. Another possibility is that calling patterns are affected by differences in social relationships. Mori (1975) attributed frequent occurrences of contact calling by groomers in the Koshima troop, particularly during interactions involving unrelated females, to extraordinarily high competition between females in the troop. The vocalizations might be uttered by subordinate animals to 'appease' dominant ones (cf. Blount 1985). It is most likely, however, that patterns of contact call usage are determined randomly in the study troops, through a stochastic process such as 'cultural drift' (Cavalli-Sforza & Feldman 1981), since the expected social and hygienic functions of allogrooming are likely to be correlated with grooming duration (Silk 1987). The variability of calling behaviour reported here might have occurred through processes similar to those involved in the emergence of human cultural behaviour. By comparing such 'culture' in non-human primates with that in humans, we gain fruitful perspectives on the origin and evolution of human culture (Sakura 1987). I am very grateful to Y. Sugiyama, N. Masataka, M. Kawai, T. Hasegawa and T. Fushimi for their comments on this study and on an earlier draft of this article; the managing staffs of the Koshima, the Shiga and the Choshi-kei troops for their kind help
Animal Behaviour 38, 5
902
50
4(3
~
2O
IO ~ I N
116 59 63 Groomer
1 t, ,1
116 59 63 Groomee
11963
11963
Kin
Non-kin
11963
1196.3
Dominclnf Subordinate
Figure 1. Usage of contact calls preceding grooming in three macaque troops. [] the Koshima; 9 the Shiga; [] the Choshi. The bars show the likelihood of contact calls being uttered by the groomer; by the groomee; between relatives; between non-relatives; from dominant animals to subordinate ones; and from subordinate animals to dominant ones. Information about kin relations and rank relations among group members was not available in the Choshi-kei troop. Solid lines over bars represent significant difference at the level of P < 0.01; dotted lines at the level of P < 0'05.
during the field work; and P. Newton for his assistance with the English revision. This study was financed in part by a Grant-in-Aid for Special Project Research on Biological Aspects of Optimal Strategy and Social Structure from the Japan Ministry of Education, Science and Culture. OSAMU SAKURA Primate Research Institute, Kyoto University, Inuyama City, Aichi 484, Japan.
References Altmann, J. 1974. Observational study of behaviour: sampling methods. Behaviour, 49, 227-267. Blount, B. G. 1985. 'Girney' vocalizations among Japanese macaque females: context and function. Primates, 26, 424-435. Cavalli-Sforza, L. L. & Feldman, M. W. 1981. Cultural
Green. S. 1975a. Variation of vocal pattern with social situation in the Japanese monkey (Macacafuscata): a field study. In: Primate Behavior: Developments in the Field and Laboratory Research. Vol. 4 (Ed. by L. A. Rosenblum), pp. 1-102. New York: Academic Press. Green, S. 1975b. Dialects in Japanese monkeys: vocal learning and cultural transmission of locale-specific behavior? Z. Tierpsychol., 38, 304-314. Itani, J. 1963. Vocal communication of the wild Japanese monkey. Primates, 4, 11-66. Masataka, N. 1989. Motivational referents of contact calls in Japanese monkeys. Ethology, 80, 265-273. Mori, A. 1975. Signals found in the grooming interactions of wild Japanese monkeys of the Koshima troop. Primates, 16, 107-140. Sakura, O. 1987. Theoretical notes on primate sociobiology: defense and extension. Reichourui Kenkyuu (Primate Research), 3, 33-42. Silk, J. B. 1987. Social behavior in evolutionary perspective. In: Primate Societies (Ed. by B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker), pp. 318 329. Chicago: The University of Chicago Press.
Transmission and Evolution: A Quantitative Approach. Princeton: Princeton University Press. Goodall, J. 1986. The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, Massuchusetts: The Belknap Press of Harvard University Press.
(Received I November 1988; revised 14 March 1989; MS. number: sc-492)
Animal Behaviour, 38, 5
allows I C l b to be held in the reset state, preventing generation of the solenoid driver pulse. The remainder of the circuit simply emulates a user by electrically pressing the Start button twice. I C l a produces a 0.5-s pulse to turn on transistor TR3 via D4, closing the relay (RLA) which is connected to the three contacts of the timer Start button. It also initiates a delay pulse of 0.5 s generated by IC2a, the end of which triggers IC2b to produce a 0.5-s pulse which closes RLA again via 195 and TR3. Since each pressing of the Start button activates the sounder in the timer, it is necessary to use a crude monostable pulse generator consisting of TR2 and the components connected to its base to reset I C l a and prevent its repeated triggering. The solenoid driver pulse generated by I C l b lasts long enough to render the monostable pulse generator immune to retriggering by the sounder. The total reset to restart time for the timer is 1.0 s and should be added to the delay time preselected on the timer. The camera used is a 35 mm Olympus AF1 compact, which is particularly suitable since it has automatic film wind-on and exposure facilities. It is mounted on a tripod fitted with an aluminium bracket carrying the solenoid which presses the shutter release button. Since it is a weatherproof model, no additional protective measures are necessary to use it in the field. In the present study the camera controller is being used to provide a photographic record of the attendance pattern of rooks, Corvus fi'ugilegus L., at a rookery during daylight hours throughout the year. The requirement for data collection over a long period makes an automatic technique essential. This record is used to monitor changes in attendance pattern at the rookery over the annual cycle. Of particular interest is the pattern of attendance during the autumn (September-November). This period marks a resurgence in sexual behaviour in thc rook, and rookery attendance is used to examine one potential adaptive function of this autumn sexuality, namely nest-site selection. High levels of attendance are indicative of a temporal commitment to the nest site midway between breeding seasons. The apparatus is sited in a hide providing a view across a section of the rookery at canopy level. Seven nest sites are monitored and the rooks can be distinguished from about 15 m away. To record the attendance of rooks, the timer is set to release the shutter at half-hour intervals. A large-figure liquid crystal digital clock suspended in the field of view provides a precise record of the time of the exposure. This rather crude system of verification might be avoided by using a more expensive camera model equipped with a data-back, thereby render-
ing the clock superfluous. A 36-exposure film allows monitoring of the rookery for between 30 and 72 h depending on seasonal changes in daylength. Once exposed, the film is developed and printed as a contact sheet, and each frame examined for the presence of rooks. The camera controller is also being used to monitor the frequency of appearance of scavenging birds at a sheep carcass in the field over much longer periods. For this a Bauer C500XLM stopframe 8 mm cine camera is being used enclosed with the controller within a splashproof box. Since this camera has a remote input, a solenoid is unnecessary. The remote jack is connected to B and OV and diode D2 is removed. In addition to the two applications described here, the controller could easily be adapted to operating other recorders, dispensers or feeders with a relay attached to A, B. The described apparatus' simplicity, cheapness and adaptability make it an extremely useful alternative to commercial apparatus. RICHARD S. RUTNAGUR MARTIN D. BURNS MICHAEL H. HANSELL
Department o f Zoology, Glasgow University, Glasgow G12 8QQ, Scotland, U.K. References Martin, P. & Bateson, P. 1986. Measuring Behaviour. Cambridge: Cambridge University Press. Mudge, G. P., Aspinall, S. J. & Crooke C. H. 1987. A photographic study of seabird attendance at Moray Firth colonies outside the breeding season. Bird Study, 34, 28-36.
(Received 22 February 1989; revised 6 April 1989; MS. number: sc 494)
Variability in Contact Calls between Troops of Japanese Macaques: a Possible Case of Neutral Evolution of Animal Culture Within-species variation in the structure of primate social signals is well documented, but examples of the use of the same signal in different functional contexts are rare. Female chimpanzees, Pan troglodytes, of the eastern and western races use the same gesture (pointing to the back) in different contexts, namely as an invitation to an infant and during aggressive interactions (Goodal11986). To date, no such functional differences in the use of the same vocalization have been described, although the use
Short Communications of contact calls appears to vary between troops of Japanese macaques (Macacafuscata: Itani 1963; Green 1975a; Masataka 1989). For example, almost all grooming bouts were preceded by contact calls in the Koshima troop in Mori's (1975) study, whereas this was seldom the case in a different troop transplanted to the U.S.A. (Blount 1985). In the study described in this paper, I examined such variability further by comparing the relationship between calling and grooming in three troops of Japanese macaques, including that studied by Mori (1975). Three artificially provisioned, free-ranging troops of Japanese macaques (the Shiga A1 in Nagano Prefecture, the Choshi-kei on Shodoshima Island and the Koshima troops) were observed using both the sequential sampling method and the focal animal sampling method (Altmann 1974). Focal animals were chosen randomly among adult females and their grooming behaviour and vocalizations were recorded. I studied the Shiga A1 between October and December 1984 (200 h), between October and December 1985 (200 h) and in May 1986 (75 h); the Choshi-kei between January and February 1986 (60 h); and the Koshima b~'tween August and September 1986 (80 h). 'Girneys' and 'coos' were exclusively vocalized immediately before grooming contacts. The duration of grooming did not vary with respect to the types of preceding vocalizations (Mann-Whitney U-test, Z=0-879, N1=80, N2=10, P>0-05, two-tailed). Thus the two sounds were lumped together for the following analysis. Grooming bouts following these contact calls lasted longer than those without contact calls (Mann-Whitney U-tests; Koshima: Z=2.66, N~=46, N2=53; Shiga: Z = - 2 . 1 , N~=13, N2=47; Choshi: Z = 1.97, NI = 11, N2 = 23; P < 0-05 for each troop, two-tailed), regardless of whether the call was given by groomer or groomee (Koshima: Z=0-55, N1=42, N 2 = l l ; Shiga: U = I 8 , N l = 7 , N2=6; Choshi: U=9, N~=4, N2=7; P > 0 . 0 5 for each troop, two-tailed). The patterns of contact calling did not vary seasonally in the Shiga troop (groomer used contact call: X2=0-42, df= 1, P > 0.05; groomee used contact call: Z2= 2-84, df= 1, P > 0.05). In the Koshima troop contact calls were uttered frequently by the groomers, wherease they were uttered mostly by the groomees in the Shiga and the Choshi troops (Fig. 1). Pair-wise comparisons showed that the likelihood differed significantly between the Koshima and the Choshi troops (Z2=9'11, df=l, P<0"01) and between the Koshima and the Shiga troops (X2=5.13, df=l, P<0-05), but not between the Shiga and the Choshi troops (Z2=0.76, df= 1, P > 0.05). Similarly the probabilities with which contact calls were
901
uttered by groomees were significantly different between the Koshima and the Shiga troops (Z2=22-15, df= 1, P<0.01) and between the Koshima and the Choshi troops (Z2=5.60, d f = l , P<0'05), but not between the Shiga and the Choshi troops (Z2=0.92, df= 1, P>0.05). A comparison of my data with those of Mori (1975) revealed that contact call usage in the Koshima troop did not differ in 1975 and 1986 (Z2=0-764, df= 1, P>0.05), suggesting this pattern of vocal usage has remained constant, possibly as a result of cultural transmission. Contact calls were more often used between nonrelatives in the Koshima than in the Shiga (Fig. 1). With regard to the dominance relations of grooming participants, contact calls were directed from the subordinate to the dominant animals (Fig. 1), as found by Blount (1985). There are a number of possible explanations for the differences between the three troops in the way contact calls are used during grooming. For example, they may logically reflect differences in the way in which animal keepers care and provision monkeys in the troops (cf. Green 1975b). However, the animal keepers enter the provisioning area solely to distribute food to the monkeys in the study troops. In such circumstances grooming interactions rarely occur. Thus it is unlikely that the keepers affected the differences between troops described here. Another possibility is that calling patterns are affected by differences in social relationships. Mori (1975) attributed frequent occurrences of contact calling by groomers in the Koshima troop, particularly during interactions involving unrelated females, to extraordinarily high competition between females in the troop. The vocalizations might be uttered by subordinate animals to 'appease' dominant ones (cf. Blount 1985). It is most likely, however, that patterns of contact call usage are determined randomly in the study troops, through a stochastic process such as 'cultural drift' (Cavalli-Sforza & Feldman 1981), since the expected social and hygienic functions of allogrooming are likely to be correlated with grooming duration (Silk 1987). The variability of calling behaviour reported here might have occurred through processes similar to those involved in the emergence of human cultural behaviour. By comparing such 'culture' in non-human primates with that in humans, we gain fruitful perspectives on the origin and evolution of human culture (Sakura 1987). I am very grateful to Y. Sugiyama, N. Masataka, M. Kawai, T. Hasegawa and T. Fushimi for their comments on this study and on an earlier draft of this article; the managing staffs of the Koshima, the Shiga and the Choshi-kei troops for their kind help
Animal Behaviour 38, 5
902
50
4(3
~
2O
IO ~ I N
116 59 63 Groomer
1 t, ,1
116 59 63 Groomee
11963
11963
Kin
Non-kin
11963
1196.3
Dominclnf Subordinate
Figure 1. Usage of contact calls preceding grooming in three macaque troops. [] the Koshima; 9 the Shiga; [] the Choshi. The bars show the likelihood of contact calls being uttered by the groomer; by the groomee; between relatives; between non-relatives; from dominant animals to subordinate ones; and from subordinate animals to dominant ones. Information about kin relations and rank relations among group members was not available in the Choshi-kei troop. Solid lines over bars represent significant difference at the level of P < 0.01; dotted lines at the level of P < 0'05.
during the field work; and P. Newton for his assistance with the English revision. This study was financed in part by a Grant-in-Aid for Special Project Research on Biological Aspects of Optimal Strategy and Social Structure from the Japan Ministry of Education, Science and Culture. OSAMU SAKURA Primate Research Institute, Kyoto University, Inuyama City, Aichi 484, Japan.
References Altmann, J. 1974. Observational study of behaviour: sampling methods. Behaviour, 49, 227-267. Blount, B. G. 1985. 'Girney' vocalizations among Japanese macaque females: context and function. Primates, 26, 424-435. Cavalli-Sforza, L. L. & Feldman, M. W. 1981. Cultural
Green. S. 1975a. Variation of vocal pattern with social situation in the Japanese monkey (Macacafuscata): a field study. In: Primate Behavior: Developments in the Field and Laboratory Research. Vol. 4 (Ed. by L. A. Rosenblum), pp. 1-102. New York: Academic Press. Green, S. 1975b. Dialects in Japanese monkeys: vocal learning and cultural transmission of locale-specific behavior? Z. Tierpsychol., 38, 304-314. Itani, J. 1963. Vocal communication of the wild Japanese monkey. Primates, 4, 11-66. Masataka, N. 1989. Motivational referents of contact calls in Japanese monkeys. Ethology, 80, 265-273. Mori, A. 1975. Signals found in the grooming interactions of wild Japanese monkeys of the Koshima troop. Primates, 16, 107-140. Sakura, O. 1987. Theoretical notes on primate sociobiology: defense and extension. Reichourui Kenkyuu (Primate Research), 3, 33-42. Silk, J. B. 1987. Social behavior in evolutionary perspective. In: Primate Societies (Ed. by B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker), pp. 318 329. Chicago: The University of Chicago Press.
Transmission and Evolution: A Quantitative Approach. Princeton: Princeton University Press. Goodall, J. 1986. The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, Massuchusetts: The Belknap Press of Harvard University Press.
(Received I November 1988; revised 14 March 1989; MS. number: sc-492)