Conspecific Influences on Vigilance Behavior
in Wild Chimpanzees
Nobuyuki Kutsukake
Received: 20 January 2006 / Revised: 20 June 2006 / Accepted: 24 July 2006 / Published online: 11 July 2007
# Springer Science + Business Media, LLC 2007
Abstract Diurnal primates rely on visual monitoring behavior to collect various kinds of ecological and social information. Vigilance behavior is monitoring specifically to detect external threats. Previous studies of vigilance behavior were focused mainly on the influence of predation threats, whereas the influences of conspecific factors, such as intragroup threats, have been relatively unstudied. Individual vigilance is predicted to be inversely related to the group size or the number of individuals nearby if the main target of the vigilance is a predation threat and positively related if the main target of the vigilance is a conspecific threat. I studied wild chimpanzees (Pan troglodytes schweinfurthii) in Mahale Mountains National Park, Tanzania, and measured the vigilance duration when they are resting on the ground via 2-min focal observation. In both males and females, vigilance duration increased as the number of individuals nearby increased. This result agrees with the idea that the chimpanzees are vigilant toward other group members. In addition, maternal vigilance monitors and protects the safety of dependent offspring as the duration of maternal vigilance was longer when a dependent infant was separated from its mother than when the offspring was in contact with its mother. The results indicate that the vigilance behavior in wild chimpanzees was affected by conspecific factors.
Keywords chimpanzee . conspecific monitoring . group size effect . predation . vigilance
DOI 10.1007/s10764-007-9156-2
N. Kutsukake
Department of Cognitive and Behavioral Science, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan
N. Kutsukake
Department of Biological Sciences, Graduate School of Sciences, The University of Tokyo, Tokyo, Japan
N. Kutsukake (*)
Laboratory for Biolinguistics, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama, Japan
e-mail: [email protected]
Introduction
Diurnal primates heavily rely on visual monitoring behavior to collect various kinds of ecological and social information. Vigilance behavior is monitoring behavior used mainly to detect external threats. Researchers commonly assume the main function of vigilance behavior is a search for predation threats (Caro2005). However, recent studies highlight the importance of conspecific factors as a determinant of vigilance. For example, in mammal and bird species, individuals increase their vigilance (probably against conspecifics) in the presence of a competitive conspecific (wading birds: Barbosa2002; giraffes, Giraffa camelopardalis: Cameron and du Toit 2005; nutmeg manikins, Lonchura punctulata: Coolen2002; oystercatchers, Haematopus ostlalegus: Goss-Custard et al.1999; bald eagles, Haliaeetus leucocephalus: Knight and Knight 1986; chimpanzees, Pan troglodytes: Kutsukake 2006; small eastern quolls, Dasyurus viverrinus and Tasmanian devils, Sarcophilus laniarius: Jones 1998; rabbits, Oryctolagus cuniculus: Roberts 1988; northwestern crows, Corvus caurinus: Robinette and Ha2000; mountain gorillas, Gorilla gorilla: Watts1998). Part of the vigilance is directed toward group members (yellow baboons, Papio cynocephalus: Alberts 1994; red-chested moustached tamarins, Saguinus labiatus and squirrel monkeys, Saimiri sciureus: Caine and Marra 1988; Treves 2000), particularly toward higher-ranking ones (talapoin monkeys, Miopithecus talapoin: Keverne et al. 1978). In addition, maternal vigilance functions to monitor and to protect dependent offspring from both predation and conspecific threats (Caro2005). Mothers show elevated vigilance relative to nonmothers in mammals (African herbivorous mammals: Burger and Gochfeld 1994). Maternal vigilance increases when the probability of an attack on the infant from a predator or conspecific is high (rhesus macaques, Macaca mulatta: Maestripieri 1993; black howlers, Alouatta pigra: Treves et al. 2003) or infanticide is likely (Thomas’s langurs, Presbytis thomasi: Steenbeek et al.1999).
One problem in studies of vigilance behavior is the difficulty to distinguish vigilance behavior directed toward specific threats from undirected, general monitoring behavior. The problem has arisen for two reasons. First, specifying the target of monitoring behavior is difficult or impossible in free-moving individuals. Second, vigilance and monitoring are not necessarily mutually exclusive (Treves 2000). In light of the problem, I use vigilance in a broad sense without specifying its function, i.e., detecting external threats, and monitoring only when its function is clearly not to detect threats.
Another problem in previous vigilance studies is that the degree with which individual vigilance is sensitive to threats from predation or conspecifics remains unclear. Investigating the relationship between vigilance levels and group size is essential to evaluate whether vigilance is directed mainly toward predators, conspecifics, or both. Theoretically, an individual’s vigilance should decrease as the group size increases. Various mammal and bird studies have confirmed the negative relationship between an individual’s vigilance level and group size, the so- called group size effect (Caro 2005; Elgar 1989; Quenette 1990). Some primate studies have shown that individual vigilance does not relate to group size, but inversely relates to the number or density of near neighbors or both (Rose and Fedigan1995; Steenbeek et al.1999; Treves1998,1999b,2000; van Schaik and van
Noordwijk 1989). Conversely, if conspecific factors strongly affect vigilance, then vigilance levels should increase as the group size or the number of proximate individuals increases (Hirsch2002; Kutsukake2006; Treves1999a) because conditions in which group members are in proximity create more possibilities for group member interactions. However, even when conspecific factors affect vigilance, demonstrating the influence of conspecifics on vigilance may be difficult. When both predation pressure and conspecific factors affect vigilance at the same time, decreased antipredator vigilance and increased vigilance due to conspecific factors may offset each other and vigilance may not vary with the group size or the number of proximate individuals (Tchabovsky et al.2001; Treves1999a). One way to avoid the problem is to study a species under weak predation pressure (Hirsch2002).
I investigated vigilance behavior in wild chimpanzees (Pan troglodytes schweinfurthii) in Mahale Mountains National Park, Tanzania. Chimpanzees live in multimale, multifemale societies, in which group members associate in temporary parties of various sizes and compositions (Goodall 1986). Previous studies have shown that predation pressure is weak in the species (Goodall1986; Nishida et al.2003). For example, leopards (Panthera pardus) constitute the only potential chimpanzee predator at the site, but it is not obvious whether chimpanzees were actually preyed on by leopards in the Mahale (Hiraiwa-Hasegawa et al. 1986; Kutsukake 2006; Nishida et al.2003; cf. Boesch1991; Zuberbühler and Jenny 2002).
I previous investigated (Kutsukake 2006) vigilance behavior via instantaneous sampling and showed that conspecific factors strongly influence vigilance: 1) males increased their level of vigilance as the number of individuals ≤3 m increased; 2) in situations in which there is ≥1 individual nearby, the level of maternal vigilance was higher when a dependent infant was separated from its mother than when it was in contact with its mother. In contrast, the level of maternal vigilance was not affected by the infant’s relative position when there was no other individual nearby. However, the results are based on observations in which various social factors were not controlled. This is not to say that the temporal social settings are not important determinants of their vigilance behavior (Roberts 1995); instead, they may prevent sophisticated testing of relationships between group size and vigilance behavior. To overcome the problem, I controlled for the temporal social settings and investigated the social determinants of vigilance behavior. To increase the accuracy of recording vigilance, I used a different observational method than the one used in my previous study (Kutsukake 2006). Moreover, I collected data when the chimpanzees were resting and when they were on the ground—where an encounter with leopards is possible— because measuring vigilance during nonforaging activity offers an alternative opportunity to test the group size effect (Arenz2003; Randler2005).
In particular, we address the following questions. Is chimpanzee vigilance sensitive to threats from predation, conspecifics, or both? In social settings in which there are individuals nearby and there is a probability of an attack on an infant, does maternal vigilance increase when an infant strays from its mother relative to when the infant is in a safe position, i.e., in contact with her? In social settings in which there is no individual nearby, do mother chimpanzees still increase their vigilance when the infant strays from her relative to when it is in contact with her?
Methods
Study Site and Group
I examined wild chimpanzees in M-group at the Mahale Mountains National Park on the eastern shore of Lake Tanganyika in western Tanzania. Researchers have been studying Mahale’s wild chimpanzees since 1965 (Nishida1990), and all individuals, except for a few recently immigrated females, were well habituated. I made observations between September and December 2000 and between February and September 2001 (Kutsukake2003, 2006; Kutsukake and Castles2004; Kutsukake and Matsusaka 2002). During the study period, M-group ranged from 51 to 54 individuals, including 8 adult males (>15 yr) and 20 adult females. In addition, I included 1 adolescent male (PM) in the adult class because he had reached adult body size and received pant-grunts from adult females. I selected all 9 adult males and 9 adult females as observation targets (TableI). I chose the females so that the age distribution was not biased and represented the group composition. More importantly, I chose well-habituated females because a human presence influences the anxiety level and vigilance behavior of shy females. Because female reproductive condition may influence vigilance behavior, I conducted all observa- tions when the focal females were not estrous. All focal females had dependent
Table I Identities of focal individuals and sample size that met criteria for data collection ID Birth Dominance ranka No. of 2-min focal observation
(No. of neighbors ≤3 m)
0 1 2 3 4 5 6 >7 Total
Male DE 1963? 4 6 3 1 2 3 1 16
MA 1977 5 4 5 5 2 1 1 1 19
FN 1978? 1 8 3 4 2 17
HB 1980? 7 7 2 2 1 3 15
DG 1981? 2 8 2 3 4 17
BB 1981 8 7 4 2 3 16
AL 1985 3 7 2 6 1 1 17
CT 1985? 6 7 2 1 1 1 2 1 15
PM 1988 9 4 5 2 1 3 15
ID Birth Offspringb
Female FT 1963? 88M (PM), 99F 4 4 3 1 1 1 2 16
OP 1971? 86F, 91M, 98M 7 2 1 2 1 1 1 15
PI 1972? 91M, 00F 3 2 6 1 2 2 1 17
JN 1974? 95F, 00F 6 5 1 1 2 15
XT 1975? 95M, 00Fc 4 3 3 2 2 2 16
MJ 1980? 96M, 01Fc 6 2 1 2 2 2 1 16
AK 1981? 98F 5 2 2 2 1 1 1 1 15
CY 1982? 98M 4 1 2 3 3 3 16
AB 1982 98F 10 1 2 2 15
aI assessed dominance rank among 9 adult males via ad libitum sampling of the direction of pant-grunt vocalizations (Kutsukake2003).
b88M indicates a male offspring was born in 1988 within the group during the study period.
cInfants born during the study period.
offspring whose ages at the beginning of the observations ranged from 5 mo to 5 yr (mean age: 2.2 yr). Of the 9 focal females, 1 female (XT) gave birth soon after the start of observations and 1 (MJ) gave birth later in the observation period (TableI). For the latter mother, I used the data from before the birth.
Observation Methods
I observed the 18 individuals via continuous focal individual sampling (Altmann 1974). On each observation day, I chose 1 focal individual to follow for as long as possible; I based the choice of the focal individual on the criterion that data be accumulated evenly for every individual. I did not observe the same individual on 2 successive days (Kutsukake 2003). By continuous focal observation (in total 1100 h), an auditory encounter with leopards occurred 10 times. Typically, chimpanzees climbed a tree and gave alarm calls. The reactions were identical to chimpanzee behavior in a group in which predation by leopards occurred (Boesch 1991). In addition, Hiraiwa-Hasegawa et al. (1986) previously observed the killing of a leopard cub by chimpanzees at the study site. Though we detected no evidence of predation by leopards, the episodes suggest that they are a threat to chimpanzees. The data collected via continuous focal observation show that infants risk being attacked by other group members. On average infants receive 0.06 aggressive acts/ h (calculated from the 531 h of continuous focal observational data on 9 females), and in one case, an infant suffered bleeding injures from an attack by the α-male.
During the continuous focal observation, I conducted 2-min focal observations (Altmann 1974) to measure the total vigilance duration during resting. I used a stopwatch to measure the total vigilance duration. Though researchers have commonly used the observational method in previous studies of primate vigilance, they did not attempt to control for activity, posture, or various other settings that might affect vigilance behavior during the observations (Hirsch2002; Smith et al. 2004; Treves 1997,1998,1999a,b,c,2000; Treves et al.2001,2003) but only controlled for the effects of these variables statistically. For example, some researchers categorized activity into forage, rest, and mixed without mentioning what percent of time the focal individual was foraging or resting during the mixed category (Treves et al.2003). It is also reasonable to assume that a field of vision differs according to the posture of the focal individuals, which could affect vigilance behavior. I collected the data only when the focal individual was resting because previous study has already shown that vigilance levels in chimpanzees are lower during foraging than during resting (Kutsukake2006). Also, vigilance levels were higher when chimpanzees were on the ground where an encounter with leopards is possible compared to when they are in trees (Kutsukake 2006). To control for the factors, I gathered data only when the following conditions were met: 1) the focal individual was resting, 2) the focal individual was on the ground, 3) the researcher could observe more than half of the focal individual’s face (to ensure that the observer could watch for vigilance directly), 4) the individuals ≤10-m from the focal individual did not change, 5) the individuals
≤3 m did not change their position, 6) visibility was ≥10 m, 7) there was no other species that might be a target for hunting by the chimpanzees (particularly red colobus), 8) chimpanzee vocalizations did not occur, 9) no aggressive interaction had occurred for 10 min before the start of data collection, 10) the chimpanzees were not
patrolling after an encounter with another group for at ≥1 h before data collection, and 11) the chimpanzees did not encounter a leopard for ≥1 h before data collection. In addition, 12) when observing the mother chimpanzee, I categorized the position of her infant dichotically as within reach or apart from her, and infant position did not change during the 2-min observation. For example, I labeled an infant that kept within reach of the mother during the 2-min observation as in contact. I did not count individuals
<4 yr in conditions 3 and 4.
Authors of previous studies on primates used various definitions of vigilance behavior, e.g., movement of the head (Steenbeek et al. 1999), or scanning their surroundings (Cowlishaw1998; Treves1999a). Such differences in the definition of vigilance behavior may be linked to characteristics of the study species. In wild chimpanzees, the clearest definition of vigilance available is that an individual stands up and fixes its gaze on the surrounding environment. However, researchers have observed most cases of such vigilant behavior only after a chimpanzee had heard the vocalization of a leopard or of chimpanzees in a neighboring group; its occurrence was too rare during the focal observations of my study for quantitative analysis. Therefore, I focused on a lower level of vigilance behavior, that involved gazes fixed on the surrounding environment in a head-up, stationary sitting posture, i.e., it did not include glancing toward food handled by the focal individual, the ground nearby, or the individual’s own body, but it included glances toward group members.
I made observations only when all of the conditions held for 2 min. If one of the conditions was violated, the observations ceased and I discarded the data. I collected data once a day for each focal individual to avoid pseudoreplication. I collected >15 focal observations per a focal individual (TableI), and in total, analyzed 288 2-min samples.
Statistical Analyses
I analyzed total vigilance duration as a percentage of 120 s and set it as a dependent term in the generalized linear mixed model (Schall 1991) with binomial error structures. Mixed models allow both fixed and random components to be fitted to a model. I fitted the identity of the focal individual as a random term. Random terms consider repeated sampling within the same focal individuals. Because the variables affecting the vigilance level should differ by sex, i.e., an infant influences female vigilance only, I analyzed data for males and females separately.
Fixed explanatory terms included number of neighbors ≤3 m (continuous: 0–11 individuals), the number of individuals ≤10 m (continuous: 0–12 individuals), and infant’s position (categorical: contact or separate, for female analysis only). There is a significant correlation between the number of individuals ≤3 m and the number of individuals ≤10 m (r = 0.80, p < 0.0001). To avoid the problems caused by collinearity, I put each independent variable in the model separately and included 1 independent term with the stronger influence in the model. In accordance with Crawley (2002), I included all likely explanatory variables and a possible 2-way interaction in the maximal model and excluded terms sequentially until the model included only terms whose elimination would significantly decrease the Akaike Information Criterion of the model.
Results
The individual mean of vigilance duration in 2 min is 72.4 (SE: 2.8) s (minimum= 5.2 s; maximum =120 s) in males and 72.0 (SE: 2.8) s (minimum=6.7 s; maximum = 120 s) in females.
In males, vigilance duration increased as the number of neighbors ≤3 m increased (TableII; Fig.1) but not by the number of individuals ≤10 m.
In females, vigilance duration was affected by infant position, number of individuals ≤3 m, and the number of individuals ≤10 m. Vigilance duration was higher when the infant was at a distance than when in contact with the mother (Fig.2). Also, the number of neighbors ≤3 m and the number of individuals ≤10 m both positively affected the vigilance duration (Fig. 2). I retained the number of individuals ≤10 m in the final model because it had a greater influence on the vigilance than the number of neighbors ≤3 m excluded. The interaction between the number of individuals ≤10 m and the infant’s position was excluded from the model
Table II Factors affecting the vigilance duration
Male Female
b SE df t p b SE df t p
No. of individuals ≤3 m 0.16 0.06 137 2.62 0.01a 0.1 0.05 131 2.19 0.03 No. of individuals ≤10 m 0.04 0.05 137 0.89 0.38 0.12 0.04 130 2.95 0.004a Infant position (contact < separate) – – – – – −0.73 0.21 130 −3.50 0.001a
aFactors that remained in the final model.
Fig. 1 Relationship between vigilance duration (s in 2 min) and number of individuals ≤3 m in males. Individual means ± 1 SE are shown. Alone refers to the situation in which there is no individual ≤3 m from the focal individuals. 3+ refers to the situation in which there are ≥3 individuals ≤3 m from the focal individuals.
(p=0.72), suggesting that maternal vigilance was high regardless of the number of individuals ≤10 m.
Discussion
Vigilance duration increased as the number of group members nearby, i.e., ≤3 m or 10 m; increased, both in male and female chimpanzees, which agrees with my previous study of vigilance behavior during broader social settings did and showed that the number of group members ≤3 m correlates positively with vigilance level (Kutsukake 2006). The result also fits with the idea that the vigilance is directed mainly to conspecifics rather than to the risk of predation (Hirsch2002).
Despite numerous studies from which researchers have reported an inverse relationship between vigilance and group size or the number of group members nearby (Caro2005), why do wild chimpanzees in my study not fit this pattern? One possibility relates to the low predation pressure on Mahale chimpanzees (Nishida et al. 2003). Hirsch (2002) reported a positive relationship between the time for vigilance and the number of neighbors in brown capuchins living under low predation pressure. By comparing the result to other populations of capuchins that live under high predation pressure and whose vigilance declines as the number of neighbors increases, Hirsch (2002) attributed the positive relationship between vigilance and number of neighbors to the low predation pressure the population faces. Even if there is a predation threat to some extent, vigilance activities for ca.
Fig. 2 Relationship between vigilance duration by females (s in 2 min) and the number of individuals within 10 m. Individual means + 1 SE are shown. A solid line indicates the duration of maternal vigilance when the infant was separated from the mother. A dashed line indicates the duration of maternal vigilance when the infant was in contact with the mother. Alone refers to the situation in which there are no individuals ≤10 m from the focal individuals. 3+ refers to the situation in which there are ≥3 individuals
≤10 m from the focal individuals.
60% of the time chimpanzees spent resting alone (Fig. 1) might be sufficient to detect leopards. Another possible reason relates to the cost of vigilance. Vigilance conflicts with various other activities such as foraging, grooming, and sleeping (Maestripieri1993; Treves 2000). However, because vigilance and resting are not mutually exclusive, the cost of being vigilant while resting may be low relative to the costs during foraging, i.e., decreases in foraging efficiency. Therefore individuals may not need to decrease vigilance during resting. Also, the increase in vigilance was slight; vigilance increased by ca. 12 s per 2-min focal when there were ≤3 individuals nearby compared to when there was none. The reason for the slight increase is unknown, but it may indicate that the effect of conspecific threats, i.e., positive effect of the number of group members nearby, was partly set off by the effect of predation threat, i.e., negative effect of the number of group members nearby (Tchabovsky et al.2001; Treves1999a).
Independent of the number of group members nearby, maternal vigilance duration increased when the infant was separated from the mother relative to when the infant was in contact with her (Fig.2), which agrees with the view that vigilance functions to monitor and to protect infants (Maestripieri1993; Steenbeek et al.1999; Treves et al. 2003). When an infant is separated from its mother, she needs to monitor the surroundings because it risks aggression from other individuals (Otali and Gilchrist 2006). In addition, the higher vigilance levels in females when there is no individual nearby relative to when there is may suggest that infants also risk being predated on to some extent. Using the instantaneous sampling method, Kutsukake (2006) also found that, in broader social settings than the ones in the present study, maternal vigilance increased when the infant was separated from its mother, but the increase was confirmed only when there were neighbors and the maternal vigilance did not vary according to the infant position when there was no neighbor. I used data on infants separated from their mothers for 2 min during the focal observations. In the previous study, the period of separation may have been much shorter. Consequently, it may be that mothers increase their vigilance only when their infants are separated from them for a long duration.
There are several limitations to my study. First, it is based on a relatively small sample size because of the strict observation conditions and it did not allow me to examine factors other than the number of individuals nearby and their effects on vigilance. For example, both males and females are more vigilant when they are near infrequent association partners than when they are near common association partners (Kutsukake2006; Watts1998). Future studies designed to test the effect of neighbor identity may elucidate the effects of other social factors on vigilance levels. Another limitation is that it is difficult to distinguish between vigilance and monitoring in the field. Therefore, it is possible that the individuals used monitoring behavior for different purposes. For example, the vigilance duration of females without infants was similar to that of males (Figs.1 and 2). Though I did not aim to test the sex differences of vigilance behavior, one may predict that females with straying infants should be more vigilant than males. However, males and females may use vigilance for other sex-specific purposes and if so, it casts doubt on the usefulness of direct comparisons between males and females. Because males that affiliate frequently tend to form coalitions or alliances to attack a rival male and the coalitions or alliances strongly affect dominance rank (de Waal1982; Nishida and Hosaka1996) it may be
important for adult males to collect social information by monitoring behavior such as who is associating with whom. If it may have increased the monitoring duration in males, a similar level of vigilance duration between males and mothers could be expected.
In summary, I used more refined observational methods that controlled for various confounding factors better than the previous studies of primate vigilance, and added empirical data to the growing evidence that conspecific factors, in addition to predation risks, affect individual vigilance in social animals. Unfortunately, many previous vigilance studies have tended to ignore conspecific factors. To understand the determinants of vigilance behavior more comprehensively, it would be promising to investigate social influences on vigilance in various species in which conspecific vigilance appear to be important (Treves2000). For example, species with a high level of intragroup competition and risk of conspecific aggression, such as macaques and baboons, may be good subjects, in particular if the population lives under a weak predation pressure. Other species living in a highly complex society, e.g., spotted hyenas (Crocuta crocuta), may also be an interesting species in which to study social influences on vigilance.
Acknowledgments I thank the Tanzanian Commission for Science and Technology, the Serengeti Wildlife Research Institute, the Mahale Mountains Wildlife Research Centre, and Tanzania National Parks for permitting our research and for their support while I was in Tanzania. I also thank research assistants Toshisada Nishida, Kenji Kawanaka, Shigeo Uehara, Kazuhiko Hosaka, Michio Nakamura, Shiho Fujita, James Wakibara, Takahisa Matsusaka, and Watongwe, as well as other colleagues of the research team including Chisa Tokimatsu, for their support in various ways. I thank Toshikazu Hasegawa for his supervision and support during the study, as well as Toshimichi Nemoto and his family for their support. Tim H. Clutton-Brock and 2 reviewers gave critical comments and Michael Sheehan for correcting the English, for which I am grateful. Monbusho Scientific Research Fund (Basic Research A1, no. 12375003 to T. Nishida) and JSPS Research Fellowships for Young Scientists funded the study.
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