Predation as a Determinant of Minimum Group Size in ...

Published online: January 28, 2013

Folia Primatol 2012;83:332–352 DOI: 10.1159/000339808

Predation as a Determinant of Minimum Group Size in Baboons© Free Author Caroline M.

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Abstract Predation risk places a pressure on animals to adopt mechanisms by which they reduce their individual risk of being preyed on. However, a consensus on methods of determining predation risk has yet to be reached. One of the most widespread ways in which animals respond to predation risk is by living in groups. Minimum permissible group size is the smallest group size that animals are able to live in, given–thefor habitat© Free Author Copy personal use only specific predation risk they face. We explore ways in which predation risk can be meaANY DISTRIBUTION OF THIS ARTICLE WITHOUT WRITTEN CONSENT FROM S. KARGER AG, BASEL IS A V sured and analyse its effect on minimum observed group size in baboons. Using data Written permission to distribute the PDF will be granted against payment of a permission fee, which is on predator density, habitat composition and baboon body size, we investigate the impact of the components of predation risk on baboon group size, and derive an equation that best predicts minimum group size. Minimum group size in baboons is related to predator density and female body mass. Both of these elements can, in turn, be estimated from environmental variables. These findings present support for the argument that group living in primates is a response to predation risk and offer potentially new Copyright © 2013 S. Karger AG, Basel ways of investigating carnivore and primate ecology.

Introduction

Predation has been described as ‘the most important single factor in the interpretation of baboon ecology and social behavior’ [Devore and Hall, 1965]. More specifically, predation risk has been proposed to be the primary driving force behind group living in primates [van Schaik, 1983]. However, whilst predation may be the

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Caroline Bettridge Division of Biology and Conservation Ecology School of Science and the Environment Manchester Metropolitan University Chester Street, Manchester M1 5GD (UK) E-Mail c.bettridge @ mmu.ac.uk

main cause of adult mortality in some baboon populations [Busse, 1980], in others it appears rare or altogether absent [Jolly, 1972; Wrangham, 1980]. Rather than being a response to predation, Wrangham [1980] argued that group living evolved to allow the defence or control of food resources. A common argument among critics of the predation risk model has been that if gregariousness were an effective defence against predation, then one should expect to see a negative relationship between predation rate and prey group size [Cheney and Wrangham, 1987]. Using predation rate to infer predation risk may be an inaccurate method for a number of reasons: first, there is the argument that predation rate reflects the current rather than the intrinsic predation risk [Janson, 2003]; that is, the observed predation rate represents the residual risk that the animals cannot control by their antipredator strategies [Hill and Dunbar, 1998]. As the effort invested in antipredator behaviour such as grouping increases, direct predation is likely to decline. Risk effects, the costs of antipredator behaviour, do not necessarily correlate with direct predation and can exist even when the predation rate is zero [Creel and Christianson, 2008]. Secondly, researchers rarely witness successful or even attempted predation, leaving the cause of mortality subject to guesswork. It is therefore likely that relying on recorded predation attempts gives a lower estimate of the predation risk actually faced by the prey. It is also likely that it is the perceived predation risk on the part of the prey species, rather than the actual predation rate, which is important in influencing group living in animals [Frid and Dill, 2002; Willems and Hill, 2009]. Suitable measures of intrinsic predation risk have been suggested as: predator density, attack frequency, predator success per attack and individual vulnerability [Janson, 2003]. Previous studies have used measures such as predator diversity [Anderson, 1986], attack rate [Hill and Lee, 1998], encounter rate [Oliveira and Dietz, 2011] or a combination of models of predator-prey interactions and habitat structure [Lima, 1987; Cowlishaw, 1997a, b], to measure levels of intrinsic predation risk. Here, we investigate a number of measures other than predation rate in an attempt to predict the relative level of intrinsic predation risk faced by baboon populations across Africa. We do this by looking for relationships between each of the measures and the minimum group size recorded for individual baboon populations. Predation is a complex process that prey can attempt to break down at any or all of the composite stages: (i) predator encounter, (ii) predator attack, (iii) prey capture, and (iv) individual capture probability or vulnerability [Lima and Dill, 1990; Cowlishaw, 1994]. Group living is perhaps most often viewed as acting at the fourth of these stages, reducing an individual’s probability of being captured by a predator via the dilution effect [Hamilton, 1971], but also has additional benefits such as increased vigilance [Cheney and Wrangham, 1987; Isbell, 1994] or active defence [Cowlishaw, 1994; Cheney et al., 2004]. In this paper, we concentrate on the other ways in which group living may come into play: by affecting the likelihoods of an encounter between predator and prey, a predator attack and a subsequent prey capture. For an attack to occur, a predator must first locate its prey. The likelihood of an encounter between predator and prey will be influenced by the density and the distribution of both predators and prey. For example, a higher density and scattered distribution of predators may increase the chances of an encounter between predator and prey.

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The effects of predator abundance may be mediated both by antipredator behavior and landscape attributes [Schmitz, 2007; Heithaus et al., 2009]. Once an encounter occurs, the probability that it will result in capture of a prey individual depends on a number of factors. Firstly, a predator has to decide whether to attack the prey. This decision will be influenced by several considerations, including the size of the prey group encountered. The ability to surprise the prey may also be critical to the predator’s decision to attack. Increased vigilance, arguably a result of group living, often leads to earlier detection of the predator and thus may deter a predator from attacking. This is especially true for ambush predators, who rely on surprise in their method of attack. Where a predator does choose to attack, they may be more likely to face active defence from larger groups, reducing their chance of making a kill. Baboons have been seen to attack [Cheney et al., 2004], and even kill leopards [Cowlishaw, 1994]. In this example, group composition, as well as group size, is important, as it is usually male baboons that take part in mobbing of predators. Once a predator attacks a group, the vulnerability of each individual in that group will depend on factors such as body size and means of escape or defence. The risk of capture will also depend on the probability of the prey escaping once the predator attacks. There are two main factors likely to heavily influence the chances of success of an attack. The first is the ability of the predator to ambush their prey; the closer a predator is to its prey before being detected, the more likely the attack is to be successful. The second is the availability of refuges or cover that enable the prey to escape or hide once it becomes aware of an attack. While the first factor will be affected by the vigilance of the group (and hence arguably show an effect of group size), both of these factors can also be related to the habitat, specifically the vegetation structure, in which the predator and prey species live. Landscape features interact with antipredator behaviour such as gregariousness, to determine the probability of an encounter and prey capture [Heithaus et al., 2009]. Vegetation and habitat type have been argued to affect predation risk in two contrasting ways [Dunbar, 1996; Cowlishaw, 1997a, b]. The first is by influencing the probability of attack by a predator: risk of attack correlates positively with degree of bush level vegetation cover. Baboons at Amboseli, Kenya, give more alarm barks and are more frequently attacked by predators in wooded areas of their range [Altmann and Altmann, 1970]. At Mikumi in Tanzania, baboons bunch more closely and act nervously in areas where the vegetation makes it difficult to see stalking predators [Rasmussen, 1983], while at Tsaobis, Namibia, both their nervousness and risk of exposure to attack were most heavily influenced by the degree of cover [Cowlishaw, 1993, 1997a]. Studies have shown that baboons [Hill, 1999] and vervet monkeys [Willems and Hill, 2009] select habitats on the basis of their visibility – a feature closely linked to the degree of bush level cover. Studies on predators such as leopards and lions have also shown that attacks are more successful as the degree of cover increases [Van Orsdol, 1984; Bothma and Leriche, 1986]. In contrast, tree cover is argued to decrease the predation risk for baboons [Dunbar, 1996]. Several studies have recorded baboons being nervous in very open areas away from trees or other suitable refuges [Whiten et al., 1991; Dunbar, 1989 (gelada)]. So, while dense, bush level cover may increase the predation risk, tree cover may reduce it especially from terrestrial predators. In addition to changes in behaviour, minimum group size in baboons has been reported to be a positive function

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of the degree of bush level cover, and a negative function of the density of large trees [Dunbar, 1996], adding support to the argument that group size is a reflection of predation risk. However, in a test of this hypothesis, Hill [1999] failed to identify a significant relationship between minimum group size and vegetation cover. Finally, the physical size of an individual may affect its susceptibility to predation and influence the benefit of forming groups. Increased body mass has been argued to be an adaptation to predation [Cheney and Wrangham, 1987]. The variation in body mass between different populations and subspecies of baboons allows us to investigate this on a finer scale. Many of the arguments above focus on ways in which larger group sizes reduce an individual’s predation risk. However, larger groups may be more conspicuous and easier for predators to locate. In ungulates at least, there is evidence that some predators, such as African wild dogs, are more likely to attack larger groups of prey [Creel and Creel, 2002]. In this case, the benefits of increased vigilance, early warning and the dilution effect must be traded off against the cost of an increased chance of attack. We argue that if group living is an adaptive response to predation risk, then the minimum group size in which a species can exist should reflect the level of predation risk perceived by the animals themselves. This claim is difficult to test. Whilst the costs incurred by larger group sizes, as a result of within-group feeding competition [Dunbar, 1980, 1988; Hill, 1999], mean that there is good reason not to expect primates to live in increasingly large group sizes, there are several reasons why it is also unlikely that the group sizes observed in natural populations will be the smallest that could survive. One is that the minimum permissible group size would in reality be a very unstable position. If one individual died, the group size would immediately fall below the minimum needed to reduce individual predation risk to an acceptable level. A second reason is that group sizes are the result of the behaviour of a number of individuals, whose interests may conflict with each other. For example, a group may be larger than the minimum permissible group size for that environment. Individuals in that group may be suffering the costs of increased within-group competition; however, they may still be better off than if the group fissioned. A group can only fission if both of the resulting smaller groups are larger than the minimum permissible group size for that habitat. While the interrelationship between group size and distribution, habitat type and predation risk is complex, increased group size could arguably reduce the predation risk at each of the four stages. Following Hill and Dunbar [1998], we argue that predation risk influences minimum group size in primates. By identifying variables that are associated with larger minimum baboon group sizes (i.e. predator density, vegetation cover and type, or baboon body mass), we hope to provide additional or alternative indicators of predation risk for semiterrestrial primates.

Methods Data Collection In order to explore the relationships between predator density, vegetation, prey body mass and group size, we compiled data on the minimum and mean group sizes recorded at baboon study sites from published and unpublished sources. Data are given in table 1.

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Table 1. Minimum and mean reported baboon group sizes (n), and leopard and lion densities (n/km2) Site

Min.

Papio cynocephalus anubis Nairobi, Kenya Gilgil, Kenya Gombe, Tanzania Budungo, Uganda Chololo, Kenya QEI, Uganda Shai Hills, Ghana Bole, Ethiopia Manyara, Tanzania Serengeti, Tanzania Murchison, Uganda Awash, Ethiopia Laikipia, Kenya

12 35 18 30 29 32 14 17 51 10 14 16 51

Papio cynocephalus cynocephalus Ruaha, Tanzania Tana River, Kenya Amboseli, Kenya Mikumi, Tanzania Masalini, Kenya Kariba, Zimbabwe Papio cynocephalus hamadryas Awash, Ethiopia Erer Gota, Ethiopia Dogali, Eritrea

Leopard

Lion

Lat.

Long.

Sources

42.1 65.0 38.3 41.3 43.3 45.0 19.1 19.5 66.0 22.0 27.6 55.8 101.0

0.130 0.080 0.200 0.250 0.070 0.090 0.000 0.160 0.100 0.140 0.180 0.080 0.100

0.110 0.230 0.000 0.050 0.140 0.090 0.000 0.000 0.080 0.070 0.050 0.050 0.160

–1.37 –0.22 –4.67 1.73 –0.88 –0.17 5.92 9.42 –3.20 –2.20 2.12 8.92 0.42

36.86 36.27 29.63 31.55 36.25 30.00 0.05 38.55 35.45 34.55 32.12 40.04 36.75

1 2, 3 4, 5 6–8 9, 10 8, 11, 12 13 14 15 15 16 17–19 20

24 74 18 18 25 12

71.6 78.8 50.8 80.2 42.5 46.0

0.040 0.110 0.040 0.110 0.140 0.110

0.050 0.030 0.040 0.040 0.050 0.020

–7.53 –1.92 –2.64 –7.40 –2.78 –16.30

34.66 40.83 37.25 37.23 38.10 28.40

21 22 15, 23, 24 25 26 27

51 69 7

54.0 83.0 188.0

0.080 0.120 0.080

0.050 0.030 0.000

8.92 9.53 15.38

40.04 41.40 38.81

18, 28 29 30

89.2

0.130

0.040

13.01

–13.03

31.6 79.4 47.2 78.0 22.5 34.4 38.3 49.0 34.3

0.090 0.060 0.040 0.090 0.000 0.000 0.080 0.080 0.020

0.170 0.030 0.050 0.000 0.000 0.000 0.000 0.070 0.000

–25.45 –19.46 –22.63 –26.51 –29.22 –34.43 –34.14 –27.64 –22.38

29.45 22.81 30.18 28.23 29.49 20.57 18.41 32.23 15.75

Papio cynocephalus papio Nikola Koba, Senegal Papio cynocephalus ursinus Loskop, SA Okavango, Botswana Honnet, SA Suikerbosrand, SA Giants Castle, SA De Hoop, SA Cape Point, SA Mkuzi, SA Tsaobis, Namibia

16 7 30 3 4 17 6 28 22

Mean

31 32 334 34, 35 36 27, 37, 38 39 40 41 42

Min. = Minimum baboon group size; mean = average baboon group size; Lat. = latitude; Long. = longitude; QEI = Queen Elizabeth National Park; SA = South Africa ; Leopard = estimated leopard density (n/km2); Lion = estimated lion density (n/km2). 1 = Devore and Hall [1965]; 2 = Harding [1976]; 3 = Eley et al. [1989]; 4 = J. Oliver and D. Rasmussen, pers commun. to R.I.M.D.; 5 = Ransom [1981]; 6 = Popp [1978]; 7 = Popp [1983]; 8 = Patterson [1976]; 9 = Barton [1989]; 10 = Kenyatta [1995]; 11 = Patterson [1973]; 12 = Rowell [1969]; 13 = Depew [1983]; 14 = Dunbar and Dunbar [1974]; 15 = Altmann and Altmann [1970]; 16 = Hall [1965]; 17 = Aldrich-Blake et al. [1971]; 18 = Nagel [1973]; 19 = Brett cited in Popp [1983]; 20 = Berger [1972]; 21 = J. Oliver and D. Hawkins, pers commun. to R.I.M.D.; 22 = BentleyCondit and Smith [1997]; 23 = Altmann and Altmann [1977]; 24 = Bronikowski and Altmann [1996]; 25 = Rasmussen [1978]; 26 = Maxim and Beuthner-Samuel [1963]; 27 = Hall [1963]; 28 = Swedell [2000]; 29 = Sigg et al. [1982]; 30 = Zinner et al. [2001]; 31 = Sharmann, pers commun. to R.I.M.D.; 32 = Stoltz cited in Anderson [1981a]; 33 = Hamilton et al. [1976]; 34 = Stoltz and Saayman [1970]; 35 = Saayman [1971]; 36 = Anderson [1981a]; 37 = Whiten et al. [1987]; 38 = Henzi et al. [1997]; 39 = Hill [1999]; 40 = Davidge [1978a]; 41 = Gaynor [1994]; 42 = Cowlishaw [1993].

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We use climate data taken from the original studies from which we collated baboon group size data, or other published studies from the same site and time. If climate data were not given, we used data from the Willmott and Matsuura [2001] weather database from the time period 1950–1999 inclusive. The following climate variables were used in this study: mean annual temperature, mean monthly temperature (the mean of the 12 monthly mean temperatures), minimum and maximum annual temperatures in degrees Celsius, temperature and rainfall variation between months (calculated as the standard deviation across average values for 12 months), mean annual and mean monthly rainfall in millimetres, number of months per year with less than 50 and less than 100 mm of rainfall, and the plant productivity index P 1 2T (the number of months in the year in which rainfall, in millimetres, was more than twice the average monthly temperature). We also included Moisture Index (MI) measures [Willmott and Feddema, 1992]. The MI is an agrometeorological indicator, calculated using the ratio of annual precipitation to annual potential evapotranspiration, which provides a quantitative index of the amount of moisture available to plants. Finally, we used AVHRR satellite data on forest cover from De Fries et al. [2000] and predictive equations from Dunbar [1996] to determine the percentage of vegetation cover for each site. Full details of all abiotic variables and data sets used are given in Bettridge et al. [2010]. Our first index was the likelihood of predator encounters, estimated using the presence of individual predator species at a site. First, we used a simple count of the number of predator species present in an area. A review of predation on baboons used a combination of baboon alarm call responses and attack and consumption reports to identify potential and actual predator species [Cowlishaw, 1993]. Alarm call responses suggested a number of potential predators including lion (Panthera leo), leopard (Panthera pardus), hyaena (Crocuta crocuta, Hyaena brunnea, H. hyaena), chimpanzees (Pan troglodytes), cheetah (Acononyx jubatus), wild dog (Lycaon pictus) and black-backed and side-striped jackal (Canis mesomelas and C. adustus). When attack and consumption rates were taken into account, the 4 main predator species were identified as leopard, lion, hyaena and chimpanzees, with leopard and lion presenting the greatest threat. To this list, we added caracal (Felis caracal). Although not considered in previous studies on baboon predation, caracals are known to prey on ungulates of similar body size to baboons [Adamczak and Dunbar, 2008] and therefore could be considered potential predators of baboons. For each of the baboon populations listed in table 1, we compiled the presence or absence of each of the 8 potential predators (treating the 3 hyaena and 2 jackal species as single categories) from a combination of original publications and the UNEP and World Conservation Monitoring Centre World Database on Protected Areas (http://sea. unep-wcmc.org/wdpa/). The likelihood of an encounter between predator and prey will depend not only on the presence of a predator species, but also the density at which it occurs. As data on predator densities are difficult to obtain, we limited our analyses to the two main predator species of baboons, leopards and lions. Since data on the density of these species were not available directly for the majority of the baboon sites listed in table 1, we collated data on their density at other locations in Africa and looked for relationships between their density and ecological variables in order to predict the density at other locations. Data on leopard density were taken from Hill [1999]. Coordinates were unavailable for 5 of the sites used by Hill. This meant we were unable to obtain climate data from the Willmott and Matsuura [2001] database for these sites, so we excluded these from our analyses. This left 20 sites with information on leopard density. Lion density was calculated for 43 sites from Bauer and Van der Merwe [2004], who provide estimates of lion numbers within protected areas. We discounted all the sites where lion densities were derived from their ‘undefined methods’ because this method yielded significantly lower densities than the defined methods (MWU test: Z = 1.254, p = 0.029) [for details, see Bettridge et al., 2010]. We then used backward stepwise regression to find the equations which best predict lion and leopard density from environmental variables [for original data, see Bettridge et al., 2010]. Data were log-transformed when necessary to ensure normality. The derived equations were then used to estimate leopard and lion density for the sites in table 1.

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Table 2. Baboon body masses (kg)

Fbm

Mbm

Sources

22.8 (10) 24.4 26.5 (6) 27.1 (54) 34.4 (1) 21.5 21.1

1 2, 3 4, 5 6, 7 8 9–11 12

Papio cynocephalus anubis

Nairobi, Kenya Gilgil, Kenya Gombe, Tanzania Masai Mara, Kenya Budungo, Uganda Awash, Ethiopia Laikipia, Kenya

12.3 (39) 12.8 13.9 14.0 (23) 15.1 (3) 12.5 12.2

Papio cynocephalus cynocephalus

Ruaha, Tanzania Tana River, Kenya Amboseli, Kenya Mikumi, Tanzania

9.7 9.7 11.3 (2) 12.3

22.2 (1) 21.8

13 14 15–17 18

Papio cynocephalus hamadryas

Awash, Ethiopia Erer Gota, Ethiopia Harar, Ethiopia

9.7 11.3 (16) 11.4 (13)

16.2 19.5 (4) 21.0 (7)

18, 19 20 7

Papio cynocephalus ursinus

Loskop, SA Okavango, Botswana Honnet, SA Suikerbosrand, SA Giants Castle, SA De Hoop, SA

13.6 13.9 (17) 14.5 15.4 15.9 16.1

28.8 (19) 26.3 27.3 21.3 29.7

21 22 23, 24 25 26, 27 28

Fbm = Female body mass; M bm = male body mass; SA = South Africa; figures in parentheses indicate numbers, i.e. sample size. 1 = Devore and Hall [1965]; 2 = Harding [1976]; 3 = Eley et al. [1989]; 4 = J. Oliver and K. Rasmussen, pers. commun. to R.I.M.D.; 5 = Ransom [1981]; 6 = Popp [1978]; 7 = Popp [1983]; 8 = Patterson [1976]; 9 = Aldrich-Blake et al. [1971]; 10 = Nagel [1973]; 11 = Brett in Popp [1983]; 12 = Berger [1972]; 13 = J. Oliver and D. Hawkins, pers. commun. to R.I.M.D.; 14 = Bentley-Condit and Smith [1997]; 15 = Altmann and Altmann [1970]; 16 = Altmann et al. [1977]; 17 = Bronikowski and Altmann [1996]; 18 = Rasmussen [1978]; 19 = Swedell [2000]; 20 = Sigg et al. [1982]; 21 = Stoltz cited in Anderson [1981a]; 22 = Hamilton et al. [1976]; 23 = Stoltz and Saayman [1970]; 24 = Saayman [1971]; 25 = Anderson [1981b]; 26 = Whiten et al. [1987]; 27 = Henzi et al. [1997]; 28 = Hill [1999].

Our second index is the likelihood of a predator attacking and capturing a prey animal. This was indexed using (i) AVHRR satellite tree coverage [De Fries et al., 2000] and (ii) bush and tree cover calculated from the equations in Dunbar [1996]. Our final measure was individual prey vulnerability. The physical size of an individual may affect its susceptibility to predation and influence the benefit of forming groups. We used male and female body mass collated from published sources (table 2) as an estimate of vulnerability. We investigated the relationships between both male and female body mass on minimum group size using bivariate scatter plots and curve estimation. Finally, we used the significant components of predation risk, identified using the preceding analyses, to derive an equation that estimates minimum permissible group size for baboons. We tested the validity of this equation by comparing predicted minimum group size with observed baboon group sizes taken from published time budget studies (table 3).

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Table 3. Baboon time budget study group sizes

Site

n

Lat.

Long.

Sources

Papio cynocephalus anubis Bole Valley Ethiopia Shai Hills, Ghana Chololo, Kenya Gilgil, Kenya Masai Mara, Kenya Gombe, Tanzania Budungo, Uganda QEI, Uganda

19 19 102 54 54 43 41 51

9.42 5.92 –0.88 –0.22 –1.49 –4.67 1.73 –0.17

38.55 0.05 36.25 36.27 35.14 29.63 31.55 30.00

1 2, 3 4, 5 6, 7 8 9 10 10

Papio cynocephalus cynocephalus Amboseli, Kenya Gashaka Gumti, Nigeria Mikumi, Tanzania Ruaha, Tanzania

55 21 120 72

–2.64 7.49 –7.40 –7.53

37.25 11.71 37.23 34.66

11–14 15 16 17

Papio cynocephalus hamadryas Awash, Ethiopia Erer Gota, Ethiopia

92 83

8.92 9.53

40.04 41.40

18–20 21

Papio cynocephalus papio Nikola Koba, Senegal

89

13.01

–13.03

Papio cynocephalus ursinus Okavango Delta, Botswana Tsaobis, Namibia Cape Point, SA Giants Castle, SA Honnet, SA De Hoop, SA Mkuzi, SA

72 34 85 18 77 31 47

– 19.46 – 22.38 – 34.14 – 29.22 – 22.63 – 34.43 – 27.64

22.81 15.75 18.41 29.49 30.18 20.57 32.23

22 23–25 26 27, 28 29–31 32 3, 33 34

n = Group size; Lat. = latitude; Long. = longitude; QEI = Queen Elizabeth National Park; SA = South Africa. 1 = Dunbar and Dunbar [1974]; 2 = Depew [1983]; 3 = Hill [1999]; 4 = Barton [1989]; 5 = Kenyatta [1995]; 6 = Eley et al. [1989]; 7 = Harding [1976]; 8 = Popp [1978]; 9 = J. Oliver and D. Rasmussen, pers. commun. to R.I.M.D.; 10 = Patterson [1976]; 11 = Altmann and Altmann [1970]; 12 = Bronikowski and Altmann [1996]; 13 = D. Post, pers. commun. to R.I.M.D.; 14 = Devore and Hall [1965]; 15 = Warren [2003]; 16 = K. Rasmussen and D. Rasmussen, pers. commun. to R.I.M.D.; 17 = J. Oliver, pers. commun. to R.I.M.D.; 18 = Aldrich-Blake et al. [1971]; 19 = Nagel [1973]; 20 = Swedell [2000]; 21 = Sigg et al. [1982]; 22 = Dunbar and Nathan [1972]; 23 = Hamilton et al. [1978]; 24 = Hamilton et al. [1976]; 25 = Hamilton et al. [1975]; 26 = Cowlishaw [1993]; 27 = Davidge [1978a]; 28 = Davidge [1978b]; 29 = Hall [1963]; 30 = Whiten et al. [1987]; 31 = Henzi et al. [1997]; 32 = Stoltz and Saayman [1970]; 33 = Barrett et al. [1999]; 34 = Gaynor [1994].

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Minimum observed group size in baboons (n)

50 40 30 20 10 0 Leopard Lion

Hyaena Chim- Cheetah Wild panzee dog

Caracal Jackal

Predator species

Fig. 1. Minimum group size against presence (dark grey) or absence (light grey) of individual

predator species.

Results

Predictors of Predation Risk Figure 1 shows the median and range of minimum baboon group size in the absence (light grey) and presence (dark grey) of each of the 8 potential predator species. Minimum group size in baboons is larger in the presence of lions, leopards, hyaena and chimpanzees than in their absence. In contrast, there is no increase in minimum group size in the presence of the other potential predators. The differences are significant for both lion and leopard (lionabsent median = 12; IQ range = 5.5–17.25; n = 10; lionpresent median = 28; IQ range = 17.0–43.0; n = 17; Z = –3.010, p = 0.002; leopardabsent median = 12.0; IQ range = 5.5–16.25; n = 4; leopardpresent median = 23; IQ range = 16.0–31.5; n = 24; Z = –1.986, p = 0.046). Hyaenas showed a stronger effect on minimum group size than chimpanzees, but neither result was statistically significant (hyaenaabsent median = 15.5; IQ range = 7.0–21.0; n = 8; hyaenapresent median = 24.0; IQ range = 15.0–33.5; n = 17; Z = –1.630, p = 0.107; chimpanzeeabsent median = 18.0; IQ range = 10.0–31.25; n = 26; chimpanzeepresent median = 24.0; IQ range = 15.0–31.5; n = 4; Z = –0.998, p = 0.335). These data suggest that not all of the 8 potential predator species are associated with larger group size in baboons. Although jackals, wild dogs and cheetahs elicit alarm calls from baboons [Cowlishaw, 1993], and caracals are known to capture baboon-sized prey [Adamczak and Dunbar, 2008], none of these 4 species has been reported as capturing or killing baboons. It is possible that the minimum group size necessary to reduce predation risk from these species is far below those in which baboons live, and that baboons have therefore effectively solved the problem of defence against these predators. These species are the 4 smallest of the potential predator spe-

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Minimum observed baboon group size (n)

40

30

20

10

0 0

1

2

3

4

Number of predator species present

Fig. 2. Minimum baboon group size against number of predator species present (predator spe-

cies: lion, leopard, hyaena, chimpanzee).

cies considered in our analyses and, as such, may pose less of a threat than the larger predators. The 4 taxa shown here to be associated with larger minimum baboon group size (leopard, lion, hyaena and chimpanzee) are also identified by attack and consumption rates as baboons’ main predators [Cowlishaw, 1994]. Considering only these 4 taxa, we explored the effect of the number of predator taxa present on minimum baboon group sizes (fig. 2). Minimum baboon group sizes appear to increase in the presence of increasing numbers of predator species. The differences between minimum group sizes in the presence of 0–4 predator species are not significant, regardless of whether chimpanzees are included: Kruskal-Wallis tests: min(incl. chimp) H(4) = 4.68; p = 0.35; n = 23; min(excl. chimp) H(3) = 4.74; p = 0.20; n = 23. However, when the data are split into two groups with ‘0–1 (!2)’ and ‘2 or more (11)’ predator species, minimum group size is larger in the presence of more than one predator: median!2 = 15.5; IQ range = 8.25–19.0; n = 6; median 11 = 25.0; IQ range = 16.5–33.5; n = 17; Mann-Whitney U test: Z = –2.070, p = 0.038. We now refine our approach by estimating predator density for the two main predators, leopard and lion. Of the climatic variables available, leopard densities were best predicted by annual rainfall in millimetres (Pann; fig. 3): ln(leopard) = –10.552 + 1.256ln(Pann) (r2 = 0.44, F1, 28 = 23.40, p ! 0.001).

Lion density was best predicted by a quadratic relationship with mean monthly temperature and a positive relationship with monthly minimum MI (fig.  4). The best-fit equation is: lion = 1.354 + 0.109ⴢMImin – 0.099ⴢTmo + 0.002ⴢTmo2 (adjusted r2 = 0.47, F3, 39 = 13.54, p ! 0.001)

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ln (leopard density)

–1

–2

–3

–4 5.0

5.5

6.0

6.5

7.0

7.5

ln (annual rainfall)

Fig. 3. Leopard density (n/km2) against mean annual rainfall (mm).

where MImin = monthly minimum moisture index; Tmo = mean monthly temperature (see Bettridge et al. [2010] for detailed explanations of climate measures). Using these equations, we then estimated leopard and lion densities at the sites included in table 1, where those species are recorded as present. There is no relationship between minimum baboon group size and leopard or lion density when the two species are considered separately. However, a high density of one predator species may be matched by a low density of the other. So, sites with a low leopard density for example, might be influenced by a high lion density and vice versa. To allow for this, total predator density was calculated for each site as the sum of leopard and lion density, with 0.001 added to this, following Hill [1999], to account for the additional risk from other less important predators. This value is small enough that it is unlikely to distort any relationship between predator density and group size. However, it takes into account the fact that there is unlikely to be any location where predation risk is zero, even if the main predator species are absent. Table 1 gives the estimated predator densities at each of the baboon sites. Summing the densities of these two predators, we find a significant positive relationship with minimum baboon group size (Nmin; fig. 5). The equation explaining the greatest variance is: ln(Nmin) = 2.383 + 3.697ⴢtotal predator density (r2 = 0.172, F1, 28 = 6.217, p = 0.018).

Although there is a positive relationship between predator density and group size in baboons, the amount of variance explained is low. This, and the presence of outliers, suggests that other factors must be involved in determining the minimum group size in baboons. So far, we have identified positive relationships between minimum group size in baboons and the presence and density of predator species. These are factors that re-

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Color version available online

Lion density (n/km2)

0.25 0.20 0.15 0.10 0.05 –0.3 –0.4

–0.5

–0.6 –0.7 Ml min

–0.8

–0.9

–1.0

16

18

Me

20

nthly an mo

te m p

26

24

22

eratu

r

e (°C)

Fig. 4. Lion density against mean monthly temperature and minimum monthly MI.

late to the chance of an encounter between predator and prey, the first of the components of predation risk. The other elements of predation risk (attack and capture probability) are unlikely to relate to predator density and will depend instead on the group’s or individual’s vulnerability and their chances of escape or successful defence. We indexed the attack and prey capture risk using bush and tree densities. We used satellite tree cover [De Fries et al., 2000], and calculated bush and tree cover using the equations in Dunbar [1996]. We used scatter plots and curve estimation to identify relationships between them and minimum group size in baboons. Figure 6 shows minimum group size against bush cover. The positive relationship offers some support to the argument that increasing low-level cover increases predation risk. There is no evidence of a relationship between minimum group size and tree cover, whether using estimated values from Dunbar’s [1996] equation or the satellite forest cover [De Fries et al., 2000]. We entered the natural log-transformed variables of tree and bush cover into a stepwise regression model with natural log-transformed minimum group size as the dependent variable. The resulting equation identified only bush cover as a predictor, but was not significant: ln(Nmin) = –0.096 + 0.889ⴢln(B) (adjusted r2 = 0.141, F1, 17 = 3.945, p = 0.063).

We used body mass as a proxy for prey vulnerability. Figure 7a and b shows the relationships between minimum group size and female and male body mass. Minimum group size decreases with increasing female body mass, with the data best de-

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Minimum baboon group size (n)

80

60

40

20

0 0

0.1

0.2

0.3

0.4

Predator density (n/km2)

ln (minimum baboon group size)

Fig. 5. Minimum observed baboon group sizes against calculated total predator density.

5 4 3 2 1 2.5

3.0

3.5

4.0

4.5

ln (percentage bush cover)

Fig. 6. Minimum baboon group size against bush cover.

scribed by a logarithmic relationship. The relationship between minimum group size and male body mass is best described by a quadratic relationship, with group size initially decreasing as body mass increases, before increasing again. Only the relationship between female body mass and minimum group size is statistically significant: ln(Nmin) = 6.374 – 0.264ⴢFbm (r2 = 0.407, F1, 14 = 9.60, p = 0.008).

As female body mass was not available for all of the 36 sites where minimum baboon group size was available, we used stepwise multiple regression to find the equation that explains the greatest amount of variance in female body mass with the

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Minimum group size (n)

80 60 40 20 0 10

Minimum group size (n)

a

12

14

16

Female body mass (kg)

60

40

20

0 15

b

20

25

30

35

Male body mass (kg)

Fig. 7. a Minimum baboon group sizes against female body mass. b Minimum baboon group

sizes against male body mass.

various climatic variables as predictors, and used this equation to estimate female body mass at those sites where actual data were unavailable. Female body mass is best predicted by rainfall and temperature: Fbm = 9.670 + 0.202ⴢTmoSD2 + 0.003ⴢPann (r2 = 0.46, F2, 15 = 8.188, p = 0.004)

where Fbm = female body mass in kilograms; TmoSD = temperature variation between months; Pann = mean annual rainfall in millimetres. The preceding analyses have explored the relationships between minimum group size in baboons and a number of factors thought to influence predation risk. Of the factors considered, the only statistically significant ones are female body mass and predator density.

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Color version available online

Minimum group size (n)

60 50 40 30 20 10 0.30

0.25 Pred 0.20 0.15 a to r dens 0.10 it y (n /km 2 0.05 )

14

0

10

15

16

13 12 ss (kg) ody ma b le a m Fe

11

Fig. 8. Minimum baboon group size against female body mass (kg) and predator density/km2.

Predicting Minimum Group Size in Baboons Using the preceding equation, we calculated female body mass for all remaining sites and then entered these values, along with predator density, into a regression to obtain the best-fit equation for predicting minimum group size. Figure 8 shows minimum group size plotted against the female body mass and predator density, with the equation plane fitted. The best-fit equation is: ln(Nmin) = 5.899 – 0.260 ⴢFbm + 2.779ⴢpredator density (r2 = 0.429, F = 12.643, p ! 0.001).

We tested the validity of this equation by using it to predict minimum group sizes for baboon study populations from which time budget data have previously been recorded (table 3). Figure 9 shows that all of the observed baboon study groups fall above the predicted minimum group size for their location, and that predicted minimum group size increases with observed study group size. Discussion

We show that minimum group size in baboons is strongly related to both predator density and female body mass, and add support to the link between predation risk and group size in primates. It has repeatedly been suggested that large group size and increased cohesion are a response to predation [Gautier-Hion et al., 1983; Stacey, 1986; Dunbar, 1988; Janson and Goldsmith, 1995; Lima, 1995; Hill and Dunbar, 1998] and are thought to benefit individuals through either a dilution effect [Hamilton, 1971; Lima and Zollner, 1996; Gillespie and Chapman, 2001], collective vigilance leading to the increased chance of predator detection (’many eyes’ hypothesis [Struhsaker, 1981; Lima, 1995]), or the deterrence of predators by collective mobbing

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Group size of baboons in time budget studies (n)

120 100 80 60 40 20 0 0

10

20

30

40

50

Predicted minimum group size (n)

Fig. 9. Observed baboon group sizes against those predicted by the model. Observed group

sizes taken from time budget studies, given in table 3.

or active defence [Stanford, 1998]. The effectiveness of increased group size in reducing predation risk may also depend on the hunting technique of predator species [Shultz et al., 2004]. For example, in ungulates hunted by cheetahs and lions, attack probability decreases with increasing herd size [Van Orsdol, 1984; Fitzgibbon and Lazarus, 1995]. However, a study of the hunting behaviour of African wild dogs found that large herds of wildebeest and impala are both more likely to be encountered than small herds, and are more likely to be attacked once encountered [Creel and Creel, 2002]. The negative relationship between female body mass and minimum group size revealed by our analyses shows that populations inhabiting areas with higher predation risk are smaller-bodied. This may reflect the fact that in areas of high predation risk, females stop investing in growth and begin reproduction earlier. While we could argue that smaller body size drives the need for the baboons to form larger groups to reduce predation risk, the variation in body mass at the scale shown by baboons is perhaps unlikely to make a difference to large, cooperative hunters such as lions; the range of body masses encompassed by the baboon populations would arguably constitute small prey to such predators. Instead, the relationship between female body mass and minimum group size may reflect the classic trade-off between growth and reproduction in high-risk environments [Bettridge et al., 2010]. Our equation for predicting female body weight is similar to one earlier published by Dunbar [1990]. Both equations use rainfall and temperature as the key predictor variables. However, whereas the equation in Dunbar [1990] revealed a quadratic relationship with rainfall and used the temperature measurement of mean annual temperature, our analyses revealed a strong linear relationship with rainfall and a stronger effect of temperature variation (a variable not included in Dunbar’s analysis). We also used a slightly larger data set than the earlier study (22 populations instead of 19), but the main difference in our results may be due to the climate data

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provided by the Wilmott and Matsuura [2001] database. In reference to adult body mass, it is possible that using long-term climate data such as this may better reflect the ecological effects on body weight. Although baboons, like any animal, will be subject to short-term variations in weight due to the current availability of food, the size of an adult baboon will not have been solely determined by the ecological conditions in the year it was studied, but is more likely to be a long-term effect of the environmental conditions it experienced many years before, during its infancy and juvenile years. In contrast to our expectations, we were unable to find a significant relationship between forest cover and minimum group size. Previous studies [Dunbar, 1996; Cowlishaw, 1997b] have suggested that density of vegetation should influence predation risk in two possible ways. Firstly, trees provide refuges for primates to escape predators, so predation risk (and hence minimum group size) should decrease with increasing tree density. However, as vegetation (particularly low-level bush cover) becomes denser, it becomes easier for an ambush predator such as a leopard to surprise its prey, and predation risk will increase as bush level cover increases. Leopards may prefer to hunt in areas of intermediate vegetation density [Balme et al., 2007]. It has also been argued that animals might employ the contrasting strategy of reducing group cohesion; with groups dispersing into smaller parties in low-visibility environments such as dense forests, and thereby reducing the risk of detection by predators [Dunbar, 1988; Boesch and Boesch, 1989; Stanford, 1995; Treves, 1999]. If both factors operate, the relationship between minimum baboon group size and forest cover may be more complex than our linear analysis could reveal. An alternative possibility is that there was insufficient variance in forest cover in the study sites in our data set. Because observation conditions tend to be difficult and animals habituate less readily in forested habitats, baboons have only very rarely been studied in habitats where forest cover is high. It is also possible that the measure of satellite forest cover used does not provide fine enough detail to identify any relationship. A recent study on predation risk in golden-headed lion tamarins (Leontopithecus chrysomelas) suggests that predation risk differs between forest types – a finding the authors relate to canopy density [Oliveira and Dietz, 2011]. Although the approach used by Dunbar [1996] of calculating tree and bush cover from climatic variables may provide a more accurate small-scale indication of vegetation cover, the level of tree cover predicted by his equations are unlikely to provide an accurate estimation of tree cover across different habitat types [Bettridge, 2010]. The equations produced in this paper, based on fairly simple, easy to come by ecological variables, go some way to providing estimates of the densities of leopard and lion and may prove helpful for researchers. Our attempt to estimate lion density based on biotic factors is similar to that of Celesia et al. [2010], and our findings reflect the results of their analyses. Both studies identify temperature as a key variable in predicting lion density. The slight difference in the temperature measure used (mean monthly vs. mean annual temperature) and the relationship (quadratic in this study vs. linear negative in Celesia et al. [2010]) is probably at least partly due to the use of slightly different data sets. The importance of rainfall and its interaction with soil quality or type (reflected in our study by the use of monthly minimum MI) is also identified by both studies. In terms of assessing predation risk, our analyses suggest that predator density is a key predictor of minimum group size. However, our data also indicate that where

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predator densities are not available, using measures such as the number of predator species present offers a reliable, if crude, index of the predation risk that a species faces. Given these considerations, it seems that predator-prey relationships need to be studied more effectively from the perspective of the predator. By gaining an idea of how often a predator attacks a particular group, in relation to how often it attacks other groups of the same species, it might be possible to add something to our understanding of an individual’s predation risk in relation to overall predator density at a site. In summary, this paper has shown that minimum group size in baboons can be related to predator density and female body mass. Both of these elements can, in turn, be estimated from environmental variables. These findings offer support for the argument that group living in primates is a response to predation risk, and highlight the value of a modelling approach to investigating carnivore and primate ecology. Acknowledgments We thank Guy Cowlishaw, Susanne Shultz and two anonymous reviewers for their helpful comments on earlier versions of this paper. This research was conducted whilst C.B. was funded by the British Academy Lucy to Language Project.

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Folia Primatol 2012;83:332–352

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