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Foraging in captive hamadryas baboons: implications for enrichment
Applied Animal Behaviour Science 88 (2004) 101–110
Foraging in captive hamadryas baboons: implications for enrichment Megan Jones, Neville Pillay∗ Ecophysiology Studies Research Group, School of Animal, Plant, and Environmental Sciences, University of the Witwatersrand, Private Bag 3, WITS 2050, Johannesburg, South Africa Received 2 September 2003; received in revised form 18 February 2004; accepted 5 March 2004
Abstract Many animals will work for food even if food is freely available or the animal is satiated, suggesting that foraging behaviour is inherently rewarding and that there is a behavioural need to forage. We investigated whether members of a hamadryas baboon (Papio hamadryas hamadryas) troop at the Johannesburg Zoo, South Africa would forage in non-provisioned areas of their enclosure when excluded from a high quality, clumped, monopolisable food source by another member of the troop. We studied foraging behaviour during two baseline treatments when enclosures were not altered, and during four experimental treatments in which we introduced either an empty small box (SBE), a small box containing food (SBF), an empty big box (BBE), or a big box containing food (BBF). We also recorded aggressive interactions during all treatments. During the SBF treatment, individuals excluded from the device by the dominant male increased foraging elsewhere, without any concomitant increase in aggressive behaviour compared with baseline values. In contrast, foraging rates at the device increased during the BBF treatment, as did incidences of aggression. We suggest that the redirected foraging behaviour provided by the SBF treatment could be exploited as a form of environmental enrichment. © 2004 Elsevier B.V. All rights reserved. Keywords: Hamadryas baboons; Foraging; Behavioural contagion; Secondary reward systems; Environmental enrichment
1. Introduction Foraging is an elaborate, multi-stage behaviour comprising appetitive (goal-seeking) and consummatory (goal-satisfying) phases. Appetitive components include locating, selecting, gathering or capturing, and processing food items, whereas food ingestion is consummatory behaviour (Lindburg, 1998). Because the many stages of foraging are internally regulated ∗
Corresponding author. Tel.: +27-11-717-6459; fax: +27-11-403-1429. E-mail address: [email protected] (N. Pillay). 0168-1591/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2004.03.002
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by both physiological and psychological consequences, an animal’s behavioural need to forage will decrease only if the animal performs and experiences the consequences of both appetitive and consummatory components of feeding. Captive rats and pigeons choose to work for food by pressing a lever or pecking a disk, respectively, even if the same food is freely available (Neuringer, 1969). In pigs, which usually root and feed concurrently, freely available food does not curtail the occurrence of rooting which has a separate motivational system and rewarding properties independent of the availability of food (Nicol, 1995). Social foragers may coincidently or deliberately provide conspecifics with information about food resources, so enhancing the foraging efficiency of group members by indicating when and where to eat, suggesting which available foods are suitable for consumption, and demonstrating appropriate techniques to process these foods (Laland and Plotkin, 1990; Galef and Giraldeau, 2001). This increased efficacy in foraging is considered one of the main benefits of group living (Dunbar, 1988; Coussi-Korbel and Fragaszy, 1995; Gillespie and Chapman, 2001). In contrast, within-group feeding competition is a cost of sociality (Pruetz and Isbell, 2000; Gillespie and Chapman, 2001). Conspecifics can influence the behaviour of group members in a number of ways (Laland and Plotkin, 1990; Nicol, 1995). One mechanism is behavioural contagion whereby a demonstrator’s behaviour increases the frequency or intensity of the same behaviour in the observer (Galef, 1998; Nicol, 1995). An increase in group foraging levels in response to individuals watching a demonstrator forage have been observed in a diverse range of species including red-winged blackbirds (Agelaius phoenicius), turtles (Peromyscus maniculatus), chickens, pigs, cattle, and ponies (Forkman, 1991; Nicol, 1995). An individual’s physiological and psychological states may also motivate foraging, as well as reinforce these feeding behaviours (Spruijt et al., 2001). Activities with distant survival and reproductive value, and for which the fitness consequences are not necessarily immediately experienced, appear to be guided by hedonic reinforcement, creating the rule: “conditions that are momentarily pleasurable enhance long-term fitness”. This proximate internal reinforcer, or secondary reward, is produced by the concerted action of the opioid and dopaminergic systems in the limbic and frontal areas of the brain (Everitt et al., 2001; Spruijt et al., 2001). When an animal is unable to perform both appetitive and consummatory components of complex natural behaviours such as foraging, its physiological and psychological welfare, defined as the balance between positive and negative affects and experiences (Spruijt et al., 2001), may suffer (Hughes and Duncan, 1988). A prime example is the restriction of a captive animal’s appetitive foraging opportunities because of being fed an easily consumed commercial diet provided in predictable spatial and temporal locations. The field of environmental enrichment addresses, among other things, the above-mentioned concerns about the welfare of captive animals, and has instituted a system in which interventions necessary for physiological and psychological well-being can be objectively designed, implemented, and assessed (Dawkins, 1983; Maple, 1998; Shepherdson, 1998). Although many attempts have been made to enhance captive well-being through simulating natural conditions, and thereby encouraging behaviours which are shaped over evolutionarily time (Poole, 1998), thus far the most successful environmental enrichment protocols are those which specifically promote foraging and grooming (Crocket, 1998); these behaviours which trigger the opioid and dopamine systems in the brain, and have internal motivation and
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reinforcement (Spruijt et al., 2001). Foraging enrichment, however, can increase aggression among group members competing for a food resource (Lutz and Novak, 1995). In an earlier study on feeding enrichment in hamadryas baboons (Papio hamadryas hamadryas) at the Johannesburg Zoo, South Africa, anecdotal observations suggested that when baboons were denied access to a foraging device containing novel but limited food items, foraging activity increased in non-provisioned areas of the enclosure (Saacks and Jones, unpublished data). Similar qualitative findings were reported by Shepherdson et al. (1989) who provided a group of meerkats (Suricata suricatta) with a mealworm dispenser, and observed an increase in their digging behaviour throughout the enclosure. In this study, we tested whether a foraging hamadryas baboon cues other group members to increase foraging activity in non-provisioned areas of the enclosure (hereafter referred to as foraging elsewhere). We predicted that (1) a monopolisable, high quality food resource would increase levels of foraging elsewhere, and would also result in increased aggression because of intra-troop competition for the food; and (2) a relatively less clumped, and non-monopolisable high quality food source would not increase aggressive behaviours, nor increase foraging elsewhere, although it is known to increase foraging at the provisioned source (Smith and Mills, 1996; Saacks and Jones, unpublished data).
2. Materials and methods 2.1. Subjects A seven-member hamadryas baboon troop, housed at the Johannesburg Zoo, South Africa served as subjects for this study. All individuals were related, except the founding pair of the ␣-male (13 years) and an old female (12 years). One castrated male (7 years) was the offspring of this pair. The ␣-female (8 years) and a younger castrated male (6 years) were both sired by the ␣-male, by dams no longer members of the group. A subadult female (3 years), and a juvenile female (1 year) were the progeny of the ␣-male and ␣-female. The troop was housed in an open-roofed, concrete, enclosure measuring approximately 230 m2 . The enclosure contained a central, 6 m high fibreglass rock-like formation as well as a number of logs/branches placed in either fixed or movable positions. The troop’s night room, 1.8 m × 4.6 m × 2.2 m, opened directly into the open-roofed enclosure. The troop could freely access their night room except during cleaning times, and when behavioural recordings were made. The baboons were confined to their night room between 7:00 and 10:00 h, during which time the outdoor enclosure was cleaned and, if necessary, experimental apparatus introduced. Despite the cleaning, fallen leaves and/or small, discarded food parts from the previous day could usually be found in the enclosure. However, the baboons only rarely searched for or consumed these items. The troop was fed a morning meal of fruit and vegetables whilst confined to their night room. Other foods such as sunflower seeds, horse cubes and peanuts were provided as part of standard enrichment protocols; these protocols were continued for the duration of this project during non-observational times. Water was available ad libitum in shallow depressions in and around the fibreglass rock formation.
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2.2. Procedure and apparatus This study was conducted in a sequentially ordered format, comprising baseline treatment (n = 3 days), experimental treatment (n = 24 days), and post experimental baseline treatment (n = 5 days). For the experimental phases, each of the following four treatments (n = 6 days per treatment) was introduced in random order: • Big box food (BBF)—a 90 cm × 90 cm × 25 cm open-topped wooden box, with a fine weld mesh base (for drainage), was attached to the concrete floor of the enclosure by a central rawl bolt through its base. The box was filled with a mixture of wood chips and straw to a depth of about 15 cm, into which substrate 250 g raw peanuts and 125 g finer sprinkle nuts were scattered. All seven animals were able to access the box. • Big box empty (BBE)—the big box, as described above, was placed into the enclosure but without any peanuts. • Small box food (SBF)—one 30 cm × 30 cm × 30 cm closed wooden box mounted on a 50 cm × 30 cm base was attached to the floor of the concrete enclosure by two rawl bolts screwed through 9 mm diameter holes on either side of the base. A 10 cm diameter opening on the upper surface of the box provided access to the interior of the box, which contained a 20 cm diameter plastic ball. An additional wooden base, into which 24 equally spaced 3 cm diameter and 1.5 cm deep cylindrical depressions had been drilled, was fitted to the inside lower surface of the box. Only one animal could access the interior of the box at any given time. The box was filled with 250 g raw peanuts that could only be procured by a baboon manoeuvring the ball and retrieving the food items from the depressions into which the peanuts had settled. • Small box empty (SBE)—the small box, as described above, was placed in the enclosure, but without being baited with peanuts. Peanuts were used because they were prized food items for the hamadryas baboons, and were readily monopolisable by the ␣-male (Jones, personal observations). In addition, the small size of the nuts, especially when presented as sprinkle nuts, increased the searching and processing time, and hiding the peanuts in wood chips/straw, or within a difficult-to-access box, decreased the baboons’ foraging efficiency, ensuring that the peanuts were not completely consumed before the end of the observation session. 2.3. Data collection and analysis Data were collected between March and August 2002. Observations were made for a 30 min period immediately after the baboons were released from their night room (approximately 10:00 h). The number of individuals foraging at the device, the number of individuals foraging elsewhere in the enclosure, and the total number of individuals observed were recorded using instantaneous sampling with a 15 s inter-scan interval. In addition, the frequency of overt aggression was recorded using continuous sampling. Foraging was defined as any one of the following: actively searching for, harvesting, processing (peeling, stripping outer covering), and consuming food. Overt aggression was defined as a physical interaction in which one animal bites, grapples with, or chases another (Gil-Burmann et al.,
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1998). Each complete interaction, rather than each behavioural component, was scored as an aggressive bout. Data from daily foraging observations were converted to a group foraging ratio of number foraging elsewhere (total number observed − number foraging at the box) + 0.1 (0.1 was added to prevent division by zero). The median ratio, as well as the first and third interquartiles, was calculated for each day’s observations. Nonparametric tests with two-tailed significance levels were used throughout to compare data among experimental treatments. Data collected during baseline observation were not included in the statistical analyses because no device was present. Results were considered significant if P < 0.05. A Friedman analysis of variance was used to compare median ratio scores, first and third interquartile scores, the number of animals foraging at the device, and frequency of overt aggression across the four experimental treatments, and Dunn’s multiple comparisons post-hoc tests were employed to determine specific differences. The relationship between the frequency of aggression and the number of individuals foraging at the treatment apparatus was analysed using Spearman’s rank correlation. 3. Results 3.1. Foraging
0.25 0.2 0.15 0.1 0.05
SBF
SBE
BBF
BBE
PE baseline
0 baseline
foraging elsewhere ratio
Foraging elsewhere (Fig. 1) varied significantly among experimental treatments for the median (Fr = 13.909, P = 0.0030; Friedman ANOVA) and third quartile values (Fr =
treatment Fig. 1. Median foraging elsewhere during the two baseline treatments and four experimental treatments. Error bars denote first and third quartiles. Only values above zero are shown. Baseline data are provided for comparison, and were not included in the statistical analyses. PE baseline: post-experimental baseline; BBE: big box empty; BBF: big box food; SBE: small box empty; SBF: small box food.
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15.273, P = 0.0016), but not for the first quartiles (Fr = 3.667, P = 0.2998). Dunn’s multiple comparisons post-hoc tests conducted on the median foraging elsewhere ratios did not reveal differences among treatments, possibly because the many zero values in the data sets decreased the power of the tests. However, post-hoc tests applied to data from the third quartile showed significant differences between the BBE and SBF treatments (P < 0.05), and the BBF and SBF treatments (P < 0.01). For the BBE and SBE treatments, foraging elsewhere was comparable to the low values recorded during the baseline and post-experimental baseline study, although this was not analysed statistically. Very few individuals foraged at the box (BBE: 0, 0, 0 (median, first quartile, third quartile); SBE: 0, 0, 0). For the BBF treatment, foraging elsewhere was comparable to the baseline, but the number of animals foraging at the box was greater compared with other experimental treatments (6, 5.25, 6). During the SBF treatment only one animal at a time (almost exclusively the ␣-male) was able to access the device (1, 1, 1). However, animals excluded from the small box increased their foraging efforts in non-provisioned areas of the enclosure. The redirected foraging behaviours were predominantly appetitive, although animals occasionally found and consumed fallen leaves or remnants from the previous day’s enrichment scatter feed. 3.2. Aggression
20 15 10 5 SBF
SBE
BBF
BBE
PE baseline
0 baseline
aggression frequency
The frequency of aggressive encounters varied significantly among treatments (Fr = 13.655, P = 0.0034). Aggression was highest during the BBF treatment, and lower for the other three experimental treatments, although these differences in aggression were only significant between BBF and SBE (Dunn’s post-hoc test; Fig. 2). Aggression was lower during the two baseline treatments than for any of the experimental treatments, but this was not compared statistically. The median number of individuals at the device varied significantly among treatments (Fr = 15.000; P = 0.0018). More animals foraged at the device during the BBF treatments (6) than during the SBF treatment (1), and the BBE and SBE treatments (0). Aggression
treatment Fig. 2. Median aggression (number of aggressive interactions per 30 min) in the two baseline treatments and four experimental treatments. Error bars denote first and third quartiles. Only values above zero are shown. Baseline data are provided for comparison, and were not included in the statistical analyses. PE baseline: post-experimental baseline; BBE: big box empty; BBF: big box food; SBE: small box empty; SBF: small box food.
aggression frequency
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25 20 15 10 5 0 0
1
2
3
4
5
6
7
median number of animals at device
Fig. 3. The relationship between aggression frequency (number of aggressive incidents per 30 min) and median number of individuals at BBE, BBF, SBE, or SBF (n = 24).
frequency during all four treatments was strongly correlated with the number of individuals at the device (Spearman r = 0.7847, P < 0.0001, r 2 = 0.6392; Fig. 3).
4. Discussion Group foraging levels in non-provisioned areas of the enclosure were significantly higher than baseline levels when one of the seven hamadryas troop members, usually the ␣-male, fed from a monopolisable foraging device (SBF). Group foraging levels did not differ from baseline values for the other experimental treatments, both when no food was present (SBE, BBE), and when the food source was not monopolisable (BBF). Foraging elsewhere values were similar during the SBE and BBE treatments, as well as baseline treatments, indicating that the changes in foraging frequency were a reaction to the availability and distribution of food, and not to the devices themselves. For the BBF treatment, there was little foraging elsewhere as feeding at the device precluded simultaneous foraging in non-provisioned areas of the enclosure. Overt aggression was virtually absent during baseline and experimental treatments, except during the experimental BBF treatment, in which aggression levels were significantly higher than during other treatments. The frequency of aggressive attacks was related to the number of animals at the feeding site, and not contingent only on the availability of food. Aggression bouts typically began among the ␣-female, juvenile female, and castrated males, with one or more animals crouching and screaming, occasionally grappling with one another, and then fleeing. The ␣-male intervened in about 50% of these instances, biting one or more of the troop members and chasing them away from the feeding site. No animals appeared to be injured during these encounters. Free-ranging hamadryas baboons, like most primates, spend at least 60% of their waking hours foraging (Kummer, 1971; Lutz and Novak, 1995). As the foods consumed in nature are in low abundance and scattered, appetitive activities take up a large proportion of total foraging time: there is movement from one feeding site to another, seeds are taken from their pods, tubers uprooted, and rocks overturned to find insects and small vertebrates (Kummer, 1971). This contrasts with the very low rates of foraging observed for primates in captivity (Chamove and Anderson, 1989; Molzen and French, 1989; Saacks and Jones, unpublished data; data collected during baseline treatment in this study).
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The results from this study confirm the prediction that introducing a non-monopolisable food source (BBF) increases foraging levels within the group, but the apparent enrichment benefits derived were offset by an increase in overt aggression. However, we found that when a monopolisable food was provided which only the ␣-male could access (SBF), group members that were excluded from the food source increased their foraging behaviours elsewhere in the enclosure, without a concomitant increase in aggression. Whereas previous studies of provisioned primate and other mammal groups have shown that rates of aggression increased dramatically when food resources are highly clumped (Dunbar, 1988), our results suggest that this is not necessarily the case. Indeed, overt aggression may be avoided when a dominant individual is able to monopolise a food source using indirect (ritualised) aggressive behaviour (e.g., brow-raising, ground beating, staring, advancing towards troop members), while subordinates are able to withdraw to other areas of the enclosure. This creates an advantageous social tactic in competitive foraging situations (Held et al., 2000). Hence, overt aggression need not necessarily ensue from a clumped resource, and can even be forestalled if indirect aggression by one (dominant) animal precludes the grouping of other individuals near a clumped resource. Crowding of animals, rather than the scarcity of the clumped food, appears to produce aggression (Barton et al., 1996). This study shows that appetitive foraging behaviours can be encouraged independently of consummatory behaviours, and suggests an alternative to standard foraging enrichment protocols in which the focus is on promoting appetitive behaviours through slowing down the consummatory process, by rather encouraging solely appetitive behaviours. Indirectly promoting appetitive foraging behaviours may be of particular value for animals on restricted energy diets. Moreover, even if one individual monopolises an enrichment device intended to enrich the entire group, this does not inevitably result in other group members not benefiting from the introduced device. However, we admit this applies largely to social species which forage as a group. Behavioural contagion of foraging, brought about by observing the ␣-male exploiting the food device in the SBF treatment, appeared to cue group members to begin foraging in non-provisioned parts of the enclosure. The importance an animal attributes to seeing a conspecific forage, and whether it acts on this information, depends on two factors (Nicol and Pope, 1994; Coussi-Korbel and Fragaszy, 1995). (1) Demonstrator identity influences social learning, possibly because observers learn that certain animals are better predictors of food rewards than others (Nicol and Pope, 1999). Further studies are required to test whether individual characteristics of an animal exploiting a device influence the behavioural contagion of foraging. (2) The animal’s level of hunger may determine the importance attributed to the cues received from a foraging demonstrator. We predict that this potential method of enrichment would be most effective if implemented when the animals are relatively hungry, as would occur a few hours before a standard meal time. Increased foraging elsewhere can thus be considered environmental enrichment, as appetitive behaviours appear to be proximally rewarded and regulated by internal reinforcing systems. This secondary reward system could select for animals performing appetitive behaviours, deriving rewards even when there is no physiological need for an ultimate goal to be satisfied. If an animal’s welfare is regarded as good when positive affective states, such as pleasure, predominate over negative affective states, such as stress (Spruijt et al., 2001), environmental enrichment should also aim to activate the secondary reward systems which
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are the neural substrate for positive affect. In addition to enhancing the welfare of a captive animal by altering its external environment, interventions aimed primarily at manipulating the internal environment of an animal, or mental state, can likewise be seen as enriching. For captive hamadryas baboons, this welfare goal may well be realised by harnessing their natural biology, specifically that of foraging style and social structures, to create opportunities for behavioural contagion of foraging and redirected appetitive foraging behaviours.
Acknowledgements Thanks to the staff members of the Johannesburg Zoo who enabled us to conduct this study—Philip Cronje (Curator Alpha Section), Armstrong Mdoda (Keeper Alpha Section), Lukas Mogajane (Animal Attendant Alpha Section), Ekson Mohlala (Animal Attendant Alpha Section), and Mathew van Lierop (Enrichment Coordinator). MJ thanks the National Research Foundation for postgraduate support.
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Laland, K.N., Plotkin, H.C., 1990. Social learning and social transmission of foraging information in Norway rats (Rattus norvegicus). Anim. Learn. Behav. 18, 246–251. Lindburg, D.G., 1998. Enrichment of captive mammals through provisioning. In: Shepherdson, D.J., Mellen, J.D., Hutchins, M. (Eds.), Second Nature: Environmental Enrichment for Captive Animals. Smithsonian Institution Press, Washington, pp. 262–276. Lutz, C.K., Novak, M.A., 1995. Use of foraging racks and shavings as enrichment tools for groups of rhesus monkeys (Macaca mulatta). Zoo Biol. 14, 463–474. Maple, T.L, 1998. Foreword. In: Shepherdson, D.J., Mellen, J.D., Hutchins, M. (Eds.), Second Nature: Environmental Enrichment for Captive Animals. Smithsonian Institution Press, Washington, pp. xii–xiv. Molzen, E.M., French, J.A., 1989. The problem of foraging in captive callitrichid primates: behavioural time budgets & foraging skills. In: Segal, E.F. (Ed.), Housing, Care and Psychological Wellbeing of Captive Primates. Noyes Publications, New Jersey, pp. 89–101. Neuringer, A.J., 1969. Animals respond for food in the presence of free food. Science 166, 399–401. Nicol, C.J., 1995. The social transmission of information and behaviour. Appl. Anim. Behav. Sci. 44, 79–98. Nicol, C.J., Pope, S.J., 1994. Social learning in small flocks of laying hens. Anim. Behav. 47, 1289–1296. Nicol, C.J., Pope, S.J., 1999. The effects of demonstrator social status and prior foraging success on social learning in laying hens. Anim. Behav. 57, 163–171. Poole, T.B., 1998. Meeting a mammal’s psychological needs: basic principles. In: Shepherdson, D.J., Mellen, J.D., Hutchins, M. (Eds.), Second Nature: Environmental Enrichment for Captive Animals. Smithsonian Institution Press, Washington, pp. 83–96. Pruetz, J.D., Isbell, L.A., 2000. Correlations of food distribution and patch size with agonistic interactions in female vervets (Chlorocebus aethiops) and patas monkeys (Erythrocebus patas) living in simple habitats. Behav. Ecol. Sociobiol. 49, 38–47. Shepherdson, D.J., Brownback, T., James, A., 1989. A mealworm dispenser for the slender-tailed meerkat (Suricata suricatta) at London Zoo. Int. Zoo. Yearbook 28, 268–271. Shepherdson, D.J., 1998. Introduction: tracing the path of environmental enrichment in zoos. In: Shepherdson, D.J., Mellen, J.D., Hutchins, M. (Eds.), Second Nature: Environmental Enrichment for Captive Animals. Smithsonian Institution Press, Washington, pp. 1–14. Smith, L.A., Mills, D.S., 1996. Evaluation of the provision of a forage box to increase the normal behaviour shown by captive Papio hamadryas baboons within the optimal exhibit area of their enclosure. In: Proceedings of the 30th International Congress of the International Society for Applied Ethology, Guelph, Ont., Canada, 14–17 August 1996. Spruijt, B.M., van den Bos, R., Pijlman, F.T.A., 2001. A concept of welfare based on reward evaluation mechanisms in the brain: anticipatory behaviour as an indicator of the state of reward systems. Appl. Anim. Behav. Sci. 72, 145–171.
Foraging in captive hamadryas baboons: implications for enrichment Megan Jones, Neville Pillay∗ Ecophysiology Studies Research Group, School of Animal, Plant, and Environmental Sciences, University of the Witwatersrand, Private Bag 3, WITS 2050, Johannesburg, South Africa Received 2 September 2003; received in revised form 18 February 2004; accepted 5 March 2004
Abstract Many animals will work for food even if food is freely available or the animal is satiated, suggesting that foraging behaviour is inherently rewarding and that there is a behavioural need to forage. We investigated whether members of a hamadryas baboon (Papio hamadryas hamadryas) troop at the Johannesburg Zoo, South Africa would forage in non-provisioned areas of their enclosure when excluded from a high quality, clumped, monopolisable food source by another member of the troop. We studied foraging behaviour during two baseline treatments when enclosures were not altered, and during four experimental treatments in which we introduced either an empty small box (SBE), a small box containing food (SBF), an empty big box (BBE), or a big box containing food (BBF). We also recorded aggressive interactions during all treatments. During the SBF treatment, individuals excluded from the device by the dominant male increased foraging elsewhere, without any concomitant increase in aggressive behaviour compared with baseline values. In contrast, foraging rates at the device increased during the BBF treatment, as did incidences of aggression. We suggest that the redirected foraging behaviour provided by the SBF treatment could be exploited as a form of environmental enrichment. © 2004 Elsevier B.V. All rights reserved. Keywords: Hamadryas baboons; Foraging; Behavioural contagion; Secondary reward systems; Environmental enrichment
1. Introduction Foraging is an elaborate, multi-stage behaviour comprising appetitive (goal-seeking) and consummatory (goal-satisfying) phases. Appetitive components include locating, selecting, gathering or capturing, and processing food items, whereas food ingestion is consummatory behaviour (Lindburg, 1998). Because the many stages of foraging are internally regulated ∗
Corresponding author. Tel.: +27-11-717-6459; fax: +27-11-403-1429. E-mail address: [email protected] (N. Pillay). 0168-1591/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2004.03.002
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by both physiological and psychological consequences, an animal’s behavioural need to forage will decrease only if the animal performs and experiences the consequences of both appetitive and consummatory components of feeding. Captive rats and pigeons choose to work for food by pressing a lever or pecking a disk, respectively, even if the same food is freely available (Neuringer, 1969). In pigs, which usually root and feed concurrently, freely available food does not curtail the occurrence of rooting which has a separate motivational system and rewarding properties independent of the availability of food (Nicol, 1995). Social foragers may coincidently or deliberately provide conspecifics with information about food resources, so enhancing the foraging efficiency of group members by indicating when and where to eat, suggesting which available foods are suitable for consumption, and demonstrating appropriate techniques to process these foods (Laland and Plotkin, 1990; Galef and Giraldeau, 2001). This increased efficacy in foraging is considered one of the main benefits of group living (Dunbar, 1988; Coussi-Korbel and Fragaszy, 1995; Gillespie and Chapman, 2001). In contrast, within-group feeding competition is a cost of sociality (Pruetz and Isbell, 2000; Gillespie and Chapman, 2001). Conspecifics can influence the behaviour of group members in a number of ways (Laland and Plotkin, 1990; Nicol, 1995). One mechanism is behavioural contagion whereby a demonstrator’s behaviour increases the frequency or intensity of the same behaviour in the observer (Galef, 1998; Nicol, 1995). An increase in group foraging levels in response to individuals watching a demonstrator forage have been observed in a diverse range of species including red-winged blackbirds (Agelaius phoenicius), turtles (Peromyscus maniculatus), chickens, pigs, cattle, and ponies (Forkman, 1991; Nicol, 1995). An individual’s physiological and psychological states may also motivate foraging, as well as reinforce these feeding behaviours (Spruijt et al., 2001). Activities with distant survival and reproductive value, and for which the fitness consequences are not necessarily immediately experienced, appear to be guided by hedonic reinforcement, creating the rule: “conditions that are momentarily pleasurable enhance long-term fitness”. This proximate internal reinforcer, or secondary reward, is produced by the concerted action of the opioid and dopaminergic systems in the limbic and frontal areas of the brain (Everitt et al., 2001; Spruijt et al., 2001). When an animal is unable to perform both appetitive and consummatory components of complex natural behaviours such as foraging, its physiological and psychological welfare, defined as the balance between positive and negative affects and experiences (Spruijt et al., 2001), may suffer (Hughes and Duncan, 1988). A prime example is the restriction of a captive animal’s appetitive foraging opportunities because of being fed an easily consumed commercial diet provided in predictable spatial and temporal locations. The field of environmental enrichment addresses, among other things, the above-mentioned concerns about the welfare of captive animals, and has instituted a system in which interventions necessary for physiological and psychological well-being can be objectively designed, implemented, and assessed (Dawkins, 1983; Maple, 1998; Shepherdson, 1998). Although many attempts have been made to enhance captive well-being through simulating natural conditions, and thereby encouraging behaviours which are shaped over evolutionarily time (Poole, 1998), thus far the most successful environmental enrichment protocols are those which specifically promote foraging and grooming (Crocket, 1998); these behaviours which trigger the opioid and dopamine systems in the brain, and have internal motivation and
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reinforcement (Spruijt et al., 2001). Foraging enrichment, however, can increase aggression among group members competing for a food resource (Lutz and Novak, 1995). In an earlier study on feeding enrichment in hamadryas baboons (Papio hamadryas hamadryas) at the Johannesburg Zoo, South Africa, anecdotal observations suggested that when baboons were denied access to a foraging device containing novel but limited food items, foraging activity increased in non-provisioned areas of the enclosure (Saacks and Jones, unpublished data). Similar qualitative findings were reported by Shepherdson et al. (1989) who provided a group of meerkats (Suricata suricatta) with a mealworm dispenser, and observed an increase in their digging behaviour throughout the enclosure. In this study, we tested whether a foraging hamadryas baboon cues other group members to increase foraging activity in non-provisioned areas of the enclosure (hereafter referred to as foraging elsewhere). We predicted that (1) a monopolisable, high quality food resource would increase levels of foraging elsewhere, and would also result in increased aggression because of intra-troop competition for the food; and (2) a relatively less clumped, and non-monopolisable high quality food source would not increase aggressive behaviours, nor increase foraging elsewhere, although it is known to increase foraging at the provisioned source (Smith and Mills, 1996; Saacks and Jones, unpublished data).
2. Materials and methods 2.1. Subjects A seven-member hamadryas baboon troop, housed at the Johannesburg Zoo, South Africa served as subjects for this study. All individuals were related, except the founding pair of the ␣-male (13 years) and an old female (12 years). One castrated male (7 years) was the offspring of this pair. The ␣-female (8 years) and a younger castrated male (6 years) were both sired by the ␣-male, by dams no longer members of the group. A subadult female (3 years), and a juvenile female (1 year) were the progeny of the ␣-male and ␣-female. The troop was housed in an open-roofed, concrete, enclosure measuring approximately 230 m2 . The enclosure contained a central, 6 m high fibreglass rock-like formation as well as a number of logs/branches placed in either fixed or movable positions. The troop’s night room, 1.8 m × 4.6 m × 2.2 m, opened directly into the open-roofed enclosure. The troop could freely access their night room except during cleaning times, and when behavioural recordings were made. The baboons were confined to their night room between 7:00 and 10:00 h, during which time the outdoor enclosure was cleaned and, if necessary, experimental apparatus introduced. Despite the cleaning, fallen leaves and/or small, discarded food parts from the previous day could usually be found in the enclosure. However, the baboons only rarely searched for or consumed these items. The troop was fed a morning meal of fruit and vegetables whilst confined to their night room. Other foods such as sunflower seeds, horse cubes and peanuts were provided as part of standard enrichment protocols; these protocols were continued for the duration of this project during non-observational times. Water was available ad libitum in shallow depressions in and around the fibreglass rock formation.
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2.2. Procedure and apparatus This study was conducted in a sequentially ordered format, comprising baseline treatment (n = 3 days), experimental treatment (n = 24 days), and post experimental baseline treatment (n = 5 days). For the experimental phases, each of the following four treatments (n = 6 days per treatment) was introduced in random order: • Big box food (BBF)—a 90 cm × 90 cm × 25 cm open-topped wooden box, with a fine weld mesh base (for drainage), was attached to the concrete floor of the enclosure by a central rawl bolt through its base. The box was filled with a mixture of wood chips and straw to a depth of about 15 cm, into which substrate 250 g raw peanuts and 125 g finer sprinkle nuts were scattered. All seven animals were able to access the box. • Big box empty (BBE)—the big box, as described above, was placed into the enclosure but without any peanuts. • Small box food (SBF)—one 30 cm × 30 cm × 30 cm closed wooden box mounted on a 50 cm × 30 cm base was attached to the floor of the concrete enclosure by two rawl bolts screwed through 9 mm diameter holes on either side of the base. A 10 cm diameter opening on the upper surface of the box provided access to the interior of the box, which contained a 20 cm diameter plastic ball. An additional wooden base, into which 24 equally spaced 3 cm diameter and 1.5 cm deep cylindrical depressions had been drilled, was fitted to the inside lower surface of the box. Only one animal could access the interior of the box at any given time. The box was filled with 250 g raw peanuts that could only be procured by a baboon manoeuvring the ball and retrieving the food items from the depressions into which the peanuts had settled. • Small box empty (SBE)—the small box, as described above, was placed in the enclosure, but without being baited with peanuts. Peanuts were used because they were prized food items for the hamadryas baboons, and were readily monopolisable by the ␣-male (Jones, personal observations). In addition, the small size of the nuts, especially when presented as sprinkle nuts, increased the searching and processing time, and hiding the peanuts in wood chips/straw, or within a difficult-to-access box, decreased the baboons’ foraging efficiency, ensuring that the peanuts were not completely consumed before the end of the observation session. 2.3. Data collection and analysis Data were collected between March and August 2002. Observations were made for a 30 min period immediately after the baboons were released from their night room (approximately 10:00 h). The number of individuals foraging at the device, the number of individuals foraging elsewhere in the enclosure, and the total number of individuals observed were recorded using instantaneous sampling with a 15 s inter-scan interval. In addition, the frequency of overt aggression was recorded using continuous sampling. Foraging was defined as any one of the following: actively searching for, harvesting, processing (peeling, stripping outer covering), and consuming food. Overt aggression was defined as a physical interaction in which one animal bites, grapples with, or chases another (Gil-Burmann et al.,
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1998). Each complete interaction, rather than each behavioural component, was scored as an aggressive bout. Data from daily foraging observations were converted to a group foraging ratio of number foraging elsewhere (total number observed − number foraging at the box) + 0.1 (0.1 was added to prevent division by zero). The median ratio, as well as the first and third interquartiles, was calculated for each day’s observations. Nonparametric tests with two-tailed significance levels were used throughout to compare data among experimental treatments. Data collected during baseline observation were not included in the statistical analyses because no device was present. Results were considered significant if P < 0.05. A Friedman analysis of variance was used to compare median ratio scores, first and third interquartile scores, the number of animals foraging at the device, and frequency of overt aggression across the four experimental treatments, and Dunn’s multiple comparisons post-hoc tests were employed to determine specific differences. The relationship between the frequency of aggression and the number of individuals foraging at the treatment apparatus was analysed using Spearman’s rank correlation. 3. Results 3.1. Foraging
0.25 0.2 0.15 0.1 0.05
SBF
SBE
BBF
BBE
PE baseline
0 baseline
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Foraging elsewhere (Fig. 1) varied significantly among experimental treatments for the median (Fr = 13.909, P = 0.0030; Friedman ANOVA) and third quartile values (Fr =
treatment Fig. 1. Median foraging elsewhere during the two baseline treatments and four experimental treatments. Error bars denote first and third quartiles. Only values above zero are shown. Baseline data are provided for comparison, and were not included in the statistical analyses. PE baseline: post-experimental baseline; BBE: big box empty; BBF: big box food; SBE: small box empty; SBF: small box food.
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15.273, P = 0.0016), but not for the first quartiles (Fr = 3.667, P = 0.2998). Dunn’s multiple comparisons post-hoc tests conducted on the median foraging elsewhere ratios did not reveal differences among treatments, possibly because the many zero values in the data sets decreased the power of the tests. However, post-hoc tests applied to data from the third quartile showed significant differences between the BBE and SBF treatments (P < 0.05), and the BBF and SBF treatments (P < 0.01). For the BBE and SBE treatments, foraging elsewhere was comparable to the low values recorded during the baseline and post-experimental baseline study, although this was not analysed statistically. Very few individuals foraged at the box (BBE: 0, 0, 0 (median, first quartile, third quartile); SBE: 0, 0, 0). For the BBF treatment, foraging elsewhere was comparable to the baseline, but the number of animals foraging at the box was greater compared with other experimental treatments (6, 5.25, 6). During the SBF treatment only one animal at a time (almost exclusively the ␣-male) was able to access the device (1, 1, 1). However, animals excluded from the small box increased their foraging efforts in non-provisioned areas of the enclosure. The redirected foraging behaviours were predominantly appetitive, although animals occasionally found and consumed fallen leaves or remnants from the previous day’s enrichment scatter feed. 3.2. Aggression
20 15 10 5 SBF
SBE
BBF
BBE
PE baseline
0 baseline
aggression frequency
The frequency of aggressive encounters varied significantly among treatments (Fr = 13.655, P = 0.0034). Aggression was highest during the BBF treatment, and lower for the other three experimental treatments, although these differences in aggression were only significant between BBF and SBE (Dunn’s post-hoc test; Fig. 2). Aggression was lower during the two baseline treatments than for any of the experimental treatments, but this was not compared statistically. The median number of individuals at the device varied significantly among treatments (Fr = 15.000; P = 0.0018). More animals foraged at the device during the BBF treatments (6) than during the SBF treatment (1), and the BBE and SBE treatments (0). Aggression
treatment Fig. 2. Median aggression (number of aggressive interactions per 30 min) in the two baseline treatments and four experimental treatments. Error bars denote first and third quartiles. Only values above zero are shown. Baseline data are provided for comparison, and were not included in the statistical analyses. PE baseline: post-experimental baseline; BBE: big box empty; BBF: big box food; SBE: small box empty; SBF: small box food.
aggression frequency
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25 20 15 10 5 0 0
1
2
3
4
5
6
7
median number of animals at device
Fig. 3. The relationship between aggression frequency (number of aggressive incidents per 30 min) and median number of individuals at BBE, BBF, SBE, or SBF (n = 24).
frequency during all four treatments was strongly correlated with the number of individuals at the device (Spearman r = 0.7847, P < 0.0001, r 2 = 0.6392; Fig. 3).
4. Discussion Group foraging levels in non-provisioned areas of the enclosure were significantly higher than baseline levels when one of the seven hamadryas troop members, usually the ␣-male, fed from a monopolisable foraging device (SBF). Group foraging levels did not differ from baseline values for the other experimental treatments, both when no food was present (SBE, BBE), and when the food source was not monopolisable (BBF). Foraging elsewhere values were similar during the SBE and BBE treatments, as well as baseline treatments, indicating that the changes in foraging frequency were a reaction to the availability and distribution of food, and not to the devices themselves. For the BBF treatment, there was little foraging elsewhere as feeding at the device precluded simultaneous foraging in non-provisioned areas of the enclosure. Overt aggression was virtually absent during baseline and experimental treatments, except during the experimental BBF treatment, in which aggression levels were significantly higher than during other treatments. The frequency of aggressive attacks was related to the number of animals at the feeding site, and not contingent only on the availability of food. Aggression bouts typically began among the ␣-female, juvenile female, and castrated males, with one or more animals crouching and screaming, occasionally grappling with one another, and then fleeing. The ␣-male intervened in about 50% of these instances, biting one or more of the troop members and chasing them away from the feeding site. No animals appeared to be injured during these encounters. Free-ranging hamadryas baboons, like most primates, spend at least 60% of their waking hours foraging (Kummer, 1971; Lutz and Novak, 1995). As the foods consumed in nature are in low abundance and scattered, appetitive activities take up a large proportion of total foraging time: there is movement from one feeding site to another, seeds are taken from their pods, tubers uprooted, and rocks overturned to find insects and small vertebrates (Kummer, 1971). This contrasts with the very low rates of foraging observed for primates in captivity (Chamove and Anderson, 1989; Molzen and French, 1989; Saacks and Jones, unpublished data; data collected during baseline treatment in this study).
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The results from this study confirm the prediction that introducing a non-monopolisable food source (BBF) increases foraging levels within the group, but the apparent enrichment benefits derived were offset by an increase in overt aggression. However, we found that when a monopolisable food was provided which only the ␣-male could access (SBF), group members that were excluded from the food source increased their foraging behaviours elsewhere in the enclosure, without a concomitant increase in aggression. Whereas previous studies of provisioned primate and other mammal groups have shown that rates of aggression increased dramatically when food resources are highly clumped (Dunbar, 1988), our results suggest that this is not necessarily the case. Indeed, overt aggression may be avoided when a dominant individual is able to monopolise a food source using indirect (ritualised) aggressive behaviour (e.g., brow-raising, ground beating, staring, advancing towards troop members), while subordinates are able to withdraw to other areas of the enclosure. This creates an advantageous social tactic in competitive foraging situations (Held et al., 2000). Hence, overt aggression need not necessarily ensue from a clumped resource, and can even be forestalled if indirect aggression by one (dominant) animal precludes the grouping of other individuals near a clumped resource. Crowding of animals, rather than the scarcity of the clumped food, appears to produce aggression (Barton et al., 1996). This study shows that appetitive foraging behaviours can be encouraged independently of consummatory behaviours, and suggests an alternative to standard foraging enrichment protocols in which the focus is on promoting appetitive behaviours through slowing down the consummatory process, by rather encouraging solely appetitive behaviours. Indirectly promoting appetitive foraging behaviours may be of particular value for animals on restricted energy diets. Moreover, even if one individual monopolises an enrichment device intended to enrich the entire group, this does not inevitably result in other group members not benefiting from the introduced device. However, we admit this applies largely to social species which forage as a group. Behavioural contagion of foraging, brought about by observing the ␣-male exploiting the food device in the SBF treatment, appeared to cue group members to begin foraging in non-provisioned parts of the enclosure. The importance an animal attributes to seeing a conspecific forage, and whether it acts on this information, depends on two factors (Nicol and Pope, 1994; Coussi-Korbel and Fragaszy, 1995). (1) Demonstrator identity influences social learning, possibly because observers learn that certain animals are better predictors of food rewards than others (Nicol and Pope, 1999). Further studies are required to test whether individual characteristics of an animal exploiting a device influence the behavioural contagion of foraging. (2) The animal’s level of hunger may determine the importance attributed to the cues received from a foraging demonstrator. We predict that this potential method of enrichment would be most effective if implemented when the animals are relatively hungry, as would occur a few hours before a standard meal time. Increased foraging elsewhere can thus be considered environmental enrichment, as appetitive behaviours appear to be proximally rewarded and regulated by internal reinforcing systems. This secondary reward system could select for animals performing appetitive behaviours, deriving rewards even when there is no physiological need for an ultimate goal to be satisfied. If an animal’s welfare is regarded as good when positive affective states, such as pleasure, predominate over negative affective states, such as stress (Spruijt et al., 2001), environmental enrichment should also aim to activate the secondary reward systems which
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are the neural substrate for positive affect. In addition to enhancing the welfare of a captive animal by altering its external environment, interventions aimed primarily at manipulating the internal environment of an animal, or mental state, can likewise be seen as enriching. For captive hamadryas baboons, this welfare goal may well be realised by harnessing their natural biology, specifically that of foraging style and social structures, to create opportunities for behavioural contagion of foraging and redirected appetitive foraging behaviours.
Acknowledgements Thanks to the staff members of the Johannesburg Zoo who enabled us to conduct this study—Philip Cronje (Curator Alpha Section), Armstrong Mdoda (Keeper Alpha Section), Lukas Mogajane (Animal Attendant Alpha Section), Ekson Mohlala (Animal Attendant Alpha Section), and Mathew van Lierop (Enrichment Coordinator). MJ thanks the National Research Foundation for postgraduate support.
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