Linköping University | Department of Physics, Chemistry and Biology Type of thesis, xx hp | Educational Program: Physics, Chemistry and Biology Spring or Autumn term 20xx | LITH-IFM-x-EX—yy/xxxx—SE: 20/3798
Title: ‘Social interactions in chimpanzees (Pan troglodytes) and
their responses to enrichments’.
Author’s name: Eirini-Spyridoula Chatziiosifidou
Examiner: Tom Lindström Supervisor: Mats Amundin
Contents
1 Abstract ………...…………... 1
2 Introduction ……….…... 1
3 Materials and methods ………. 3
3.1 Animals and site…………...……….…...… 3
3.2 Experimental set-up ………...…… 4
3.3 Data analysis ………...………... 10
4 Results ………... 12
4.1 Effect of the type of the enclosure on chimpanzees’ social interactions….…12 4.2 Effect of the presence of enrichment on chimpanzees’ social interactions….14 4.3 Effect of the type of enrichment on chimpanzees’ social interactions...16
4.4 Social Dynamics in the chimpanzees’ group…………...…18
5 Discussion ………... 21
6 Societal and ethical considerations ……….… 25
7 Acknowledgments ………. 25
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1. Abstract
Chimpanzees are highly social animals, presenting a wide variety of social interactions among them. In this study, we compared the social dynamics in a group of 20 captive chimpanzees at Kolmården Wildlife Park between two different exhibits: outdoors (summer) and indoors (autumn). Furthermore, different types of enrichment were offered in both environments and we investigated how the presence and the type of enrichment (food-based) affected the social interactions in the group. Then, we used the frequencies of the social interactions to analyse the social dynamics in the group. Our results showed that the chimpanzees had significantly higher frequencies of proximity, allogrooming and displacement in the outdoor exhibit compared to indoor one and higher frequencies of threat and display indoors compared to outdoors. Moreover, we found that associative and affiliative behaviours increased in both outdoor and indoor exhibits when enrichment was absent compared to when it was present and also when enrichment was absent compared to when food-based enrichment was offered. Furthermore, three pairs of individuals, all mother-daughter dyads, were found to have preferred relationships. In the allogrooming network, one female, the only one that was in estrus, was found to be the most common recipient of allogrooming. Finally, the oldest male, father of all offspring, was, as expected, ranked as the most dominant in the group, based on the agonistic interactions. Our results may be used by the zoo staff to further develop their management practices to improve chimpanzees’ welfare.
Keywords: captive chimpanzees, social dynamics, social interactions, aggression, enrichment
2. Introduction
Chimpanzees (Pan troglodytes) belong to the family Homininae (AZA Ape TAG, 2010). As primates, they are highly social animals, whose societies are characterized by perpetual associations and high levels of cooperation among individuals (Sousa & Casanova, 2006). However, the fact that the individuals compete for resources such as food and water may lead to
2 aggression among them (de Waal, 1996). The reasons that may lead to such aggressive interactions are personal defense, protection of certain conspecifics and competition (Sousa & Casanova, 2006). Another factor that can lead to aggression in captive chimpanzees is limited space (Stevens et al., 2008). The ‘spatial crowding hypothesis’ suggests that chimpanzees under crowded conditions are subject to increased conflicts of interest (de Waal, 1989). In long-term crowding conditions, for example during winter when chimpanzees are housed in smaller indoor exhibits for a long period of time, it has been found that their aggressive interactions are increased. As a consequence, they increased their affiliative behaviour, such as grooming, which helps to cope with the crowded conditions (Nieuwenhuijsen & de Waal, 1982).
Chimpanzees in the wild spend most of their time foraging for food and taking part in complex social activities, while at the same time exhibiting a great ability for problem solving (Costa et al., 2014). In a zoo setting, chimpanzees need a high level of social and environmental complexity to bring the expression of their behavioural repertoire and their activity status as close as possible to that of their wild conspecifics (Celli et al., 2003). Without such social and environmental complexity, they might develope health and behavioural problems (Novak et al., 2006). Abnormal behaviours can be described as any behaviour that is not present in the behavioural repertoire of a species in the wild (Costa et al., 2014).
One way of avoiding such unwanted behaviours is to offer environmental enrichments, which can be defined as any actions taken to improve the physical and psychological wellbeing of captive animals (Shepherdson et al., 1998). For example, enrichment devices that stimulate foraging and grooming have been shown to reduce abnormal behaviour and simultaneously increase the chimpanzees’ activity level (Baker, 1997). Moreover, it has been found that while inappropriate or poorly distributed enrichment might increase aggressive interactions between the individuals, enrichment that is species, sex, age and background appropriate can reduce aggression and abnormal behaviour. Thus, the use of appropriate enrichment can improve the welfare of primates in captivity (Honess & Marin, 2006).
The aim of this study was to investigate the social interactions in a group of 20 captive chimpanzees and to identify differences in the frequency of these interactions between the outdoor and indoor exhibits. Furthermore, different types of enrichment were offered to the chimpanzees in both environments and a second aim of this study was to identify if and how the presence and
3 the type of enrichment (food-based) affected the social interactions in the group. Finally, with our study we aimed at gaining a better understanding of the social dynamics in the group, e.g. to identify which individuals have closer relationships, display higher levels of aggression etc.
3. Materials and Methods 3.1. Animals and site
A group of 20 captive chimpanzees (Pan troglodytes) at Kolmården Wildlife Park in Sweden were studied. Figure 1 depicts the genealogical chart of this group.
Figure 1: Genealogical chart of the chimpanzees’ group. Individuals with black colour have
passed away. The other colours define in which group chimpanzees are divided into when they are trained in separation for handling skills. For instance, Claudius, Fiffi and Figaro belong to the blue-coloured group and are placed in the same holding area when they are to be trained individually.
4 During data collection, the chimpanzees had controlled access to three areas: the indoor exhibit, the outdoor exhibit and the off-display group cages. In the summer period, they spent most of their time in the outdoor exhibit. This exhibit included wooden shelters that provided shade and protection (e.g. from rain). In the winter period, they spent most of the time in the indoor exhibit, and had access to the outdoor exhibit only for short periods of time when the weather was good. No observations were done in the cages. Figure 2 illustrates parts of the chimpanzees’ outdoor and indoor exhibits.
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Figure 2: Part of the chimpanzees’ outdoor (left) and indoor exhibits (right).
3.2. Experimental setup
Initially, there was a three-week period of learning how to recognize all the 20 individuals, while at the same time allowing the chimpanzees to get used to the presence of the observer. After this period, two study periods followed: Period 1 (25 June- 18 August, outdoors) and Period 2 (1 October- 20 November, indoors). Scan sampling with 10 minutes’ intervals was used to record the behaviour of all animals at the same time. Each session lasted 2 hours and was repeated twice per
5 day (morning and afternoon). Each period resulted in 138 hours of observations. The behaviours that were recorded are shown in Table 1.
Table 1: Behavioural ethogram adapted from Funkhouser et al. (2018).
Behaviour Definition
A. Association
Proximity Any individual within another individual’s
scope. Proximity during locomotion refers to an individual within another’s individual scope and moving to the same direction.
B. Affiliation
Allogrooming Picking through hair or at skin of another individual, removing dandruff and possible debris with hands and/or mouth. Does not include pulling hair and the actor does not receive grooming simultaneously.
Simultaneous grooming
Picking through hair or at skin of another individual, removing dandruff and possible debris with hands and/or mouth, while the other individual returns the same behaviours simultaneously. Does not include pulling hair.
Play Non-aggressive interactions involving two or
more individuals. Includes rough-and-tumble play, quiet play, object play, self-play, social
6 play initiation that might be accompanied by
play-face and/or laughing.
C. Agonism
Displacement Approaching and overtaking the physical territory from another individual.
Display Aggressive behaviour without any clear and identifiable recipient. It may include pilo-erection and behaviours such as beating on or moving inanimate objects, stomping, slapping, swaying, hooting, chest-eating, running.
Fight Mutual contact aggression that becomes a
state.
Submission Includes crouching, bobbing, fleeing, avoiding, fear grimacing, bared teeth creaming, pant grunting.
Threat Aggressive behaviours of an individual
towards another individual that do not include any physical contact. Includes lunge and rush.
Other aggression Aggressive behaviours that include some physical contact between individuals. It might include wrestling, lunge, hit, grub, scratch, bite, pilo-erection or other behaviours perceived as agonistic in nature.
D. Other
Interaction with the enrichment
The animal is having physical contact with the enrichment.
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Other behaviours Include behaviours that are not included in the previous definitions.
Out of sight The individual cannot be seen by the observer.
Different types of enrichment were offered to the chimpanzees both in the outdoor and indoor exhibits. The type of the enrichment and the days that they were offered were based on an enrichment schedule made entirely by the zookeepers. In total, 37 different enrichments were offered, belonging to the following categories: 1) sensory, 2) object-based, 3) social, 4) food-based and 5) species-specific.
Some days more than one enrichment were combined. Table 2 includes all the enrichments that were used and the category into which they belong. Figure 3 illustrates two different enrichments: the swings and green boxes with small holes containing pellets.
Table 2: Enrichments that were used and the category into which they belong.
Enrichment Type of enrichment
CINNAMON
1) Sensory
CUPS WITH CARDAMOM CACAO
SPICES SWINGS
2) Object-based
TRIANGLE SWINGS
CURTAIN FROM FIREHOSES BLUEBERRY PLANTS
LEATHER HAMMOCKS CLOTHES
METAL TRIANGLES Wood? WOOL
8 NEWSPAPERS
WOOD WOOL 3) Social
COCONUT
4) Food-based
GRASS RICE
PAPERS WITH PELLETS NETS WITH CABBAGES ICE CUBE WITH PEAS PAPER BAGS WITH FOOD HONEY PLANK
FIREHOSES WITH PELLETS FROZEN VEGETABLES PIPES WITH HONEY TUBES WITH HONEY
LABYRINTH WITH PELLETS PAPER CUPS
LABYR BOXES W. PELLETS
BARRELS with small holes containing PELLETS
POPCORN
BALLS with small holes, containing PELLETS
BUCKETS WITH PELLETS WOODS WITH RAISINS DEVICES WITH YOGHURT
EGGS 5) Species-specific
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Figure 3: Two different enrichments: A) Swings (offered in the outdoor exhibit) (left) and B)
Green boxes with small holes containing pellets (offered in the indoor exhibit) (right).
Enrichment was not present on every day of our study. In total, enrichment was present for 48 hours in the outdoor exhibit and 38 hours in the indoor exhibit. The no-enrichment period was longer than the enrichment one. For this reason, for both the outdoor and indoor exhibits, we randomly removed data from the no-enrichment period to match it with the duration of the enrichment period.
On the enrichment days, enrichments that belonged to the five different categories presented in Table 2 were used. Unfortunately, we only collected sufficient data with the food-based enrichments. Thus, we could only compare the social interactions of the chimpanzees between the food-based enrichment days and the no-enrichment days. Food-based enrichment was present for 17 hours in the outdoor exhibit and 23 hours in the indoor exhibit. As above, for both outdoors and indoors, we randomly removed data from the no-enrichment period to match it with the duration of the food-based enrichment.
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3.3 Data analysis
A. Effect of the enclosure and enrichment on chimpanzees’ social interactions
In order to compare the effect of the exhibit on the chimpanzees’ social interactions, we applied a One Sample Chi-square test in SPSS for each behaviour. We hypothesized that, due to the spatial crowding hypothesis (de Waal, 1989), the number of aggressive interactions would be higher in the indoor exhibit compared to the outdoor one. Furthermore, the number of affiliative interactions, which are supposed to help to cope with the crowded conditions (Nieuwenhuijsen & de Waal, 1982), would be expected to be higher indoors compared to outdoors. The null hypothesis for the One Sample Chi-square test assumes that there is no difference of the social interactions between the two exhibits.
The One Sample Chi-square test was also applied to compare the social interactions in the group between the enrichment and the no-enrichment days, regardless of the type of enrichment, in the indoor and outdoor exhibit, separately. We hypothesized that the number of aggressive interactions would be lower when enrichment was present compared to when it was absent. Furthermore, we hypothesized that the frequency of associative and affiliative behaviours would be higher when enrichment was present compared to when it was absent.The null hypothesis for the One Sample Chi-square test assumes that there is no difference in the social interactions between the enrichment and no-enrichment days.
To identify the specific effect of the food-based enrichment, we also applied the One Sample Chi-square test to compare the social interactions in the group between the food-based enrichment and the no-enrichment days, in the indoor and outdoor exhibit, separately. We hypothesized that the number of aggressive interactions would be lower when food-based enrichment was present compared to when it was absent. Furthermore, we hypothesized that the frequency of associative and affiliative behaviours would be higher when food-based enrichment was present compared to when it was absent. The null hypothesis for the One Sample Chi-square test assumes that there is no association between the presence of food-based enrichment and the social interactions of the chimpanzees.
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B. Social and hierarchical structure analysis (SOCPROG)
We used SOCPROG, a set of programs that analyses data on animal associations (Whitehead, 2009), to perform social and hierarchical structure analyses. We used proximity (symmetric associations), allogrooming (asymmetric interactions) and agonism (asymmetric interactions) in these analyses (see Table 1). Agonism included the following aggressive behaviours: threat,
submission, displacement and other aggression. Because submission is supposed to be directed
from lower to higher ranking individuals (Waal, 1982), we reverse-coded the submissive interactions, so the actors of the dominant behaviours were the ‘winners’ (Funkhouser et al., 2018). For example, the submissive behaviour of Mamba towards Marco, in the analysis would be converted to Mamba being the recipient of an aggressive action by Marco. Thus, Marco would be the winner. In that way, all the aggressive behaviours would be directed from higher to lower ranking individuals.
We calculated association indexes across associative matrices (symmetric) and interaction indexes across agonistic and allogrooming matrices (asymmetric) for all dyads. An association index estimates the proportion of time individuals spend together in proximity (‘simple ratio’) and an interaction index estimates the proportion of time individuals interacted with each other (‘simple ratio’) (Whitehead, 2019). We then used the associative matrices in order to do a hierarchical cluster analysis in SOCPROG, which illustrates the clustering of relationships between individuals (Funkhouser et al., 2018).
We conducted a test for preferred and avoided relationships in SOCPROG.This test is conducted on associative measures. Thus, we only used the proximity data. This analysis produces random association matrices (1000 permutations) for a specific number of individuals (three or more) to test against the observed data (Funkhouser et al., 2018). For the null hypothesis to be rejected, the distribution of the observed association indexes should be significantly different from the distribution of the random association indexes (Funkhouser et al., 2018). This test generates significantly preferred dyads (with a significantly high association index compared to other dyads in the group) and significantly avoided dyads (with a significantly low association index compared to other dyads in the group) (Funkhouser et al., 2018).
Furthermore, we tested the hypothesis that an asymmetric interaction measure is reciprocal. Thus, the rate of interactions between individuals A and B is correlated with that between B and A
12 (Hemelrijk, 1990). If there is no correlation, the interaction measure is considered to be unidirectional (Hemelrijk, 1990). Two types of reciprocity were tested:
Absolute reciprocity: Individuals return interactions to other individuals based on the absolute
frequency of interactions that they receive, compared with the overall distribution of these interactions within the population (Hemelrijk, 1990).
Relative reciprocity: Individuals return interactions to another individual based on the frequency
of interactions that they receive from that other individual, relative to the rates at which they receive interactions from other members of the population (Hemelrijk, 1990).
We used the Mantel Z-test to examine absolute reciprocity and the Kr-test to assess relative reciprocity (Whitehead, 2019). The Mantel Z-test is the standard test for correlations between two association measures and it can be affected by large or small outlying values (Mantel, 1967). The Kr-test identifies if there is any correlation between ‘Measure 1’and ‘Measure 2’. In the Kr-test, the values in each row of the matrix are compared to all other values within that row (Hemelrijk, 1990). Thus, the Mantel Z-test compares each dyad’s proportion of interactions with all other dyads and the Kr-test compares each dyad’s proportion of interactions with other dyads with the same actor (Hemelrijk, 1990).
Finally, we used SOCPROG to analyse the dominance hierarchy in the chimpanzee group. We used three different methods:
1) The ‘I&SI’ method of de Vries (1998) that minimizes the sum of the rank differences between individuals with inconsistent ranks.
2) Brown’s (1975) method that minimizes the ratio of dyadic interaction rates in which a lower ranking individual is actor.
3) Crow’s (1990) method that maximizes the sum, over dyads, of the difference between the two interaction rates multiplied by the difference in ranks.
4.Results
13 The One Sample Chi-square test indicated that there was a statistically significant difference of the number of proximity, allogrooming, displacement, threat and display (see Table 1) between the outdoor and indoor exhibit. More specifically, we found that the number of proximity interactions was higher in the outdoor compared to the indoor exhibit (χ2(1) = 110.89, p = 0.000).
Also, the number of allogrooming (χ2(1) = 13.98, p = 0.000) and the number of displacement (χ2(1)
= 9.66, p = 0.002) were higher in the outdoor enclosure compared to the indoor one. On the other hand, we found that the number of threat (χ2(1) = 9.47, p = 0.002) and display (χ2(1) = 75.84, p = 0.000) were higher when the chimpanzees were indoors compared to outdoors. Table 3 presents all the p-values from the comparison of the number of each of the social behaviours between the indoor and outdoor enclosure. Figure 4 illustrates the number of social interactions in the indoor and outdoor enclosure, only for the behaviours, for which a significant difference was found between the two enclosures.
Table 3: Comparison of all the social behaviours (PRO: Proximity, ALL: Allogrooming, PLA:
Play, SGR: Simultaneous grooming, DIC: Displacement, DIS: Display, SUB: Submission, THR: Threat, AGR: Other aggression) between the indoor and outdoor enclosure, as calculated by One
Sample Chi-square test in SPSS (significant p-values in bold).
Behaviours PRO ALL PLA SGR DIC DIS SUB THR AGR
P-values Higher outdoors 0.000 Higher outdoors 0.000 No diff 0.184 No diff 0.259 Higher outdoors 0.002 Higher indoors 0.000 No diff 0.170 Higher indoors 0.002 No diff 0.931
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Figure 4: Number of proximity (PRO), allogrooming (ALL), displacement (DIC), threat (THR)
and display (DIS) in the outdoor and indoor exhibit.
4.2. Effect of the presence of enrichment on the chimpanzees’ social interactions
The One Sample Chi-square test indicated that there was a statistically significant difference in the number of proximity between the enrichment days and the no-enrichment days in both the outdoor (χ2(1) = 18.32, p = 0.000) and indoor exhibit (χ2(1) = 6.55, p = 0.001). In particular, the number of
proximity was higher when enrichment was absent than when enrichment was present in both
exhibits. Furthermore, the number of allogrooming was higher when enrichment was absent compared to when enrichment was present in both the outdoor (χ2(1) = 6.71, p = 0.010) and indoor exhibit (χ2(1) = 49.73, p = 0.000). In the outdoor exhibit, the number of play was higher when enrichment was absent compared to when the enrichment was present (χ2(1) = 25.66, p = 0.000). On the other hand, in the indoor enclosure, the number of play was higher when the enrichment was present compared to when the enrichment was absent (χ2(1) = 4.43, p = 0.035). In the indoor exhibit, the number of simultaneous grooming was higher when the enrichment was absent compared to when the enrichment was present (χ2(1) = 21.55, p = 0.000). Table 4 presents all the p-values from the comparison of all the social behaviours between the enrichment and no-enrichment days both outdoors and indoors. The total number of social interactions, for the behaviours showing a significant difference between enrichment and no-enrichment days, is illustrated in figures 5 and 6, for the outdoor and indoor exhibit, respectively.
Table 4: Comparison of all the social behaviours (PRO: Proximity, ALL: Allogrooming, PLA:
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Threat, AGR: Other aggression) between the enrichment and no-enrichment days, in the outdoor
and indoor exhibits, respectively, as calculated by One Sample Chi-square test (significant p-values in bold).
Behaviours PRO ALL PLA SGR DIC DIS SUB THR AGR
Outdoors P-values Higher w/o enrichment 0.000 Higher w/o enrichment 0.010 Higher w/o enrichment 0.000 No diff 0.799 No diff 0.465 No diff 0.077 No diff 0.132 No diff 0.157 No diff 1.000 Indoors P-values Higher w/o enrichment 0.001 Higher w/o enrichment 0.000 Higher w enrichment 0.035 Higher w/o enrichment 0.000 No diff 0.317 No diff 0.428 No diff 0.285 No diff 1.000 No diff 0.052
Figure 5: Number of proximity (PRO), allogrooming (ALL) and play (PLA) interactions in
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Figure 6: Number of proximity (PRO), allogrooming (ALL), play (PLA) and simultaneous
grooming (SGR) interactions in enrichment and no-enrichment days in the indoor exhibit.
4.3 Effect of the type of enrichment on chimpanzees’ social interactions
The One Sample Chi-square test indicated that the number of proximity was significantly higher on the days without enrichment compared to the food-based enrichment days in the outdoor exhibit (χ2(1) = 10.13, p = 0.001). Furthermore, the One Sample Chi-square test indicated that the number
of allogrooming was significantly higher on the days without enrichment compared to the food-based enrichment days in both outdoor (χ2(1) = 15.1, p = 0.000) and indoor exhibit (χ2(1) = 63.71,
p = 0.000). In the outdoor exhibit, the number of play was significantly higher on the days without enrichment compared to the days with food-based enrichment (χ2(1) = 18.75, p = 0.000). Finally, in the outdoor exhibit the number of simultaneous grooming was significantly higher in the no-enrichment days compared to the food-based no-enrichment ones (χ2(1) = 8.02, p = 0.005). Table 5
presents all the p-values from the comparison of all the social behaviours between the food-based enrichment and no-enrichment days both outdoors and indoors. Figures 7 and 8 illustrate the number of social interactions in the no-enrichment days and the days with food-based enrichment, for the behaviours, where significant differences were found between the different types of enrichment in both outdoor and indoor exhibit, respectively.
Table 5: Comparison of all the social behaviours (PRO: Proximity, ALL: Allogrooming, PLA:
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Threat, AGR: Other aggression) between the food-based enrichment and no-enrichment days, as
calculated by One Sample Chi-square test in SPSS (significant p-values in bold).
Behaviours PRO ALL PLA SGR DIC DIS SUB THR AGR
Outdoors P-values Higher w/o enrichment 0.001 Higher w/o enrichment 0.000 Higher w/o enrichment 0.000 Higher w/o enrichment 0.005 No diff 0.808 No diff 0.217 No diff 1.000 No diff 1.000 No diff 0.532 Indoors P-values No diff 0.677 Higher w/o enrichment 0.000 No diff 0.388 No diff 0.639 No diff 0.317 No diff 0.317 No diff 0.317 No diff 0.637 No diff 0.491
Figure 7: Number of allogrooming (ALL), play (PLA), proximity (PRO) and simultaneous
grooming (SGR) in no-enrichment days and days that food-based enrichment was used in the
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Figure 8: Number of allogrooming (ALL) in no-enrichment days and days that food-based
enrichment was used in the indoor exhibit.
4.4 Social Dynamics in the chimpanzees’ group
A. Dyadic indexes
Across all chimpanzee dyads, associative indexes averaged 0.29 ± 0.28 (SD), ranging between 0.00 (most dyads) and 0.79 (Maggan-Citrus). Across all dyads, allogrooming rates averaged 30.00 ± 32.84 (SD), ranging between 0.00 (most dyads) and 158.00 (Mango-Fiffi) and agonistic interaction rates averaged 3.80 ± 2.48 (SD), ranging between 0.00 (most dyads) and 7.00 (Mika-Mona).Within the allogrooming network, Fiffi was the most common recipient of allogrooming. Within the agonistic network, Claudius was the most frequent actor in aggressive interactions, but never the recipient. Figure 9 depicts the hierarchical cluster for the associative network.
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Figure 9: Associative hierarchical cluster analysis, based on association indexes in SOCPROG.
B. Preferred and avoided relationships
The test for preferred and avoided relationships from the association data (proximity) was significant (p=0.000); therefore, the null hypothesis was rejected. This test identified three dyads with significantly preferred relationships and the rest of the relationships were significantly avoided. Table 6 includes the preferred and avoided relationships between the individuals, as calculated by SOCPROG.
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Dyads Relationship Association index p-value
Maggan-Citrus Preferred 0.79 0.000 Madicken-Mygun Preferred 0.69 0.000 Marianna-Marley Preferred 0.57 0.000 Claudius-Fiffi Avoided 0.29 0.000 Madicken-Maud Avoided 0.17 0.000 Mango-Fiffi Avoided 0.18 0.000 Fred-Fiffi Avoided 0.16 0.000
Other dyads Avoided <0.10 0.000
C. Test for reciprocity or unidirectionality
The test for reciprocity for the allogrooming network found no significant absolute reciprocity, but a significant relative one (Mantel Z-test, p = 0.065; Kr-test, p = 0.01). This shows that the chimpanzees in this groupreturned allogrooming to another individual based upon the frequency of allogrooming that they received from that other individual, relative to the rates at which they receive this behaviour from other members of the group (Hemelrijk, 1990). Furthermore, the test found no significant absolute reciprocity, but a significant relative reciprocity for the agonistic network (Mantel Z-test, p = 0.193; Kr-test, p = 0.015). This means that individuals returned agonistic interactions to another individual based upon the frequency of agonistic interactions that they received from that other individual, relative to the rates at which they received these behaviours from other members of the group (Hemelrijk, 1990).
D. Dominance hierarchy
We calculated the dominance rank for each individual using three different methods (see 3.3 Data analysis). Claudius was consistently ranked as the most dominant and Martin as the second most dominant, whereas Mamba was consistently ranked as the least dominant. All the other individuals were ranked in different positions across the three different ranking methods. Table 7 shows the dominance rank for each individual using the three methods, as calculated by SOCPROG.
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Table 7:Dominance rank for each individual using three different methods.
The ‘I&SI’ method (de Vries 1998)
Brown’s (1975) method Crow’s (1990) method
1.Claudius 1.Claudius 1.Claudius
2.Martin 2.Martin 2.Martin
3.Mariana 3.Mariana 3.Mika
4.Marko 4.Marko 4.Marko
5.Mika 5.Mika 5.Figaro
6.Mango 6.Mango 6.Fiffi
7.Fred 7.Fred 7.Mango
8.Figaro 8.Figaro 8.Mariana
9.Fiffi 9.Mia 9.Maggan
10.Mia 10.Maggan 10.Marley
11.Maggan 11.Fiffi 11.Citrus
12.Madicken 12.Mona 12.Mia
13.Mona 13.Marie 13.Fred
14.Marie 14.Madicken 14.Marie
15.Maud 15.Maud 15.Madicken
16.Citrus 16.Marit 16.Marit
17.Marley 17.Marley 17.My-Gun
18.My-Gun 18.Citrus 18.Maud
19.Marit 19.My-Gun 19.Mona
20.Mamba 20.Mamba 20.Mamba
4. Discussion
In this study, we compared the social interactions in a group of 20 captive chimpanzees in three conditions: between the outdoor (summer) and indoor (autumn) exhibit, between the presence and the absence of enrichment and between the presence of food-based enrichment and the absence of
22 enrichment. Furthermore, this investigation examined the social structure and dominance hierarchy of the group. We found that three pairs of individuals had preferred relationships and one female chimpanzee that was in estrus for some part of our study was the most common recipient of allogrooming. Based on the allogrooming and agonistic networks, we found that the individuals reciprocally displayed allogrooming and agonism. Moreover, based on the agonistic interactions, we calculated the dominance rank for each individual. Our results contribute to a better understanding of social interactions between the individuals in this group of chimpanzees and how these interactions are being affected by factors such as the exhibit and different types of enrichment. Such a knowledge can help the animal caretakers in many ways in order to improve the animals’ welfare.
The chimpanzees showed significantly higher frequencies of proximity, allogrooming and
displacement in the outdoor exhibit compared to the indoor one and higher frequencies of threat
and display in the indoor exhibit compared to the outdoor one. It has been found that chimpanzees prefer shade much more than direct sunlight in captive environments (Duncan & Pillay, 2013). The first period of the study in the outdoor exhibit took place in the mornings and afternoons during summer, when the majority of the outdoor exhibit was exposed to direct sunlight except in a few shelters that offered shade. In this period, the chimpanzees spent much more time in the shelters than in the direct sun. At the same time, higher levels of displacement were recorded in the outdoor exhibit compared to the indoor one. The reason for this is that a dominant chimpanzee would overtake the place in the shelter from sub-dominant chimpanzee, outdoors at a higher rate than indoors, because there was no direct sunlight in the indoor exhibit. Furthermore, since they would spend most of the day in the shelters in the outdoor exhibit, this would force them to stay closer to each other compared to indoors. Thus, they would present higher frequency of proximity and affiliative behaviours such as allogrooming. Moreover, in this study, higher frequencies of
threat and display, which are aggressive interactions, were found in the indoor exhibit compared
to the outside one, but no significant difference in play was found between the two environments. According to Stevens et al. (2008), higher rates of aggression and play are seen in chimpanzee groups in indoor exhibits, compared to outdoor ones. This increase in aggression can be explained by the ‘spatial crowding’ hypothesis that suggests that chimpanzees under crowded conditions display increased conflicts of interest (de Waal, 1989). It has also been found that together with
23 these aggressive interactions, chimpanzees may also increase their affiliative behaviour, such as grooming or play, to cope with the crowded conditions (Nieuwenhuijsen & de Waal, 1982). Moreover, higher frequencies of proximity, allogrooming and play were found in the outdoor exhibit when enrichment was absent compared to when it was present. Also, higher frequencies of
proximity, allogrooming and simultaneous grooming but lower frequencies of play were found in
the indoor exhibit when enrichment was absent compared to when it was present. This can be explained by the fact that on enrichment days the chimpanzees would spend more time exploring and manipulating the enrichment, at the cost of lower frequencies of associative and affiliative behaviours compared to no-enrichment days. The lower frequencies of play when enrichment was absent in the indoor exhibit may be due to the variety of enrichments that was used. Thus, a future follow-up of this project should focus on a smaller range of selected enrichments to allow for analysis of the effect of each specific enrichments on the social interactions of the group.
Furthermore, we found higher frequencies of proximity, allogrooming, play and simultaneous
grooming in the outdoor exhibit on no-enrichment days compared to food-based enrichment days.
Also, higher frequencies of allogrooming were found in the indoor exhibit on no-enrichment days compared to food-based enrichment days. As mentioned above, lower frequencies of associative and affiliative behaviours when enrichment was present may be due to the fact that the chimpanzees would spend more time exploring/manipulating the enrichment. Considering that in the wild primates explore and manipulate novel objects primarily in the context of searching for food (Anderson, 1990), investigating the food-based enrichment would be of higher priority to the chimpanzees than engaging in associative or affiliative behaviours.
Three pairs of individuals (Maggan-Citrus, Madicken-My-Gun and Mariana-Marley) were found to have the strongest, most preferred relationships. All these dyads are mother-juvenile daughter (born 2015-16) relationships, and their strong relationship are expected since it is known that mothers and daughters tend to have high association indexes (Williams et al., 2002). Furthermore, some males (Mango, Claudius, Fred) spent more time closer to Fiffi compared to the other females. Fiffi was the only female in the group that was in estrus for some part of the study, thus these males stayed closer to her possibly to increase their possibility to gain access to mating.
Allogrooming is one of the most prevalent affiliative behaviours in nonhuman primates (Goosen,
24 (Boesch & Boesch-Ackerman, 2000). Previous studies have shown that male-to-female
allogrooming interactions increase during the beginning of swelling and at menstruation (Wallis,
1992). Therefore, it was expected that Fiffi, the only female in the group that was in estrus for some part of our study, was the recipient of the highest allogrooming rates. Furthermore, in the
allogrooming network a significant relative reciprocity was found. Chimpanzees can exchange
grooming, as an interchange currency, for itself (Arnold and Whiten, 2003) or for other acts such as agonistic support, i.e. when an individual intervenes in an aggressive conflict to support one party against the other (Hemelrijk, 1994), tolerance (Henzi & Barrett, 1999), food (De Waal, 1997), and cooperative services in breeding groups, such as infant support, food-sharing with infants, and territorial defense (Lazaro-Perea et al., 2004).
Within the agonistic network, Claudius was the most frequent actor in aggressive interactions, but never the recipient. Thus, all the three ranking methods defined him as the most “dominant” because he was “winning” (or acting) in more agonistic interactions than he was “losing” (or receiving) (Funkhouser, 2018). Agonistic interactions are fundamental in establishing dominance within the group (Newton-Fisher, N. E., 2004). The dominant individual (with the higher probability of winning any contest) can obtain the contested resource with only a minimum expense of time and energy, whereas the subordinate individual (with the lower probability of winning) avoids wasting time and energy in a contest it will probably lose (Newton-Fisher, N. E., 2004).
In conclusion, with our results, we aim to help the zoo staff to develop better management practices and improve the chimpanzees’ welfare. This can be achieved bygaining further knowledge about the social behaviour between the individuals and how it is being affected by different factors, such as the type of exhibit, different exhibit features, diet, presence/absence of enrichment, type of enrichment etc. Fiffi, as the only female in estrus, was as expected found to be the most common recipient of allogrooming and Claudius, being the only non-castrated male and the dominant one, was also as expected the most frequent actor in aggressive interactions. Therefore, these two individuals can significantly affect the groups’ stability and aggressive interaction rates. This knowledge can help the zoo staff to be more prepared in case of attrition of these individuals. In such a case, a temporary separation of individuals that are mostly connected with Claudius and Fiffi could diminish possible increased aggression. Moreover, it should be noted that the use of a
25 randomized enrichment schedule could provide novelty and prevent that the animals get habituated to the enrichment. However, testing selected enrichments only for the study period and not a wide variety of different ones every day could provide us with more detailed information about the specific effects of each enrichment on the chimpanzees’ interactions. It might make it possible to identify if they prefer specific types of enrichment and not only measure the effect of the presence or absence of enrichment on their social interactions. Future research should focus on a systematic selection of enrichments that are tested in a randomized manner and examine how they would affect the social interactions of the chimpanzees.
5. Societal & ethical considerations
With this study, we aimed at contributing to a better understanding of the social interactions in Kolmården’s group of chimpanzees and how enrichment and the type of exhibit, and features in these exhibits, affected them. With this knowledge, the zoo staff can, if needed, introduce the appropriate changes according to the chimpanzees’ needs, on a group and individual level, and thereby improve the animals’ welfare. In a zoo setting, chimpanzees may be more stressed compared to the wild. In the summer period, there is a high number of visitors that might affect them negatively. In the winter period, the more limited space in the indoor exhibit might increase aggression in the group. Moreover, chimpanzees in a zoo setting, even if it is naturalistic like in Kolmården, lack the social and environmental complexity that they would naturally meet in the wild. Also, chimpanzees in a zoo have a balanced, but restricted diet. As a result of all these limitations, they might not be able to fully express their natural behavioural repertoire and may even develop abnormal behavior patterns. For all these reasons, it is very important to gain a as much knowledge as possible about the social dynamics of such a group of chimpanzees and how it is being affected by different physical and management factors.
6. Acknowledgements
I would like to thank my supervisor, Mats Amundin for his contribution to this project and his help throughout the whole period of the study. Furthermore, I would like to thank Jennie Westander and all the Kolmården staff for their support and cooperation during my data collection. Especially,
26 I would like to thank the staff in the Apehouse at Kolmården zoo for their tolerance and the daily support that they offered me during my data collection.
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