The Effects of the Death of a Group Member on the Behavior of Tufted Capuchins (Sapajus apella)

Transcription

1 The Effects of the Death of a Group Member on the Behavior of Tufted Capuchins (Sapajus apella) Lindsey M. Engelbert Department of Biological Foundations of Behavior Franklin & Marshall College Project Advisor: Dr. Elizabeth V. Lonsdorf Department Honors Oral Defense Committee: Dr. Daniel R. Ardia Dr. Alexis Q. Castor Dr. Lauren H. Howard Dr. Elizabeth V. Lonsdorf Submitted: 3 April, 218 Graduated: 12 May, 218

2 Table of Contents List of Figures... 2 List of Tables 2 Abstract. 3 Introduction.. 3 Methods.. 11 Study Subjects and Housing. 11 Behavioral Monitoring Protocol Social Network Metrics Behavioral Metrics.. 12 Data Analysis Results 14 Social Network Changes.. 14 Behavioral Changes. 15 Discussion.. 19 Acknowledgements 23 References.. 23 Appendix 39 1

3 List of Figures Figure 1. Pre and post-death grooming social networks 27 Figure 2. Changes in grooming degree.. 29 Figure 3. Changes in grooming dyadic strength 3 Figure 4. Pre and post-death proximity social networks 32 Figure 5. Changes in proximity dyadic strength 34 Figure 6. Average affiliation rate Figure 7. Average female affiliation rate Figure 8. Average aggression rate.. 37 Figure 9. Average male aggression rate. 37 Figure 1. Average anxiety-related behavior rate.. 38 Figure 11. Average pace rate. 38 Figure A1. Average contact rate. 4 Figure A2. Average grooming rate. 4 Figure A3. Average scratching rate 41 Figure A4. Average yawning rate List of Tables Table 1. Hypotheses... 1 Table 2. Study subjects and their demographics Table 3. Cohesion measures for grooming and proximity social networks Table 4. Behavioral changes in response to death. 18 Table A1. Ethogram of behaviors

4 Abstract The field of animal thanatology has expanded dramatically in recent years. Recent findings have revealed that a wide range of species exhibit behavioral changes in response to the death of a conspecific and, in particular, in response to the dead body itself. Thus far, the majority of the literature has focused on nonhuman primate responses to death, presumably due to the information it offers regarding the evolution of human grief. However, like with other species, the majority of this research has concentrated on responses to the actual body of the deceased. There is comparatively little research examining the effects of the death of a conspecific on group behavior in both the short and long term. Additionally, despite the conclusion that animals alter their behavior in response to death, there is little agreement regarding the significance of such findings. My study aims to address this gap in the literature by examining social network and behavioral changes in a group of captive, tufted capuchins (Sapajus apella) following the death of a group member. I generated grooming and proximity social networks for the six months leading up to the death and the six months following the death, and calculated and compared the corresponding social network metrics of degree, strength, and cohesion. Additionally, I calculated and compared the colony s rate of affiliative, agonistic, and anxiety-related behaviors across six time periods (three before and three after). My results showed that grooming degree (number of grooming social partners) increased for the group as a whole, while grooming strength (frequency of grooming interactions) increased only for the individual with the closest bond to the deceased. I also found that male rates of aggression generally increased following the death, while pacing (an anxiety-related behavior) increased for all group members. My study revealed that even the death of a low-ranking individual has the potential to alter the social network and behavior of the entire group. However, it is unclear whether these changes are a product of grief or merely readjustment following the removal of a group member. Introduction Human responses to the death of an acquaintance or loved one are still not well understood and vary substantially depending on the grieving individual in question, the relationship to the deceased, and the circumstances surrounding the death (Walker et al., 1977). Despite this variation, however, trends in post-death responses do emerge. For example, those individuals with extensive social networks are thought to recover more quickly and fully than 3

5 those who are less connected (Walker et al., 1997). These conclusions are further supported by findings that larger social networks are associated with lower levels of glucocorticoids in grieving individuals (Burke et al., 21). Although the importance of social networks has been widely acknowledged (Burke et al., 21; Laakso & Paunonen-Ilmonen, 22; Strobe et al., 21; Walker et al., 1997), these networks are subject to change following the death of a close acquaintance. For example, the death of a child may result in either permanent or temporary alterations in relationships between spouses and close colleagues (Laakso & Paunonen-Ilmonen, 22). These changes in relationships can be either positive or negative, with the later change associated with increased stress (Burke et al., 21; Laakso & Paunonen-Ilmonen, 22). For centuries, the ability to grieve was widely considered a uniquely human characteristic; however, recent research has revealed a diverse range of species which exhibit many of the same behavioral responses to the death of a conspecific as described above in humans (King, 213). However incomplete our knowledge of humans understanding of death and grief may be, even less is known about animal thanatology. There is much debate regarding the degree to which animals understand or even recognize the death of a conspecific (Appleby et al., 213; King, 213). Many researchers argue that animals continued care for and proximity to a deceased individual, demonstrates a lack of recognition of the implications of death (Allen & Hauser, 1991; Appleby et al., 213, Biro et al., 21). For example, research has revealed that a dingo mother continued to care for and transport her deceased pup for several days following its death (Appleby et al., 213). Similar behavior was echoed in a giraffe cow s prolonged vigilant behavior towards her dead calf s body (Bercovitch, 213). Although some may view these behaviors as a lack of understanding of death (Allen & Hauser, 1991), others believe it is instead reflective of the strength of mother-infant bonds or the potential ambiguity surrounding the state of the deceased individual (Appleby et al., 213). In captive animals, previous research has demonstrated the importance of allowing a dying individual to remain in their social group, both for the welfare of the dying individual and the group (Pierce, 213). Therefore, studies of animal thanatology may also be important for improving the animal welfare of captive individuals. Distinct behavioral changes in non-mothers in response to the body of a deceased conspecific have also been observed in several species. Bates et al. (28) and McComb et al. (26) have found that elephants display increased interest in the remains of conspecifics when compared to the remains of morphologically similar species, such as rhinos and buffalo. This 4

6 curiosity towards the remains of conspecifics has been demonstrated regardless of the strength of genetic or social relationships to the deceased individual (Douglass-Hamilton et al., 26). Dolphins behaviors have also been seen to change following the death of a conspecific. Individuals who were seen diligently caring for a dying conspecific prior to its death, subsequently abandoned the body shortly after the conspecific died (Pierce, 213). These changes in behavior directed towards the conspecific support claims that cetaceans may have an awareness of death. Similarly, chimpanzees are seemingly able to differentiate between live and dead individuals, demonstrating different caring behaviors towards the two (Boesch & Boesch- Achermann, 2). While severely injured individuals receive constant cleaning and care for their wounds from others, deceased individuals receive no such care (Boesch & Boesch- Achermann, 2). Non-human primate responses to death have been of particular interest due to the valuable insights such behaviors may provide into the evolution of human responses to death (Anderson, 211; Stewart et al., 212). Like with humans, non-human primates reactions may be influenced by the circumstances of an individual s death (Anderson, 211, 216; Stewart et al., 212). For example, Anderson et al. (21) observed caring behavior after the peaceful death of an elderly female chimpanzee in a captive setting. Since the elderly individual had demonstrated increasingly lethargic behavior leading up to her death, her group mates relatively calm reaction might be explained by their opportunity to adjust to and prepare for the death. These subdued behaviors are highly reminiscent of humans responses to peaceful deaths (Anderson et al., 21). Similarly, Stewart and colleagues (212) found that chimpanzees who encountered the dead body of a female group member displayed less aggressive behaviors than when group members responded to the sudden and dramatic death of an adult male in the community (Teleki, 1973). Boesch and Boesch-Achermann (2) reported similar observations of loud and aggressive behaviors directed towards the body of an adolescent female that had recently been killed by a leopard. These more aggressive reactions to sudden and traumatic deaths may be reflective of fear or anxiety (Engh et al., 26). However, regardless of what drives these different behavioral responses, these findings suggest that primate responses to the death of a familiar conspecific are contingent upon the circumstances surrounding the death. In both humans and nonhuman primates, responses to the death of an individual vary depending on the remaining individuals age and sex. For example, male chimpanzees are 5

7 notably more aggressive towards the deceased than females and often even beat and drag the body (Anderson et al., 211; Boesch & Boesch-Achermann, 2). Although the literature does not attempt to explain these sex differences in reactions to the death of a conspecific, it is possible that these differences are a result of males and females differing roles in the social group. For example, male chimpanzees generally rank higher in the dominance hierarchy than females and are known to engage in aggressive displays to assert this dominance (Boesch & Boesch-Achermann, 2). Although juvenile chimpanzees are often prevented from approaching the bodies of deceased individuals (Teleki, 24), when they are allowed to approach, they typically touch the body more than their older counterparts (Stewart et al., 212). This seemingly more curious behavior exhibited in juvenile chimpanzees could be explained by a less complete understanding of death, a phenomenon that is found across human children (Anderson, 216; Slaughter & Griffiths, 27). These observations of chimpanzees indicate variability in individual s responses to the death of a familiar conspecific that is likely contingent upon the responding individual s age and sex (Anderson, 216). Much of the previous research on primate thanatology has focused on individual s responses to the death of an infant and, in particular, changes in the mothers behaviors towards their deceased infant s body (Biro et al., 21; Cronin et al., 211; Fashing et al., 211; Hosaka et al., 2). In both chimpanzees (Biro et al., 21) and gelada baboons (Fashing et al., 211) deceased infants were carried for prolonged periods, using techniques never observed with live infants. In addition, in contrast to the protective behavior demonstrated towards live infants, both species allowed juveniles to handle and groom the infants dead bodies (Biro et al., 21; Fashing et al., 211). These apparent differences in behavior concerning dead infants suggest an understanding of the implications of death among certain primate species. Less research has been conducted on behavioral responses to the death of an adult, and these studies typically highlight the group s reactions to the actual body of the deceased (Anderson et al., 21; Boesch & Boesch-Achermann, 2; Buhl, et al., 212; Teleki, 1973; Van Leeuwen et al., 216). Far fewer studies have concentrated on group-level social dynamics following the death of a familiar conspecific, and these have predominantly reported on the death of a dominant individual due to their integral position in the social network. For example, aggressive behaviors in three separate groups of captive lowland gorillas increased significantly following the death of the silverback male (Hoff et al., 1998; Less et al., 21). The authors 6

8 attributed this drastic increase in aggression to the theory that silverback males function as a control role (Hoff et al., 1998). It is therefore unclear whether such responses are a result of grief or mourning, or are simply adjustments in the dominance hierarchy. Regardless of the explanation behind these results, these and similar findings have led researchers in the field of animal thanatology to conclude that the degree of social integration of the deceased individual may influence the group s response (Anderson, 211, 216). Additionally, as in humans, the presence of alternative social partners for animals may help buffer the effects of losing a group member (Anderson, 216). In female chacma baboons, increased stress following the death of a close relative was alleviated within a month due to an increase in grooming rates and the number of grooming partners (Engh et al., 26). This suggests that, like humans, a more extensive social network is beneficial for handling the death of a close associate. However, our knowledge regarding changes in behavior in the months following the death of a group mate is still fairly limited. As seen above, much of the research on primate thanatology is limited to apes (Anderson, 21; Biro et al., 21; Boesch & Boesch-Achermann, 2; Hoff et al., 1998; Hosaka et al., 2; Less et al., 21; Stewart et al., 212; Teleki, 1973; Van Leeuwen et al., 216) and Old World monkeys (Buhl et al., 212; Campell et al., 216; Engh et al., 26; Fashing et al., 211). Much less research has been conducted on New World monkeys reactions to the death of a familiar conspecific, presumably because they are more distantly related and therefore may provide less insight into the evolutionary roots of human behavior. An observational study done on wild common marmosets examined the behavioral responses of a group to a dying dominant female, as well as their responses to her body after her death (Bezerra et al., 214). However, aside from responses to dead infants, the above article constitutes the extent of thanatologyrelated studies conducted on New World monkeys. The current study therefore attempts to help fill this void in the literature by examining group members reactions to the death of a lowerranking adult male capuchin. Tufted capuchins are a New World monkey native to northern South America. Their social structure and general behavior are well described in Fragaszy et al. (24) and is summarized below. Matrilines form the structural basis of social relationships, with mothers and daughters forming bonds that are stable well into adulthood. Although grooming rates between mothers and daughters are high, the benefits of kinship are generally more apparent in decreased 7

9 rates of aggression rather than increased grooming. In captivity, female-female bonds are not restricted to kinship and are generally stronger than both male-male bonds and between-sex bonds. Although dominant males in the wild exhibit high rates of aggression towards more submissive individuals, captive capuchins are generally much more tolerant. Male-female relationships are markedly asymmetrical, with nonreciprocal female grooming of males, and females directing the majority of their avoidance and submissive behaviors towards males. However, males are fairly tolerant of females and rarely direct their aggression towards them. Capuchin dominance rankings are relatively integrated and although the alpha male will always rank above the alpha female, females will frequently rank above more submissive males. Franklin & Marshall College houses two colonies of tufted capuchins. In one of these, a low-ranking male member of the group (Izzy) died from an infection in June of 217. Izzy s condition had been deteriorating in the several weeks leading up to his death, and the day before his demise he fell grievously ill. After medical intervention, he was kept overnight in a cubicle adjacent to the colony s enclosure, where all group members were able to view him. The following morning, his condition had deteriorated further and the decision was made to euthanize him. He was subsequently removed from the cubicle and euthanized. His body was not returned to the colony due to concerns regarding his potentially infectious status. Due to the nature of capuchin social relationships, I examined shifts in the group s social dynamics and behaviors following the loss of their group member. I first analyzed changes in the colony s social network. Social network analysis (SNA) allows for the investigation of social structures by evaluating a set of social units (nodes) and the connections (edges) between them (Brent et al., 211). I therefore used this framework to investigate changes in individual measures of degree (number of social partners) and strength (frequency of interactions), following the individual s death. I also calculated metrics concerning changes in the group s overall cohesion (number of ties present in the group). Additionally, I investigated changes in specific behaviors immediately following the death, as well as the transience of these changes in behavior over time by examining if and how long it took the group to return to baseline (predeath) levels. Finally, I assessed if social bond strength with the deceased was correlated with the magnitude of the response to the death of the individual. I used a standardized, long-term behavioral monitoring dataset, collected over the past year, to assess these behavioral and social network changes. 8

10 I hypothesized that the colony s social network would alter in the absence of the deceased individual. I constructed two separate social networks, using individuals physical proximity to one another and bidirectional grooming. For both social networks, I predicted that those individuals with the strongest bonds to the deceased would increase in degree and strength (for already existing bonds) in an attempt to compensate for the loss (see Engh et al., 26 and Silk et al., 26). Since animals have a finite amount of time to devote to maintaining social relationships, I predicted these changes would occur as a result of the reallocation of time already devoted to social effort. In other words, individuals would redistribute social efforts previously directed towards the deceased individual to strengthen remaining bonds and create new ones. For group-level measures, I predicted that cohesion for both social networks would increase, since increased cohesion is correlated with increases in individual measures of strength (see Table 1 for a summary). I also predicted several changes in group behavior. First, the groups anxiety-related behaviors would increase immediately following the individual s death, but would gradually return to baseline levels over time (see Engh et al., 26 and Less et al., 21). Second, agonistic behavior between males would increase initially, due to the disruption of the social group, with a gradual return to baseline levels (see Hoff et al., 1998 and Less et al., 21). Third, in contrast to the males, I predicted an increase in female-female affiliative behaviors that would be strongest immediately following the death, as they expanded and strengthened relationships to compensate for the loss (see Engh et al., 26 and Silk et al., 26) (see Table 1 for a summary). 9

11 Table 1. Predicted changes in social network and behavior following the death of Izzy. HYPOTHESIS CHARACTERISTIC/LEVEL DIRECTIONALITY 1a Proximity social network 1b Grooming social network 2 Behavioral changes Strength/Individual Degree/Individual Cohesion/Group Strength/Individual Degree/Individual Cohesion/Group Anxiety (scratch, yawn, pace, abnormal body manipulation) /Individual Agonistic (displace, steal food, aggression)/individual Affiliative (contact, groom, social play, share food)/individual Increase for those closely bonded to the deceased, no change for others Increase for those closely bonded to the deceased, no change for others Increase Increase for those closely bonded to deceased, no change for others Increase for those closely bonded to the deceased, no change for others Increase Increase for all group members Increase between males Increase between females HYPOTHESIS SUPPORTED? No N/A Yes for immediate, no for overall Yes No Yes for immediate, no for overall Numerically yes for overall, yes for pace Numerically yes No 1

12 Methods Study Subjects and Housing The subjects of this study were the nine individuals in the Fummer colony of tufted capuchins (Sapajus apella) in the Franklin & Marshall College Vivarium. The colony contained six adult males and three adult females (see Table 2), all of whom were related through the matriline. The deceased individual, Izzy, was 13 years old at the time of his death. The colony was housed in an indoor enclosure with temperature regulated at 8 F (see Lonsdorf et al., 216 for a detailed schematic). They were maintained on an artificial sunrise/sunset light cycle, with light turning on gradually at 6 am and turning off gradually until 8 pm. The colony was provided a daily meal of Mazuri Primate Diet supplemented with fresh produce. Table 2. Demographic information for each of the study subjects. ID BIRTHDATE SEX AGE AT IZZY S DOMINANCE DEATH ON 6/9/17 RANK Casey 12/19/99 Male 17 High Dixie 12/27/8 Female 8 High Felix 6/11/3 Male 13 Low Gracie 1979 Female 38 Low Hector 1/25/7 Male 1 Low Jesse 2/27/2 Male 15 Medium Lucky 3/16/1 Female 16 High Marcel 4/95 Male 21 High Rusty 4/8/97 Male 19 Medium Behavioral Monitoring Protocol All behavioral and social information were obtained from ongoing behavioral observations on the colony. These observations were performed in a room adjacent to the colony s enclosure that was obscured by one-way glass, allowing researchers to observe the monkeys natural behavior (see Lonsdorf et al., 216 for a detailed schematic). Observations were completed by a team of researchers who had achieved.9 or higher on an inter-observer reliability test. Behavioral monitoring began in the fall of 215 and observations were collected at least once a week on every monkey (see Appendix Table A1 for a list of behaviors). Behavioral observations consisted of a ten-minute focal sample with state behaviors (behaviors of considerable duration; Altmann, 1974) recorded instantaneously every thirty seconds, along 11

13 with the focal individual s proximity to any conspecific within one meter s distance. The recipient of any social behavior was also recorded. Event behaviors (virtually instantaneous behaviors) were collected on an all occurrence basis, so that all instances of the given behavior occurring during the specified time frame were recorded (Altmann, 1974). Prior to each session, all activities concerning the monkeys within the last two hours were recorded (ex. cleaning, feeding, husbandry, enrichment, research, etc.), as well as recent time each capuchin spent inside their testing cubicles, which females were in heat, and any fights that occurred immediately before the start of the follow. Social Network Metrics In order to analyze social network changes in degree, strength, and cohesion, I constructed networks for both the six months prior to and the six months following Izzy s death, using UCINET software. Since the data used in this study was collected from multiple members of the same group whose interactions overlapped, the data violated the assumption of independence that is required by most traditional inferential statistics (Brent et al., 211). However, the UCINET program addresses this problem by using matrix correlations that are calculated directly from the observed datasets (Brent et al., 211), methods that previous researchers studying primate social networks have utilized (Seyfarth, 198; Silk, 1992). For this study, I constructed networks for two separate measures: (1) proximity (proportion of time spent within one meter s distance of one another) and (2) grooming (for both giver and receiver: number of instances of picking through someone else's fur or skin with fingers or mouth). Behavioral Metrics I used the behavioral monitoring data to measure changes in both social and anxietyrelated behaviors: (1) affiliative (positive interactions), (2) agonistic (negative interactions), and (3) anxiety (stress-related; see Table 2). In order to evaluate the transience of significant behavioral changes, I compared time periods for the six months prior to Izzy s death to the time periods following his death. First, for each individual, I assessed the amount of time engaged in affiliative and agonistic behaviors. Affiliative behaviors included grooming, contact, social play, and sharing food, while agonistic behaviors included displacement, stealing food, and aggression. Second, since the death of a close relative can be extremely stressful for individuals, I compared rates of anxiety-related behaviors. These included pacing, scratching, yawning, and abnormal body manipulation. These behavioral changes were compared to individuals bond 12

14 strength with the deceased (calculated from the social network analysis) to assess if bond strength was correlated with an individual s relative reaction to the death. Data Analysis I used SPSS version 24 for all statistical analyses. For the network metrics, changes in each individual s values of average dyadic strength and degree (for both the proximity and grooming networks) for the six months before and the six months after the death were assessed using Wilcoxon signed-rank tests. The Wilcoxon signed-rank test is a non-parametric alternative to the paired-samples t-test (Wilcoxon, 1945). I calculated each individual s average dyadic strength by the number of interactions that occurred between the dyad over the sum of the total number of interactions of each of the individuals in the dyad. I then averaged dyadic strengths for each individual. In order to determine changes in group cohesion, I calculated density (number of ties in the network/number of possible ties in the network), as well as the network s average degree (average of each individual s ties), for the six months before and the six months after Izzy s death. Additionally, I calculated the network s average degree and density for the two months immediately prior to the death and the two months immediately following the death. The combination of these analyses allowed for a qualitative assessment of the group s changes in cohesion. In order to analyze changes in the colony s percentage of time spent engaged in affiliative, agonistic, and anxiety-related behaviors, both before and after Izzy s death, I grouped the data into distinct time periods in such a way as to balance both the amount of time elapsed and the number of follows completed. These periods, 1 through 6, were as follows: 1) December of 216 and January 217, 2) February and March, 3) April, May, and the first week of June, 4) the remainder of June and July, 5) August and September, and 6) October and November. Izzy died in early June between the cutoff for periods 3 and 4. For each period, I calculated average rates of engagement in affiliative, agonistic, and anxiety-related behaviors across all group members. I then used a series of Friedman tests to compare the percentage of time the colony spent engaged in affiliative, agonistic, and anxiety-related behaviors for these time periods. The Friedman test is a non-parametric equivalent to the one-way repeated measures ANOVA used when the assumption of normality is violated (Friedman, 1937). If the Friedman test for a particular behavior was significant, I conducted a series of follow up Wilcoxon signed-rank tests to assess significant differences between particular periods. Additionally, Wilcoxon signed-rank 13

15 tests were performed to investigate changes in the rates of these behaviors during the entire six months before Izzy s death and the entire six months after. Results Social Network Changes Since two networks of differing sizes cannot be directly compared, I took two approaches to compare social network analyses to account for the colony s loss of a group member. The first approach normalized each individual s value of strength and degree by dividing each value by the number of individuals in the respective network minus one (x/(n-1); Borgatti et al., 213). The second approach removed Izzy from the pre-death network. This required the removal of all grooming and proximity measures concerning the deceased individual. In other words, this method effectively compared pre (six months before) and post-death (six months after) measures as though Izzy had never been a member of the colony. Since the results of both approaches closely reflected one another, I report only the results of the normalized approach here. In order to address my hypotheses regarding social and behavioral changes in individuals that were strongly bonded to the deceased, I first examined dyadic grooming and proximity strength to determine these individuals. A larger weight was given to grooming measures, as it is more predictive of bond strength than proximity. Only one individual, Gracie, was strongly bonded (.836 and.363 for grooming and proximity strengths respectively) to the deceased. The individual with the next highest bond was Marcel (.63 and.43) who was closely followed by Jesse (.59 and.11). Given that only one group member was strongly bonded to the deceased, I examined the associated hypotheses qualitatively rather than statistically. For the grooming networks (see Figures 1a and 1b), there was a statistically significant difference in total degree between the measures for the six months before death and the six months after death (z = , p <.5). However, there was not a significant difference pre and post-death for individual s average grooming strength (z = , p =.11; see Figure 3). There was very little change in the group s overall cohesion pre and post-death for both average degree (.444 compared to.472) and density measures (.49 compared to.59; see Table 3). However, there was a more defined increase in the group s overall cohesion between the period immediately preceding the death (Period 3) and the period immediately following it (Period 4) for both average degree (.156 compared to.25) and density (.17 compared to.31) measures (see Table 3). The only individual with a close bond to the deceased (see Figures 1a and 4a), 14

16 Gracie, experienced both an increase in grooming degree (.556 to.625; see Figure 2) and average grooming strength between the six months before and after the death (.16 to.23; see Figure 3d). Given the small size of the enclosure, there was no variation in degree for the proximity networks (see Figure 4a and 4b). Since all individuals were in proximity to all other individuals at least once during the six months before and after the death, proximity measures for degree were not meaningful, and were therefore excluded from further analyses. However, there was a significant difference in individuals average proximity strength for the six months before and after the death (z = , p <.1; see Figure 5). Gracie was among those who increased their average proximity strength following Izzy s death (.8 to.13; see Figure 5d). The colony s overall cohesion was consistent across pre and post-death networks for both average degree (1 compared to 1) and density (.111 compared to.125; see Table 3). However, there was a slight increase in the group s overall cohesion between the time period immediately preceding the death (Period 3) and the time period immediately following the death (Period 4) for both average degree (.333 compared to.417) and density (.37 compared to.52) measures (see Table 3). Table 3. Cohesion measures for grooming and proximity social network analyses. NETWORK Grooming Proximity COHESION MEASURE Average Degree Density Average Degree Density TIME RANGE PRE DEATH Pre vs. Post Death Period 3 vs. Period Pre vs. Post Death Period 3 vs. Period Pre vs. Post Death 1 1 Period 3 vs. Period Pre vs. Post Death Period 3 vs. Period POST DEATH Behavioral Changes Several behaviors occurred at frequencies too low to merit further analysis. These behaviors included: affiliative behavior: social play and sharing food, agonistic behavior: 15

17 stealing food, and anxiety-related behavior: abnormal body manipulation. I also excluded the displace behavior from analysis, as it was not integrated into the behavioral monitoring ethogram until May of 217. Therefore, the final analyses focused on grooming and contact for affiliative behaviors, aggression for agonistic behaviors, and pace, scratch, and yawn for anxiety-related behaviors. There was not a significant difference in either the colony s rate of overall affiliative behavior (X 2 (5) = 5.444, p =.364; see Figure 6) or in females rate of overall affiliative behavior (X 2 (5) = 4.333, p =.52; see Figure 7) between time periods. Rates of colony-wide affiliative behavior (z = -.59, p =.953) and female affiliative behavior (z = -1.69, p =.285) did not significantly change from the six months before to the six months after death. There was also not a significant difference between the colony s percentage of time engaged in aggressive behavior between periods (X 2 (5) = 4.394, p =.582; see Figure 8) or for the six months before and the six months after the death (z = -.533, p =.594). Although the rate of aggressive behavior for males did not significantly differ between periods (X 2 (5) = 4.396, p =.494) there was a numerical increase in aggression rate between the time period immediately before Izzy s death (Period 3; M =.37) and the time period immediately after his death (Period 4; M =.62; see Figure 9). There was not a significant difference between males rate of aggressive behavior for the six months before and after the death (z = , p =.173). Additionally, there was not a significant difference in the colony s rate of all anxiety-related behaviors between periods (X 2 (5) = 1.524, p =.62), although there was a numerical increase in these behaviors immediately before the death (Period 3: M =.125) and immediately after the death (Group 4; M =.15) that continued to increase in the following time periods (Group 5: M =.157, Group 6:.188; see Figure 1). Finally, there was not a significant difference in overall anxiety-related behaviors between the six months before and after Izzy s death (z = , p =.173). There was, however, a significant difference in the colony s percentage of time spent pacing across time periods (X 2 (5) = 27.94, p <.1; see Figure 11), as well as between the six months before and the six months after the death (z = , p <.1; see Table 4 for a summary). To further examine these changes, I conducted a series of Wilcoxon signed-rank tests using an alpha level of.17 to correct for multiple comparisons (Dunn, 1961). The rate of pacing significantly increased between periods 3 and 4 (z = , p <.17) and periods 3 and 6 (z = , p <.17); and marginally increased between periods 3 and 5 (z = -2.1, p =.36; see Figure 11). 16

18 Comparisons of Gracie s rates of affiliative, aggressive, and anxiety-related behaviors in the period immediately preceding (Period 3) and following Izzy s death (Period 4) revealed: 1) a decrease in her affiliative rate (.53 to.6), 2) no change in her aggression rate (. to.1), and 3) an increase in her anxiety rate (.74 to.121). 17

19 Table 4. Statistical results for all behaviors analyzed over time group and pre and post-death. BEHAVIOR Aggression Contact Groom Total Affiliative Pace Scratch Yawn Sum Anxiety BEHAVIORAL CATEGORY Agonistic Affiliative Affiliative Affiliative Anxiety Anxiety Anxiety Anxiety LEVEL SIGNIFICANT (YES/NO) TIME (PERIOD/PRE VS. POST) X 2 OR Z- VALUE Group No Period X 2 = Group No Pre vs. Post Z = Males No Period X 2 = Males No Pre vs. Post Z = Group No Period X 2 = Group No Pre vs. Post Z = Females No Period X 2 = Females No Pre vs. Post Z =. 1. Group No Period X 2 = Group No Pre vs. Post Z = Females No Period X 2 = Females No Pre vs. Post Z =. 1. Group No Period X 2 = Group No Pre vs. Post Z = Females No Period X 2 = Females No Pre vs. Post Z = Group Yes Period X 2 = Group Yes Pre vs. Post Z = Group No Period X 2 = Group No Pre vs. Post Z = Group No Period X 2 = Group No Pre vs. Post Z = Group No Period X 2 = Group No Pre vs. Post Z = P-VALUE 18

20 Discussion The current study examined both behavioral and social network changes in a colony of captive capuchins following the death of a group member. My findings generally supported the hypothesis that the colony s proximity and grooming social networks would change after the death of a groupmate. Overall, each individual s number of grooming partners (degree) increased despite the loss of a group member. Additionally, the results supported the hypothesis that no group-wide increase in grooming strength would occur. Instead, only the individual closest to the deceased experienced an increase in their frequency of grooming interactions. Gracie, Izzy s mother and only close bond, increased her grooming strength with almost all group members, except for the dominant males. Surprisingly, there was a group-wide increase in strength for the proximity networks. Prior to Izzy s death, Gracie s two closest bonds were to her son Izzy and another lowranking male, Hector. The subsequent increase in Gracie s grooming degree and strength following the death has two possible explanations. The first is well-documented in the primate thanatology literature, and posits that this increase in strength and degree is a result of compensation for the loss of a close bond. This explanation is supported by a study by Engh et al. (26), which revealed that female chacma baboons who lost a close relative to predation experienced a significant increase in glucocorticoid levels in the month following the death. However, by the second month, glucocorticoid levels in these females had returned to baseline levels, which was attributed to these females increasing their grooming degree and strength with other individuals (Engh et al., 26). It is therefore possible that Gracie compensated for the loss of this important bond by widening and strengthening her social network. However, a possible alternative explanation exists for the increase in Gracie s bond strength and degree. Throughout his life, Izzy demonstrated atypical physical features, nonstandard behaviors, and abnormal social interactions. Years of both anecdotal and behavioral data on the deceased individual revealed that he did not interact with other group members in a way that was characteristic of capuchin social relationships. These observations, coupled with unofficial vet diagnoses, postulated that Izzy might have had a genetic disorder comparable to that of autism in humans. As a result, he did not form strong social bonds with anyone other than his mother. It is therefore possible that Izzy s special needs were preventing Gracie from expanding her social network, and ultimately causing her to remain peripheral in the group. 19

21 These two hypotheses regarding the expansion of Gracie s social network are not necessarily mutually exclusive: it is possible that both explanations played a role in her increased sociality following Izzy s death. The other individual that displayed a dramatic increase in their number of grooming partners, as well as the strength of their bonds, was Dixie, a medium-raking and relatively young female. Since Dixie did not possess a bond with Izzy prior to his death, this increase in degree and strength is likely not a result of compensation for the loss. Instead, it can more likely be attributed to her transition into sexual maturity. This explanation is supported by the creation and strengthening of social bonds with mostly high and medium-ranking adult males (Figure 2b: (CA & DI), (DI & HE), (DI & MA)). I examined group-level changes in cohesion for the two months immediately preceding (Period 3) and following (Period 4) the death and found an increase in cohesion for both the grooming and proximity networks. However, despite these short-term increases in cohesion, the group s overall cohesion for both the grooming and proximity social networks did not increase when examining the entire six months following the death. This discrepancy in cohesion measures can likely be attributed to the transience of the group s response to Izzy s death. The results of this study did not support the hypothesis that affiliative behaviors would increase among females following the death of a group member (see Figure 9). In fact, females rate of affiliative behaviors experienced a fairly dramatic drop following the individual s death, which only returned to baseline levels four months later (see Figure 1). These findings were surprising considering the increase in both grooming degree and strength for two of the three females in the colony. However, it is possible that this decrease in affiliation may have been a result of decreases in male-female interactions rather than a decrease in female-female interactions. This explanation is made all the more likely considering the strong bond between Izzy and Gracie, and the total absence of Gracie grooming any individual in the few months immediately following Izzy s death. Interestingly, however, Gracie s grooming indegree (number of individuals who groomed her) following the death increased from zero individuals to four, which is reflected in her dyadic grooming strengths (see Figure 3d). That is, Gracie did not groom anyone in the first few months following the death, but considerably more individuals groomed her. The decrease in Gracie s grooming rate, coupled with her fairly dramatic increase in anxiety-related behaviors following the death is reflected in the human and nonhuman primate 2

22 literature. Among humans, social isolation and bereavement are associated with increases in stress hormones (Segerstrom & Miller, 24), but such stress responses are often mediated by social contact and affiliation, particularly among females (Sapolsky et al., 1997). In Gracie s case, the decrease in affiliative behavior is a result of the loss of an integral social partner. These changes coincided with an increase in anxiety-related behaviors, as well as the number of other individuals grooming her. The results of this study numerically supported the hypothesis that rates of aggression would increase among males after the death (see Figure 9). This effect was relatively long lasting, only returning to baseline levels four months later. These results are supported in the primate literature, which has found that aggressive behaviors in groups of captive lowland gorillas increased dramatically following the death of the groups silverback males (Hoff et al., 1998; Less et al., 21). However, it is difficult to ascertain if this increase in aggression in males is a form of bereavement or merely the result of shifting dominance hierarchies following the death of a male. Given the low rank of the deceased individual in this study, it is unlikely that his death was the cause of a shift in social hierarchy. However, this does not eliminate the possibility that this increase in aggression was a result of such a shift, especially considering the increase in rank of a previously medium-ranking male eight months after the death. Lastly, the results of this study numerically supported the hypothesis that anxiety-related behaviors would increase following the death of the group member (see Figure 1). In particular, the group s percentage of time spent pacing increased significantly following Izzy s death, and continued to increase throughout the following six months (see Figure 11). Examination of individual pacing rates revealed that this continued increase was driven by a combination of Felix, Jesse, Marcel, and Rusty. Although these individuals did not have a strong bond with the deceased, their increased rates of pacing could be attributed to shifts in the dominance hierarchy. All individuals were established as either low or medium rank in the months immediately surrounding Izzy s death. However, dominance testing completed in the spring of 218 revealed that Marcel s rank had increased to high. It is therefore possible that Marcel s shift in the dominance hierarchy affected the stress levels of other males, as he worked to increase his rank. This explanation might also explain the increase in dyadic strength in proximity for Marcel and Lucky, as Lucky is the alpha female of the group. 21

23 To date, very little research has been conducted on New World monkeys regarding behavioral responses to the death of an individual. The results of the current study revealed that group responses to the death of a group member included changes in the group s social network, as well as some behavioral changes. Considering the peripheral position of the deceased, these results imply that even the death of a less integral group member can impact the group s social network and behaviors. This study also demonstrates that the death of group member predominantly disrupts the behavior of those most closely bonded to the deceased. Gracie exhibited a dramatic increase in her anxiety-related behaviors following Izzy s death. The subsequent decrease in grooming of others in the months following his death contradicts the literature (see Engh et al., 26), and could therefore be symptomatic of a depressive state. It is also interesting to note the group s change in behavior towards Gracie immediately following the death, especially considering the nature of capuchin social relationships. As outlined in Fragaszy et al. (24), female-female grooming is generally reciprocal and female-male bonds are markedly asymmetrical with nonreciprocal female grooming of males. However, in the several months following Izzy s death, Gracie did not groom anyone but experienced a sizable increase in both the number of males and females that groomed her. One could therefore speculate that the group was aware of the substantial loss Izzy s death had on Gracie s life and was therefore attempting to support her during this difficult time. The work present here is among one of the first attempts in the field of animal thanatology to document group-level behavioral changes in response to a death. However, it is still not clear whether these changes in social relationships and behaviors are a result of grief or merely a product of the group readjusting to the loss of a group member. Such conclusions may be impossible to determine, as it is difficult to infer emotions, such as grief, in animals without anthropomorphizing. However, regardless of the explanation, the increase in anxiety-related behaviors after Izzy s death emphasizes the importance of monitoring these behaviors in captive primates. Documenting these group-level behavioral changes is therefore an important focus for future studies if we are to better understand the impacts of the death of a conspecific on primate group behavior and social networks. 22

24 Acknowledgments I would like to thank the entire primate research team over the past two years for their tremendous assistance during data collection. Further thanks is owed to Lillian Basom, Richelle Wagner, and the entire vivarium staff for their flexibility and assistance with this project, as well as their devotion to the monkeys. Many thanks go out to my Honors Defense Committee for their time and advice throughout this project. Lastly, thank you to Dr. Elizabeth Lonsdorf for fostering my love for research and for believing in me every step of the way. Without her, this project would not have been possible. This project is completed in loving memory of Izzy. References Allen, C. & Hauser, M. D Concept attribution in nonhuman animals: Theoretical and methodological problems in ascribing complex mental processes. Philosophy of Science, 58, Altmann, J Observational study of behavior: sampling methods. Behaviour, 49, Alves, F., Nicolau, C., Dinis, A., Ribeiro, C. & Freitas, L Supportive behavior of freeranging Atlantic spotted dolphins (Stenella frontalis) toward dead neonates, with data on perinatal mortality. Acta Ethologica, 18, Anderson, J. R., Gillies, A. & Lock, L. C. 21. Pan thanatology. Current Biology, 2, R349 R351. Anderson, J. R A primatological perspective on death. American Journal of Primatology, 73, Anderson, J. R Comparative thanatology. Current Biology, 26, R543-R576. Appleby, R., Smith, B. & Jones, D Observations of a free-ranging adult female dingo (Canis dingo) and littermates responses to the death of a pup. Behavioural Processes, 96, Bates L. A., Poole, J. H. & Byrne, R. W. 28. Elephant cognition. Current Biology, 18, Bercovitch, F. B Giraffe cow reaction to the death of her newborn calf. African Journal of Ecology, 51, Bezerra, B. M., Keasey, M. P., Schiel, N. & Souto, A Responses towards a dying adult group member in a wild new world monkey. Primates, 55,