The Social Behavior and Dynamics of Old Ring Tailed Lemurs Lemur

i
THE SOCIAL BEHAVIOR AND DYNAMICS OF OLD RING-TAILED LEMURS (LEMUR

CATTA) AT THE DUKE LEMUR CENTER
By
Kathleen Marie McGuire
B.S., Georgia Institute of Technology, 2014
A thesis submitted to the faculty of the University of Colorado in partial fulfillment of the
requirement for the degree of Master of Arts.
Department of Anthropology
2017
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This thesis entitled:

The Social Behavior and Dynamics of Old Ring-tailed Lemurs (Lemur catta) at the Duke Lemur
Center written by Kathleen Marie McGuire
has been approved for the Department of Anthropology
_____________________________________________________
Dr. Michelle L. Sauther (Committee Chair)
_____________________________________________________
Dr. Herbert H. Covert
_____________________________________________________
Dr. Joanna E. Lambert
Date
The final copy of this thesis has been examined by the signatories, and we
find that both the content and the form meet acceptable presentation standards
of scholarly work in the above mentioned discipline.
IACUC protocol # A168-14-07

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Abstract
McGuire, Kathleen Marie (M.A. Anthropology)
The Social Behavior and Dynamics of Old Ring-tailed Lemurs (Lemur catta) at the Duke Lemur
Center
Thesis directed by Professor Michelle L. Sauther
There has been little emphasis within primatology on the social and behavioral strategies
old primates might use to meet the challenges of senescence while maintaining social engagement,
such as assuming a group role like navigator. Understanding how old primates maintain sociality
can reveal how behavioral flexibility might have facilitated an increase in longevity within the
order. Using focal sampling of old (N = 9, 10+ years) and adult (N = 6, <10 years) Lemur catta at
the Duke Lemur Center, activity budgets, social interactions, and group traveling information were
recorded and compared from May to August of 2016. I found that both male and female old lemurs
maintained sociality in the group, with older females being more social than adults. I failed to
support the second hypothesis that older individuals would have a behavioral profile distinct from
adults. Finally, I found preliminary support that older females help care for a daughter’s offspring
in the form of carrying. These results indicate that social manifestations of age and senescence
depend on a myriad of factors such as environment, life history, and individual personalities. This
research also reveals the importance of decoupling ideas of chronological age, being an old
individual, with senescence because somatic decline depends on these other factors besides age.
Understanding these complex interactions is essential as we strive to define senescence and explore
how age has shaped evolutionary trajectories among primates.

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Dedication
This thesis is dedicated to “Mom” Syble Sweat, a primate grandmother who taught me the
importance of family and the pursuit of knowledge.
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Acknowledgements
First, I would like to thank my advisor Dr. Michelle Sauther for her patience and essential
support during all stages of this research and thesis. I would also like to thank Dr. Herbert Covert
and Dr. Joanna Lambert for their mentorship as I developed and executed this work. I am also
incredibly grateful to the Duke Lemur Center staff for permitting me to conduct my research. In
particular, I thank Dr. Sara Zher, Andrea Katz, Erin Shaw, and Dr. Erin Ehmke for their
unwavering enthusiasm and for providing essential information about the histories of these lemurs.
I am incredibly grateful to Dr. James Millette for taking the time out to discuss aspects of my data
collection, management, and analysis.
I would also like to thank my family Michael P., Michael C., and Oliver McGuire for their
love and support. I appreciate the many hours of conversation with Brittany Miles and Elizabeth
McMillian about statistics, old age, and writing that helped to foster this research and thesis.
Getting the opportunity to pursue my passion for primate social behavior would not have been
possible without Dr. Linda Green and Dr. Joe Mendelson and their research project at Zoo Atlanta.
Finally, thank you to Charles Hughes who endures my endless discussion of primates and their
social lives, while relentlessly encouraging me to pursue this work.
Funding for this study was provided by the University of Colorado, Department of
Anthropology and the University of Colorado Boulder Graduate School. This work would have
not been possible without the support of these institutions.

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Table of Contents
Chapter 1: Introduction ............................................................................................................... 1

Senescence .................................................................................................................................. 1
Why Studying “Old” Primates Matters ...................................................................................... 4
Old Social Involvement in Nonhuman Primates ........................................................................ 7
Individual Factors and Old Primate Social Behaviors .............................................................. 10
The Social Role of Older Primates ........................................................................................... 11
Lemur catta as a Suitable Model for Primate Aging ................................................................ 12
Studying Aging in Captivity ..................................................................................................... 13
Lemur catta Mortality at the Duke Lemur Center .................................................................... 14
Infants and Juveniles (Birth to 2 years) ................................................................................ 14
Adults (2-10 years) ............................................................................................................... 17
Old Adults (10+ years) ......................................................................................................... 18
Study Aims and Hypotheses ..................................................................................................... 19
Chapter 2: Methods .................................................................................................................... 21
Study Site .................................................................................................................................. 21
Study Animals........................................................................................................................... 23
Behavioral Methods .................................................................................................................. 23
Data and Statistical Methods .................................................................................................... 26
Chapter 3: Results ...................................................................................................................... 28
Degree of Sociality ................................................................................................................... 28
Proximity ............................................................................................................................... 28
Physical Contact ................................................................................................................... 29
Activity Budgets ....................................................................................................................... 31
Locomotion (Travel and Movement)..................................................................................... 31
Feeding and Foraging .......................................................................................................... 34
Resting .................................................................................................................................. 34
Frequency of Behaviors ............................................................................................................ 40
Agonistic Point Events .......................................................................................................... 40
Affiliative Point Events ......................................................................................................... 41
Grooming .............................................................................................................................. 42
Stink Fights ........................................................................................................................... 43
Vocalizations ......................................................................................................................... 44
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Individual Factors ..................................................................................................................... 46

Dominance Rank ................................................................................................................... 46
Social Roles .............................................................................................................................. 48
Case Studies .............................................................................................................................. 48
Aracus ................................................................................................................................... 48
Sprite ..................................................................................................................................... 50
Shroeder ................................................................................................................................ 50
Lilah ...................................................................................................................................... 51
The Other Individuals ........................................................................................................... 52
Chapter 4: Discussion ................................................................................................................. 54
Discussion of Results in Terms of Study Hypotheses .............................................................. 54
Decoupling Chronological Age and Senescence .................................................................. 54
Individual Variation and the Disposable Soma Hypothesis ................................................. 55
Primate Buffers against Senescence-Associated Mortality .................................................. 61
Captivity Caveats ...................................................................................................................... 64
Small Sampling Size and Limited Group Composition........................................................ 64
Reduction in Agonism among Individuals ........................................................................... 65
Conclusions .................................................................................................................................. 67
Bibliography ................................................................................................................................ 68
Appendix 1: Behavioral Definitions .......................................................................................... 78
Appendix 2: Sampling Schedule ................................................................................................ 85
Appendix 3: Pedigree Charts for Study Subjects .................................................................... 86
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List of Tables
Table 1. Previous Work on Aged Primate Sociality……………………………………………...8
Table 2. Cause of Death Information for Infants and Juveniles at the Duke Lemur Center…........16
Table 3. Cause of Death Information for Adults at the Duke Lemur Center……………………...17
Table 4. Cause of Death Information for Old Individuals at the Duke Lemur Center…………….18
Table 5. Study Animals………………………………………………………………………..…24
Table 6. Mean Physical Contact Time Comparison between Old and Adult Females with and
without Liesl and Infants…………………………………………………………………………29
Table 7. Female Individual Analysis of Physical Contact Time………………………………….30
Table 8. Mean Physical Contact Time Comparison between Old and Adult Males with and without
Liesl and Infants…………………………………………………………………………………30
Table 9. Locomotion, Travel, and Movement Comparisons between Adult and Old Females…...32
Table 10. Male Individual Analysis of Locomotion and Movement Times……………………...32
Table 11. Male Individual Analysis of Travel Times…………………………………………….33
Table 12. Locomotion, Travel, and Movement Comparisons between Adult and Old Males with
and without Aracus and Licinius included……………………………………………………..…33
Table 13. Female Individual Analysis of Feeding/Foraging Times……………………………...34
Table 14. Analysis of Old and Adult Female Total, Solitary, and Social Resting Times…………35
Table 15. Female Individual Analysis of Total Resting Time……………………………………35
Table 16. Female Individual Analysis of Social Resting Time………………………………….36
Table 17. Female Individual Analysis of Solitary Resting Time…………………………………37
Table 18. Female Individual Analysis of Solitary Resting Time Not In Proximity with at Least
One Group Member………………………………………………………………………………37
Table 19. Analysis of Old and Adult Male Total, Solitary, and Social Resting Times………….38
Table 20. Male Individual Analysis of Social Resting Time……………………………………..38

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Table 21. Male Individual Analysis of Solitary Resting Time…………………………………...39
Table 22. Analysis of Adult and Old Male and Female Total, Solitary, and Social Sleeping
Times……………………………………………………………………………………………..39
Table 23. Female Agonistic Event Counts Based on Act Initiated, Received, or Unknown……...40
Table 24. Female and Male Agonistic Event Counts Based on Act Initiated, Received, or
Unknown…………………………………………………………………………………………41
Table 25. Male Agonistic Event Counts Based on Act Initiated, Received, or Unknown………..41
Table 26. Female Affiliative Event Counts Based on Act Initiated, Received, or Unknown……41
Table 27. Male Affiliative Event Counts Based on Act Initiated, Received, or Unknown……….41
Table 28. Female Total Grooming Event Counts Based on Act Initiated, Received, or
Unknown…………………………………………………………………………………………42
Table 29. Male Total Grooming Event Counts Based on Act Initiated, Received, or Unknown…42
Table 30. Female Grooming (Unidirectional) Event Counts Based on Act Initiated, Received, or
Unknown…………………………………………………………………………………………43
Table 31. Male Grooming (Unidirectional) Event Counts Based on Act Initiated, Received, or
Unknown…………………………………………………………………………………………43
Table 32. Female Mutual Grooming (Bidirectional) Event Counts Based on Act Initiated,
Received, or Unknown…………………………………………………………………………...43
Table 33. Male Mutual Grooming (Bidirectional) Event Counts Based on Act Initiated, Received,
or Unknown………………………………………………………………………………………43
Table 34. Female Affiliative Vocalization Event Counts Based on Act Initiated, Responding, or
Unknown…………………………………………………………………………………………44
Table 35. Male Affiliative Vocalization Event Counts Based on Act Initiated, Responding, or
Unknown…………………………………………………………………………………………44
Table 36. Male and Female Affiliative Vocalization Event Counts Based on Act Initiated,
Responding, or Unknown………………………………………………………………………...44
Table 37. Female Alerting and Antipredator Vocalization Event Counts Based on Act Initiated,
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Table 38. Male Alerting and Antipredator Vocalization Event Counts Based on Act Initiated,
Table. 39. Social Ranks of Study Individuals……………………………………………………47
Table 40. Non-Maternal Carrying Behavior of Griselda…………………………………………48
Table 41. Male Individual Analysis of Social Proximity Time………………………………….49

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List of Figures
Figure 1. Infant/Juvenile Causes of Death……………………………………………………….16
Figure 2. Adult Causes of Death…………………………………………………………………17
Figure 3. Old Individual Causes of Death……………………………………………………….19
Figure 4. Map of the Duke Lemur Center’s Natural Habitat Enclosures………………………..22
Figure 5. Average Time Spent More Than Two Meters Away From Group Members…………28
Figure 6. Average Time Spent in Physical Contact with at Least One Group Member…………30
Figure 7. Average Time Spent in Physical Contact with at Least One Group Member Compared
between Old Males and Females…………………………………………………………………31
Figure 8. Percent Leading During Travel Between Old and Adult Individuals…………………46
Figure 9a. & 9b. Pictures of Lilah……………………………………………………………….51

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Chapter 1: Introduction
Senescence
As a species, humans are living longer. In 1955, the average life expectancy was 48, in
1995 it was 65 (WHO 1998). The World Health Organization predicts that human global life
expectancy is currently around 80 years old (WHO 2015). As older individuals continue to
represent more of the global population, understanding the aging process and the physical effects
that age can have on the body can facilitate efforts to improve the quality of life for older
individuals.
Old is a term used to describe a group individuals that have lived for a relatively long time
for their species. Therefore, being old is often based on the average or maximum life expectancy
of a species. The assumed state of an old individual is that they are aging or are experiencing
senescence. However, organisms such as some turtle species and naked mole rats exhibit little
evidence of physical aging (Finch 2009), indicating that some organisms can be old but not
necessarily be senescent. For the purposes of this study, I will use old to describe individuals
beyond the expected life span of wild lemurs (10-15 years). To date, very few wild ring-tailed
lemurs live beyond 15, and the majority disappear between 10-15 years of age (Bennett et al.
2016).
Senescence has been broadly defined as the phenotypic change in an animal associated
with advanced age (Monaghan et al. 2008). This change is typically connected with a decline in
somatic function, which theoretically should result in a reduction in fitness and an increase in both
extrinsic and intrinsic mortality. Extrinsic mortality is death as a result of environmental factors
such as predation and disease. For example, if an individual has a severe loss in hearing, they might
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not hear the call of a predator or the warning vocalizations of their social group and are not able to
evade capture and death. Intrinsic mortality is death as a result of physical and functional
degradation of an organism’s body. For example, if the cells in an individual’s heart stops working,
it can result in death due to cardiovascular failure. Because of this association between senescence
and higher rates of intrinsic and extrinsic mortality, the challenge becomes understanding why
natural selection would favor life history patterns that produce senescent individuals.
Three hypotheses seek to explain the relationship between senescence and fitness. The first
suggests that because individuals die as the result of extrinsic factors, selection declines with age
relative to that individual’s reproductive value (Haldane 1941, Medawar 1952). The second
hypothesis of antagonistic pleiotropy argues that particular alleles that confer benefits on survival
and reproduction early in life are favored by natural selection despite negative effects later in life
(Williams 1957). The third disposable soma hypothesis suggests that there are trade-offs between
reproduction and somatic maintenance that leads to a decline in function due to the accumulation
of damage in favor of resource allocation towards reproduction and support of offspring
(Kirkwood 1977, 2002, Kirkwood and Holliday 1979). Some research has supported the latter two
hypotheses of antagonistic pleiotropy and disposable soma (Kirkwood & Austad 2000, Wilson et
al. 2008). These hypotheses have been tested on a mechanistic level with observations of free
radicals, methylation patterns (Maegawa et al. 2017), and other factors affecting the life
expectancies of individuals (see Monaghan et al. 2008).
Though mechanistic-based studies are important to understand how senescence occurs on
a metabolic and cellular level, evolution does not occur in a vacuum but is shaped by the
ecological, environmental, and demographic context in which individuals live. Therefore, studies
of diverse taxa in the wild are essential when exploring these questions. Researchers have used a
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myriad of variables to operationalize senescence at the individual, population, and species scales,
which makes comparing senescence across taxa more challenging. Some researchers have defined
senescence as the decline in age-specific survival and fecundity (Galliard et al. 1994, Promislow
1991). Others have measured age at death as a means of measuring senescence, which does not
accurately account for sources of extrinsic mortality (Monaghan et al. 2008). One of the challenges
with using life-history variables to approximate senescence is that these variables can be affected
by other factors such as the environment in which animals live and, one would posit, social factors.
For example, Ricklefs and Cadena (2007) measured the relationship between fecundity and
longevity in captive mammals as a proxy for senescence but offered no extensive discussion about
the mechanistic means of how the captive environment tends to extend life in these populations.
To begin exploring these metrics, sources of mortality must be explored.
Other researchers have tried to create holistic metrics such as a physiological frailty index
(Antoch et al. 2017) to approximate the overall degree of physical senescence in individuals,
accounting for multiple age-correlated factors such as grip strength, red blood cell count, and
hemoglobin. These methods directly describe aspects of individual health and ways in which
physiological changes occur. Focusing on specific phenotypical manifestations of advanced age
can also provide a starting place for targeting specific genetic mechanisms for senescence. Such
direct measurements of health can also reveal how the environmental and ecological context might
affect senescence (Brownikowski et al. 2005). This lack of consensus regarding how researchers
describe and measure senescence impairs the ability to compare across taxa. Nevertheless, the
comparative method is a powerful tool to provide a means of understanding how animals differ in
their patterns of senescence and what factors have affected the evolution of senescence.
4
Age-associated decline can affect the behavior of an individual and can provide insight into
how these changes affect aspects of survival. Most research has looked at how age affects behavior
with respect to predation and foraging (Roach and Carey 2014). For example, research with horses
(Mota et al. 2005), fish (Reznick et al. 2004) and birds (Cosantini et al. 2008) indicates that older
individuals experience a reduction in athletic ability with age; this reduction can make older
individuals easier to catch by predator species and lead to higher mortality (Fuller and Keith 1980,
Slobodkin 1968). With respect to foraging, studies with birds (Catry et al. 2006, Lecomte et al.
2010) indicate that some species experience a reduction in efficiency years before death.
Therefore, older individuals might become less able to extract energy from the environment, which
can be determined based on behavioral observations.
Why Studying “Old” Primates Matters
The diverse taxa of the primate order generally are longer-lived for their body size
compared to other mammals (Charnov and Berrigan 1993, Jones and MacLarnon 2001). Being old
in the wild often is considered to be a disability that leads to rapid death (Nussey et al. 2013, Roach
and Carey 2014). However, senescence is present in a variety of wild taxa; a recent review (Nussey
et al. 2013) highlighted 340 studies of 175 animal species that showed signs of senescence in the
wild, not only indicating that wild individuals certainly experience senescence but also that the
relationship between advanced age and increased mortality is more complex. One possible means
of reducing the effect of disability or senescence is to flexibly modify behavior which is
characteristic of the primate order (Jones 2006). For example, impaired primates living with
reduced dentition (Millette et al. 2009) and congenital limb malformations (Turner et al. 2012)
learn to accommodate these physiological challenges and survive with their disabilities. Because
5
of their capacity to flexibly modify their behavior, primates might have a greater capacity to
accommodate senescence compared to other taxonomic groups.
Degree of sociality has been thought to explain possible differences in senescence among
taxa (Promislow 1991). The primate order is characterized by highly social species with most
living in social groups (Fleagle 2013). Therefore, comparison among primates could provide a
robust means of investigating how social factors might affect the evolution of senescence across a
broad range of ecological and environmental contexts. Evidence suggests that patterns of
senescence are less evolutionarily constrained, allowing for species to respond flexibly to forces
of evolution even at the population level (Bronikowski et al. 2011). Aspects of group living seem
favorable for increasing lifespans in taxa and possibly buffering against environmental challenges
through anti-predator behaviors, inherited dominance, and collective knowledge (Roach and Carey
2014). The primate order has also been of particular interest in exploring the roles of older
individuals in the social environment because intelligence in conjunction with sociality provides
both experience and wisdom to the group at large. In exploring how primates can inform larger-
scale patterns of senescence in the animal kingdom, we must first define what an old primate is
and what behavioral patterns characterize this cohort of individuals.
Defining Old Primates and Their Behavioral Profile
Primatologists have been classifying individuals as old for decades but lack a consensus
on a unified definition of what old actually is. The assumption of this classification is that there is
some delineation between a regular adult in the social group and an old individual. The implied
difference is that these older individuals are senescent, but research on primate gerontology is still
very much in its infancy and lacks a consensus on what exactly old is. The few studies that have
been conducted reveal this important problem associated with studying these older individuals
6
(Table 1.). Many researchers often used the third trimester of life (Corr 2000, McDonald 1988,
Taylor 2008). Others use the age at which females experience a decline in fecundity (Kato 1999).
One study (Almeling et al. 2016) even used the inability to get a peanut out of a tube as indicative
of functional decline that meant a primate was old. Therefore, it is essential to explore the behavior
of old primates so that a concrete and standard definition of old can be established.
To distinguish old individuals as a distinct life history cohort, we need to achieve a better
understanding of what aspects of senescence are used to define this cohort as old. Use of the last
trimester of life standard accounts for chronological but not physical age. This standard assumes
that all individuals in the last trimester of life are experiencing senescence equally, which is not
the case in different environments. For example, across a range of ages the ring-tailed lemurs at
the Bezà Mahafaly Special Reserve experienced severe dental wear and loss based on utilization
of the tamarin fallback food (Cuozzo and Sauther 2006). These results indicate that aspects of
physiology might appear to be experiencing decline well before an old age, depending on the
environment. Therefore, it becomes important to establish a clear definition of old with a more
detailed perspective of physiology so that we have an understanding of what normal, both
behaviorally and physiologically, looks like in this age cohort. Furthermore, establishing the old
profile enables researchers to clearly determine pathological conditions that deviate from the old-
age norm.
The majority of social and behavioral studies addressing questions of aging in primates are
with species of macaque (Table 1). Establishing a “primate pattern,” if possible, with respect to
the behavior of old individuals must incorporate other species besides macaques because primates
exhibit a large range of behavioral and phenotypic plasticity. Defining an old behavioral profile
based primarily on macaque research would not adequately represent patterns for the whole order,
7
and if researchers are to compare primates to other groups, a more representative sampling of
primate behavioral and social gerontology much be conducted.
Old Social Involvement in Nonhuman Primates
One key way that researchers have expected primates to modify their behavior to
accommodate the challenges of senescence is to reduce their degree of sociality. Informed by
disengagement and activity theory from human social gerontology (Achenbaum and Bengtson
1994, Cumming and Henry 1961, Lemon et al. 1972), early studies on the social engagement of
older primates predicted that these individuals would withdraw from the social group due to the
physiological demands of aging. Theories of disengagement imply that social behaviors are less
essential and might be reduced to allow for greater time spent on essential behaviors such as
foraging and predator avoidance. The majority of studies on social gerontology have used macaque
species as study subjects and have focused primarily on captive populations (Table 1.). The results
of these studies have provided little support for social disengagement in older primates. Work with
female Japanese and stump-tailed macaques found that older individuals spent significantly less
time interacting socially compared to younger individuals (Hauser and Tyrell 1984, Nakamichi
1984, Nakamichi 1991). Kato (1999) validated these results but also found that individual
differences in the social behavior of aged Japanese macaque females were dependent on factors
such as individual rank and season. Other research with Japanese (McDonald 1988) and rhesus
macaques (Williams 1982) found no indication of social withdrawal but rather more time spent
resting. More recent work (Almeling et al. 2016) with Barbary macaques found that older
individuals are more interested in their social environment compared to younger individuals.
8
Table 1. Previous Work on Older Primate Sociality. Adapted from Table 1.1 in Corr (2000) and
updated with current literature. *Indicates experimental studies.
Study
# of Period/Data Definition Basis for
Citation Species Subjects Sex Amount of Old Definition of “Old”
Williams L. Rhesus
(1982) Macaque 18 F 7 months Unknown Unknown
Fitts S. Rhesus
(1982) Macaque 10 F 8 hours 25+ years Unknown
Nakamichi Japanese Estimation of senility in
M. (1984) Macaque 14 F 4 months 20+ years Itoigawa (1982)
Maximum lifespan in
Hauser et al. Japanese captivity and physical
(1984) Macaque 18 F 2.5 months 18+ years characteristics
Maximum lifespan in
Hauser et al. Stumptail captivity and physical
(1984) Macaque 14 F 3 months 18+ years characteristics
McDonald Japanese
M. (1988) Macaque 40 F 15 months 20+ years Third trimester of life
Huffman, M.
(1990) Chimpanzee 9 F&M 10 months 41+ years Unknown
Nakamichi Japanese
M. (1991) Macaque 23 F 230 hours 20+ years Hauser et al. (1984)
Lipold et al. Rhesus
(1992) Macaque 12 F 3 months Unknown Unknown
Picq J. Grey Mouse
(1992) Lemur 12 F&M 2 months 9+ years Unknown
Parks K. Rhesus
(1993) Macaque 7 F 15 years Unknown Unknown
Soumi et al. Rhesus 16-20
(1993) Macaque 8 F&M 15 years years Unknown
Veenema et Long-tailed Prior studies in cognitive
al. (1997) Macaque 35 F&M 485 hours 14+ years decline in this species
Taylor L.
(1996) Lemurs 34 F&M 540 hours 18+ years Last trimester of life
Kato E. Japanese
(1999) Macaque 16 F 383 hours 21+ Decline in fertility
Baker K.
(2000) Chimpanzee 34 F&M 240 hours 30+ years Unknown
Corr J. Rhesus
(2000) Macaque 49 F&M 627 hours 20+ years Last trimester of life
Veenema et Long-tailed Prior studies in cognitive
al. (2001) Macaque 55 F 485 hours 14+ years decline in this species
Nakamichi Japanese Behavioral findings of this
M. (2003) Macaque 85 F 261 hours 15+ years study
Inability to get peanut out of
Almeling et Barbary tube; offer no discussion of
al. (2016)* Macaque 118 F&M N/A 19+ years this benchmark
Ryu et al. Bonobos
(2016) Chimpanzee 14 F&M 4 months 40+ years Distance while grooming
9
Physiological challenges such as a reduction in hearing, cognition, and even eyesight can
possibly impair a primate’s ability to function in the social group. Yet, rather than distancing
themselves from the group, many aged primates learn to accommodate these physical challenges.
As noted previously, older bonobos suffering from long-sightedness tend to groom at farther
distances away from the receiving individual than younger bonobos (Ryu et al. 2016). If aged
primates are behaviorally accommodating the challenges of senescence, theoretically the profile
of their social behavior should be distinct from younger individuals.
Social contact time can be described as the duration an individual spends engaged in a
specific behavior involving another member of the group like grooming and social resting. Other
researchers (e.g. Corr 2000, Taylor 2008) have used proximity to individuals as a metric for social
contact as well. Behavioral frequencies are how often an individual engages in a particular
behavior. Directionality, such as initiating or receiving grooming behavior, is also measured to
determine if old individuals are passively or actively maintaining sociality. For example, an
individual who only receives grooming approaches from other individuals might be maintaining
passive social engagement. Notably among the frequency analysis, previous work with aged
female Japanese macaques suggests that old individuals might use affiliative vocalizations to
maintain social relationships with unrelated individuals at lower energetic costs (Mitani 1986).
Recent work (Kulahci et al. 2015) suggests that ring-tailed lemurs utilize this strategy to groom
other individuals at a distance. Therefore, aged lemurs might use vocalizations to maintain
sociality at a lower energetic cost to themselves.
The Biology of Aging in Primates
Older primates must accommodate the challenges associated with physiological decline as
they age, which might hinder their involvement in the group, requiring them to modify their
10
behavior to maintain social engagement. Therefore, while I do not directly measure aspects of
physiology in this study, understanding the physiological context of age is also important in
characterizing the old behavioral profile of these primates. One of the key debates in the
physiology of aging is the frequency of reproductive senescence that is observed in human females.
Many individuals may reach an age that leads to a decline in fecundity (Kato 1999, King et al.
2005, Parga and Lessenau 2005, Wright et al. 2008,), but few exhibit complete reproductive
termination (Pavelka and Fedigan 1999) with a post-reproductive lifespan.
Some studies have also found age-related decline in other physiological systems besides
reproduction. Among lemurs in particular environments, age-associated tooth wear has been found
(Cuozzo and Sauther 2006, King et al. 2005), but many of these species utilize behavioral strategies
to accommodate this dental wear and loss and are able to survive for many years despite these
impairments (Cuozzo and Sauther 2006, Millette et al. 2009). Research with bonobos (Ryu et al.
2016) indicates that, during grooming, older individuals will have a greater distance between their
fingers and their eyes, indicating that these individuals are long-sighted. Hearing loss and loss of
eyesight in older hanuman langurs also has been seen (Borries 1988). Other researchers have
documented a reduction in cognitive function among macaques (Corr et al. 2002, Veenema 1997,
2001). Learning how old primates navigate these biological challenges can not only provide insight
into the methods of accommodating disability but also how these adjustments could have
facilitated the selection for longer lifespans in the primate order. Once again, characterizing the
normal behavioral profile for wild species also allows for researchers to identify pathology in an
individual or a population (Singleton et al. in press).
Individual Factors and Old Primate Social Behaviors

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Individual-specific factors such as sex, dominance rank, membership in a dominant
matriline, and reproductive history may influence the social behavior of old primates. Early work
in social gerontology expected the social behavior of old primates to look generally the same.
Notably, many of the studies investigating primate social gerontology have only focused on
females of particular species. In contrast, studies that compared the social engagement of older
males and females have found differences between the sexes. Older female rhesus macaques spend
less time in social contact compared to younger females, while aged males spend more time
compared to younger males, suggesting that there is not a species-specific strategy to
accommodating the challenges of senescence but sex-based strategies might exist (Corr 2000).
Kato (1999) was one of the first researchers to find that sociality varied not only with age but also
with dominance rank and season in Japanese macaque females. Nakamichi (2003) found that high-
ranking old female Japanese macaques received grooming from unrelated individuals at the same
frequencies as younger high-ranked females, while lower-ranked females mainly associated with
kin during grooming. Studies of captive lemurs also found sex differences in the social engagement
of old individuals but documented the opposite of what has been found in macaques: older males
were more socially withdrawn than older females (Taylor 2008). Importantly, in this study, aged
females maintained their dominance over males, indicating that female dominance in lemur species
does not change with increased age. The sex differences in social engagement could be the result
of both female dominance in lemur species and the fact that males do not remain in their natal
groups after reaching sexual maturity. Female individuals have more experience and kin
relationships to facilitate their continued sociality compared to male individuals. These findings
reveal that aged social strategies seem to differ based on dominance rank and perhaps other factors.
The Social Role of Older Primates

12
One of the strategies old primates might utilize to maintain sociality is to assume a specific
role in the social group. Research with other long-lived mammals has indicated that older females
assume important roles based on their prior experiences. In killer whales, post-menopausal females
will lead their social group to food resources during times of scarcity (Brent et al. 2015). Old
female elephants are more sensitive to predatory threats, presumably based on their experience,
and are able to protect their social groups (McComb et al. 2011). In primates, older members might
fulfill specific roles in the social group like aunt, grandmother, or group navigator (Maxim 1979).
It has even been suggested that a post-reproductive lifespan in females could have evolved so a
mother could care for a daughter’s offspring and increase her own reproductive success (Hawkes
et al. 1997). While this “grandmother hypothesis” continues to be debated, some work with langurs
have found support that older females will aid grandchildren in a facultative manner, when the
cost is low and the likelihood of aggression is minimal (Borries et al. 1991). Research in wild
populations of L. catta (Soma et al. 2012) and macaques (Wooddell et al. 2016) have shown that
the death of an old “grandmother” in a social group leads to social instability.
Lemur catta as a Suitable Model for Primate Aging
L. catta (ring-tailed lemur) are strepsirrhine primates endemic to southwestern
Madagascar. They have relatively long life-spans in the wild (up to 15 years of age, Sauther
unpublished data). They live in large (up to 30 individuals) multi-male, multi-female groups, with
minor sexual dimorphism between males and females (Kappler 1990, Cuozzo unpublished data).
This study species provides an important context to explore questions of social gerontology
because of the complexity and dynamic nature of their social groups (Sauther et al., 1999). L.
catta’s lack of body size sexual dimorphism, like many other strepsirrhines, helps to weigh the
trade-offs between reproduction and somatic maintenance between the sexes with more ease
13
because males do not seem to be allocating more resources to large increases in body size like
those observed in anthropoid primates (Kappler 1990). Additionally, they exhibit true female
dominance over males in both feeding and non-feeding contexts (Sauther et al. 1999). Kin-based
group living can provide the asset of inherited status that can increase the survival of an individual
such as matrilineal rank and dominance (Odling-Smee et al. 2003). The context of female
dominance in L. catta provides a concrete means of investigating the relationship between kin-
based and inherited advantages and aging. Results could also inform social behavior before the
rise of catarrhine primates which can identify possible behavioral patterns that could be deeply-
rooted in the primate order.
Studying Aging in Captivity
With more individuals in captivity representing the older age cohort, it is also important to
characterize what the social needs of these primates are. For example, in captive chimpanzees,
older individuals displayed lower levels of activity and object manipulation but still maintained
social engagement with others (Baker 2000). Practices of placing older individuals into smaller
social groups or even alone in captivity might be counterproductive for their wellbeing. Therefore,
understanding what the social needs are of aged individuals can improve husbandry efforts to help
maintain healthy populations in captivity.
Besides the direct implications of husbandry research, captive populations provide an
important context in which to study the social and physiological effects of aging to further
conservation efforts. These environments generally lead to a reduction in extrinsic mortality due
to the access to medical care and resources as well as lower rates of predation, although this will
vary depending on their housing conditions. As a result, mammals tend to live longer in captivity
(Lemaitre et al. 2013, Tidiere et al. 2016) with a large percentage of captive populations consisting
14
of old individuals. As ring-tailed lemurs in the wild are suffering reductions in population numbers
in areas where good census data is available (Gould and Sauther 2016; LaFleur et al., 2016), it
becomes even more essential to preserve the captive populations with the hope of potentially re-
establishing wild populations and maintaining genetic diversity in the species. Therefore,
understanding not only the social context of aging for these captive populations but also sources
of mortality for old individuals is also crucial for successful husbandry and conservation of this
species. If captivity helps to reduce the impact of extrinsic sources of mortality, the question
becomes what leads to mortality in these environments?
Lemur catta Mortality at the Duke Lemur Center
To explore the question of how do old lemurs die in captivity, I utilized Duke Lemur Center
(DLC) records to find trends in mortality of ring-tailed lemurs. I classified the deaths of 126
individuals into categories based on the reported cause of death information from the records
keeper (Zher 2017). I then divided these individuals into three age categories: Infant/Juvenile (0-
2 years old), Adult (2-10 years old), and Old (10+ years old). In this study, an individual was
considered old based on the tendency of wild L. catta individuals to disappear between 10-15 years
of age (Bennett et al. 2016). It should also be noted that ring-tailed lemurs experience a decline in
fecundity after the age of ten in captivity (Parga and Lessnau 2005). Because of the smaller sample
sizes, I did not conduct a formal statistical analysis, but I do report percentages based on general
classification of cause of death. The “other” category includes causes of death that occur only one
time in the data sample. Examples would include deaths due to infection, pneumonia, and
pneumothorax.
Infants and Juveniles (Birth to 2 years)

15
The majority of the individuals in the data set died between birth and two years of age at
the DLC (N=91). Of these deaths, 35% in this age range (Table 2) are categorized as missing from
the enclosure and were not seen again (Figure 1). DLC records (Zher 2017) indicate that many of
the deaths classified as missing are probably due to predation, but other sources of mortality cannot
be ruled out. At Berenty Reserve, 20% of infants were reported missing within the first month and
50% within the first year with little clear cause of death (Nakamichi et al. 1996).
Of deaths in this age category 23% are due to trauma, with 3% of these trauma-related
deaths resulted from injuries related to a fall and 2% based on injuries related to predation. Records
also note that the other 18% of trauma-related deaths are most likely the result of falls, predation,
or injury due to group conflict. Many infant deaths at the DLC have been tied to bite wounds and
other injuries sustained from group conflict, with younger mothers having a significantly higher
likelihood of losing infants to bite wounds (Charpentier and Drea 2013). According to DLC
records (Zher et al. 2014), the youngest maternal age of conception for a ring-tailed lemur was
1.34 years; this youngest mother was one of the individuals in this study (Liesl), who is still alive.
However, 52.94% of infants, where maternal age at conception was less than two years old, died
within the first year. In the wild, very few females at Berenty Reserve (Koyama et al. 2001) and
no females at Bezá Mahafaly Special Reserve (Sussman 1991) give birth at two years of age.
Therefore, while infant mortality among these extremely young ring-tailed lemur females is still
high, these findings also suggest that the captive environment allows for an earlier age at
parturition than in the wild, perhaps due to nearly-unlimited food resources.

16
Table 2. Cause of Death Information for Infants and Juveniles at the Duke Lemur Center.
*Deaths due to “Other” include aspiration of stomach contents, moderate focal cardiomyocyte
degeneration, and heart-interventricular septal defect.
Cause of Death Subset Count Percentage
Missing 32 35.17%
Trauma Total 21 23.07%
From Fall 3 3.30%
Predation 2 2.20%
Euthanized Total 8 8.80%
Euthanized due to Trauma 6 6.60%
Unknown 10 10.99%
Infection 2 2.20%
Stillbirth 10 11.00%
Failure to Thrive 3 3.30%
Premature 2 2.20%
Other* 3 33.33%
Infant/Juvenile Causes of Death

2.20%
3.30%
3.30% Missing
Trauma
11.00% Euthanized
2.20% 35.17%
Unknown
Infection
10.99%
Stillbirth
Failure to Thrive
8.80%
Premature
23.07%
Other
Figure 1. Infant/Juvenile Causes of Death. These percentages represent cause of death

information for 91 individuals from the Duke Lemur Center.
17
Adults (2-10 years)
Among adults (N=18) with recorded deaths at the DLC, 44.44% died due to trauma
(Figure 2) with 13% of these deaths being from injuries sustained from a fall or from predation
(22.22%). More individuals in this age category were euthanized (16.67%) compared to infants.
Table 3. Cause of Death Information for Adults at the Duke Lemur Center. *Deaths due to
“Other” include pneumonia and pneumothorax.
Cause of Death Subset Count Percentage
From Fall 2 11.11%
Predation 4 22.22%
Due to
Infection 1 5.56%
Unknown 3 16.67%
Cardiac-Related
Death 2 11.11%
Other* 2 11.11%
Adult Causes of Death
11.11%
Trauma
11.11%
Euthanized
44.44%
Unknown
16.67% Cardiac-Related Death
Other
16.67%
Figure 2. Adult Causes of Death. These percentages represent cause of death information for 18
individuals from the Duke Lemur Center.
18
Old Adults (10+ years)
The oldest male in this data set was 31, and the oldest female was 26. Among aged
individuals (N=17), a little less than half (41.18%) (Table 4) had to be euthanized (Figure 3) due
to a broad range of causes such as stroke, paralysis, and renal failure. Two lemurs (11.76%) died
from pneumonia. Importantly, death related to predation is not as prevalent as the other age cohorts
discussed. Though the sample size is small, it appears that old ring-tailed lemurs at the DLC die
from causes that often are seen in modern, old humans such as stroke, pneumonia, and organ
failure. In 2015, the leading causes of death in the United States of individuals above 65 years old
were heart disease, cancer, chronic low respiratory disease, and cerebrovascular causes like stroke
(National Center for Health Statistics 2016). If lemurs are dying of old age in this captive setting,
the question becomes how does the physiological effects of old age impact these lemurs socially
and what strategies do individuals use to navigate this landscape. Perhaps, there are aspects of the
ring-tailed lemur social environment that helps to accommodate these old lemurs.
Table 4. Cause of Death Information for Older Individuals at the Duke Lemur Center.
*Deaths due to “Other” include unknown cause of death, infection, multifocal acute hemorrhage,
and shock.
Cause of
Death Subset Count Percentage
Due to Cardiac Failure 2 11.77%
Due to predation 2 11.77%
Pneumonia Total 2 11.76%
Other* Total 4 23.53%
19
Old Individual Causes of Death
23.53%
Euthanized
41.18%
Pneumonia
Trauma
Other
23.53%
11.76%
Figure 3. Old Individual Causes of Death. These percentages represent cause of death
information for 17 individuals from the Duke Lemur Center.
Study Aims and Hypotheses
The primary goal of this study was to characterize the social behavior of old ring-tailed
lemurs at the Duke Lemur Center. Based on reviews of the literature on primate aging, I developed
the following research questions:
1. Do older individuals of both sexes maintain sociality with increased age?
2. Accounting for individual factors such as rank, reproductive history, and number of
offspring, is the social behavior, measured by time budgets and frequency of
behaviors, of aged individuals distinct from younger groups?
3. Do older individuals exhibit specific social patterns indicative of roles such as
grandmother or group navigator?
To address these questions, I tested the following hypotheses:

20
1a. Old individuals will exhibit levels of sociality, measured by time and frequency of
social behaviors, similar to those of other age groups.
1b. Old females will exhibit higher levels of sociality in the group compared to old males.
2. The social behavior of older individuals will be distinct from those of younger age groups
to behaviorally accommodate the somatic challenges of old age.
i. Older individuals will spend more time resting than younger individuals.
ii. Older individuals will initiate social interactions less frequently than younger
individuals.
iii. Older individuals will vocalize for affiliative purposes more frequently than
younger individuals to maintain social relationships using less energy.
3. Old individuals will exhibit specific behavioral patterns indicative of social roles.
i. Old individuals will lead during group travel with a higher frequency than
adults. This behavioral pattern is indicative of a group-navigator social role.
ii. Old females will carry related infants at a higher frequency than other non-
maternal kin. This behavioral pattern is indicative of a grandmother or aunt
social role, depending on the kin relationship.

21
Chapter 2: Methods
I observed six groups of ring-tailed lemurs at the Duke Lemur Center for an 11-week period
from May to August 2016 to compare the social behavior of old and adult individuals. Early on in
the study, one of the groups (occupying NHE2) was removed from the sample due to illness.
Study Site
The Duke Lemur Center (DLC), formerly the Duke Primate Center, consists of nine natural
habitat enclosures (NHEs) within the Duke Forest in Durham, North Carolina, United States of
America (Figure 4). Each NHE is surrounded by a 1.8-meter-high chain link fence with additional
electronet fencing to prevent animal escapes. Additionally, the land 15 feet from the fence has
been cleared of vegetation to discourage leaping from the trees into areas outside of the enclosure.
Subjects were only observed when they had free-ranging access to the forest enclosure. Individuals
also had access to an indoor enclosure, outdoor enclosure, and an outdoor hallway that leads to the
NHE. Individuals were primarily observed in the natural habitat enclosures.
Free-ranging groups were provisioned once daily at a designated feeding site with
commercial primate chow and fruits and vegetables occasionally. Food items were scattered
widely at the feeding site to reduce aggressive encounters over food. The study subjects also had
access to bowls of water located around the enclosure which were replenished twice daily by DLC
husbandry staff. The study subjects would also supplement their diet from the variety of vegetation
growing in the enclosure. They were observed to eat an array of fruits, flowers, leaves, soils, and
insects in the enclosure. Other researchers (Taylor and Sussman 1985) have also observed lemurs
at the DLC eating bark, fungi, and herbs in the enclosure.

22
conducted with ring-tailed lemur groups living in NHEs 3,4,7,8, and 9. Map was obtained from
Figure 4. Map of the Duke Lemur Center’s Natural Habitat Enclosures. This study was
Gates
NHE 5
(3.0 hectares)
NHE 3
(0.8 hectares)
2 5 2
Miaro
NHE 4 Nocturnal Building
(5.8 hectares)
Tour Path
Getty
Triplex
Lemur Landing
NHE 6
the DLC Researcher’s Manual (Ehmke et al. 2016).

NHE 1 (1.7 hectares)
(0.2) Main Building
NHE 2
(3.3 hectares)
Parking Lot
NHE 9
(1.4 hectares)
Gates
Cabin Aty-Ala
NHE 7
NHE 8 (2.4 hectares)
Wes’s Shop (2.7 hectares)
23
Study Animals
When observations began in May of 2016, the sample population consisted of six groups
and a total of 19 individual lemurs. This period of time did not include the breeding season, which
at the Duke Lemur Center is between November and February (Drea 2007). This population was
selected based on which ring-tailed lemur individuals were free-ranging during the study period.
However, during the third week of data collection, one of the groups (from NHE2) had to be
quarantined due to illness, and the group was removed from the study. Therefore, a total of 15
lemurs, nine of which were considered old (>10 years of age) and six of which were considered
adults (2-9 years of age) were observed for the purposes of this study. This sample consisted of
individuals from five groups ranging in size from two to six individuals (Table 5.). All individuals
were identified using a combination of collars and physical features and all were born in captivity.
Each of the groups shared the NHE with groups of other lemur species, with which the
ring-tailed lemurs sometimes interacted. Several of the enclosures also shared a common fence
line where individuals could see adjacent groups but could not make physical contact with them
due to several meters distance between fences. Furthermore, local fauna such as red foxes (Vulpes
vulpes), raccoon (Procyon lotor), and black rat snakes (Panthrophis obsoletus) were occasionally
seen in the NHEs.
Behavioral Methods
Focal sessions were recorded using an Acer tablet personal computer (Acer America, San
Jose, California, USA) programmed with Boris for Windows software with the pre-loaded
ethogram (Appendix 1) of behaviors (Behavioral Observation Research Interactive Software,
Torino, Italy) (Friard and Gamba 2016). A Livescribe Echo Smartpen (Livescribe, Inc., Oakland,
California, USA) was also used to audio record vocal notes, including leading behaviors,
24
miscellaneous information, and to prevent loss of detail. Audio files were transcribed and used to
provide more detail and context to the recorded activity budget files. I spent the first four days of
the study refining my ethogram and data recording methods before beginning data collection for
thesis research.
Table 5. Study Animals. Code represents the four-digit number assigned to the lemurs at the DLC
at birth. Total Offspring indicates the total number of offspring that the lemur had. Surviving
Offspring indicates the number of offspring that are still alive. Family trees of the study animals
can be found in Appendix 3.
Birth Age Total Surviving
Code Sex Name Date (yrs) Category Offspring Offspring Descriptors
NHE3 (Group 2)
6534 M Aristides 3/21/1993 23.13 O 0 0 chubby
6711 F Sosiphanes 4/13/1997 19.07 O 4 2 black collar
6857 F Lilah 3/28/2005 11.11 O 0 0 gimpy arm
NHE4 (Group 3)
black RC
6440 M Aracus 5/23/1991 24.96 O 16 14 .175
6956 F Shroeder 3/22/1992 24.13 O 2 2 very large
6957 F Liesl 7/15/2008 7.81 A 6 6 mid shave
base shave;
7087 F Gretl 4/9/2012 4.07 A 0 0 no tail tip
7239 F Hedwig 3/28/2016 0.1 I 0 0 lighter color
7240 F Griselda 3/28/2016 0.1 I 0 0 darker color
NHE7 (Group 4)
2 colored
6909 F Sierra Mist 5/1/2008 8.01 A 0 0 eyes
6835 M Berisades 3/28/2004 12.11 O 0 0
NHE8 (Group 5)
orange RC
6528 M Licinius 3/17/1993 23.15 O 0 0 .614
6831 F Tellus 3/18/2004 12.13 O 0 0 teal RC .545
NHE9 (Group 6)
6863 F Sprite 3/17/2001 15.14 O 13 13 short tail
orange RC
7084 M Jones 3/17/2012 4.13 A 0 0 .714 w/tag
black RC
7086 M Stewart 3/30/2012 4.1 A 0 0 .654
7176 F LuLu 3/19/2014 2.13 A 0 0 mid shave
25
A total of 637 data files (318.5 hours) were generated, each representing one 30-minute
focal session. In the final analysis, 560 files were analyzed, representing 280 hours of observation.
77 data files were not included in the analysis because the group was removed from the sample
due to illness (NHE2) or the focal follows were incomplete in duration. Because of the inequitable
ratio of old and young adult lemurs, less time was spent following each old individual (15 hours)
compared to young individuals (23 hours), but the total amount of time spent observing individuals
from each age group was approximately the same (Old: 139.5 hours, Adults: 140.5 hours).
At the beginning of sampling, I randomly assigned social groups to particular days using a
random number generator. A day of data collection was seven to eight hours of data collection,
while a half-day was three to four hours of data collection. When the NHE2 was removed from
the sample, I randomly reassigned the sampling schedule due to the reduction in sample size,
particularly in the young age group (Appendix 2). Due to husbandry practices at the DLC, it
sometimes became necessary to switch the group I was following or cease following a particular
group. If this occurred, I followed the social group randomly assigned to the next day of
observation and picked up the prior group the next day they were free-ranging again. On several
occurrences, I followed groups for only a half a day but did my best to make sure that groups were
sampled at different times of the day. A nonrandom sampling strategy was utilized to maintain an
equitable number of observations between old and adult individuals. A focal follow was terminated
and removed from analysis if the individual was out of view for more than ten minutes. When
possible, I avoided repeat observations of the same individual, trying to make sure that at least one
observation period separated these focal follows. However, in the smaller social groups, repeat
observations of the same individual were recorded if the other group members were not found.
26
For each observational period the following data were recorded: focal animal ID,
observation time, behavioral state, behavioral direction, social partner ID, number of individuals
within two meters of focal animal, and notes collected ad libitum. Behavioral direction indicated
if a particular behavior was initiated by the focal individual or received from another member of
the social group. All occurrences of agonistic behaviors were also recorded for the creation of
dominance hierarchies. Dominance hierarchies were established using methods from Sauther
(1992) and Taylor (1986). During a focal observation period, if the subject engaged in a
vocalization, type, and directionality (initiated vocalization or responding to another individual’s)
were also recorded. Ring-tailed lemurs have different types of vocal calls (Macedonia 1993);
therefore, I classified calls into three different categories: affiliative, alerting and antipredator, and
agonistic vocalizations. All behaviors recorded are listed in Appendix 1, adapted based on an
ethogram developed by Sauther (1992) and modified by Millette (2007).
Data and Statistical Methods
Data processing and analysis was conducted in JMP (JMP 13, SAS Institute Inc., Cary,
North Carolina, USA). Significant differences between age categories were assessed using
students t-tests and Tukey-Kramer Honest Significant Difference (HSD) tests. Due to the
directional nature of the hypotheses, one-tailed t-tests were used and were conducted in JMP. Both
tests were used and reported to indicate the strength of the statistical results with respect to the
hypotheses tested. When comparing count data, a Fisher’s exact test was used due to small sample
sizes. An ANOVA was used to determine if individual identity significantly predicted the variation
among times in the activity budget such as time in physical contact, travel, etc. If a particular
individual was found to be a major cause of variation, a Tukey-Kramer all pairs post-hoc analysis
was conducted to determine patterns in individual activity budgets. This method of comparison
27
was used because it allowed for the significance level to be held constant across all pair-wise tests.
For all statistical tests, significance was set at α≤0.05.

28
Chapter 3: Results
Degree of Sociality
Proximity
Not accounting for sex, old individuals spent significantly more time per focal
follow alone, more than two meters away from a group member (Old mean = 739.77 ± 33.25,
Adult Mean = 503.54 ± 32.82; DF = 557.85; t=-5.06; p<0.0001). When sex is accounted for, both
old females (Old mean = 709.14 ± 45.47, Adult Mean = 455.35 ± 37.28; DF = 314.89; t=-4.32;
p<0.0001) and males (Old mean = 778.61 ± 48.58, Adult Mean = 599.40 ± 63.36; DF = 185.59;
t=-2.24; p=0.026) spent significantly more time alone than adult individuals. This relationship was
still significant between female age categories when Liesl was removed from the data set (Old
mean = 709.14 ± 44.24, Adult Mean = 557.25 ± 46.54; DF = 295; t=-2.37; p=0.0093) (Figure 5).
Liesl and interactions with her infants were removed from parts of the analysis because she was
expected to have more physical contact with other individuals because she had nursing infants
during data collection.
900
Old
800
Adult
Seconds Per Focal Follow
700
600
500
400
300
200
100
0
Female Male
Sex
Figure 5. Average Time Spent More Than Two Meters Away from Group Members. This
comparison reflects measures of proximity without Liesl and her infants. Error bars reflect the
standard error of the mean.
29
Physical Contact
As mentioned before, proximity to group members might not be an accurate
measure of sociality compared to physical contact. Not accounting for sex, adult individuals spent
significantly more time in physical contact with other individuals compared to old lemurs (Old
mean = 268.73 ± 26.35, Adult Mean = 340.57 ± 30.13; DF = 548.78; t=1.79; p=0.037). Among
females, adults spent significantly more time in physical contact with others than old females (Old
mean = 317.60 ± 36.33, Adult Mean = 410.45 ± 39.16; DF = 340.91; t=1.74; p=0.0415) (Table
6.).
Table 6. Mean Physical Contact Time Comparison between Old and Adult Females with and
without Liesl and Infants. This relationship was not significant when a Tukey comparison was
conducted.
Adult Female Old Female
Means Means D.F. t-value p-value
With Liesl and Infants 410.45 ± 39.16 317.60 ± 36.33 340.91 1.74 0.0415
Without Liesl and
Infants 218.02± 33.88 308.61 ± 36.32 294.9 -1.82 0.0346
However, the variation in physical contact time was strongly predicted by individual
(ANOVA, F=14.37, DF=8, p<0.0001), and the post-hoc analysis indicated that Liesl spent
significantly more time in physical contact with group members compared to all of the other
females in this study (Table 7). Because this high physical contact time was most likely a function
of Liesl having two infants, I also conducted the physical contact analysis without these individuals
(Figure 6). When these individuals were excluded from the analysis, the inverse significant
relationship was found: old females spent significantly more time in physical contact with other
individuals than adult females (Old mean = 308.61 ± 36.32, Adult Mean = 218.02 ± 33.88; DF =
294.9; t=-1.82, p=0.035) (Table 6.). No significant relationship in physical contact time between
old and adult males was found both including and excluding Liesl and her infants (Table 8.).
30
Table 7. Female Individual Analysis of Physical Contact Time. The connecting letters reports
reflect the results of comparisons for all pairs using the Tukey-Kramer Honest Significant
Difference test.
Physical Contact
Connecting
Individual Mean Letters
Liesl 980.87 A
Sosiphanes 428.95 B
Lilah 347.19 B
Shroeder 338.13 B
Lulu 291.22 B
Tellus 282.68 B
Sierra Mist 234.94 B
Sprite 196.73 B
Gretl 146.89 B
Table 8. Mean Physical Contact Time Comparison between Old and Adult Males with and
without Liesl and Infants. This relationship was not significant when a Tukey comparison was
conducted.
Adult Male Old Male p-
Means Means D.F. t-value value
With Liesl and 201.56 +/- 206.74 +/-
Infants 41.91 37.50 202.54 -0.092 >0.05
Without Liesl and 201.56 +/- 203.37 +/-
Infants 41.91 37.61 202.82 -0.032 >0.05
400
Old
350
Adult
Seconds Per Focal Follow
300
250
200
150
100
50
0
Female Male
Sex
Figure 6. Average Time Spent in Physical Contact with at Least One Group Member. This
comparison reflects measures of physical contact without Liesl and her infants.
31
Furthermore, when comparing physical contact time between old males and females, old
females were found to spend significantly more time per focal in physical contact with other
individuals, excluding Liesl and her infants, compared to old males (Old Female Mean = 308.61
± 36.32, Old Male Mean = 203.37 ± 37.61; DF = 270.49; t=-2.01; p=0.02). No significant
difference in physical contact time between adult males and females was found, especially when
Liesl was removed from the analysis (Adult Female Mean = 218.02 ± 33.88, Old Male Mean =
201.56 ± 41.91; DF = 198.09; t=-0.31; p=0.38). These results indicate that old females are more
social than old males when using physical contact as a measure of sociality (Figure 7.).
400
350
Average Time Per Focal Follow
300
250
200
150
100
50
0
Female Male
Sex
Figure 7. Average Time Spent in Physical Contact with at Least One Group Member
Compared between Old Males and Females. This comparison reflects measures of physical
contact without Liesl and her infants.
Activity Budgets
Locomotion (Travel and Movement)
As a group, old lemurs spent significantly more time per follow in locomotion (Old
Mean = 270.43 ± 12.23, Adult Mean = 206.88 ± 11.84; DF = 557.29; t=-3.73; p=0.0001). When
32
broken down by sex, a significant difference between time spent in locomotion between old and
young females does not exist (Table 9.). Individual identity was not found to significantly predict
any variation in female locomotion times (ANOVA; F=1.48; D.F.=8; p=0.37), travel (ANOVA;
F=1.95; D.F.=8; p=0.07), and movement (ANOVA; F=1.21; D.F.=8; p=0.54).
Table 9. Locomotion, Travel, and Movement Comparisons between Adult and Old Females.
No significant difference was found between age groups when comparisons were conducted using
a Tukey-Kramer Honest Significant Difference test.
Adult Female Old Female
Behavior Means Means D.F. t-value p-value
Locomotion 223.81 ± 12.83 230.35 ± 14.24 328.4 -0.34 0.37
Travel 20.57 ± 3.47 28.63 ± 4.30 312.16 -1.46 0.07
Movement 203.24 ± 11.59 201.72 ± 12.32 333.24 0.09 0.54
Individual identity was found to significantly explain variation in male locomotion
(ANOVA; F=8.25; D.F.=5; p<0.0001), travel (ANOVA; F=3.32; D.F.=5; p=0.0066), and
movement (ANOVA; F=8.84; D.F.=5; p<0.0001). The old male Aracus had a significantly higher
amount of locomotion and movement activity than most of the other males (Table 10.).
Table 10. Male Individual Analysis of Locomotion and Movement Times. The connecting
letters reports reflect the results of comparisons for all pairs using the Tukey-Kramer Honest
Significant Difference test.
Locomotion Movement
Mean Connecting Mean Connecting
Individual (seconds/follow) Letters Report (seconds/follow) Letters Report
Aracus 441.18 A 420.8 A
Licinius 356.22 A B 297.14 A B
Berisades 271.76 B C 245.92 B C
Aristedes 219.8 B C 189.26 B C
Jones 178.71 C 170.81 B C
Stewart 167.49 C 147.82 C
Licinius was found to spend significantly more time traveling (Table 11.) than the two
young males Stewart (Tukey-Kramer HSD, p=0.035) and Jones (Tukey-Kramer HSD, p=0.0016).
33
Therefore, in comparing these behaviors between age categories, I also conducted the comparison
without Aracus for locomotion and movement and Licinius for travel.
Table 11. Male Individual Analysis of Travel Times. The connecting letters reports reflect the
results of comparisons for all pairs using the Tukey-Kramer Honest Significant Difference test.
Travel
Individual Mean Connecting Letters Report
Licinius 59.08 A
Aristedes 30.51 A B
Berisades 25.84 A B
Aracus 20.38 A B
Stewart 19.67 B
Jones 7.89 B
A significant difference (t=-4.69, p<0.0001) between old and younger male locomotion
time exists, even when Aracus is removed (t=-3.25, p=0.0007) from the data set, indicating that
old males spent more time moving around in general than the two adult males. When locomotion
is broken down between movement and travel, old males spend significantly more time traveling
than adults (t=-2.69, p=0.0039). However, when Licinius is removed from the analysis, this
relationship is no longer significant (Table 12). Old males spend significantly more time (t=-4.39,
p<0.0001) moving than adults, even if Aracus is removed (t=-2.81, p=0.0027).
Table 12. Locomotion, Travel, and Movement Comparisons between Adult and Old Males
with and without Aracus and Licinius included. *Indicate comparisons where the Tukey-
Kramer Honest Significant Difference test was significant.
Behavior Young Male Old Male D.F. t-value p-value
Locomotion* 173.22 ± 24.28 321.27 ± 20.21 195.11 -4.69 <0.0001
Locomotion without
Aracus* 173.22 ± 24.28 282.58 ± 23.24 184.73 -3.25 0.0007
Travel* 13.66 ± 5.08 34.06 ± 5.65 214.82 -2.69 0.0039
Travel without Licinius 13.66 ± 5.08 25.63 ± 14.78 182.7 -1.61 >0.05
Movement* 159.56 ± 22.98 287.20 ± 17.76 186.55 -4.39 <0.0001
Movement without
Aracus* 159.56 ± 22.98 244.11 ± 19.37 180.16 -2.81 0.0027
34
Feeding and Foraging
Overall, old and adult feeding and foraging times did not differ significantly (Old
Mean = 80.01 ± 7.99, Adult Mean = 96.71 ± 9.27; DF = 547.61; t=1.36; p=0.91), and there were
no sex differences for these behaviors (Old Female Mean = 72.61 ± 10.03, Adult Female Mean =
92.75 ± 10.99; DF = 341; t=1.35; p=0.91) (Old Male Mean = 89.39 ± 12.91, Adult Male Mean =
104.58 ± 17.11; DF = 183.61; t=0.71; p=0.76). The ANOVA indicated that individual identity
strongly explained the variation in feeding and foraging time for females (F=2.42; DF=8; p=0.02)
but not males (F=0.32; DF=5; p=0.90). The post-hoc analysis among the females (Table 13)
indicated that Lulu spent significantly more time feeding and foraging per focal than Liesl (Tukey-
Kramer HSD, p=0.0048) and Sprite (Tukey-Kramer HSD, p=0.0321).
Table 13. Female Individual Analysis of Feeding/Foraging Times. The connecting letters
reports reflect the results of comparisons for all pairs using the Tukey-Kramer Honest Significant
Difference test.
Feed/Forage
Individual Mean Connecting Letters
Lulu 161.72 A
Gretl 81.71 A B
Tellus 80.96 A B
Shroeder 78.28 A B
Sosiphanes 76.57 A B
Sierra Mist 74.07 A B
Lilah 68.8 A B
Sprite 58.79 B
Liesl 52.65 B
Resting
For total resting, no significant difference was found between old and adult
individuals for total resting time (Old Mean = 1129.63 ± 18.87, Adult Mean = 1083.61 ± 23.65;
DF = 532.61; t=-1.52; p=0.06). Old females spend significantly more time resting than adult
females (t=-3.91, DF=340.89, p<0.0001) (Table 14). Comparison of total resting time significantly
35
varied by individual (ANOVA; F=9.69; D.F.=8; p<0.0001); post-hoc analysis indicated that Sprite
spent significantly more resting time than Gretyl (Tukey-Kramer HSD, p=0.0161) and Liesl
(Tukey-Kramer HSD, p<0.0001) and that Liesl spent significantly less total time resting than all
of the other females (Table 15). Therefore, I conducted the comparisons between female resting
age categories with and without Liesl in the analysis. When the age comparison is conducted
without Liesl included, the significant difference in female resting time disappeared (Table 14).
Table 14. Analysis of Old and Adult Female Total, Solitary, and Social Resting Times.
Adult Female Old Female D.F. t-value p-value

With Liesl 1005.64 ± 27.74 1151.18± 24.88 340.89 -3.91 <0.0001
Total Without
Resting Liesl 1099.61± 30.14 1151.18± 24.88 278.83 -1.32 0.09
With Liesl 193.39 ± 26.4 168.52 ± 24.71 340.79 0.69 0.75
Social Without
Resting Liesl 140.78 ± 30.94 168.52 ± 24.71 274.6 -0.7 0.20
With Liesl 812.25 ± 33.70 982.66 ± 33.28 338.9 -3.6 0.0002
Solitary Without
Resting Liesl 958.82 ± 34.93 982.66 ± 33.28 292.12 -0.49 0.31
Table 15. Female Individual Analysis of Total Resting Time. The connecting letters reports
Difference test.
Total Resting
Connecting
Sprite 1287.88 A
Tellus 1169.95 A B
Lulu 1122.81 A B
Lilah 1088.21 A B
Shroder 1064.28 A B
Gretl 1028.03 B
Liesl 717.63 C
36
A significant amount of the variation in social resting time among females was explained
by individual variation (ANOVA, F=3.19, DF=8, p=0.0017) with Liesl spending significantly
more time in social rest than Sprite (Tukey-Kramer HSD, p=0.017) and Gretl (Tukey-Kramer
HSD, p=0.0002) (Table 16). No significant differences in time spent in social rest were found
when Liesl was both included and excluded from the comparison (Table 14). Old females spend
more time in solitary rest (t=-3.6, p=0.0002), but this significant relationship disappears if Liesl is
removed from the analysis. A significant amount of the variation in solitary resting time among
females was explained by individual variation (ANOVA, F=13.83, DF=8, p<0.0001) with all
females spending significantly more time (Tukey-Kramer HSD, p<0.05) in solitary rest than Liesl
(Table 17). Therefore, when Liesl is removed from the data analysis for solitary rest the
significance between old and adult females is no longer present.
Table 16. Female Individual Analysis of Social Resting Time. The connecting letters reports
Difference test.
Social Resting
Connecting
Liesl 354.66 A
Lulu 225.86 A B
Lilah 176.71 A B
Tellus 173.15 A B
Shroeder 170.49 A B
Sprite 91.46 B
Gretl 42.02 B
Old females spent significantly more time (Old Mean = 468.46 ± 38.03, Adult Mean =
291.62 ± 29.72; DF = 296.97; t=-3.69, p=0.0001) resting by themselves with no individuals within
two meters of them compared to adult females, even when Liesl is removed from the analysis (Old
37
Mean = 468.46 ± 38.03, Adult Mean = 368.80 ± 36.12; DF = 286.93; t=-1.9, p=0.0292). Individual
strongly predicted the variation in time spent resting not in proximity to group members (ANOVA,
F=10.30, DF=8, p<0.0001). The post-hoc analysis indicates that Sprite spent significantly more
time resting alone than most of the other females while Liesl spent the least amount of time solitary
resting alone (Table 18).
Table 17. Female Individual Analysis of Solitary Resting Time. The connecting letters reports
Difference test.
Solitary Resting
Connecting
Sprite 1196.42 A
Tellus 996.8 A B
Gretl 986 A B
Lilah 911.5 A B
Lulu 896.95 B
Shroeder 893.79 A B
Liesl 362.97 C
Table 18. Female Individual Analysis of Solitary Resting Time Not In Proximity with at Least
One Group Member. The connecting letters reports reflect the results of comparisons for all pairs
using the Tukey-Kramer Honest Significant Difference test.
Solitary Resting (NN=0)
Connecting
Sprite 692.36 A
Tellus 653.02 A B
Sierra Mist 545.06 A B C
Lulu 371.58 B C D
Lilah 369.09 B C D
Sosiphanes 328.54 C D E
Shroeder 288.99 C D E
Gretl 193.75 D E
Liesl 53.06 E
38
Adult males spent significantly more time resting total than Old males (t=2.78, p=0.003)
(Table 19.). Total resting time was strongly predicted by individual (ANOVA, F=2.91, DF=5,
p=0.0146), but a post-hoc analysis of total resting time indicated no significant differences among
males (Table 20.). This significant difference existed for solitary resting (t=2.45, p=0.0076) but
not for male social resting (Table 19.). Both social (ANOVA, F=2.80, DF=5, p=0.018) and solitary
resting (ANOVA, F=2.59, DF=5, p=0.0269) times were strongly predicted by individual identity
among males. Licinius spent significantly more time in social rest (Tukey-Kramer HSD, p=0.0215)
than Aracus (Table 20.). Stewart spent significantly more time in solitary rest than Licinius (Table
21.). Adult males spent significantly more time resting in close proximity to at least one group
member compared to old males (Old Mean= 501.18, Adult Mean= 699.49; DF=167.20; t=2.90,
p=0.0021).
Table 19. Analysis of Old and Adult Male Total, Solitary, and Social Resting Times.
Adult Male Old Male DF t-value p-value
Total Resting 1238.71 ± 39.78 1102.30 ± 28.85 178.85 2.78 0.003
Social Resting 123.07 ± 33.57 128.49 ± 28.40 196.91 -0.12 0.45

Solitary
Resting 1115.64 ± 46.38 973.81 ± 34.70 182.62 2.45 0.0076
Table 20. Male Individual Analysis of Social Resting Time. The connecting letters reports
Difference test.
Social Resting
Connecting
Licinius 260.17 A
Jones 174.62 A B
Berisades 165.22 A B
Aristides 77.92 A B
Stewart 69.28 A B
Aracus 6.72 B
39
Table 21. Male Individual Analysis of Solitary Resting Time. The connecting letters reports
Difference test.
Solitary Resting
Connecting
Stewart 1151.07 A
Jones 1081.69 A B
Aracus 1029.52 A B
Aristides 971.93 A B
Licinius 829.16 B
Sleeping
No significant differences in total, social, and solitary sleeping times for both males and
females were found (Table 22.).
Table 22. Analysis of Adult and Old Male and Female Total, Solitary, and Social Sleeping
Times.
Adult Mean Old Mean D.F. t-value p-value
Total Females 92.22 ± 18.94 85.45 ± 18.63 339.1 0.26 0.60
Sleeping Males 105.77 ± 26.79 58.54 ± 20.1 182.96 1.41 0.92
Social Females 36.52 ± 12.62 28.22 ± 11.3 340.87 0.49 0.69
Sleeping Males 28.30 ± 18.69 17.35 ± 9.84 143.3 0.52 0.70
Solitary Females 55.71 ± 14.10 57.23 ± 13.47 340.3 -0.08 0.47
Sleeping Males 77.47 ± 18.52 41.19 ± 17.65 207.89 1.42 0.92
Auto-grooming
No significant differences between adult and old auto-grooming were found overall (Old
Mean = 116.62 ± 8.20, Adult Mean = 120.88 ± 7.72; DF = 555.71; t=0.38; p=0.65) or within the
sexes (Old Female Mean = 116.22 ± 10.62, Adult Female Mean = 131.11 ± 9.18; DF = 322.93;
t=1.06; p=0.86) (Old Male Mean = 117.12 ± 12.88, Adult Male Mean = 100.54 ± 13.94; DF =
205.46; t=-0.87; p=0.19).
Allo-grooming
40
No significant differences between female adult and old total allo-grooming time was
found (Old Mean = 101.27 ± 11.00, Adult Mean = 85.18 ± 8.85; DF = 311.73; t=-1.14; p=0.13).
When grooming is broken down based on directionality (mutual vs. unidirectional), older females
spent significantly more time engaged in mutual grooming (Old Mean = 70.36 ± 8.37, Adult Mean
= 37.50 ± 4.94; DF = 255.87; t=-3.38; p=0.0004). Adult females spent significantly more time
engaged in unidirectional grooming behavior (Old Mean = 30.91 ± 5.50, Adult Mean = 47.67 ±
6.17; DF = 340.81; t=2.03; p=0.02). No significant differences were found between old and adult
males in total allo-grooming (Old Mean = 47.59 ± 7.92, Adult Mean = 39.87 ± 8.51; DF = 206.05;
t=-0.66; p=0.25), mutual grooming (Old Mean = 39.06 ± 7.07, Adult Mean = 27.66 ± 5.73; DF =
213.89; t=-1.25; p=0.11), or unidirectional grooming (Old Mean = 8.53 ± 2.34, Adult Mean =
12.21 ± 3.51; DF = 168.89; t=0.87; p=0.81).
Frequency of Behaviors
Agonistic Point Events
The number of agonistic events initiated and received did not significantly differ
between adult and old females (Fisher’s Exact Test, p=0.54) (Table 23.). Females initiated
agonistic acts more than males (Fisher’s Exact Test, p<0.0001) (Table 24.). The number of
agonistic events initiated and received did not differ between adult and old males (Fisher’s Exact
Test, p=0.38), with males more likely to be recipients of agonistic acts (Table 25.).
Table 23. Female Agonistic Event Counts Based on Act Initiated, Received, or Unknown.
Table probability using a Fisher’s Exact Test is P=0.0405 with p=0.54.
Initiated Received Unknown Total
Old 51 21 0 72
Young 77 39 2 118
Total 128 60 2 188
41
Table 24. Female and Male Agonistic Event Counts Based on Act Initiated, Received, or
Unknown. Table probability using a Fisher’s Exact Test with p<0.0001.
Initiated Received Total
Female 94 59 153
Male 6 58 64
Total 100 117 217
Table 25. Male Agonistic Event Counts Based on Act Initiated, Received, or Unknown. Table
probability using a Fisher’s Exact Test is P=0.041 with p=0.38.
Initiated Received Unknown Total
Old 5 34 5 44
Young 1 24 1 26
Total 6 58 6 70
Affiliative Point Events
The number of affiliative events initiated and received did not differ between adult
and old individuals of both sexes (Tables 26. & 27.).
Table 26. Female Affiliative Event Counts Based on Act Initiated, Received, or Unknown.
Table probability using a Fisher’s Exact Test is P=0.036 with p=0.41.
Initiate Received Unknown Total
Old 53 66 1 120
Young 64 65 0 129
Total 117 131 1 249
Table 27. Male Affiliative Event Counts Based on Act Initiated, Received, or Unknown. Table
probability using a Fisher’s Exact Test is P=0.177 with p=0.81.
Initiate Received Total
Old 24 27 51
Young 11 15 26
Total 35 42 77
42
Grooming
When comparing the initiation and receiving information for grooming bouts, I
found that adult females initiated significantly more grooming events (69.41%) than old females
(30.59%) (Fisher’s Exact Test; p<0.0001) (Table 28.). Among the males, I found that adult
individuals received significantly more (59.1%) grooming behaviors than old males (40.91%)
(Fisher’s Exact Test; p=0.02) (Table 29.). When directionality is broken down based on grooming
type, adult females still initiate significantly more unidirectional grooming bouts (77.59%) than
old females (22.415%) (Fisher’s Exact Test; p<0.0001) (Table 30.). No significant difference in
adult and old male directionality in grooming was found (Fisher’s Exact Test; p=0.77) (Table 31).
Looking at mutual grooming, adult females initiate significantly more mutual grooming bouts
(57.82%) than old females (42.18%) (Fisher’s Exact Test; p=0.0001) (Table 32.), whereas, old
males initiate more mutual grooming bouts (62.71%) than adult males (37.29%) (Fisher’s Exact
Test; p=0.01) (Table 33.).
Table 28. Female Total Grooming Event Counts Based on Act Initiated, Received, or
Unknown. The Fisher’s Exact Test one-tail probability is p<0.0001.
Old 156 145 301
Adult 354 78 432
Total 510 223 733
Table 29. Male Total Grooming Event Counts Based on Act Initiated, Received, or Unknown.
The Fisher’s Exact Test one-tail probability is p=0.02.
Old 55 45 100
Adult 43 65 108
Total 98 110 208
43
Table 30. Female Grooming (Unidirectional) Event Counts Based on Act Initiated, Received,
or Unknown. The Fisher’s Exact Test one-tail probability is p<0.0001.
Old 67 77 144
Adult 232 41 273
Total 299 118 417
Table 31. Male Grooming (Unidirectional) Event Counts Based on Act Initiated, Received,
or Unknown. The Fisher’s Exact Test one-tail probability is p=0.77.
Old 18 17 35
Young 21 25 46
Total 39 42 81
Table 32. Female Mutual Grooming (Bidirectional) Event Counts Based on Act Initiated,
Received, or Unknown. The Fisher’s Exact Test one-tail probability is p=0.0001.
Old 89 68 157
Young 122 37 159
Total 211 105 316
Table 33. Male Mutual Grooming (Bidirectional) Event Counts Based on Act Initiated,
Received, or Unknown. The Fisher’s Exact Test one-tail probability is p=0.0122.
Old 37 28 65
Young 22 40 62
Total 59 68 127
Stink Fights
Stink fighting is a directed, agonistic encounter during which a male rubs carpal
spurs against his sternal glands and then moves his tail in the face of the receiving individual (Jolly
1966). During the course of the entire period of data collection, I only recorded five occurrences
of stink fighting. Both occurrences of stink fighting by Aracus were directed towards Randy, the
male inhabiting the enclosure across the fence. Licinus’ single recorded stink fight was directed at
44
Jones across a fence, and both of Berisades’ stink fight occurrences were directed at individuals of
another species sharing an enclosure with him.
Vocalizations
Old females responded to affiliative vocalizations at a significantly higher
frequency (61.15%) than adult females (53.76%) (Fisher’s Exact Test; p=0.038) (Table 34). No
significant difference existed between the number of initiated versus responded affiliative
vocalizations for males of the different age groups (Fisher’s Exact Test; p=0.93) (Table 35). Males
initiated more affiliative vocalizations whereas females tended to respond more (Fisher’s Exact
Test; p<0.0001) (Table 36).
Table 34. Female Affiliative Vocalization Event Counts Based on Act Initiated, Responding,
or Unknown. The Fisher’s Exact Test one-tail probability between initiated and received events
is p=0.038.
Initiating Responding Unknown Total
Old 108 170 5 283
Adult 160 186 0 346
Total 268 356 5 629
Table 35. Male Affiliative Vocalization Event Counts Based on Act Initiated, Responding, or
Unknown. The Fisher’s Exact Test one-tail probability between initiated and received events is
p=0.93.
Initiating Responding Total
Old 135 57 192
Adult 34 22 56
Total 169 79 248
Table 36. Male and Female Affiliative Vocalization Event Counts Based on Act Initiated,
Responding, or Unknown. The Fisher’s Exact Test one-tail probability between initiated and
received events is p<0.0001.
Female 268 356 5 629
Male 169 79 0 248
Total 437 435 5 877
45
No significant differences were found between the number of initiated and responded
alerting and antipredator vocalizations (Fisher’s Exact Tests; p=0.09, p=0.94) (Tables 37 & 38)
for both sexes based on age. Old individuals of both sexes participated in more alerting and
antipredator vocalizations compared to adult individuals, but this difference is most likely a
function of the NHE that these individuals inhabited rather than age (see discussion).
Table 37. Female Alerting and Antipredator Vocalization Event Counts Based on Act
Initiated, Responding, or Unknown. The Fisher’s Exact Test one-tail probability between
initiated and responding events is p=0.09.
Old 111 173 0 284
Young 5 2 1 8
Total 116 175 1 292
Table 38. Male Alerting and Antipredator Vocalization Event Counts Based on Act Initiated,
Responding, or Unknown. The Fisher’s Exact Test one-tail probability between initiated and
responding events is p=0.94.

Old 29 56 1 86
Young 5 19 0 24
Total 34 75 1 110
Leading Behavior
No significant difference in group travel leading behavior was found between adult
and old females. However, old males were found to lead group travel (56%) with a greater
frequency (Fisher’s Exact Test, p=0.0030) than adult males (18%) (Figure 8).
46
60% 56%
Old Adult
50%
Percentage of Leading 40%
30%
23%
21%
20% 18%
10%
0%
Female Sex Male
Figure 8. Percent Leading During Travel Between Old and Adult Individuals.
Individual Factors
Dominance Rank
All females were socially dominant to males in both feeding and non-feeding
contexts, indicating that, even with older age, females are still socially dominant to males. Due to
the lack of agonistic interactions during feeding, separate ranks based on feeding and non-feeding
context could not be constructed (Table 39.). Females still maintained social dominance with
advanced age, indicating that this dominance persists in old females consistent with findings in
other lemur taxa (Taylor 2008). In two of the social groups with more than one female, the oldest
females (Sosiphanes and Sprite) were socially dominant to the other female in the group. In both
cases, the younger females (Lilah and Lulu) were the daughters of the dominant female, consistent
with studies in wild populations (Sauther 1992; Pereira 1993; Nakamichi et al. 1997). These
findings also show that old females are not being targeted by younger individuals as a means to
rise in rank, consistent with research on other species of lemur at the DLC (Taylor 2008).
47
Liesl was the most dominant female of her social group, ranking above both her mother
(Shroeder) and her daughter (Gretl). Liesl was the only female in this population who had
dependent infants and was still lactating during the study period. Yet, she spent less time overall
(52.65 seconds) per focal feeding than many of the other females studied, though this was not
significantly different from other females. Liesl’s dominance over her mother in the social group
could be a function of her infants, giving her greater access to foods to meet her needs for lactation.
Due to the composition of the social groups at the DLC, I was not able to compare how
advanced age affects the social rank of males but such a question will be an important area for
future inquiry.
Table. 39. Social Ranks of Study Individuals. In all instances, males were subordinate to
females.
Sex Name Age Category Rank
NHE 3
M Aristides 23 O --
F Sosiphanes 19 O 1
F Lilah 11 O 2
NHE 4
M Aracus 24 O --
F Shroeder 24 O 3
F Liesl 7 A 1
F Gretl 4 A 2
F Hedwig 0.1 I --
F Griselda 0.1 I --
NHE 7
F Sierra Mist 8 A --
M Berisades 12 O --
NHE 8
M Licinius 23 O --
F Tellus 12 O --
NHE 9
F Sprite 15 O 1
M Jones 4 A 2
M Stewart 4 A 1
F LuLu 2 A 2
48
Social Roles
Infant Care
One of the primary ways that I measured infant care was the amount of time that
particular individuals carried the infants Hedwig and Griselda. Over the course of my study, only
two other individuals Shroeder, their grandmother, and Aracus, their father, were observed to carry
an infant besides Liesl (Table 40). Furthermore, both of these individuals carried only Griselda
specifically and not her sister Hedwig or both infants at the same time.
Table 40. Non-Maternal Carrying Behavior of Griselda.

Mean Time
Individual Relationship (seconds) N
Aracus Father 9.809 1
Shroeder Grandmother 57.298 11
Gretl Sister 0 0
Case Studies
Grouping the data from subjects based on certain characteristics (age, sex, etc.) was an
important way to address my hypotheses. However, rather than constructing a concrete behavioral
profile for old ring-tailed lemurs, I found that the effects of aging must be understood at the
individual level. While I was able to explore a few individual factors that seem to affect behavioral
patterns in old lemurs like sex and dominance rank, these factors did not seem to adequately
capture the range of individual variation that I observed. The following case studies provide more
depth to the primary finding that senescence affects individuals differentially based on
characteristics of the animal like personality, life history, and even disability.
Aracus
Aracus is a 24-year old male living in the only social group I sampled with infant
individuals. He was the father of the infants, Hedwig and Griselda, and was the only male in the
49
social group. Of all of the males in my sample, Aracus spent the most time per focal follow
(average: 441.18 seconds) in locomotor behaviors (traveling and moving), which was significantly
different (Table 10.) from four of the five other males. When locomotion is broken down based on
duration, Aracus spent the most time moving (average: 420.80 seconds) which was significantly
different than four of the other five males (Table 10.). With respect to travel, Aracus was among
the middle males in time spent traveling (Table 11.). Among the males, he spent the second least
amount of time in proximity to group members, but this relationship is not significantly different
from any of the other males (Table 41.). Aracus seemed to actively avoid members of his social
group at times, which might explain his inclination to move around the enclosure by himself.
Table 41. Male Individual Analysis of Social Proximity Time. Social proximity was considered
to be within two meters or less of at least one group member. The connecting letters reports reflect
the results of comparisons for all pairs using the Tukey-Kramer Honest Significant Difference test.
This post-hoc analysis was conducted after the ANOVA for physical contact time among the males
was strongly predicted (F=2.85, DF=5, p=0.0164) by individual.
Social Proximity
Connecting
Jones 1294.47 A
Aristedes 1000.83 A B
Stewart 984.94 A B
Aracus 965.34 A B
Licinius 837.51 B
Aracus also spent the least amount of time in social rest (average: 6.72 seconds),
but this time was only significantly different (Table 20.) from Licinius. When observing Aracus,
he would commonly investigate parts of the enclosure that were nearby for other ring-tailed lemurs
that were across the fence. He also is among the top two of individuals in number of times
approaching or scent marking the researcher or their chair (N=16 times). Aracus has been in
numerous research studies during his time at the DLC and is known to be incredibly cooperative
50
(Zher 2016). Therefore, his inclination to greater movement could be in part related to his prior
experiences with humans in captivity.
Sprite
Sprite is a 15-year old female living in a social group with her daughter (Lulu), her
son (Jones), and her grandson (Stewart). Sprite spent the most amount of time among the females
solitarily resting (1196.42 seconds on average/follow) and was significantly different from Liesl
and Lulu (Table 17.). Sprite also spent the second least amount of time in social rest (91.46
seconds/focal) after Gretl, but this relationship was only significantly different from Liesl (Table
16). Sprite spent the least amount of time each focal (185.5 seconds) in locomotion, but this
relationship was not significantly different from the other females in the sample. When observing
Sprite, she would often select a tree in which to rest while her group members would explore the
forest and feed.
Shroeder
Shroeder is a 24-year old female living in a social group with her daughter (Liesl),
unrelated male (Aracus), and three granddaughters (Gretl, Griselda, and Hedwig). Her daughter
Liesl is the highest-ranked female of the social group. According to DLC records, the last time
Shroeder was pregnant with an infant she “stole” Liesl’s newborn infant and cared for it until DLC
staff realized that she was still pregnant (Zher 2016). After her own infant was born, Liesl’s infant
was seen trying to nurse from Shroeder and would even ride on her back. During the study period,
Shroeder was observed carrying her daughter’s infant Griselda (Table 40), but never her other
granddaughter Hedwig. She spent the most time carrying Griselda compared to the non-maternal
members of the social group.

51
Lilah
Lilah is an 11 year old female living in NHE3 with her mother Sosiphanes and an
unrelated male Aristedes. Sosiphanes was found to be dominant over her daughter. In September
2007, at two years of age, Lilah broke her left humerus, requiring her to have surgery (Zehr 2017).
Researchers think that she obtained nerve damage either post-surgery or from the injury itself
which required several months (until March 2008) with a splint and physical therapy. By May of
2008, sensation had returned to her arm, and she was able to move the digits of her left hand, but
she seldom used her arm after this time. Researchers at the DLC suspect that the joints became
stiff during her recovery. Therefore, at this point in her life, she began not putting weight on this
arm, holding it out to her left when she moved. She has been able to use the arm for support (Figure
9.).
a. b.
Figure 9a. & 9b. Pictures of Lilah. This image of Lilah depicts her resting with her left forelimb
positioned out to the left of her body. She holds her arm in a similar manner when walking or
running. b) This image is a close-up side view of how Lilah uses her arm for occasional stability
when at rest. Note that she does not place significant weight on it.
In April of 2012, during the application of flea and tick medication, she broke her left ulna
and radius, which were in a splint until the end of May 2012. DLC records note that this additional
52
injury did not seem to cause any additional lack of mobility in her left arm than was already there
(Zher 2017). Therefore, Lilah had spent approximately nine years living with the challenges of her
injured left arm before the data in this study were collected. Individual-based analysis of activity
budgets indicate that this impaired older lemur does not spend her time differently than other
females in this study. It should be noted, that she spent the most time of all of the females (mean:
299.91 seconds/follow) in locomotion, but this was not found to be significantly different to any
of the other females. Lilah’s impairment does not seem to result in drastic modifications to her
activity budget compared to other females.
The Other Individuals
While I have emphasized particular findings for the four individuals above, I
wanted to highlight characteristics of the other individuals in this study to be mindful of in the
interpretation of my results. Aristides is a 23-year-old male living with the two non-related females
Sosiphanes and Lilah in NHE3. It should also be noted, that when Aristides was younger, he was
castrated during two separate mating seasons by members of his social group. Sosiphanes is also
a member of NHE3 and is the 19-year-old mother of Lilah.
Liesl is a seven year old female living with her three daughters, mother, and non-related
male Aracus in NHE4. Liesl during the duration of this study was still lactating and allowing the
infants Hedwig and Griselda to nurse from her. Towards the end of the data collecting period, she
tended to carry one of her daughters, Hedwig. Gretl is Liesl’s four-year-old daughter who had no
occurrences of infant carrying in the social group. It should also be noted that during data
collection, a family of foxes was living in NHE4, which affected the frequency of antipredator
vocalizations observed in this study.

53
Sierra Mist is an eight-year-old female living in NHE7 with Berisades, a 12-year-old male.
Several years before this data was collected Berisades escaped the NHE enclosure in which he was
living and was eventually found at an elementary school before he was returned to the DLC. The
period of data collection was the first time Berisades was allowed to free-range since escaping
from his enclosure.
Tellus is a 12-year-old female living with 23-year old Licinius in NHE 8. It should be noted
that during the sampling period, several raccoons were living in NHE8 which affected the
antipredator vocalization rate of these individuals.
Jones is a four-year-old male living in NHE9 with Sprite, two-year old Lulu, and Stewart
whom is the same age as Jones. Jones, Stewart, and Lulu frequently spent their mornings exploring
the enclosure while Sprite often selected a tree and rested separately from the group.
54
Chapter 4: Discussion
Discussion of Results in Terms of Study Hypotheses
Decoupling Chronological Age and Senescence
In this study, I used the age in which ring-tailed lemurs often disappear in wild
environments as a means of operationalizing old in this population. I expected to observe a clear
difference in the social and behavioral profile of these old individuals compared to adults, but the
data do not support this hypothesis. Age did not explain any of the variation in locomotion, feeding,
and resting between old and adult individuals. My failure to support this hypothesis indicates that
age-related benchmarks do not adequately distinguish senescent individuals from other cohorts
within this captive population.
The struggle of primatologists and bio-gerontologists to operationalize old in conjunction
with my own findings reveals that age-related approximations of senescence inadequately describe
aging individuals. Patterns of senescence are not only individual-dependent, but different
mammalian systems and tissues seem to experience rates of senescence at different times
(Hayward et al. 2015). Though we observe a general trend of physiological decline associated with
advanced age, different factors can reduce or hasten this decline. This suggests that strictly age-
dependent means of defining senescence like the standard used in this study should also include
metrics that focus on individual, somatic variation like the physiological frailty index (Antoch et
al. 2017). It is also critical that age-related descriptor of old be decoupled with ideas of aging and
senescence. My work has shown that senescence is strongly dependent on ecological,
demographic, and life history factors in addition to expected association with chronological age.
One significant reason why the old cohort cannot be clearly distinguished from adults is
that individuals exhibit a vast range of behavioral variability even within the small population of
55
this study. Much of the significant variation that I observed disappeared with the removal of one
individual from the analysis. For example, Liesl spent the least amount of total time resting than
the other females (Table 15); when she was removed from the analysis, the significant differences
in female resting time disappeared (Table 14). Liesl’s status as a lactating female with two infants
resulted in significant differences in her behavior compared to the other females in this study. Such
individual variation in status affects the construction of a categorical behavioral profile based on
chronological age because different individuals can experience life history milestones like first
reproduction at different ages in their life.
Individual Variation and the Disposable Soma Hypothesis
Differences in life history patterns are particularly key in captive settings like the Duke
Lemur Center where curators must manage which individuals are going to be reproducing and
which ones are not. For example, only five of the 15 individuals in this study have ever produced
offspring (Table 5): Sosiphanes, Aracus, Shroeder, Liesl, and Sprite. Liesl was just over a year old
when she gave birth to her first infant whereas her mother Shroeder was 15 (Zehr et al. 2014).
Such artificially-imposed differences in reproduction provide an important means of observing
senescence under the disposable soma theory of aging.
The disposable soma hypothesis predicts that individuals that start breeding at a later age
should experience lower levels of senescence because a delay in reproduction allows for resources
to be allocated towards somatic maintenance and survival (Kirkwood and Rose 1991). Based on
this hypothesis, the lack of behavioral and social differences between the old and adult individuals
in this study may be explained by only one third of the population having produced offspring.
Because most of the individuals have not had to allocate resources towards reproduction, the
majority of these resources, which are more abundant in captive settings, can be directed towards
56
somatic maintenance. If these individuals are allocating resources towards maintenance, I expect
them to be exhibiting fewer signs of senescence than individuals who have been reproductive,
particularly those who were reproducing earlier in life.
Female costs for reproduction are viewed to be higher not only in mammals but also in
primates due to the costs of gestation and lactation (Russell and Lummaa 2009). Among
haplorrhine primates, males tend to allocate energy towards the growth of larger body size to
enable male-male competition for females (Leigh 1992). However, ring-tailed lemurs do not
exhibit sexual dimorphism in body size (Kappeler 1990). Therefore, we should not expect ring-
tailed lemur males to invest more energy in the growth of a larger body size, but rather allocate
resources to other means of competition such as physical agility. Notably, at the Duke Lemur
Center, because breeding pairs are established and placed in the environment to give them the best
possible chance of producing offspring, males have reduced pressure to invest in traits essential
for competition. This reduction in male-male competition is further supported by the minimal
frequency of stink-fighting (five total occurrences) observed during this study. Because of the size
monomorphism and reduced competition in captivity, I expect that females in this environment
would be allocating more energy directly to reproductive efforts than males. For the females that
have been reproductive, under the disposable soma theory, we should expect higher rates of
senescence, especially in females that are reproductive earlier in life.
The differential allocation of resources can help to explain some of the individual variation
in behavior if I compare the two reproductive old females in this study, Sprite and Shroeder. As
mentioned previously, Sprite spent a significant amount of time resting away from her social group
compared to other old females in this study. Though she was not the oldest female (12 years old),
Sprite had not only had the most total offspring but also the most surviving offspring (N=13)
57
among the three reproductive females (Table 5). She gave birth to her first infant at age four (Zher
et al. 2014). Shroeder, by contrast, was very active in her social group to the point of helping to
carry her infant granddaughter Griselda. She was also the oldest female (age 24 years) but only
had two offspring, both of which were still alive at the time of this study (Table 5). She gave birth
to her first infant, Liesl, at 12 years of age (Zher et al. 2014). Behaviorally, Sprite seems to be
exhibiting a lower level of activity than Shroeder despite the fact that she is 12 years younger than
her. The differences in fecundity between these two females could explain why behaviorally Sprite
seems less-active than Shroeder. This comparison further supports my assertion that
chronologically-based means of describing aging does not adequately represent patterns of
senescence.
If older individuals such as Sprite experience a decline in metabolic rate, they might spend
more time resting to accommodate this challenge and reduce energy expenditure. For example,
impaired Japanese macaques will spend more time resting as a possible means of accommodating
the extra energy expenditure associated with moving with their injury (Turner et al. 2012). The
only other individual in this study who had high levels of fecundity was Aracus, but he did not
seem to experience a reduction in activity level compared to other males. This contrast further
reveals how differential reproductive investment between the sexes could affect patterns of
senescence. My findings indicate that there are differences in behavior among old individuals,
suggesting that advanced age variably affects physiology. If senescence affects individuals
differently, we might expect to see a range of strategies that animals use to accommodate the
challenges of physiological decline.
This comparison highlights the importance of individual-based research in wild
populations where humans do not artificially select which animals are reproducing and
58
contributing to the gene pool. Though only a few individuals in this study produced offspring,
recent curation efforts at the Duke Lemur Center seem to have produced a more genetically-diverse
population of captive ring-tailed lemurs (Grogan et al. 2017). Research with captive mammal
populations, with ring-tailed lemurs included in the analysis, indicates that early in life
reproduction and fecundity does not lead to a reduction in longevity (Ricklefs and Cadena 2007).
However, longevity does not indicate the degree of senescence and quality of life for individual
animals, especially since they all have access to medical care. Future research should look at
sources of mortality among individuals based on their degree of fecundity in both captive and wild
populations. Such work could reveal not only how reproductive effort affects somatic aging but
also would provide specific mechanisms to target for future cellular and genetic aging research.
These efforts could also help to improve the quality of life for captive individuals to support efforts
to maintain and expand the genetic diversity of the captive gene pool of the species.
In failing to support my hypothesis that I would observe an age-specific behavioral profile
indicative of senescence, I found that the cohort-based approach is ineffective in furthering our
understanding of aging. I have already discussed above how age and fecundity can help explain
differences among individuals with respect to behavioral patterns associated with aging.
Dominance rank can also lead to considerable variation among individuals when observing
behavioral indicators of senescence. Females were found to initiate more agonistic events than
males which is consistent for this species due to female dominance. These results along with my
findings on rank (Table 39) indicate that not only do older females maintain social dominance over
males, but they also indicate that younger females are not targeting older females as a means of
rising in rank. These findings are consistent with those in other lemur species at the DLC (Taylor
2008). Future work in a larger wild population can help to discern if this is a species-specific
59
pattern or if perhaps it is a function of the captive environment. Older and low-ranking female
baboons have been found to experience higher rates of injury than those younger and higher-ranked
(Archie et al. 2014). All of the old females in my sample population except for Shroeder and Lilah,
who was below her mother in rank, were the dominant female in their social group. Therefore, it
is difficult to determine if this lack of targeted aggression by old females is a result of their higher
dominance rank or their age. Targeting of handicapped or senile female ring-tailed lemurs has been
documented in a wild population (Takahata et al. 2014), indicating that the conditions of my study
might have helped to buffer older individuals from targeted aggression.
The presence of kin in the social group can also differentially impact the behavior of
individuals. Older females were found to spend more time in physical contact with other
individuals compared to older males (Figure 7), providing support for my hypothesis that females
would exhibit higher degrees of sociality compared to males. This is consistent with findings in
other lemur species (Taylor 2008) and could be the result of female dominance or greater presence
of kin in the social group. Greater physical contact among older females could be a function of the
group compositions of my sample; all females in groups larger than a pair were living with kin
(Appendix 3). Related females are more likely to maintain close proximity and grooming
relationships both in the wild (Nakamichi and Koyama 1997) and in captivity (Taylor 1986), while
unrelated individuals generally spend more time alone. The presence of kin in the social group
might help to increase the survival of old individuals by providing more social partners,
particularly for grooming. Conversely, older individuals with less kin support might be at a
disadvantage that might make them more susceptible to extrinsic sources of mortality. For
example, grooming plays an essential role not only in solidifying social bonds but also in removing
parasites that could lead to infection and even death.

60
Senescence and disability are often viewed as equivalent states with respect to fitness: that
the old and disabled will not survive due to impairment. However, Lilah’s case study reveals that,
in the captive setting of the Duke Lemur Center, her injury does not seem to impair her activity
compared to other females. Millette et al. (2009) found that dentally impaired ring-tailed lemurs
spent more time feeding and foraging in the early afternoon rather than resting like other members
of their social group. Foraging while others are resting reduces the competition over food objects
and could be a way to compensate for their impairment. In this study food stealing occurred only
three times in Lilah’s social group during the observation period, but two of those three times
Sosiphanes stole food from Lilah. Lilah’s injury might impede her ability to obtain and hold onto
food in a group-feeding context. If Lilah were in a larger social group where there might be more
competition to obtain and keep food, she might have to utilize an alternative strategy to meet
energetic and nutritional needs, such as foraging while others are resting.
Furthermore, Sosiphanes’ presence in Lilah’s social group could be an important social
resource for her. Notably, disabled Japanese macaque females were found to have less social
affiliates than unimpaired individuals (Turner et al. 2014). These authors indicate that presence of
kin in a group helps to increase the number of social partners a disabled individual has. Therefore,
having a related female in Lilah’s group might have significantly bolstered her level of sociality
compared to her being in a group with an unrelated female. Overall, the smaller social group size
in this provisioned environment along with maternal presence in the group might provide a buffer
for Lilah. This case study reveals how individual-dependent factors like disability and social group
composition interact to affect behavior and sociality. This capacity to modify behavior and benefit
from the social environment are two possible key factors that have helped primates to
accommodate the challenges of aging that have led to longer lifespans in the primate order.
61
Primate Buffers against Senescence-Associated Mortality
Based on my findings, the ability to be behaviorally flexible and the benefit of social groups
could help buffer some individuals from both extrinsic and intrinsic sources of mortality. As an
order, primates have a great capacity for behavioral flexibility that allows for many species to
occupy a diverse variety of environments and niches. Part of this plasticity is being able to
accommodate challenges through modification in the amount of time spent on an activity or how
the activity is done often to reduce the amount of energy expended. Sprite’s reduction in activity
level in this study could be a behavioral modification to accommodate the physiological challenges
associated with senescence. Furthermore, older females were found to respond to affiliative
vocalizations at a significantly higher frequency than adult females. No significant difference was
found between male age groups, but males tended to initiate affiliative vocalizations while females
responded with a higher frequency. These results suggest that older females might be using
vocalizations as a means of grooming close social group members from a distance. Ring-tailed
lemurs are more likely to respond to a frequently-groomed partner’s affiliative vocalizations than
an individual that they rarely groom (Kulahci et al. 2015); this groom-at-a-distance strategy of
maintaining close ties within a social group could be a way for older individuals to maintain social
ties while expending less energy. A similar pattern has been observed in older Japanese macaque
females as a means of maintaining social relationships with non-kin social partners with reduced
energetic cost (Mitani 1986). Behavioral flexibility may be an essential tool to accommodate the
challenges associated with senescence. Learning to accommodate these challenges would have led
to gradual increases in longevity and could explain the trend towards longer lifespans in the
primate order.
62
I found support for the hypothesis that older ring-tailed lemurs would maintain engagement
in the social group. Old individuals might have a higher motivation to be social because it helps to
buffer these individuals against extrinsic sources of mortality, like predation and parasitism, that
group living helps to prevent. Evidence in Barbary macaques (Almeling et al. 2018) suggests that
older primates might have a higher motivation to be social than younger individuals in the social
group. No significant differences in initiated and received affiliative events between the age groups
existed. Therefore, I failed to support the hypothesis that old individuals would initiate more social
interactions than adult individuals. These results suggest that not only are old individuals still
socially engaged in the group, but that they are also actively pursuing affiliative interactions rather
than passively receiving the social advances of other members. This active pursuit of social
behaviors also supports the idea that old individuals are still motivated to engage in social behavior.
Therefore, higher degrees of sociality in older ring-tailed lemurs of a wild population could provide
a selective advantage against extrinsic mortality.
Social groups also can provide inherited advantages such as higher rank or association with
a dominant matriline (Roach and Carey 2014). For example, had Sprite been living in a wild social
group, though she might experience a decline in activity level as a result of the reproduction-
maintenance trade off, her higher fecundity might help to buffer her against this challenge because
she might have more support from her female offspring. Future work should examine both the
costs and benefits sociality might confer to older individuals. For example, the highly-agonistic
social environment observed with ring-tailed lemurs might be more stressful for lower-ranked
females (Cavelli et al. 2003), which could lead to faster physiological decline in certain systems.
Social groups also allow for individuals with varying levels of experience live together.
Older individuals have been thought to contribute their experience and wisdom to collectively
63
support the whole social group by fulfilling a specific role in the group (Roach and Carey 2014).
With respect to my third research question, I found very preliminary indications that ring-tailed
lemur old individuals might fill the role of grandmother in the social group. Shroeder carried her
granddaughter Griselda both on average more times but also more frequently than other non-
maternal kin in this study (Table 40). These findings indicate that older individuals have the
potential to take on an allomaternal role in this species. Similar patterns have been found in
chimpanzees (Hayaki 1988) and hanuman langurs (Borries 1988). Future work exploring this
question should take into account the potential energetic cost that allmothering might have on an
individual.
During the mating season, Shroeder was given a contraception injection, but she was not
on birth control during the rest of the year. Her prior behavior indicates that she might be
particularly interested in infants when she does not have her own. Allomothering is common in
both captive (Taylor 1986, Periera and Izard 1989) and wild ring-tailed lemurs (Gould 1992).
Instances of facultative grandmothering in hanuman langurs suggest that these individuals seem
to only help out their grandchildren when there is minimal cost to themselves, especially since
these old individuals showed signs of visual and hearing impairment (Borries 1988). Therefore,
grandmaternal carrying might have been observed in the captive setting of the DLC because of the
energetic buffers this environment can provide since food is nearly-unlimited. Furthermore, the
presence of a grandmother in the social group of a wild populations seems to provide stability to
the social group, with more females being evicted and higher levels of aggression occurring right
after her death (Soma and Koyama 2012). Similar observations have been documented in rhesus
macaques (Wooddell 2016) suggesting that older individuals can also play an essential role in
reducing stress levels by helping to stabilize the social group. Such social roles might not only
64
help the fitness of individuals but also the group as a whole. While aspects of the social group
might differentially help older individuals more, the group can benefit from the experience and
wisdom of having old individuals actively engaged in the group. Having value to the whole group
could reduce the socially-negative effects of senescence-associated impairment. For example,
individuals might not target an older female if she helps guide them to food resources during times
of scarcity. Furthermore, the interactions between senescence and sociality are heavily
environment-dependent. It is thus important to note how the captive environment has shaped my
findings.
Captivity Caveats
Small Sampling Size and Limited Group Composition
In finding a location for my study, locating a captive population with an adequate sample
size proved to be a challenge. As noted above, the sizes of the social groups of my sample
population are considerably smaller than those seen in the wild. These smaller groups limited the
degree to which I could measure how aging might affect factors such as social rank, number of
offspring, and social network size. For example, I had no means of determining how older age
might affect male-male interactions and social rank because I had no social groups that contained
more than one old male or a combination of old and adult males. Had old males been allowed to
interact with other males, their measures of sociality could have been similar to old females, as
affiliative social interactions among males in the same social group are high during the non-mating
season (Gould 1999). Observing more male-male interactions would also helped to describe how
males might differentially allocate resources in favor of competition for mating opportunities.
Understanding male competition is essential for understanding how reproduction-maintenance
trade-offs can affect patterns of senescence in this sexually monomorphic species.

65
Older males were found to spend significantly more time in total locomotion and moving.
Older males were also found to lead more instances of group traveling than younger males.
However, I was not able to conclude that these higher rates of locomotion and leading during travel
were a function of these older males’ age. In wild populations (Gould 1999, Nakamichi and
Koyama 1997), males in the social group frequently seek to drive out solitary or migrating males
from a particular group’s territory. Part of this male-male agonism are stink fights which are
observed fairly frequently in the wild. As noted before, I observed only five total instances of stink
fighting between males during the course of my entire study. Therefore, the higher rates of travel
seem to be more a function of the captive environment rather than age: males were moving around
more to look for other ring-tailed lemur males.
Other research (Corr 2000) on primate social gerontology was able to characterize rhesus
macaque social networks, finding that aged female networks were smaller, while old males had
larger networks compared to those younger. A network-based approach helps to quantify and
characterize which individuals from all the options an animal chooses to affiliate with. The smaller
social groups of my sample provide very limiting social options. Therefore, I was not able to apply
such an approach to this sample population to small social groups.
Reduction in Agonism among Individuals
A practice when feeding the lemurs at the DLC was to spread out the food throughout a
designated feeding site. This was done to reduce female agonism during feeding so that each
individual in a social group could have equitable access to the provisioned foods. This practice
severely impaired my ability to establish dominance ranks for the individuals in this study in the
context of feeding. Furthermore, a significant amount of the agonism among individuals in wild
populations are in the context of feeding. For example, only 14% of the agonism observed at the
66
Bezà Mahafaly Special Reserve could be categorized as non-feeding (Sauther 1993). Therefore,
this reduced-agonistic state of the DLC might not adequately represent species-specific patterns
with respect to age.
Additionally, all of the social groups in my study consisted of females from the same
matriline per group, with either maternal or grandmaternal relationships between older individuals
and those younger. Therefore, the composition of these groups might help to remove the agonistic
pressure during feeding that can often occur between multiple matrilines. Tension among
matrilines can even be fatal at the DLC (Charpentier and Drea 2013) and in wild populations
(Kittler and Dietzel 2016). This single matrilineal group composition might enable the old females
to maintain their high rank with less challenges than if there were more than one matriline present.
67
Conclusions
Old ring-tailed lemurs at the Duke Lemur Center still maintained their engagement in the
social group. Old females appeared to be more socially engaged than adults. These results indicate
that in this captive setting, age-associated physiological change does not appear to impair an
individual’s ability to remain engaged in the social group. I also found that, as a whole, the old
behavioral profile of both male and female individuals was not distinct from adults. These results
suggest that older individuals do not have to significantly modify their behavior to accommodate
age-related physiological challenges, at least in a captive setting. Most of the differences that I
observed between the age categories, such as those with male locomotion and number of
antipredator vocalizations, were most likely a function of the captive environment. I found
preliminary support that old females can help care for their daughter’s offspring (grandmothering)
in the form of carrying an infant on her back.
This work reveals how aspects of captivity can affect the study of behavioral and social
manifestations of senescence which further reveals the importance of testing these questions in the
wild. My study provides concrete evidence that research with senescence should decouple old age
and senescence as the same phenomenon, in that one can occur without the other. Furthermore,
work with senescence should focus on inter-individual variation rather than differences between
the old and adult cohorts. Important individual factors like sex, rank, kin relationships, and
disability can affect patterns of senescence. This research reveals how behavioral flexibility and
sociality can help buffer aging primates against somatic decline with possible implications for the
increase in longevity across the primate lineage.

68
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Appendix 1: Behavioral Definitions

Definitions are based upon an ethogram for ring-tailed lemurs developed and utilized by Sauther
(1992) and further refined by Millette (2007) with the addition of Stink Fight (s) and Displace (d)
as separate behaviors. I also included infant-related behaviors: Riding(r) and Nursing(n).
Event/Point Behaviors
Agonistic
Bite (b) – The mouth is used to forcefully and agonistically grasp a social partner with
the dental apparatus. Biting behavior is directional, and may be initiated by the animal against a
social partner or may be received from a social partner. Behavior has been combined into the
category of “Agonism” for purpose of analysis.
Cuff (c) – Animal makes contact with the palm of the hand or wrist against the head or
face of a social partner. Cuffing behavior is directional, and may be initiated by the animal
towards a social partner or may be received from a social partner. Behavior has been combined
into the category of “Agonism” for purpose of analysis.
Chase (h) – Animal locomotes towards and pursues a social partner who withdraws and
departs away from the animal directing the chase. The directing animal peruses the social partner
following withdraw for at least one meter. Chasing is a directional behavior and may be initiated
by the focal animal towards a social partner or may be received from a social partner. Behavior
has been combined into the category of “Agonism” for purpose of analysis.
Displace (d) – Animal moves towards another animal and causes that animal to vacate its
location. This is a directional behavior, and may be initiated by the focal animal towards a social
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partner or may be received from a social partner. Behavior has been combined into the category
of “Agonism” for purpose of analysis.
Fight (f) – Agonistic encounter between the focal animal and a social partner involving
biting, grappling, chasing and physical contact. Fight is a directional behavior. Initiated is scored
if focal animal unidirectionally commences Fight towards a social partner. Received is scored if
a social partner unidirectionally commences FI towards the focal animal. Behavior has been
combined into the category of “Agonism” for purpose of analysis.
Food Steal (f) – Animal displaces an animal engaged in feeding and then consumes that
animal’s food item. Food steal may also involve taking a food item from an animal through use
of agonistic behaviors such as fighting, cuffing or biting. Food steal is a directional behavior.
Initiated is scored if focal animal takes a social partners food. Received is scored if a social
partner takes the focal animal’s food item. Behavior has been combined into the category of
“Agonism” for purpose of analysis.
Jump Fight (j) – Agnostic encounter in which one individual attacks another through
jumping. Behavior has been combined into the category of “Agonism” for purpose of analysis.
THIS BEHAVIOR WAS NOT OBSERVED.
Nip (n) -- Animal uses the anterior dentition to quickly and lightly grasp a social partner
with the anterior portion of the dental apparatus. Nipping behavior is directional, and may be
initiated by the animal towards a social partner or may be received from a social partner.
Behavior has been combined into the category of “Agonism” for purpose of analysis.
Slap (s) – Animal makes contact with the palm of the hand against a social partner. This
behavior is directional, and may be initiated by the animal towards a social partner or may be
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received from a social partner. Behavior has been combined into the category of “Agonism” for
purpose of analysis.
Stink Fight (s) – An agonistic encounter in which an animal rubs the carpal spurs against
the sternal glands, “charges” the tail with the carpal spurs, and subsequently directs the tail
towards the face of a social partner. Direction of the tail towards a social partner is also
accompanied by movement of ears to a posterior position in which they lie flat against the head.
Directing stink fight is limited to male individuals, although males may attempt to SF with
females. SF is a directional behavior. Initiated is scored if focal animal unidirectionally
commences SF towards a social partner. Received is scored if a social partner unidirectionally
commences stink fight against the focal animal. Mutual is scored if both animals initiate SF
simultaneously. Behavior has been combined into the category of “Agonism” for purpose of
analysis.
Affiliative
Approach (a) – Focal animal locomotes within one meter of a social partner, or a social
partner locomotes within one meter of the focal animal. AP is a directional behavior. Initiated is
scored if the focal animal locomotes to within one meter of a social partner. Received is scored
if a social partner locomotes to within one meter of the focal animal.” Behavior has been
combined into the category of “Affiliative” for purpose of analysis.
Nose Poke (n) – Focal animal and a social partner briefly touch noses. Nose poking is
most frequently seen as two animals approach and “greet.” NO is a mutual social behavior.
Other (Socially Neutral)

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Scent Mark (s)-- Focal animal marks a target object (most frequently a small branch or
tree) utilizing scent glands in the anal/genital region, carpal spurs and the sternal glands,.
Behavior has been combined into the category of “Other” for purpose of analysis.
Defecate (D) – Focal animal excretes feces through the anus.
Stand (S) – Individual maintains a vertical posture in which the posterior limbs are used
to support the entire weight of the body and the anterior limbs are not in contact with the ground
or other substrate. Standing may be accompanied by visual monitoring.
Urinate (U) – Focal animal excretes urine through the urethral opening.
State Behaviors
Affiliative
Nearest Neighbor (N)— Establishes the number of social group members are within 2
meters of the focal individual. Can be 0-6 individuals.
Social Groom (g) – Individual is observed pass the toothcomb or anterior portion of the
muzzle (in cases of toothcomb loss) through the fur. Grooming is most frequently observed to
feature a rhythmic anterior-posterior movement of the head during which the toothcomb is used
to remove ectoparasites. Grooming behavior is frequently marked by licking in addition to
passing the toothcomb through the fur. Grooming is a directional behavior. Social grooming may
consist of initiated grooming in which the focal animal is subject to grooming by conspecific
partner, received grooming where the focal animal grooms a conspecific partner, and mutual
grooming in which the focal directs grooming towards a social partner while simultaneously
receiving grooming.
Social Rest (R) -- Focal animal is not engaged in any other defined behavior and is in
physical contact with at least one other individual. Resting behavior features a lack of any
82
locomotor activity. If an observed behavior cannot be categorized but includes physical contact
with another individual, social rest is assigned.
Social Sleep (S) – Focal animal is motionless with eyes closed and is in physical contact
with at least one other individual. Sleep may be scored with the eyes slightly open (e.g. the pupil
is obscured) as individuals frequently only partially close their eyes. If eyes open while
attempting to determine closure status or the eyes are obscured rest is scored.
Infant-Related States
Riding (r)—One or more infants cling to the ventral or dorsal surface of focal individual
while the focal individual is moving. If individual is not moving, then infant(s) and focal are in
social rest.
Nursing (n)—One or more infants seen to be making oral contact with focal individual’s
nipple. If mouth to nipple contact is not visible, then social rest is used.
Other
Drink (d) -- Focal animal ingests water through the mouth. Water may be ingested either
by licking a water source or by using the hand to “cup” water from a source. Drink may be
scored for either ingestion of water from a concentrated source such as a bucket of water or a
puddle, or by licking items as dew-wet leaves or damp concrete. Behavior has been combined
into the category of “Other” for purpose of analysis.
Feed/Forage (f) – Focal animal searches for, selects, manipulates, processes, and ingests
food items. Behavior commences with processing a food item or mastication. Feed/forage
behavior is broken once the focal animal has been observed to cease mastication. Behavior has
been combined into the category of “Other” for purpose of analysis.

83
Mate (m) – Focal animal engages in copulatory behavior with a conspecific social
partner and most frequently includes intromission of the penis into the vulva. Intrasexual
mounting behaviors are also included within MA. THIS BEHAVIOR WAS NOT OBSERVED.
Movement (m) – Individual locomotes across a distance not less than one meter but no
greater than 10 meters. Movement includes all forms of locomotion (e.g. walking, leaping,
climbing, running and, galloping), but does not include minor repositioning or postural changes
while engaged in other behaviors.
Out of View (O) – Individual is not visible to the observer.
Play (p) – Individual engages in behaviors which may include mock fighting, non-
agonistic chasing, light wrestling, jumping, and high-velocity movement or travel. Play may be a
social behavior or a solitary behavior. Social play is typically accompanied by a “play face,”
marked by a wide gape of the mouth without bearing of teeth. Behavior has been combined into
the category of “Other” for purpose of analysis.
Solitary groom (g) -- Individual is observed pass the toothcomb or anterior portion of the
muzzle (in cases of toothcomb loss) through their own fur. Grooming is most frequently
observed to feature a rhythmic anterior-posterior movement of the head during which the
toothcomb is used to remove ectoparasites. Grooming behavior is frequently marked by licking
in addition to passing the toothcomb through the fur.
Solitary Rest (R) -- Focal animal is not engaged in any other defined behavior. Resting
behavior features a lack of any locomotor activity. If an observed behavior cannot be
categorized, RE is assigned.
Solitary Sleep (S) – Focal animal is motionless with eyes closed and making no physical
contact with other individuals. Sleep may be scored with the eyes slightly open (e.g. the pupil is
84
obscured) as individuals frequently only partially close their eyes. If eyes open while attempting
to determine closure status or the eyes are obscured rest is scored.
Sun (S) -- Focal animal exposes the ventral surface towards the sun in a stereotyped
vertical sitting position where the arms are placed laterally to the torso and legs. Sunning animals
often close the eyes or turn the head away from the sun. In such cases of closed eyes, sleep is not
scored. Sun may be scored if one arm is not placed laterally to the torso or inside legs, if as to
maintain balance or prevent a fall. Sun occurs most frequently during cold periods.
Travel (T) – Individual locomotes for a distance greater than 10 meters. Movement
includes all forms of locomotion (e.g. walking, leaping, climbing, running and, galloping).
Individual may pause for a short period (no more than 2-3 seconds) during a travel bout, as to
engage in activities such as locating the next point of movement or viable substrate, prepare to
leap, or wait for another individual to clear from the line of movement. Traveling behavior was
designated individual (I) traveling if focal individual and/or some of the group was moving or
group (G) traveling if all individuals were involved in the behavior. Behavior is considered a
subset of the locomotion behaviors.
Watch Observer (W) – Individual visually monitors and/or visually tracks the observer.
Visual monitoring must be clearly directed towards the observer. Short “glances” directed
towards the observer or monitoring in which the animal monitors several visual targets in rapid
succession are not included within this behavioral category.

85
Appendix 2: Sampling Schedule
Sampling Date of Sampling Date of

Day Sample Group # Day Sample Group #
1 23-May No Sampling: July 4th
2 24-May No Sampling: July 4th
3 25-May 31 6-Jul NHE7
4 26-May 32 7-Jul NHE3
W. 1 5 27-May NHE3 W. 7 33 8-Jul NHE9
No Sampling: Memorial Day 34 11-Jul NHE4
6 31-May NHE4 35 12-Jul NHE3
7 1-Jun NHE4/NHE* 36 13-Jul NHE4
8 2-Jun NHE4 37 14-Jul NHE4
W. 2 9 3-Jun NHE2 W. 8 38 15-Jul NHE3
10 6-Jun NHE2/NHE3 39 18-Jul NHE9
NHE9/NHE
11 7-Jun NHE3 40 19-Jul 7
W. 3 14 10-Jun NHE2 W. 9 43 22-Jul NHE3
18 16-Jun NHE9 W. 47 28-Jul NHE9
W. 4 19 17-Jun NHE4 10 48 29-Jul NHE9
20 20-Jun NHE4 49 1-Aug NHE10
21 21-Jun NHE4 50 2-Aug NHE7
NHE7/NHE
22 22-Jun NHE3 51 3-Aug 8
23 23-Jun NHE4 W. 52 4-Aug NHE4
W. 5 24 24-Jun NHE9 11 53 5-Aug NHE8
25 27-Jun NHE9
26 28-Jun NHE7/NHE9
NHE7/NHE9/NHE
27 29-Jun 4
28 30-Jun NHE4/NHE9
W. 6 No Sampling: July 4th
86
Appendix 3: Pedigree Charts for Study Subjects

Pedigrees were generated thanks to open-source data from the DLC. Squares indicate males
and circles indicate females. Individuals that were included in this study are in green.
87

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THE SOCIAL BEHAVIOR AND DYNAMICS OF OLD RING-TAILED LEMURS (LEMUR

Kathleen Marie McGuire

B.S., Georgia Institute of Technology, 2014

This thesis entitled:

IACUC protocol # A168-14-07

Thesis directed by Professor Michelle L. Sauther

how age has shaped evolutionary trajectories among primates.

collection, management, and analysis.

social lives, while relentlessly encouraging me to pursue this work.

not been possible without the support of these institutions.

Chapter 1: Introduction ............................................................................................................... 1

Individual Factors ..................................................................................................................... 46

Table 5. Study Animals………………………………………………………………………..…24

Table 7. Female Individual Analysis of Physical Contact Time………………………………….30

Table 10. Male Individual Analysis of Locomotion and Movement Times……………………...32

Table 11. Male Individual Analysis of Travel Times…………………………………………….33

Table 13. Female Individual Analysis of Feeding/Foraging Times……………………………...34

Table 15. Female Individual Analysis of Total Resting Time……………………………………35

Table 16. Female Individual Analysis of Social Resting Time………………………………….36

Table 17. Female Individual Analysis of Solitary Resting Time…………………………………37

Table 20. Male Individual Analysis of Social Resting Time……………………………………..38

Table 21. Male Individual Analysis of Solitary Resting Time…………………………………...39

Table. 39. Social Ranks of Study Individuals……………………………………………………47

Table 40. Non-Maternal Carrying Behavior of Griselda…………………………………………48

Table 41. Male Individual Analysis of Social Proximity Time………………………………….49

Figure 2. Adult Causes of Death…………………………………………………………………17

Figure 3. Old Individual Causes of Death……………………………………………………….19

Figure 4. Map of the Duke Lemur Center’s Natural Habitat Enclosures………………………..22

Figure 9a. & 9b. Pictures of Lilah……………………………………………………………….51

of damage in favor of resource allocation towards reproduction and support of offspring

expectancies of individuals (see Monaghan et al. 2008).

Though mechanistic-based studies are important to understand how senescence occurs on

To begin exploring these metrics, sources of mortality must be explored.

physiological changes occur. Focusing on specific phenotypical manifestations of advanced age

can be determined based on behavioral observations.

Why Studying “Old” Primates Matters

of reducing the effect of disability or senescence is to flexibly modify behavior which is

accommodate senescence compared to other taxonomic groups.

and what behavioral patterns characterize this cohort of individuals.

Defining Old Primates and Their Behavioral Profile

detailed perspective of physiology so that we have an understanding of what normal, both

primate behavioral and social gerontology much be conducted.

Old Social Involvement in Nonhuman Primates

accommodate the challenges of senescence is to reduce their degree of sociality. Informed by

of their social behavior should be distinct from younger individuals.

behavior. Directionality, such as initiating or receiving grooming behavior, is also measured to

sociality at a lower energetic cost to themselves.

The Biology of Aging in Primates

termination (Pavelka and Fedigan 1999) with a post-reproductive lifespan.

individual or a population (Singleton et al. in press).

Individual Factors and Old Primate Social Behaviors

Individual-specific factors such as sex, dominance rank, membership in a dominant

compared to younger males, suggesting that there is not a species-specific strategy to

The Social Role of Older Primates

the death of an old “grandmother” in a social group leads to social instability.

Lemur catta as a Suitable Model for Primate Aging

L. catta (ring-tailed lemur) are strepsirrhine primates endemic to southwestern

rooted in the primate order.

Studying Aging in Captivity

maintain healthy populations in captivity.

Besides the direct implications of husbandry research, captive populations provide an

becomes what leads to mortality in these environments?