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COOPERATION, COMPETITION AND KINSHIP IN THE SOCIAL
RELATIONSHIPS AMONG SPOTTED HYENAS, CROCUTA CROCUTA

By

Sofia Anne Wahaj

A DISSERTATION

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

Department of Zoology
Program in Ecology, Evolutionary Biology and Behavior

2004

ABSTRACT

COOPERATION, COMPETITION AND KINSHIP IN THE SOCIAL
RELATIONSHIPS AMONG SPOTTED HYENAS, CROCUTA CROCUTA

B y
Soﬁa Anne Wahaj

The focus of this dissertation is on social bonds, competition, and
cooperation among related and unrelated spotted hyenas (Crocuta crocuta).
Gregarious animals that live in permanent social groups experience intra-group
competition and are expected to repair social bonds damaged by within-group
conﬂict. Indeed, reconciliation in many primates takes the form of affiliative
behavior occurring shortly after a conﬂict. Here | inquired whether reconciliation
also occurs among spotted hyenas (Crocuta crocuta), gregarious carnivores
whose social lives share much in common with those of cercopithecine primates.
An afﬁliative behavior was only identiﬁed as having a conciliatory function in
hyenas if it occurred more frequently after than before ﬁghts, and if it was also
associated with reduced rates of aggression between former opponents after
fights. Greeting behavior and friendly approach satisfied both these criteria.
Mean conciliatory tendency (CT) for individual hyenas was 11.3%, which fell at
the low end of the CT range observed among primates.

Kin selection theory predicts that social interactions should vary with
relatedness. I examined patterns of afﬁliation, association and aggression to
inquire whether spotted hyenas can distinguish among various groups of
maternal and paternal siblings. I also considered familiarity-based recognition

and phenotype matching as mechanisms hyenas might use to recognize kin. My

data clearly indicate that hyenas can discriminate among various types of
siblings, that their social behavior conforms to predictions of kin selection theory,
and that they recognize kin using mechanisms of both familiarity and phenotype
matching.

Spotted hyena cubs exhibit intense intra-litter aggression immediately
after they are born. Indirect evidence suggests that intense early sibling
aggression might function in nature to kill siblings, resulting in either obligate or
facultative siblicide. One of my aims was to determine what factors inﬂuence the
occurrence and frequency of aggression among Crocuta siblings, and another
was to use ultrasonography of pregnant females to test predictions of obligate
and facultative models of siblicide. I compared litter sizes in utero to litter sizes
after birth to determine frequency of litter reductions in both captive and field
settings. Although litters born to multiparous captive females were larger at
parturition than were litters of wild multiparous females when cubs were ﬁrst seen
above ground, litter composition did not differ. Litter reductions were common
and observed at the same rate in both captive and wild populations. Not only did
cubs from twin litters have higher survivorship than cubs from singleton or triplet
litters, but cubs from twin litters whose siblings survived for at least three months
had higher survivorship than those whose siblings died before three months of
age. These data directly contradict predictions of the obligate siblicide
hypothesis, but are consistent with those of an hypothesis suggesting that

siblicide occurs facultatively in this species.

Copyright by
SOFIA ANNE WAHAJ

2004

ACKNOWLEDGEMENTS

First and foremost, I would like to thank Dr. Kay Holekamp for her
mentorship, guidance and support throughout my graduate career. I consider
myself extremely lucky to have had the opportunity to work with someone as
special as Kay. She has helped to make all my dreams a reality, supported me
during my “growing pains”, and been an overall outstanding advisor. I cannot
thank her enough. I

I appreciate the comments and guidance provided by my committee
members, Drs. Laura Smale, Tom Getty, and Lyn Clemens. They have helped
me to think more critically and broadly. Michigan State University and the
National Science Foundation have provided me with several years of fellowship
support, for which I am very thankful. The College of Natural Sciences, the
Graduate School, the department of Zoology, as well as the program in Ecology,
Evolutionary Biology and Behavior, have all provided me with funding and
logistical support. I would also like to thank the Zoology office staff for answering
my many questions and keeping me organized. My research has been a part of
the Mara Hyena Project, which has been funded by National Science Foundation
grants IBN9309805, IBN9630667, lBN9906445, IBNO113170, and IBNO343381.
I thank the Ofﬁce of the President of Kenya for permission to conduct this
research. I also thank the Kenya Wildlife Service, the Narok County Council, and
the Senior Warden of the Masai Mara National Reserve for their cooperation.

I would like to thank Joe Kolowski for being such a special friend, having a

great sense of humor, and making my years in the field one of the most

memorable times in my life. Jaime Tanner has been a fantastic friend both in
East Lansing and in the ﬁeld, and I appreciate her sincerity and warmth. Russ
Van Horn, Cindy Wei, and Eva-Maria Muecke have provided me with consistent
support, advice and friendship throughout my graduate career. Page Van Meter
has become a wonderful friend of mine and has made this semester one of my
best semesters at MSU.

My life at Michigan State University has been enriched by my friends and
colleagues in the Holekamp lab. They have provided me with invaluable
comments and advice, as well as social outlets. I thank Sarah Benson-Amram,
Pat Bills, Erin Boydston, Stephanie Dloniak, Anne Engh, Keron Greene, Karen
Hubbard, Joe Kolowski, Suzanne La Croix, Sarah Lansing, Terri McElhinny, Toni
Lyn Morelli, Eva-Maria Mueke, Jenn Smith, Micaela Syzkman, Jaime Tanner,
Kevin Theis, Wiline Trouilloud, Russ Van Horn, Page Van Meter, and Heather
Watts for all their help. I am lucky to be part of such a large lab. Pat Bills
deserves special recognition for assisting me with all my technical problems.

I am indebted to the numerous individuals that collected data used in this
dissertation project, including Rebecca Bankson, Nancy Berry, Erin Boydston,
Susan Cooper, Stephanie Dloniak, Martin Durham, Anne Engh, Paula Garrett,
lsla Graham, Keron Greene, Tyson Harty, Kay Holekamp, Joe Kolowski, Keith
Nelson, Karen Nutt, Gabe Ording, Laura Smale, Jenn Smith, Micaela Szykman,
Jaime Tanner, Russ Van Horn, Heather Watts, Kim Weibel, and Brad White.

Ned Place, Steve Glickman, and Mary Weldele graciously gave me

lessons in ultrasonography on the hyenas in the captive colony at the University

vi

of California Berkeley Field Station. Steve provided and Mary organized the data
from the captive colony that l have used in Chapter 5. Steve also provided
valuable suggestions on many phases of my research. I would especially like to
thank Ned Place for ‘opening doors' to me at the University of California,
Berkeley. I thank both Ned Place and Steve Glickman for providing a light at the
end of the tunnel by securing me a postdoctoral position at Berkeley.

The genetic analyses on paternal kin relations in Chapter 3 could not have
been done without Kim Scribner, Russ Van Horn, and Anne Engh. I am very
thankful for their hard work in the lab. I would also like to thank Kevin Guse, Toni
Van Horn, Rachel Dreyer, Ryan Hilgris, and Jessica Schwarz for extracting data
from archived notes and collaborating with me to publish Chapters 2 and 3 of this
dissertation. I appreciate the comments and useful suggestions from Filipo
Aureli on Chapter 2. I am grateful to Susan Alberts, who provided valuable
feedback for improving Chapter 3.

l have left many friends in Kenya. John Keshe has been one of the most
kind and caring people I know. I could not have survived without him. Moses
Sairowa has taken good care of me and provided me with lots of laughs. Anne
Engh and Micaela Syzkman showed me the ropes of recording hyena behavior
and introduced me to life at hyena camp. Keith Nelson taught me
ultrasonography techniques in the ﬁeld. Jaime Tanner, Joe Kolowski, Stephanie
Dloniak, and Jenn Smith were all remarkable co-workers in the ﬁeld. I thank
Andrew Peart and Milton and Elly Kirkman for balloon rides across the Mara,

champagne breakfasts, chats around the fire and rescuing me when the land

vii

cruiser got stuck. Nigel and Barbara Dundas have welcomed me into their home
in Nairobi on numerous occasions and made my life more comfortable in Kenya.
Countless others helped me out at various times, and I thank them all.

Finally, I owe many thanks to many people that have supported me
outside of Michigan State University. Cory Monteiro and Dale Taylor have been
as strong as family to me. Natalie Bourdon has been there for me through
everything, and I love her like a sister. Chris Peterson has been a very
supportive and exceptional friend I can always count on. Dave Urbina has the
biggest heart of anyone I know and I am so lucky to have him in my life. Last,
but not least, I extend a very special thanks to my family for their unconditional
love and support throughout my life. I have been fortunate to have so many

people that care for me.

viii

TABLE OF CONTENTS
LIST OF FIGURESXI

CHAPTER 1
GENERAL |NTRODUCTION1
Overview of chapters5

CHAPTER 2

RECONCILIATION IN THE SPOTTED HYENA (CROCUTA

CROCUTA).... . 9
Introduction 10
Methods ........................................................................................... 14
Results22
Discussmn27

CHAPTER 3

KIN DISCRIMINATION IN THE SPOTTED HYENA (CROCUTA CROCUTA):

NEPOTISM AMONG SIBLINGS... .....37
Introduction38
Methods42
Result552
Discussmn58

CHAPTER4

FACTORS INFLUENCING SIBLING AGGRESSION IN THE SPOTTED HYENA

(CROCUTA CROCUTA).... . . ... ... .. ... ......74
Introduction.. 74
Methods79
Result587
Discuss10n92

CHAPTER 5

USE OF ULTRASONOGRAPHY TO TEST OBLIGATE AND FACULTATIVE

MODELS OF SIBLICIDE IN THE SPOTTED HYENA (CROCUTA

CROCUTA)... .108
Introduction .................................................................................... 108
Methods114
Results122
DlSCUSSl0n131

LITERATURE CITED ................................................................................ 147

ix

LIST OF TABLES

Table 3.1. Kin and non-kin groups compared in Chapter 3. Mean coefficient of
relatedness is indicated by ”r.” Animals indicated as “sharing a den” spent at
least 4 months living together concurrently at one or more communal dens.
“Body size” indicates whether or not the members of pairs within each group
were approximately the same size during early development. Individuals born
within a few months of each other are roughly the same size ......................... 64

Table 3.2. Predictions for interactions among spotted hyenas generated by kin
selection theory (in regular font) and by hypotheses suggesting two possible
mechanisms of kin recognition (in bold font), familiarity-based recognition and
phenotype matching. “>” denotes the prediction that greater afﬁliation, higher
rates of coalition formation, and lower rates of dyadic aggression should be seen
in one group than the other if kin recognition occurs via that mechanism, whereas
“=” denotes a prediction that the two groups should treat each other similarly.
Predictions in bold face indicate those that differ between the familiarity
hypothesis and phenotype matching hypothesis of kin recognition; in the -
remaining (non-bolded) cases, predictions of both hypotheses are the same....65

Table 3.3. Summary of results from Chapter 3, with statistically signiﬁcant
differences indicated by asterisks. Comparisons 1 — 4 (in regular font) test
predictions of kin selection theory, and comparisons 5 — 8 (in bold font) test
predictions of hypotheses suggesting mechanisms by which hyenas might
recognize kin. Asterisks indicate P < 0.05 .................................................. 66

Table 5.1. Neonatal litter sizes born to multiparous females that were directly

observed in Chapter 5 compared to those observed earlier by Frank et al. (1991 ),
who used only multiparous females in their analysis. “N” indicates the number of
litters born... ....................................................................................... 138

Table 5.2. Sex ratios among litters born to wild and captive hyenas .............. 138

LIST OF FIGURES

Figure 2.1. Rates at which a) greetings and approaches occurred within hyena

dyads during 5 min intervals before and after ﬁghts (each bar presents data from
137 individual victims), and b) aggression occurred within individual dyads during
post-ﬁght intervals with and without greetings or friendly approaches .............. 33

Figure 2.2. Latency to ﬁrst greeting or appeasement behavior after 411 ﬁghts in
which both members of each dyads could subsequently be observed for 15
minutes .............................................................................................. 34

Figure 2.3. Number of total first occurrences of conciliatory behavior occurring
during each minute-long interval before and after 698 ﬁghts .......................... 35

Figure 2.4. Percent conciliatory tendency of a) 83 individual hyenas observed to
play roles in different fights of both victim and aggressor, b) 28 individual victims
observed to interact in different fights with both kin and non-kin ...................... 36

Figure 3.1. Mean percent of scans in which individual hyenas were observed
playing and feeding together with a) full-sibling littermates and maternal half-
siblings, b) full-sibling littermates and paternal half-siblings, and c) full-sibling
littermates and non-kin. Mean association indices are also shown for each set of
animals. All pairs represented here were matched for sex, age, and relative
social rank. Sample sizes represent numbers of individuals. Statistically
significant differences are indicated with an asterisk .................................... 67

Figure 3.2. Mean percent of scans in which individual hyenas were observed
playing and feeding together with a) maternal half-siblings and non-kin, b)
maternal half-siblings and half-sibling littermates, c) maternal and paternal half-
siblings, and. Mean association indices between individual hyenas and members
of both comparison groups are also shown. All pairs represented here were
matched for sex, age, and relative social rank. Other notation is as in Figure

3.1 .................................................................................................... 69

Figure 3.3. Mean hourly rates at which coalitions formed within dyads composed
of full-sibling littermates, half-sibling littermates, maternal half-siblings, paternal

half-siblings, and non-kin. Sample sizes represent numbers of dyads. Statistically
significant differences are indicated with asterisks over brackets .................... 71

Figure 3.4. Mean percent of scans in which pairs of full- and half-sibling
littermates were observed playing and feeding together. Mean association
indices between full- and half-sibling littermates are also shown. Sample sizes
represent numbers of sibling dyads. Statistically significant differences are
indicated with an asterisk ....................................................................... 72

xi

Figure 3.5. Mean percent of scans in which individual hyenas were observed
playing and feeding together with their paternal half-siblings and unrelated
animals. Mean association indices are also shown. All pairs represented here
were matched for sex, age, and relative social rank. Other notation is as in
Figure 3.1 .......................................................................................... 73

Figure 4.1. Mean hourly rates of intra-litter aggression during each two month
age interval in the first year of life. The sample represented by each data point
includes 24 litters in which both cubs survived to 12 months. Statistically
significant differences are denoted with an asterisk .................................... 102

Figure 4.2. Mean percent of aggressive interactions between siblings during the
1-6 (black bars) and 7-12 (gray bars) month age intervals that we observed in the
contexts of ‘milk’, “solid foods’, and contexts ‘other’ than milk or solid foods. The
sample represented in each pair of bars includes 24 litters in which both cubs
survived to 12 months. Statistically significant differences are denoted with
asterisks ........................................................................................... 103

Figure 4.3. Mean hourly rates of aggression during the 1-2 month age interval
within same- and mixed-sex litters in which females (black bars) and males (gray
bars) were the dominant cubs. Sample sizes above bars represent number of
litters in each group. Other notations are as in Figure 4.2 ........................... 104

Figure 4.4. Mean hourly rates of aggression during the 1-2 month age interval
within same-sex (gray bars) and mixed-sex litters (black bars) born to mothers of
high and low rank. Other notations are as in Figure 4.3 .............................. 105

Figure 4.5. Hourly rates of intra-litter aggression during the 1-2 month age
interval as a function of local prey abundance. Sampled litters include 24 high-
ranking litters and 22 low-ranking litters ................................................... 106

Figure 4.6. Mean percent of all aggressive interactions during each two month
age interval in which hyenas directed aggression toward their litter-mates (black
bars) or towards unrelated peers within their cohorts (gray bars). The sample
here includes 21 litters in which both cubs within each twin litter survived to 12
months. Total aggressive interactions included 354 ﬁghts directed toward
siblings and 237 fights directed toward cohort peers during the ﬁrst 12 months of
life. Statistically significant differences within each age interval are indicated by
asterisks ........................................................................................... 107

Figure 5.1. Sonographic images of a) early pregnancy (gestational age here was
43 days) indicated by the presence of a gestational sac and thickened
endometrial cavity. The gray donut-shaped outer circle is the endometrial wall of
the uterine horn and the dark hypoechoic center represents the amniotic ﬂuid and
the developing fetus, b) late pregnancy (gestational age here was 97 days)
indicated by skeletal development as well as an observable heartbeat. The

xii

vertebrae and ribs of the fetus are indicated by the hyperechoic white bands
across the screen. The arrow points to the ﬂuttering cardiac region .............. 139

Figure 5.2. Percent of all litters that contained one, two or three cubs when
observed in utero and again as neonates in a) captive and b) wild hyenas
examined during pregnancy with ultrasonography. Numbers above bars
represent numbers of litters of each type ................................................. 140

Figure 5.3. Matched pairs comparisons within pregnancies of litter size before
and after birth in captive and wild hyena populations. Numbers above bars
represent numbers of pregnant females examined via ultrasonography.
Significant differences are indicated with asterisks ..................................... 141

Figure 5.4. Mean age at which cubs were observed above ground in wild litters
for which we had an opportunity to see cubs. Numbers above bars represent
litters in each group. Significant differences are noted with an asterisk .......... 142

Figure 5.5. Mean litter sizes before and after birth compared between
primiparous and multiparous hyenas in captivity and in the wild. Neonatal litter
sizes are reported for both ultrasounded and non-ultrasounded hyenas.
Numbers above bars represent litters in each group. Signiﬁcant differences are
indicated with asterisks ........................................................................ 143

Figure 5.6. Percent of wild twin litters of each type born to a) both multiparous
and primiparous females in the current study compared to expectations based on
a binomial distribution and b) multiparous females from the current study
compared to those monitored by Frank et al. (1991). Sample sizes above bars
represent number of litters of each type observed ...................................... 144

Figure 5.7. Survivorship of a) 112 singleton cubs, 208 cubs from twin litters, and
6 cubs from triplet litters; b) 26 cubs from all-female litters, 84 cubs from mixed-
sex litters, and 36 cubs from all-male litters, and c) 142 individuals from twin
litters whose litter-mate lived longer than 3 months and 32 individuals whose twin
died before 3 months of age .................................................................. 145

xiii

CHAPTER ONE
GENERAL INTRODUCTION

Many animals live in groups that contain both kin and non-kin, and they
generally cooperate and compete with individuals of both types on a daily basis.
Kin selection theory (Hamilton 1964) predicts that relatives should be more
valuable and more reliable social partners than non-kin under a wide variety of
circumstances, that relatives should compete less intensively than non-kin, and
that relatives should cooperate more frequently than non-kin. The purpose of my
dissertation is to test these predictions in one species of gregarious carnivore,
the spotted hyena (Crocuta crocuta). My dissertation compares social bonds,
competition and cooperation between related and unrelated hyenas, and the
factors that shape these phenomena. Chapters comprising my dissertation focus
on conﬂict resolution, kin discrimination, and sibling rivalry in the spotted hyena.

Living in groups inevitably involves costs to individuals, but group-living
persists because the fitness of individual group members exceeds that of solitary
conspecifics. Whereas resource competition is perhaps the most common cost
of life in groups, cooperation with group-mates to acquire or defend resources
and fend off predators are common benefits (Alexander 1974). Competitive and
cooperative behavior is often best understood, not in terms of single interactions,
but in terms of patterns of interactions between two individuals that occur over
extended time periods. Such patterns of interaction define an animal’s social
relationships (Hinde 1976). Animals that live in groups have opportunities to

form long-term cooperative relationships, and these are particularly common

among close kin (Fletcher et al. 1987). However, formation of enduring
cooperative relationships with non-kin, through mutually advantageous exchange
of beneﬁts, often represents another effective way to increase individual
reproductive success (Walters 1987).

Social relationships may have long-term adaptive consequences for the
individuals involved, particularly for long-lived animals, such as elephants,
cetaceans, carnivores and primates, who often interact with the same group
members throughout their lives. The social system of spotted hyenas resembles
that of many Old World primates (Mills 1985; Frank 1986; Henschel et al. 1987),
in which females remain in their natal group, or clan, throughout their lives while
males disperse to join other clans as adults. Spotted hyenas regularly cooperate
during group hunts, territorial advertisement and defense, and defense of
individual carcasses from both inter— and intra-speciﬂc competitors (Kruuk 1972).
Hyena social groups, called clans, are structured by linear dominance
hierarchies, much like the hierarchies that structure troops of cercopithecine
primates. Among females, dominance status is determined by maternal rank,
and rank remains quite stable throughout a female’s lifetime. Among adult
immigrant male hyenas, dominance rank appears to be determined primarily by
length of tenure in the group (Henschel et al. 1987). In stable groups of
mammals, where individuals interact repeatedly over extended time periods, the
presence of a dominance hierarchy speeds settlement of disputes over access to
particular resources (Pusey et al. 1997). In hyena society, an individual's

position in the hierarchy determines its priority of resource access, and high-

ranking females and their offspring have the best resource access in the entire
group. This superior resource access allows high-ranking females to enjoy the
greatest reproductive success (Holekamp et al. 1996). One important form of
cooperative behavior among free-living Crocuta is coalition formation (Zabel et al.
1992), which often enhances the competitive effectiveness of individuals within
the clan. Coalitionary attacks among spotted hyenas tend to reinforce the
existing dominance hierarchy (Zabel et al. 1992).

As is also true in cercopithecine primates, spotted hyenas prefer to
associate with and direct affiliative behavior toward individuals who are higher-
ranking than themselves (East at al. 1993). In fact, high-ranking female Crocuta
are more popular social companions than are lower-ranking females (Holekamp
et al. 1997). Thus, it appears that hyenas, like many primates, recognize that
some group members are more valuable social partners than others. The value
of a relationship reﬂects the magnitude of social or ecological beneﬁts likely to
accrue from it, with valuable relationships most worthy of maintenance and
protection (Kummer 1978; Cords 1988; Cords et al. 2000). When individuals
interact repeatedly over long periods of time, the security and reliability of
relationships also become important factors shaping sociality in long-lived
gregarious animals. Greeting ceremonies among hyenas, an expression of
affiliative behavior in which individuals inspect each other’s anogenital region, are
often preferentially directed at dominant animals. These greeting ceremonies
may represent one means of strengthening social bonds within the clan (Kruuk

1972; East et al. 1993).

Aggression is often a manifestation of competition within groups and it
represents an integral part of most social relationships. Aggressive behavior in
the spotted hyena occurs in a variety of contexts, and it varies in intensity from
subtle intention movements to killing bites. With their powerful musculature and
sharp teeth, spotted hyenas are well-equipped to cause serious injury to attacked
individuals. Aggressive interactions among spotted hyenas are typically
characterized by approach or attack by one or more dominant animals directed at
a lower-ranking individual, who responds with unambiguous submissive behavior
and withdrawal (Smale et al. 1993). Female Crocuta are generally more
aggressive than males, and male aggression toward other males is relatively low
in frequency and intensity (Szykman 2001 ).

Because the genetic interests of individuals are not identical, conﬂicts of
interest perpetually endanger the survival of cooperative relationships (Silk
1987). Even the most intimate kin, such as mothers and offspring, interact in
both affiliative and competitive ways (Trivers 1972; Nicolson 1987). Siblings are
often the closest relatives within a population, and they are often one another's
most direct competitors as well (Alexander 1974). Thus, relationships between
siblings represent a mix of cooperative and competitive interactions. Female
spotted hyenas give birth to one or two cubs (rarely three) in an isolated natal
den (East et al. 1989). When cubs reach 2-4 weeks of age, they transfer their
cubs to the clan’s communal den, where up to 20 offspring from several different
females may reside concurrently (Kruuk 1972). Siblings live in close proximity

during early life and interact in a variety of ways, such as huddling together,

playing together, nursing together, grooming one another, fighting, establishing
dominance relationships within the litter, and sharing food. Siblings may also
suppress one another’s growth and reproduction (Golla et al. 1999). Sibling
relationships in spotted hyenas may be shaped by a number of different
variables, and part of this dissertation focuses on elucidating factors that
determine when hyena siblings should cooperate and when they should act

selfishly.

OVERVIEW OF CHAPTERS

The highly structured group life characteristic of most gregarious species
did not evolve through a decline in aggressive and competitive tendencies, but
rather through the development of mechanisms to deal with such tendencies (de
Waal 1987). Reconciliation is one form of conﬂict resolution animals may use to
repair social relationships damaged by aggression. Reconciliation is an
important behavioral mechanism regulating social relationships and reducing
social tension in hierarchical primate societies (Aureli et al. 2000). Given that
hyenas and many cercopithecine primates live in similarly complex societies, in
Chapter Two I sought to determine whether spotted hyenas possess
reconciliation tendencies comparable to those found in primates. Here |
demonstrate that greeting and non-aggressive approach behavior serve a
conciliatory function in spotted hyena society since these behaviors occur more
frequently after than before fights, and they also tend to reduce the probability of

subsequent attack. Conciliatory tendency, a measure of reconciliation behavior,

in spotted hyenas is relatively low when compared to that documented in
primates, and may reﬂect the ﬁssion-fusion nature of hyena society. That is,
whereas cercopithecine primates live in highly cohesive societies in which
individuals are always together, spotted hyenas have the option of using
dispersive mechanisms of conﬂict resolution by separating after fights rather than
reconciling. Although kin selection theory predicts social relationships with kin
should be more valuable than those with non-kin, I found that kin exhibited lower
conciliatory tendencies than did non-kin. These results suggest relationship
security, which is higher within kin than non-kin dyads, has a stronger effect on
conciliatory tendency in Crocuta than does relationship value. The work
presented in Chapter Two has been published in Ethology (Wahaj et al. 2001).

Because kinship can have profound effects on social relationships, kin-
differentiated behavior in gregarious mammals requires significant social
discrimination abilities (Sherman et al. 1997). Although earlier studies (e.g.
Holekamp et al. 1999) suggested that Crocuta could discriminate maternal kin
from non-kin, genetic data were not available until now to permit analyses of kin
recognition abilities among other kin classes, including paternal kin. Full siblings,
half-siblings, and non-kin each share different proportions of their genes, yet all
of these kin classes overlap in time and space within spotted hyena clans.
Chapter Three demonstrates that hyenas can discriminate among these
relatedness classes, and that they cooperate most with their most closely related
kin. I further illustrate that hyenas use mechanisms of both familiarity and

phenotype matching to differentiate among various categories of siblings.

Results of Chapter Three have recently appeared in Behavioral Ecology and
Sociobiology (Wahaj et al. 2004).

Sibling rivalry in the form of sibling aggression is unusually intense and
frequent in young spotted hyena cubs (Frank et al. 1991 ). Chapter Four attempts
to determine what factors inﬂuence the occurrence and frequency of aggression
between Crocuta siblings. Independent variables considered here include cub
age, litter composition, identity of the target of aggression and resource
availability. This study illustrates intense sibling aggression during the first two
months of life, when neonates are establishing infra-litter rank relationships, with
rates of aggression decreasing thereafter. Although maternal rank did not have a
significant inﬂuence on aggression between Crocuta litter-mates in this study,
levels of local prey abundance were negatively correlated with rates of intra-litter
aggression, suggesting that resource availability inﬂuences rates of fighting
between siblings. Results of Chapter Four suggest that competitive relationships
among spotted hyena siblings are not invariant, but instead ﬂuctuate with shifting
environmental conditions.

Although spotted hyena cubs clearly display intense aggression during
early neonatal life, the adaptive significance of this early fighting is not clear. It
has been suggested in the literature that this early aggression routinely results in
sibling death (Frank et al. 1991). Obligate siblicide, as is observed in some avian
species (reviewed in Mock et al. 1997), occurs when aggression between
siblings is almost always fatal to the subordinate individual. However, in

facultative siblicide, siblings adjust fighting intensity as costs and beneﬁts of intra-

litter aggression vary with environmental conditions. Chapter Five tests
predictions of obligate and facultative models of siblicide in wild spotted hyenas
using ultrasonography techniques to assess litter reduction in captive and wild
hyenas. Litter sizes and patterns of litter reduction in captive and wild hyenas
were similar, and survivorship data suggest individuals survive better with a
sibling than without one. Thus, results from both Chapters Four and Five provide
support for the facultative model, but contradict predictions of the obligate model

of siblicide in the spotted hyena.

CHAPTER TWO

Wahaj, S. A., K. R. Guse, and K. E. Holekamp (2001). Reconciliation in the
spotted hyena (Crocuta crocuta). Ethology 107: 1057 — 1074.

CHAPTER TWO
RECONCILIATION IN THE SPOTTED HYENA (CROCUTA CROCUTA)

INTRODUCTION

Gregarious animals that live in permanent social groups experience intra-
group competition, and are therefore expected to exhibit non-dispersive forms of
conﬂict resolution (de Waal 1986; de Waal 1989). Aggression often has negative
consequences aside from injury and resource loss in that it may also damage
social relationships. An attacked animal may be uncertain about the aggressor=s
future Intent regarding either tolerance or further aggression (Aureli 1992). Thus,
behavioral mechanisms are often needed after ﬁghts to repair social relationships
and reduce the uncertainty experienced by victims of aggression regarding their
future social interactions with aggressors. De Waal & Van Roosmalen (1979)
suggested reconciliation behavior as one mechanism that might modulate
aggressive conﬂicts among primates. Deﬁning reconciliation as “any friendly
reunion between former opponents occurring soon after an agonistic conﬂict”,
they documented its occurrence in chimpanzees. Since 1979, conciliatory
behavior has also been described in many other primate species (reviewed in
Aureli et al. 2000).

Whereas affiliative post-conﬂict behavior has now been widely studied in
primates and appears to occur throughout this entire order (de Waal 1986; de
Waal 1986; Kappeler et al. 1992; de Waal 1993; Silk 1997; Aureli et al. 2000; de
Waal 2000), few data exist on post-conﬂict behavior in non-primate mammals

(reviewed by Schino 2000). Data on this from a wide array of taxa, particularly

10

from gregarious animals other than primates, are needed to develop a more
comprehensive understanding of the social conditions under which it occurs, the
cognitive capacities required for it (Kappeler et al. 1992; Kappeler 1993), and the
selective forces that have shaped its evolution (Silk 2000).

We focus here on reconciliation behavior observed among free-living
spotted hyenas (Crocuta crocuta). These are gregarious carnivores whose
complex social lives share much in common with those of cercopithecine
primates (Holekamp et al. 1991; East et al. 1993; Holekamp et al. 1999). Both
spotted hyenas and old-world primates are long-lived mammals that live in
permanent social groups, the members of which cooperate to acquire and defend
resources (Henschel et al. 1991; Harcourt 1992; Boydston et al. 2001). Spotted
hyenas also often depend on help from other group members during hunts of
large-bodied prey, defense of ungulate carcasses against inter— and intraspeciﬁc
competitors, and coalition formation important in both the acquisition and
maintenance of social rank (Kruuk 1972; Zabel et al. 1992; Holekamp et al. 1997;
Engh et al. 2000). Thus, as also occurs in primates, the enduring social
relationships found among these long-lived carnivores affect survival and
reproduction of individual group members.

Like those of many primates, social groups of spotted hyenas usually
contain multiple adult males and several matrilines of adult female kin with
offspring, including individuals from several overlapping generations. Males in
both hyena and cercopithecine primate societies disperse from their natal groups

whereas females are usually philopatric (Cheney et al. 1983; Henschel et al.

11

1987; Pusey et al. 1987; Mills 1990; Smale et al. 1997). Spotted hyenas appear
to recognize the other members of their social group as individuals using visual,
olfactory (Kruuk 1972), and acoustic cues (East et al. 1991; Holekamp et al.
1999). In social groups of Crocuta, macaques, baboons, and vervet monkeys,
adults can be ranked in a linear dominance hierarchy, members of the same
matriline occupy adjacent rank positions, and female dominance relations are
stable for extended periods and across a variety of contexts (Tilson et al. 1984;
Andelman 1985; Frank 1986). In hyenas as in many primates, an individual’s
position in the group’s hierarchy strongly determines its priority of access to food
(Kruuk 1972; Frank 1986). The one respect in which hyena societies differ from
those of cercopithecine primates is that, among adults, female hyenas are
socially dominant to males. Female dominance is very rare in primates other than
lemurs (Kappeler 1993).

Reconciliation is an important behavioral mechanism regulating social
relationships and reducing social tension in hierarchical primate societies (Aureli
et al. 2000). Given that primates and hyenas live in similarly complex societies,
we sought to determine whether spotted hyenas possess reconciliation
tendencies comparable to those found in primates. First, we inquired whether
spotted hyenas reconcile by comparing rates at which various afﬁliative
behaviors occur before and after ﬁghts, and ensuring that emission of particular
affiliative behaviors is subsequently associated with reduced aggression between
former opponents. Second, we attempted to identify variables affecting

conciliatory tendencies (CTs) among hyenas (de Waal et al. 1988; Kappeler et al.

12

1992; Chaffin et al. 1995). Speciﬁcally, we examined post-conﬂict behavior in
Crocuta in light of theoretical expectations based on potential costs and beneﬁts
to the individuals involved (Schino 2000).

Levels of direct feeding competition, both within and between social
groups, are extremely high in Crocuta, and this should theoretically favor high
rates of conciliatory behavior in this species compared to others in which feeding
competition is less intense (van Schaik 1989; Sterck et al. 1997.). On the other
hand, Crocuta live in fission-fusion societies in which dispersive conﬂict
resolution is always a viable option for individuals that are attacked by
conspecifics. Thus Crocuta might be expected to reconcile their conﬂicts less
frequently than do members of more cohesive groups, and instead avoid short-
term costs of conﬂict by separating from former opponents (Schino 2000).
Spotted hyenas are well armed, so risk of injury to recipients of aggression from
continued or escalated fighting is high in this species. Since repair of social
bonds should therefore be more valuable to recipients of aggression than
aggressors, we anticipated that recipients would be more likely to reconcile than
aggressors. Close relatives in Crocuta associate most closely, are most likely to
hunt together, and join most frequently as allies during coalition formation (Smale
et al. 1995; Holekamp et al. 1997; Holekamp et al. 1997). Therefore, if social
behavior of Crocuta conforms to predictions of the ‘valuable relationship’
hypothesis (Kummer 1978; Cords 1988), then kin should exhibit greater CTs than
non-kin. Alternatively, if relationship security (Kummer 1978; Cords 1988) affects

probability of reconciliation, then kin should exhibit lower CTs than non-kin, since

13

interactions among non-kin are considerably less predictable and more

aggressive in this species than are interactions among kin.

METHODS

Subjects and Study Site

This study took place study between June 1988 and April 1998, in the
Talek region of the Masai Mara National Reserve, Kenya, an area of open rolling
grassland. Subjects were members of one large Crocuta clan that occupied an
area approximately 65 km5. The borders of the home range of the Talek clan
have been stable since at least 1979 (Frank 1986).

All members of the Talek clan were identiﬁed by their unique spot patterns
and other conspicuous characteristics, such as ear notches. We determined the
sex of each clan member using methods described by Frank et al. (1990). We
estimated their birth dates (to _ 7 days) by using their pelage, size, and other
aspects of their appearance and behavior when cubs were first observed above
ground (Holekamp et al. 1996). Here we considered individuals up to the age of
two years to be juveniles, and older animals were classiﬁed as adults. On
average during each year of the study period (N=10 yrs), the Talek clan
contained 25 j; 1 adult females, 18 1 2 adult males, 16 j; 1 juvenile females, and
15 i 2 juvenile males.

Mother-offspring relationships were established based on regular nursing
associations, and other genealogical relationships within matrilines were as

described by Holekamp et al. (1993). Although information about paternity was

14

unavailable for many hyenas used as subjects in this study, we were able to
compare CTs between kin and non-kin by calculating coefﬁcients of relatedness
(r, Hamilton 1964) from matrilineal pedigrees for members of each hyena dyad,
based on the assumption that there is no multiple paternity within twin litters.
Because we found previously that vocal recognition of maternal kin occurs
among animals with r-values as small as 0.125 (Holekamp et al. 1999), we
defined kin here as members of dyads with r-values of 0.125 or greater.

Social ranks were determined based on wins and losses in dyadic
agonistic interactions, as described previously (Holekamp et al. 1990). Brieﬂy,
we identified the subordinate member of a dyad engaged in an agonistic -
interaction as the animal responding with retreat and appeasement behavior to
aggression directed at it by its social partner. Aggressive behaviors monitored
throughout this study included head wave, lunge, aggressive posture (ears
cocked forward while the tail was bristled and raised), chase, displace, stand
over, bite, and push. Appeasement behaviors included head-bob, grin, open-
mouth appeasement, carpal crawl, skitter away, and submissive posture (body
crouched with tail between legs and ears ﬂattened back against the head).
These behavior patterns have been described in detail elsewhere (Kruuk 1972;
Frank 1983; Holekamp et al. 1990). Outcomes of agonistic interactions were
organized into a hierarchical matrix from which each individual hyena could be
assigned an 'absolute’ social rank in the clan's dominance hierarchy (Martin et al.

1988). Rank distance was then calculated between members of each hyena

15

dyad by subtracting the absolute rank of the subordinate individual from that of

the dominant animal. '

Data Collection

Throughout the study period, observers were present in the study area at
least 23 days/month except for April 1991, when observers were present for 14
days. We observed members of the Talek clan daily from our vehicles, which we
used as mobile blinds. An observation session started when we found two or
more hyenas separated from other hyenas by at least 200m. Observation
sessions occurred at natal and communal dens, at ungulate kills, and away from
both dens and kills as, for example, when animals were traveling or resting.
Throughout every observation session, we recorded all occurrences (Altmann
1974) of aggression and appeasement behavior by all hyenas present. Agonistic
behavior recorded during every dyadic aggressive interaction included both the
aggressive behavior emitted by the initiating individual, and the response to that
aggression emitted by its victim. We assigned each aggressive act to a category
describing its intensity as low (head wave, aggressive posture), medium (lunge,
displace, stand over), or high (push, chase, bite). Responses to aggression
emitted by victims included retreat, appeasement behavior, failure to respond,
and counter-attack.

During observation sessions we conducted 30 minute focal animal
observations on particular individuals, including adults and juveniles of both

sexes. During each focal animal observation period, the following eight

16

candidate affiliative behaviors were recorded if either the focal animal directed
them toward a recent opponent or that opponent directed them toward the focal
individual: sniff, groan (a friendly ‘come-hither’ vocalization), lick, lie or rub
against, initiate play, present, greet, and friendly approach to within one meter of
the former opponent. During a greeting one hyena lifted its hind leg and offered
its genitals for inspection to the other animal, who often reciprocated and sniffed
them while raising its own hind leg. Presenting involved one hyena standing
perpendicular to its social partner and stretching both its hind legs out posteriorly
to give the social partner opportunity to sniff its belly or genitals. During a friendly
approach, the focal animal expressed no signals of aggressive intent with either
body postures or facial expressions, although the approaching animal often
showed unambiguous expressions of fear (e.g. grinning with ears back) as it
came near a former opponent (Kruuk 1972). When the recipient of an attack
responded with retreat accompanied by these signs of fearfulness, this was not
considered to be affiliative behavior. Instead this was recorded as a response to
conspecific aggression, and was therefore considered part of the original fight.
However, when an individual subsequently initiated a new interaction with its
former opponent by approaching with no aggressive intent, yet while emitting
signs of nervousness or fear, we considered this to be affiliative behavior. Given
the impressive weapons carried by these animals, and the abundant
opportunities for dispersive conflict resolution in the fission-fusion society
characteristic of this species, approach without aggression toward a recent

opponent appeared to represent an unambiguous, even risky, afﬁliative gesture.

17

When reviewing printed field notes, we selected focal animal observations
in which a dyadic agonistic interaction occurred, and in which victim and
aggressor were present within 200 m of each other for at least 5 minutes before,
and 5 minutes after, the ﬁght. A total of 220 focal animal observations were used
that involved 73 hyenas and their 87 social partners, with an average of 3.01 1
0.32 focal animal observations per individual. We recorded the occurrences of
all afﬁliative behaviors during both pre- and post-ﬁght intervals, calculated the
rates at which each occurred during the post-conﬂict interval, and used the pre-
conﬂict interval as a matched control (de Waal et al. 1983). We elected to use
the pre-conﬂict interval as a matched control period rather than use a
comparable control interval on a different day, because the same set of individual
hyenas are rarely found together at the same time and under the same
circumstances on different days in the fission-fusion society characteristic of this
species (Hofer et al. 2000). We were able to use a small subset of samples
(N=14 dyads) to compare behavior within dyads on days they fought with that
observed within 30 days of the original conﬂict, on days when they did not ﬁght.
However, we were generally unable to use these superior control intervals
preferred by primatologists in our field study, as has also been the case in some
earlier field studies of reconciliation in primates (e.g. Cheney et al. 1989) and

hyenas (e.g. Hofer et al. 2000).

18

Data Analysis ‘

We required that any afﬁliative behavior satisfy two criteria to be
considered as a functional conciliatory gesture. First, we required that a
particular affiliative behavior occur at a higher rate during the 5 min post-ﬁght
interval than during the 5 min pre-fight interval. Our rate data were not normally
distributed so we used Wilcoxon matched-pairs signed-rank tests to compare
mean rates at which particular affiliative behaviors were emitted by individuals
during the pre-ﬁght interval with mean rates of behavior exhibited by those same
individuals during the post-fight interval. After eliminating those afﬁliative
behaviors that did not occur at signiﬁcantly higher rates after than before ﬁghts,
we used Wilcoxon matched-pairs signed rank tests to compare mean rates of
attack on individuals during post-conflict periods when one of the remaining
affiliative behaviors occurred with mean rates of attack on those same individuals
during post-conﬂict periods when no afﬁliative behaviors were emitted. Functional
conciliatory behaviors were identified as those for which attack rates in the
former post-conflict intervals were lower than those observed during the latter
post-conﬂict intervals. Mann Whitney tests were used to compare rates at which
different affiliative behaviors were emitted within each time interval.

After specific affiliative behaviors were identified as having a conciliatory
function, we examined the temporal patterning of occurrences of these
behaviors, and used Chi-square tests to compare the probability of initial
occurrence of each identified affiliative behavior during each minute of both pre-

and post—conﬂict periods. Using fights as the units of analysis, we constructed a 2

l9

by 2 contingency table for each minute, in which columns represented pre- or
post-conﬂict intervals and rows whether or not initial affiliative contact was
observed during that minute. In comparing pre- and post-conﬂict intervals here,
we numbered minutes moving forward in time during the post-conﬂict period, and
moving backward in time from the conﬂict during the pre-fight interval. Thus for
example, the Chi-square analysis performed for Minute 1 compared events
occurring during the first minute after ﬁghts with those occurring during the last
minute before fights.

We next calculated CTs within hyena dyads (Veenema et al. 1994), and
inquired whether these were affected by kinship, age-sex classes of opponents,
and rank distance between opponents. In these calculations, a hyena pair was
called 'attracted’ (A) if conciliatory behavior between opponents occurred earlier
in the post- than in the pre-conﬂict interval, or if it occurred only during the post
conﬂict period. A pair was called 'dispersed' (D) if conciliatory behavior between
opponents occurred earlier in the pre- than the post-conﬂict interval, or if it
occurred only before the fight. A pair was considered 'neutral' (N) if conciliatory
behavior between opponents occurred at the same time in respective intervals,
or if no conciliatory behavior occurred in either interval. We then calculated the
CT for all hyena pairs using the formula, [CT=(A-D)/(A+D+N) * 100], suggested
by Veenema et al. (1994). A Wilcoxon matched-pairs signed rank test was used
to compare the number of attracted to the number of dispersed pairs per

individual. To compare our results with those from studies of reconciliation in

20

other species, the Wilcoxon matched-pairs signed rank test was used to compare
the number of attracted pairs to the number of dispersed pairs per individual.

In analyses of effects of speciﬁc independent variables on CT, we mainly
used individual hyenas as the units of analysis, and used individuals as their own
controls. For example, to examine the effect of kinship on reconciliation behavior,
we calculated a mean CT for each individual in its interactions with kin, and we
also calculated a mean CT for that same individual during its interactions with
non-kin. We then compared these mean CTs for kin and non-kin across all
individuals observed to interact with both groups, using a Wilcoxon signed rank
test. Similarly, to ascertain whether victims or aggressors exhibited higher-CTs,
we calculated a mean CT for each individual in interactions when it was the
aggressor, and calculated a second mean CT for that same individual when it
was the victim in ﬁghts. We then compared these mean CTs for victims and
aggressors across all individuals observed to play both roles, using a Wilcoxon
signed rank test.

Next we used the dyad as the unit of analysis to inquire whether CT varied
with the age-sex classes of the opponents involved in fights. For recipients of
aggression of each age-sex class, we calculated mean CTs in interactions with
each age-sex class of attacker, and compared these means using Kruskal-Wallis
tests. We also compared CTs of males and females using a Mann-Whitney test.
Since our study spanned several years, we were able to compare the CTs of

individual observed when they were juveniles with the CTs of those same

21

individuals when they were observed as adults, using a Wilcoxon signed rank
test.

Dyads were used as the units of analysis in Kruskal-Wallis tests to
determine whether CT varied with context in which the fight occurred (at dens,
over food at kills, or away from both dens and kills), or intensity of aggression
occurring during the fight (low, medium or high). Finally, to determine whether CT
was affected by rank distance, we regressed the CTs calculated for dyads
against the rank distance between victim and aggressor within each of those
same dyads to obtain a Spearman’s rank correlation coefficient. Differences
between groups were considered signiﬁcant when P5 0.05. All statistical tests

were two-tailed.

RESULTS

During the study period we observed 160 hyenas participating as either
victims or aggressors in 698 ﬁghts in which we could monitor the behavior of both
victim and aggressor for at least ﬁve minutes before and after the ﬁght, and in
which the full five minutes preceding the fight elapsed without any aggression
between these opponents. On average, each individual hyena was involved in
8.7 1 0.9 conﬂicts. In total, 494 different hyena dyads were involved in the 698
fights. Of the eight candidate affiliative behaviors recorded during focal animal
surveys, only five satisfied our first criterion for classification as reconciliation
behavior. That is, rates at which individuals emitted afﬁliative behaviors were

significantly higher in the post- than the pre-ﬁght interval for the following

22

behaviors: greet (Z=2.848; P=0.004), present (Z=2.807; P=0.005), friendly
approach (Z=-2.475; P=0.013), rub or lie against (Z=-2.023; P=0.043), and lick
(Z= -2.805; P=0.005). None of the other three candidate afﬁliative behaviors
satisfied our first criterion so these were not considered further (play: Z=-1.841,
NS; groan: Z=-0.631, NS; sniff: Z=0.069, NS). We subsequently treated present
and greet together as one category of affiliative behavior, which we called
’greetings,‘ and the other three behaviors that satisfied our first criterion were
treated together as ’approaches.‘

Individual hyenas initiated greetings at signiﬁcantly lower rates than they
initiated friendly approaches during both pre- and post-ﬁght intervals (Figure
2.1a: pre-conflict interval Mann Whitney U= 10350, N=137 individuals, P < 0.001;
post-conﬂict interval U= 11224, N=137 individuals, P < 0.001 ). Both greetings
(Wilcoxon 2: 3.028, N=137 individuals; P < 0.001) and approaches (Wilcoxon 2:
3.918; N=137 individuals; P < 0.001) occurred at higher rates after than before
fights (Figure 2.1a). Furthermore, hyenas experienced lower rates of attack by
their former opponents when they greeted or approached them during the post-
conflict interval than when these same individuals neither greeted nor
approached their former opponents (greeted: Wilcoxon Z= 3.290; N=19
individuals; P=0.001; approached: Wilcoxon 2: 4.871; N: 44 individuals; P <
0.001; Figure 2.1 b). Thus, both greetings and approaches satisﬁed both our
criteria for classification as conciliatory gestures.

In 411 of the 698 fights, both opponents remained together for at least 15

minutes after the conﬂict. In these 411 cases, which involved 96 hyenas that

23

participated on average, in 4.27 1- 0.43 ﬁghts per individual, we found that initial
greetings occurred most commonly during the ﬁrst two minutes immediately after
the ﬁght, but that initial greetings were observed up to 9 minutes after the ﬁght
(Figure 2.2). Similarly, initial approaches occurred most commonly during the first
three post-conﬂict minutes, but were observed up to 12 minutes after the ﬁght
(Figure 2.2). We found that over 72% of all greetings and 74% of all approaches
occurred within the first 5 minutes after the ﬁght. Therefore, in order to maximize
sample sizes in subsequent analyses, we used all 698 ﬁghts in which opponents
could be observed together for 5 min before, and 5 min after, the conﬂict.
Latency to occurrence of the ﬁrst afﬁliative behavior in these 698 ﬁghts
was greater before than after the ﬁght (Figure 2.3). Thirty two percent of initial
affiliative contacts occurred during the minute after fights, whereas only 13% of
initial affiliative contacts occurred during the last of ﬁve minutes before the ﬁght.
After identifying approaches and greetings as functional reconciliation
behaviors, we found that 14.6% of 698 ﬁghts were followed by approaches or
greetings during the 5-minute post-conflict interval, whereas only 4.4% of these
fights were preceded by these affiliative gestures during the 5—minute pre-conﬂict
interval. Of the 494 dyads involved in these ﬁghts, 17.6% had positive
conciliatory tendencies compared to 5.1% with negative conciliatory tendencies.
Spotted hyenas increased their affiliative contacts with former opponents after
conﬂicts compared with control periods in 698 fights (96 attracted pairs; 29
dispersed pairs; mean CT per individual = 11.3%). Thus individual hyenas

participated in significantly greater numbers of attracted than dispersed pairs

24

(Wilcoxon Z= -4.687; N=140 individuals; P<0.001). For 14 dyads, we were able
to calculate CTs using a matched control period on a different day within 30 days
of the observed ﬁght, when no fight occurred between these two individuals.
Here we found that CTs calculated as [(Attracted-dispersed)/ total PC-MC pairs]
did not differ from CTs calculated for the same dyads as [(Attracted-dispersed)/
total PC-BC pairs], where BC=the preconﬂict period, PC=the post-conﬂict period,
and MC= a matched control period on a different day when no ﬁght occurred.
Both calculations yielded identical mean CTs of 16.6% (Wilcoxon Z=0.00; NS;
N=14 dyads).

In 89% of 698 fights, victims were of lower social rank than aggressors.
Eighty-three hyenas were observed to be both victims in some ﬁghts and
aggressors in others. When individuals were victims, their mean CTs were
significantly higher than when they were aggressors (Figure 2.43: Wilcoxon Z= -
2.846; N=83 individuals; P=0.004). The "vast majority of 698 ﬁghts (88.4%)
occurred within non-kin dyads. Twenty-eight hyenas were observed to be
recipients of.aggression in fights with both kin and non-kin. The mean CT among
kin calculated for these 28 animals was negative, indicating that kin do not
reconcile their fights, and was significantly smaller than the mean CT calculated
for non-kin (Figure 2.4b: Wilcoxon Z=2.367; N=28 individuals; P=0.018).

We found no significant differences in CTs among dyads containing
various combinations of age-sex classes. Speciﬁcally, we compared CTs of
adult female victims when their aggressors were adult females, adult males,

juvenile females, or juvenile males, and found that CT did not vary with age-sex

25

class of the aggressor (Kruskal-Wallis T= 2.059, NS, N=97 adult female
aggressors, 8 adult male aggressors, 18 juvenile female aggressors, and 13
juvenile male aggressors, NS). We also examined the CTs of adult male victims
in various dyad types, but found no significant differences based on age-sex
class of aggressor (Kruskal-Wallis T= 2.788, NS, N=89 adult female aggressors,
19 adult male aggressors, 9 juvenile female aggressors, and 10 juvenile male
aggressors, NS). Although adult males never attacked juveniles, we found that
CTs did not vary significantly when juveniles of either sex were attacked by peers
or by adult females (juvenile female victims: Kruskal-Wallis T= 1.635, NS, N=67
adult female aggressors, 18 juvenile female aggressors, and 20 juvenile male
aggressors; juvenile male victims: Kruskal-Wallis T= 1.635, NS; N=67 adult
female aggressors, 35 juvenile female aggressors, and 22 juvenile male
aggressors). After determining that there were no signiﬁcant differences among
age-sex classes, we compared CTs among female-female dyads, female-male
dyads, and male-male dyads, but we found no differences (Kruskal-Wallis T:
1.15, N=189 female-female, 246 female-male, and 50 male-male dyads, NS).
CT also did not vary among dyads containing opponents of different ages
(Kruskal-Wallis T= 0.825, N: 215 adult-adult, 186 adult-juvenile, and 96 juvenile-
juvenile dyads, NS). We found no difference in mean CTs between male and
female victims (Mann-Whitney U: 2551.5, N=82 males and 58 females, NS), nor
did CTs calculated for juveniles differ significantly from CTs calculated for those
same individuals when they were adults (Wilcoxon 2: 0197; N=15 individuals;

NS).

26

CT did not vary with intensity of aggression recorded during a fight
(Kruskal-Wallis T: 4.65, N: 101 victims at aggression level 1, 97 victims at
aggression level 2, and 62 victims at aggression level 3; NS), nor did CT vary
with the context in which the aggression occurred (Kruskal-Wallis T: 1.40, N= 60
victims in context of dens, 55 victims in context of kills, and 39 victims away from
dens and kills; NS). Finally, when we regressed conciliatory tendencies of
individual dyad pairs against rank distance between victim and aggressor, we
observed no relationship between CT and rank distance (Rs= 0.016, N= 477

dyads, NS).

DISCUSSION

The present study documents the occurrence of post-conﬂict conciliatory
behavior among spotted hyenas in their natural habitat. During the moments
following a dyadic aggressive interaction, opponents tend to engage in friendly
approach or greeting behavior sooner and more often than they do during the
period immediately preceding the ﬁght. Spotted hyenas reconcile approximately
15% of their fights, and demonstrate an overall mean CT of 11.3%. Conciliatory
tendencies calculated previously for primates range from 3.1% in Japanese
macaques (Macaca fuscata: Chafﬁn et al. 1995) to 51.4% in Crested macaques
(Macaca nigra: Petit et al. 1997). Species differences in reconciliation may
reﬂect the amount of social cohesion necessary to survive in the wild (de Waal et
al. 1988). The CT of 11.3% we found in spotted hyenas falls relatively low on the

CT scale observed in primates (Kappeler et al. 1992), and may reﬂect the ﬁssion-

27

fusion nature of hyena society. However, chimpanzees and bonobos also live in
fission-fusion societies yet these primates reconcile far more frequently than do
spotted hyenas (de Waal et al. 1979; de Waal 1986; de Waal 1987), raising the
question of what might account for the low CT found in Crocuta.

Predation pressure on top carnivores is very low, and this is expected to
reduce frequency of reconciliation (Schino 2000). Perhaps more important,
however, is the difference between hyenas and chimpanzees or bonobos with
respect to the intensity of feeding experienced by individual group members
(Holekamp et al. 1999). Feeding competition among Crocuta is extraordinarily
intense, with group members using their formidable weaponry on a daily basis in
fights with conspecifics over ungulate carcasses. Thus, although hyenas depend
in the long run on cooperation from other clan members for survival and
reproduction, short-term costs of conﬂicts might promote unusually heavy
reliance in this species on dispersive rather than non-dispersive mechanisms of
conﬂict resolution.

East et al. (1993) found that the initiation of greetings as a form of
reconciliation accounted for 8% of greetings between adult female hyenas and
9% of greetings between adult males. As in the current study, they observed that
losers in fights were more likely to initiate post—ﬁght greetings than were winners.
Hofer & East (2000) found that 15% of Crocuta dyads engaging in conﬂicts were
followed by friendly reunions, a result identical to that obtained in the present
study. In a sample of nine hyena dyads for which Hofer & East (2000) could find

matched controls within 60 days of an observed conﬂict, they calculated a CT of

28

33.3%. Our sample of 14 dyads with matched controls within 30 days of an
observed conﬂict yielded a CT of 16.6%. Unfortunately, these sample sizes are
too small to permit meaningful comparison of CTs between hyena study
populations. However, our larger sample obtained using pre-conﬂict periods as
matched controls suggests that CTs in Crocuta are generally substantially lower
than those reported previously.

Earlier workers were unable to provide any evidence that friendly post-
conﬂict reunions actually function to restore relationships in spotted hyenas
(Colmenares et al. 2000; Hofer et al. 2000). Similarly, although many primate
studies have demonstrated the occurrence of post-conﬂict friendly reunions, very
few have actually investigated the consequences of such reunions and thus
justified use of the functional term ‘reconciliation’ (Schino 2000, but see de Waal
et al. 1983; Aureli et al. 1991; Cords 1993). Our ﬁndings that both greetings and
approaches occur significantly more frequently among hyenas after than before
conﬂicts, and that these afﬁliative gestures are associated with reduced rates of
aggression during the post-conﬂict interval, clearly indicate that repair of
damaged relationships is indeed one function of afﬁliative behavior after conﬂicts
in Crocuta. In addition to reducing the probability of subsequent aggression
((Aureli et al. 1991; Cords 1993), reconciliation in primates can also decrease
stress-related behavior (Aureli et al. 1991; Das et al. 1998). Further work will be
required to determine whether these effects are also observed among hyenas.

Our results are consistent with the hypothesis that reconciliation may be

widespread among gregarious mammals (Rowell 2000; Schino 2000). In addition

29

to the spotted hyena, post-conﬂict behavior has now been quantitatively
evaluated in three other non-primate species: bottlenose dolphins (Samuels et al.
2000), domestic goats (Schino 1998; Schino 2000), and domestic cats (van den
Bos 1997). Like most primates, all of these species except cats live in stable
social groups, and all except cats exhibit non-dispersive mechanisms of conﬂict
regulation (Schino 2000). Both cats and hyenas belong to the same
monophyletic superfamily (Feloidea) of mammalian carnivores, and are thus
closely related (Flynn 1996). However, the fact that hyenas reconcile whereas
cats do not suggests that taxonomic afﬁliations are less important determinants
of post-conﬂict behavior than selection pressures associated with living in .
groups.

Low predation pressure is expected to increase symmetry between
aggressor and victim in the initiation of reconciliation (Schino 2000). However we
observed a striking asymmetry between victim and aggressor with respect to
initiation of reconciliation. As is also true in many primates (Aureli et al. 1991;
Aureli et al. 1991; Kappeler 1993; Aureli et al. 2000), victims in hyena ﬁghts
exhibit higher CTs than do aggressors. If the purpose of early contact between
opponents after a conﬂict is to yield information about intentions or dispositions,
such information is likely to be most needed by, and most obscure to, victims of
aggression (Cords 1988), since victims are more likely than aggressors to be
uncertain about whether conﬂicts will continue. Furthermore, the fact that
aggressors rarely initiate affiliative interactions after ﬁghts suggests that the long-

term risk of relationship deterioration is low for winners in fights in this species,

30

perhaps because opportunities for losers to disperse from the clan are severely
limited (Smale et al. 1997).

The vast majority of conﬂicts observed among free-living Crocuta occur
among unrelated animals, suggesting that kin are more tolerant of each other
than non-kin. Interestingly, we found that unrelated animals reconcile after ﬁghts
whereas kin dyads do not. Kin associate more closely than do non-kin in this
species, kin serve as frequent alliance partners, and individuals direct afﬁliative
behavior towards kin more frequently than towards non-kin (East at al. 1993;
Smale et al. 1995; Holekamp et al. 1997), as is also true in various primates (e.g.
Cheney et al. 1989). Furthermore, high-ranking animals are preferred over. lower-
ranking individuals as social companions (Seyfarth 1980; Seyfarth et al. 1984;
Holekamp et al. 1997), and individual hyenas prefer to direct afﬁliative behavior
towards high-ranking non-kin (East et al. 1993). These ﬁndings suggest that
hyenas, like many primates, recognize that some group members are more
valuable social partners than others. Nevertheless, neither our comparison of kin
and non-kin, nor our analysis of effects of rank distance on CT, suggests that
relationship value is the primary determinant of post-conﬂict behavior in this
species. However, value of relationships with non-kin may be relatively high in
this species, since non-kin often join forces to repel lions and conspeciﬁcs from
ungulate carcasses, and to defend territorial boundaries (Henschel et al. 1991;
Boydston et al. 2001). Thus, keeping relationships with non-kin in good repair
should enhance the ﬁtness of individual clan members, and promote

reconciliation behavior.

31

Conciliatory tendency may be affected not only by the value of a
relationship, but also by its security (Kummer 1978; Cords 1988; Aureli et al.
2000). The value of a relationship reﬂects the magnitude of social or ecological
beneﬁts likely to accrue from it, with highly valuable relationships most worthy of
maintenance and protection. The security of a relationship reﬂects its
predictability or resilience. The tendency to reconcile should be lowest when a
relationship of low value is highly secure, and highest when a highly valued
relationship is insecure (Cords 1988). Although relationships with relatives are
more valuable than those with non-kin the former relationships are also likely to
be highly secure. Indeed, this is suggested in our data by the rarity of attacks
observed on kin. Thus, the conciliatory behavior we observed in our hyena study
population suggests that relationship security is a far better predictor of CT in this

species than is relationship value.

32

a

v

4.5 .
- Approaches

4-0 "U ‘ Greetings

 

 

 

Afliliative behav’ors / min (XI 00)

PRE POST

Interval relative to ﬁght

 

b)

Aggressions / min (XI 00)

45-
4o-

 

 

. Approaches
‘ Greetings 44

 

 

Behavior Behavior does
occurs not occur

Figure 2.1. Rates at which a) greetings and approaches occurred within hyena

dyads during 5 min intervals before and after ﬁghts (each bar presents data from

137 individual victims), and b) aggression occurred within individual dyads during

post-fight intervals with and without greetings or friendly approaches.

33

45~

4o.

35-

30-

Percent total afﬁliative behavior

25»

 

- Approaches
Greetings

 

7 9 11 13 15

Time after conﬂict (min)

Figure 2.2. Latency to first greeting or appeasement behavior after 411 ﬁghts in

which both members of each dyad could subsequently be observed for 15

minutes.

34

50-

E Pre-conﬂict
40 ’ E Post-conflict

30-

20-

Number of ﬁrst afﬁliative behaviors

10+

 

 

 

Minute of observation

Figure 2.3. Number of total ﬁrst occurrences of conciliatory behavior occurring

during each minute-long interval before and after 698 fights.

35

O)
V

10% -

Conciliatory tendency (%)

2%

0%

12% -

8%-

6% >

4% ~

 

Victim

 

Aggressor

Conciliatory tendency (%)

20% -
18% >
16% -
14% >
12% ~
10% >
8% ~
6% -
4% -
2% -
0% -
-2% .
-4% -
-6°/o

 

 

Kin Non-kin

Figure 2.4. Percent conciliatory tendency of a) 83 individual hyenas observed to

play roles in different fights of both victim and aggressor, b) 28 individual victims

observed to interact in different fights with both kin and non-kin.

36

CHAPTER THREE

Wahaj, S. A., R. C. Van Horn, T. L. Van Horn, R. Dreyer, R. Hilgris, J. Schwarz,
and K. E. Holekamp (2004). Kin discrimination in the spotted hyena (Crocuta

crocuta): nepotism among siblings. Behavioral Ecology and Sociobiology 56:
237-247.

37

CHAPTER THREE

KIN DISCRIMINATION IN THE SPOTTED HYENA (CROCUTA
CROCUTA): NEPOTISM AMONG SIBLINGS

INTRODUCTION

Kin selection theory (Hamilton 1964) predicts that genetic relatedness
should inﬂuence social behavior because animals able to interact differentially
with kin and non-kin would have higher inclusive ﬁtness than animals unable to
do so. The ability to discriminate kin from non-kin is thus a critical prerequisite for
the operation of kin selection. Kin recognition (Holmes et al. 1983) or kin
discrimination (Tang-Martinez 2001) occurs whenever kin and non-kin receive
differential treatment from conspecifics and this differential treatment is based on
characteristics that are correlated with genetic relatedness. The widespread
occurrence of nepotism (Fletcher et al. 1987; Mateo 2002) and the rarity of close
inbreeding (Hoogland 1982) suggest that many animals can recognize their
relatives.

Empirical evidence from a number of species suggests that kin-
differentiated behavior may be facilitated by two common mechanisms, both of
which involve learning (Dawkins 1982; Holmes et al. 1983; Hepper 1986;
Barnard 1990; Tang-Martinez 2001). First, in familiarity-based recognition, kin
learn to recognize one another through shared association when they interact in
contexts that vary with relatedness. Recognition may thus be based on the
location, timing, frequency or duration of social interactions, including both direct
social contact among individuals and shared association with a particular nest or

burrow, or with particular conspeciﬁcs. For example, siblings born in different

38

breeding seasons might recognize each other as kin through shared association
with a common parent (Dawkins 1982; Holmes et al. 1983; Hepper 1986;
Barnard 1990). The other mechanism that often mediates kin discrimination is
phenotype matching (Holmes et al. 1982; Lacy et al. 1983). If phenotypic
similarity is highly correlated with genotypic similarity, then recognition may result
from phenotypic comparison (Tang-Martinez 2001). Individuals that share similar
phenotypes are treated as kin. Phenotypic cues from an unfamiliar conspeciﬁc
may be compared to a template acquired either from a familiar relative or from
the discriminating individual itself (self-referent phenotype matching: Mateo et al.
2000; Hauber et al. 2001).

Most studies of kin recognition have investigated only the ability to
discriminate among maternal kin (Holmes et al. 1983; Gouzoules 1984; Fletcher
et al. 1987; Walters 1987; Wilson 1987; Waldman 1988; Pfennig et al. 1995).
However, in long-lived mammals showing considerable reproductive skew
among males, individuals can be expected to live in groups containing paternal
as well as maternal kin (Holmes 1986; Widdig et al. 2002). Nepotism among both
maternal and paternal kin can potentially increase inclusive ﬁtness, so the ability
to recognize both types of kin should be adaptive. Paternal kin recognition has
now been demonstrated in macaques (Macaca mulatta: Widdig et al. 2001),
baboons (Papio cynocephalus: Alberts 1999); Buchan et al. 2003), and ground
squirrels (Spennophi/us beldingi: Holmes 1986; Mateo 2002). Our broad

objectives here were to inquire whether recognition of paternal kin occurs in the

39

spotted hyena (Crocuta crocuta), and if so, to identify the mechanisms mediating
this recognition.

Spotted hyenas are long-lived, gregarious carnivores that reside in
permanent social groups, called clans. Clans are ﬁssion-fusion societies in
which individuals travel, rest and forage in subgroups that can change in
composition from day to day, or even from hour to hour (Kruuk 1972; Mills 1990).
Most clans contain several immigrant males and multiple matrilines of philopatric
females and their offspring, including individuals from a number of overlapping
generations (Frank 1986; Mills 1990). Modal litter size in Crocuta is two (Kruuk
1972), but members of consecutive litters born to the same female are usually
present in the clan concurrently. Social interactions within clans are strongly
affected by maternal kinship (Kruuk 1972; Mills 1990) but differential treatment of
maternal and paternal kin in Crocuta has never been studied. In other gregarious
carnivores most natal group members are close kin (Gompper et al. 1996), so
favoring any group member over other conspeciﬁcs would likely enhance an
individual’s fitness. However, Van Horn et al (2004) recently found that high
levels of male-mediated gene ﬂow among clans combined with relatively low
gene ﬂow among matrilines within a clan, reduce average relatedness among
members of a spotted hyena clan to extremely low levels; mean relatedness
among hyenas born in a clan is no higher than that among males immigrating
into the clan from multiple neighboring groups. Because mean relatedness within
a clan is so low, hyenas should be able to gain substantial fitness benefits by

favoring their kin over other group members.

40

Spotted hyenas breed throughout the year, and both males and females
mate with multiple partners (Engh et al. 2002). In addition, because females and
their cubs are socially dominant to virtually all breeding males, fathers are
constrained by their low social rank such that they have very few opportunities to
direct nepotistic behavior toward their own offspring (Van Horn et al. 2004).
Tenure in the clan held by breeding immigrant males lasts up to 9 years (Engh et
al. 2002), so paternal half-siblings frequently co-exist within a clan. In
conjunction with well-established matrilineal genealogies (Van Horn et al. 2004),
our recent identification of 12 variable microsatellite loci in Crocuta allowed us to
document both maternal and paternal kin relationships within one large hyena
clan (Libants et al. 2000; _Engh et al. 2002). Because adult male hyenas do not
participate in care of young or associate regularly with their own offspring (Van
Horn et al. 2004), paternal half-siblings represent a kin class in which familiarity
based on direct spatial or temporal association would rarely suffice to mediate kin
recognition among hyenas (Holmes et al. 1983). Thus, the ability to discriminate
paternal half-siblings from non-kin would suggest self-referent phenotype
matching as a mechanism of kin recognition in this species. Similarly Crocuta
twin litters may be sired by either one or two males (Engh et al. 2002; East et al.
2003), producing either full-sibling littermates or half-sibling littermates reared
together without unique familiarity-based cues for distinguishing between these
different types of littermates. To maximize their own inclusive fitness, hyenas

should treat full-sibling littermates better than half-sibling littermates if they can

41

distinguish between them, and self-referent phenotype matching would be the
mechanism most likely to permit this.

Here we examined recognition of both maternal and paternal kin among
multiple classes of siblings in free-living spotted hyenas. Our first goal was to
inquire whether behavioral interactions among free-living Crocuta were
consistent with expectations based on kin selection theory. Speciﬁcally, we
tested the hypothesis that hyenas sharing larger coefﬁcients of relatedness
(Hamilton’s r) would receive more afﬁliative behavior, and receive less
aggression, than would more distantly related siblings or unrelated animals. In
addition, since association patterns reveal adaptive preferences for social -
partners in the ﬁssion-fusion society typical of spotted hyenas (Holekamp et al.
1997; Szykman et al. 2001), we expected association patterns would vary among
kin classes if kin were able to recognize one another. Our second goal was to

elucidate the mechanisms enabling hyenas to recognize kin.

METHODS

Subject Animals and Study Site

Spotted hyena clans contain 10 to 90 individual members that
cooperatively defend a group territory. Virtually all males disperse from their natal
groups, but females are philopatric (Mills 1990; Smale et al. 1997; East at al.
2001). Adult members of each sex can be ranked in a linear dominance
hierarchy, with all females able to dominate all immigrant males. Female

dominance relations are stable for extended periods and across a variety of

42

contexts (Tilson et al. 1984; Frank 1986; Engh et al. 2000). An individual’s
position in the group’s hierarchy determines its priority of access to food (Kruuk
1972; Frank 1986).

Female hyenas bear litters in isolated natal dens (East et al. 1989), but
soon transfer their offspring to the clan’s communal den, where up to 20 cubs
may reside concurrently for several months. The communal den is a social focal
point for clan members, and it is frequently visited by adults and by immature
individuals who no longer use the den for shelter. After juveniles leave the
communal den, they travel throughout the home range and feed at ungulate kills
with adults. However, hyena cubs remain dependent on their mothers for-milk
until weaning, at 13-14 months of age (Holekamp et al. 1999).

This study took place in the Talek region of the Masai Mara National
Reserve, Kenya. Subjects were members of one large Crocuta clan containing
60 to 80 resident hyenas, and occupying an area of 65 km’. During this study
the Talek clan usually contained 20-25 adult females, 8 to 14 adult immigrant
males, and 35 to 45 cubs and subadults. All members of the study clan were
identified by their unique spots, and sex was determined from the dimorphic
glans morphology of the erect phallus (Frank et al. 1990). We estimated cub birth
dates (to i 7 days) using methods described previously (Holekamp et al. 1996).
Social ranks were determined based on wins and losses in dyadic agonistic
interactions. Mother-offspring relations were established on the basis of regular
nursing associations, and conﬁrmed by genetic analysis (Engh et al. 2002). To

examine predictions of kin selection theory in the study clan, we assigned

43

individual hyenas to kin groups, and compared measures of social behavior

among groups.

Assignment of individuals to kinship groups

DNA from each Talek hyena was extracted from blood or tissue, and we
genotyped individuals using eleven autosomal microsatellite loci and one X-
linked microsatellite locus as described elsewhere (Libants et al. 2000; Engh et
al. 2002). All adult males present in the clan at conception of a particular litter
were considered as potential fathers. We employed a maximum likelihood-based
approach (Thompson 1975; Meagher 1986) to assign paternity to cubs with
known, genotyped mothers using the program CERVUS (Marshall et al. 1998),
but only if data were available for at least 6 autosomal loci in sire, cub, and
mother genotypes (see Engh et al. 2002 for details). A male was considered the
sire of a cub when CERVUS assigned him paternity at 95% confidence and he
met one of the following two criteria: he was the only potential sire by simple
exclusion or, in the case of a single mismatch between the multi-locus genotypes
of the putative sire and cub, the software program KINSHIP (Goodnight et al.
1999) indicated that the two animals’ painivise genetic similarity (i.e., R in Oueller
et al. 1989) reﬂected sire-cub kinship at 95% confidence. Confidence in paternity
and kinship was determined from the simulated distribution of the ratio of two
likelihoods: the likelihood that the male was the sire of the cub (e.g., paternally
related at R = 0.05), and the likelihood that the male was not the sire of the cub

(e.g., paternally related by R = 0).

44

Our genetic analysis allowed us to assign hyenas to one of the kin groups
listed in Table 3.1. Theoretical expectations regarding differential treatment of
siblings are shown in Table 3.2. The subset of comparisons among groups
shown in bold type in Table 3.2 allowed us to test hypotheses suggesting
recognition based on familiarity or phenotype matching. We emphasize that
these hypotheses need not be mutually exclusive as more than one recognition
mechanism might operate in this species.

Paternal half-siblings (PHS) shared a common father, but had different
mothers and no known maternal relatives in common. Animals were deﬁned as
non-kin (NK) if they were known to have different fathers and if they had no
known maternal relatives in common. There was no apparent difference in body
size between full- (FSL) and half-sibling (HSL) littermates. By contrast, all
maternal half-siblings (MHS) and most (89.7%) paternal half-sibling were born in
different years, so members of MHS and PHS pairs usually differed markedly in
size until both individuals in a pair reached reproductive maturity. In addition,
full- and half-sibling littermates grew up together at the communal den, whereas
most members of other sibling classes did not. Thus possible confounds here
were that behavioral differences between littermate and non-littermate sibling
categories might reﬂect discrimination based on differences in body size or the
amount of time spent sharing a den rather than on relatedness. To address these
concerns, we compared affiliative, associative and aggressive behaviors of
unrelated animals that spent at least 4 months living together concurrently at the

den with those of unrelated animals that spent no time living together at the den.

45

We called the former cohort members (CHT) and the latter non-cohort hyenas
(NCH). CHT members were generally all of the same size, whereas this was not
true for NCH members. If hyenas discriminate among conspecifics based on
either body size or shared time at dens rather than on relatedness, then we
expected to find significant differences between CHT and NCH animals with

respect to affiliative and agonistic interactions.

Behavioral Data Collection

Behavioral data were collected between June 1988 and April 1998, when
observers were usually present in the study area at least 23 days/month. We
observed Talek hyenas from our vehicles, mainly between 0500 and 0900 h and
between 1700 and 2000 h. An observation session started when we found one
or more hyenas separated from others by at least 200 m, and ended when we
left that group. Observation sessions occurred at dens, at ungulate kills, and
away from both dens and kills. Behavioral data presented here included those
generated by both males and females monitored while they were living at the
communal den and also later in life as they traveled around the clan’s territory.
All kin and non-kin groups contained hyenas of both sexes from birth through
adulthood. We measured three classes of behaviors: affiliative behavior,
association patterns, and dyadic aggression.

Affiliative behavior: Afﬁliative behaviors included playing, feeding or
nursing together, and joining together to engage in coalitionary attacks on target

animals. All occurrences of coalitionary aggression were recorded throughout

46

every observation session as critical incidents (Altmann 1974). All other affiliative
behaviors were assessed using scan data collected at 15-20 minute intervals
throughout each observation session. During each scan we recorded the identity
and activity of every hyena present. Affiliative behaviors recorded during scans
for all hyenas in all kin groups included playing or feeding together. For
littermates we also recorded nursing together as an afﬁliative behavior. We
calculated the percent of scans in which each afﬁliative behavior occurred within
each pair of animals who were present together during at least 20 scans.

Social play behavior was recognized by the occurrence of exaggerated
movements, and by the absence of aggressive postures or vocalizations -
characteristic of agonistic interactions. Feeding together excluded nursing, and
was defined as two hyenas concurrently feeding on the same solid food item.
Feeding was observed both away from the den at ungulate kills and also at the
den when mothers provisioned cubs with solid food, although provisioning was
very rare (Holekamp et al. 1990). Feeding competition is intense in spotted
hyenas, and intolerance of concurrent feeding by conspecifics usually involves
the higher-ranking member of a pair driving the subordinate individual off the
food (Kruuk 1972). Thus, tolerance of concurrent feeding seemed a reasonable
measure of affiliative behavior. Coalitionary aggression occurred when two or
more hyenas joined together to direct aggression (defined below) against a third.
Here coalition formation was considered a cooperative behavior since individuals

risk injury to themselves by aiding other animals during ﬁghts (Zabel et al. 1992).

47

Associationpatterns: An association index for each pair of hyenas was
calculated using the twice-weight index of (Cairns et al. 1987). Thus, to calculate
an association index for a pair of animals A and B, we divided the number of
observation sessions in which both A and B were present by the sum of that
number plus the number of sessions in which either A or B was observed without
the other being present. Young hyenas are bound to the communal den until
they are 8-12 months old and their mothers visit them there daily. In addition,
cubs nurse for several months after leaving the communal den, and cubs are
dependent upon their mothers during the post-den period for agonistic aid,
protection, and for finding food (Holekamp et al. 1997). To avoid biases involving
the potential confounds of dens or mothers, both sessions at dens and sessions
in which the mother of either interacting hyena was present were excluded from
calculations of association indices. Both mature and immature hyenas found
away from dens were included in this analysis.

madic amssion: Throughout every observation session, we recorded
all occurrences of dyadic aggressive behavior as critical incidents (Altmann
1974). Aggressive behaviors included head wave, lunge, aggressive posture
(i.e., ears cocked forward with the tail bristled and raised), chase, displace, stand
over, bite, and push. Crocuta littermates often fight vigorously during their first
weeks of life (Frank et al. 1991). For littermate pairs we recorded whether or not
aggressions occurred during nursing, but all aggression among non-littermates

occurred in contexts other than nursing. The identities of all aggressors and

48

target animals were recorded. In contrast to coalitionary aggression, dyadic

aggression involved only one aggressor and one target animal.

Data analysis

Data documenting afﬁliative behaviors, association indices, and dyadic
aggression were compared among all sibling classes, between kin and non-kin,
and also between cohort and non-cohort animals (to examine effects of
differential body size on social relationships). Two types of data were used to
compare behavioral interactions among various classes of siblings: scan data
were used to document patterns of some afﬁliative behaviors (playing, feeding
and nursing together) and to measure association indices, whereas critical
incident data were used to measure dyadic aggression and coalition formation.

Playing, feeding and association: Playing and feeding together and
association indices were analyzed using pairs of hyenas as the units of analysis.
In comparing FSL and HSL, each pair of FSL (N = 7) and each pair of HSL (N =
5) contributed one data point for affiliative behaviors (playing, feeding, and
nursing together) and for association. We compared FSL and HSL values using
Mann-Whitney U-tests. In comparing the other eight pair types (1) FSL and MHS,
2) FSL and PHS, 3) FSL and NK, 4) MHS and HSL, 5) MHS and PHS, 6) MHS
and NK, 7) PHS and NK and 8) CHT and NCH) we used non-parametric
matched pairs t-tests (Wilcoxon matched-pairs signed ranks tests), with each pair
of hyenas being used only once. In each case we measured the relationships of

a focal individual (hyena A) with two other hyenas (hyenas B and C), and then

49

compared values for the A-B relationships with the values for the AC
relationships. Animals B and C in each case were matched for sex, age (1 1
year), and relative social rank, but differed in their kin relationships to A. For
example, we compared the percent of scans during which a particular affiliative
behavior was exhibited between hyena A and its full-sibling B to the percent of
scans during which hyena A and its maternal half-sibling C were engaged in that
same affiliative behavior. In this example, if hyena B was a male, both higher
ranking and older than hyena A, then hyena C was also a male, higher ranking
and older than hyena A. Note that we were not able to use this method for
comparing full- and half-sibling littermates because a given hyena could not
simultaneously have both a FSL and a HSL.

Association data were derived from scans performed in each observation
session, based on whether or not both members of a given hyena pair were
recorded as present in scans from the same observation session. We compared
the association index between hyena A and B with the association index between
A and C, where B and C were drawn from different kin groups. As in our
analyses of affiliative behavior, we controlled for sex, body size, and rank by
matching hyenas B and C as closely as possible in these respects.

Dvadic and coalitionary mression: Data collected during critical incident
sampling were used to calculate rates of both dyadic and coalitionary aggression.
Rates of coalition formation within pairs were calculated by dividing the total
number of coalitions formed between two animals by the number of hours during

which both members of that pair were present concurrently. Rates of dyadic

50

aggression for each hyena A were calculated by dividing the total number of
aggressive acts directed by hyena A at hyena B, divided by the total number of
hours A and B spent together. We stipulated that a pair of hyenas had to be
present together during at least 25 h of observation to be included in either the
aggression or the coalition data set, and each pair was used only once. Since
these data were not normally distributed, we compared hourly rates of
aggression and coalition formation among sibling groups using a Kruskal-Wallis
one-way ANOVA with relatedness class as the independent variable. We also
examined aggressive interactions according to the sex composition of the pair
tested (female-female, mixed sex, or male-male) within each relatedness group,
using a Kruskal-Wallis one-way ANOVA. Post hoc comparisons between speciﬁc
sibling groups were conducted using Mann-Whitney U tests. The sequential
Bonferroni adjustment was then used to correct for multiple testing (Rice 1989).
Because the only multiple comparisons performed in any of our analyses were
those involving coalitionary and dyadic aggression, these were the only analyses
in which Bonferroni corrections were applied. Finally, we used Mann-Whitney U
tests to compare full- and half-sibling littermates with respect to rates of
aggression observed only in the context of nursing, and to compare aggression
rates between cohort and non-cohort hyenas.

Because the hypotheses we were testing made clear, directional
predictions regarding whether or not kin should exhibit affiliative or aggressive
behavior more than non-kin, all statistical tests involving these behaviors were

one-tailed. However, because it was not clear a priori whether to expect kin to

51

associate more or less closely than non-kin, tests involving association data were
two-tailed. Differences between groups were considered significant when p 5

0.05. Throughout the paper, means (3: se) are reported.

RESULTS

Tests of predictions of kin selection theory

Four comparisons were designed to test predictions of kin selection but
could not be used to differentiate kin recognition mechanisms (comparisons 1 — 4
in Table 3.2). For each of these comparisons, we had four afﬁliative measures
(play, feeding together, association, and coalition formation). Of the 16 tests that
resulted, all but three showed signiﬁcant kin biases in the behavior in question
(Table 3.3), supporting the predictions of kin selection.

Full sibling littermates played and fed together signiﬁcantly more than did
either maternal half-siblings (play: Wilcoxon Z = -1.826, n = 4, p = 0.034;
feeding: Wilcoxon Z = -1.826, n = 4, p = 0.034, Figure 3.1a) or paternal half-
siblings (play: Wilcoxon Z = -2.524, n = 8, p = 0.006; feeding: Wilcoxon Z = -2.10,
n = 8, p = 0.018, Figure 3.1b). Full-sibling littermates also played together more
than did non-kin (Wilcoxon Z = -1.859, n = 7, p = 0.032, Figure 3.1c). Hyenas
associated more closely with their full-sibling littermates than with either their
paternal half-siblings (Wilcoxon Z = -2.521, n = 7, p = 0.006, Figure 3.1 b) or non-
kin (Wilcoxon Z = -2.366, n = 7, p = 0.009, Figure 3.10). Maternal half-siblings

played (Wilcoxon Z = -1.826, n = 4, p = 0.034, Figure 3.2a) and associated

52

together more closely (Wilcoxon Z = -2.49, n = 11, p = 0.006, Figure 3.23) than
did non-kin.

Mean rates of coalition formation among sibling classes varied
significantly overall (Kruskal Wallis T = 31.17, d.f. = 4, p < 0.001, Figure 3.3).
Full-siblings formed coalitions together at higher rates than did maternal half-
siblings (Mann Whitney U = 91.5, n = 12 FSL, n = 30 MHS, p = 0.006), paternal
half-siblings (Mann Whitney U = 97.0, n = 12 FSL, n = 53 PHS, p < 0.001), or
non-kin (Mann Whitney U = 1403.5, n = 12 FSL, n = 131 NK, p < 0.001).
Maternal half-siblings also formed coalitions together more than did non-kin
(Mann Whitney U = 2548.5, n = 30 MHS, n = 131 NK, p = 0.003).

Three comparisons failed to reveal signiﬁcant biases in affiliative behavior.
Full-sibling littermates did not associate signiﬁcantly more than maternal half-
sibllngs (Wilcoxon Z = -1.095, n = 4, p = 0.137, Figure 3.1a), nor did they feed
together significantly more than non-kin (Wilcoxon Z = -1.521, n = 7 individuals, p
= 0.064, Figure 3.10). Maternal half-siblings also did not feed together
significantly more than non-kin (Wilcoxon Z = -0.622, n = 11, p = 0.267, Figure
3.2a). However, in all three cases, results were in the direction predicted by kin
selection theory.

Mean rates of dyadic aggression among sibling types varied signiﬁcantly
overall (Kruskal Wallis T = 10.82, d.f. = 4, p = 0.029). Interestingly however,
kinship generally failed to protect hyenas from dyadic aggression. Full-sibling
littermates and maternal half-siblings did not differ with respect to the rates at

which they aggressed against each other (Mann Whitney U = 198, n = 12 FSL, n

53

= 30 MHS, p = 0.308), nor did full-siblings differ signiﬁcantly in this regard from
either paternal half-siblings (Mann Whitney U = 250, n = 12 FSL, n = 53 PHS, p =
0.12) or non-kin (Mann Whitney U = 682.5, n = 12 FSL, n = 131 NK, p = 0.225).
Rates of dyadic aggression also failed to differ between maternal half-siblings

and non-kin (Mann-Whitney U = 1961, n = 30 MHS, n = 131 NK, p = 0.493).

Tests of hypotheses suggesting kin recognition mechanisms

HSL and MHS: Half-sibling littermates did not differ from maternal half
siblings with respect to the percent of scans in which they were observed either
playing (Wilcoxon Z = -0.962, n = 5, p = 0.168, Figure 3.2b) or feeding together
(Wilcoxon Z = -0.135, n = 5, p = 0.447, Figure 3.2b). Rates of coalition formation
also failed to differ significantly between half-sibling littermates and maternal half-
siblings (Mann-Whitney U = 81.5, n = 5 HSL, n = 30 MHS, p = 0.374, Figure 3.3)
as did rates of dyadic aggression (Mann-Whitney U = 56, n = 5 HSL, n = 30 I
MHS, p = 0.183). However, half-sibling littermates associated far more closely
than did maternal half-siblings (Wilcoxon Z = -2.023, n =5, p = 0.022, Figure
3.2b).

MHS and PHS: Maternal half-siblings did not differ signiﬁcantly from
paternal half-siblings with respect to the percent of scans in which they played
together (Wilcoxon Z = 0.0, n = 3, p = 0.5, Figure 3.20), fed together (Wilcoxon Z
= -1.461, n = 4, p = 0.07, Figure 32C), or associated (Wilcoxon Z = -1.461, n = 4,
p = 0.07, Figure 3.20). Furthermore, maternal half-siblings did not form coalitions

together at higher rates than did paternal half-siblings (Mann-Whitney U = 917, n

54

= 30 MHS, n = 53 PHS, p = 0.111, Figure 3.3). After Bonferroni adjustment,
maternal half-siblings and paternal half-siblings also failed to differ signiﬁcantly in
their rates of dyadic aggression (Mann-Whitney U = 1007, n = 30 MHS, n = 53
PHS, p = 0.02).

FSL and HSL: Full-sibling littermates were observed playing together
(Mann Whitney U = 28, n = 7 FSL and 5 HSL, p = 0.04, Figure 3.4) and feeding
together on solid food (Mann Whitney U = 28, n = 7 FSL, n = 5 HSL, p = 0.044,
Figure 3.4) more than were half-sibling littermates. However, association indices
did not differ between full- and half-sibling littermates (Mann Whitney U = 9, n = 7
FSL, n = 4 HSL, p = 0.172, Figure 3.4). Full-sibling littermates tended to form
coalitions together at higher rates than did half-sibling littermates, but this
difference was not statistically significant (Mann Whitney U = 44.5, n = 7 FSL, n =
5 HSL pairs, p = 0.062, Figure 3.3).

When they were not nursing, half-sibling littermates received aggression
at almost twice the rate observed among full-sibling littermates, but this
difference was not statistically significant (Mann Whitney U = 19.5, n = 12 FSL, n
= 5 HSL, p =.0.134). Although there was no difference in the percent of scans in
which full- and half-sibling littermates were observed to be nursing concurrently
(Mann Whitney U = 22, n = 12 FSL, n = 5 HSL, p = 0.232), the mean hourly rate
of aggression during nursing between half-sibling littermates was nine times
higher than that between full-sibling littermates. Nevertheless, variance in this

measure was great, so the mean difference was not statistically significant (FSL

55

>2 = 0.048 1 0.02, HSL x = 0.446 1 0.441, Mann Whitney U = 30, n = 12 FSL, n =
5 HSL, p = 0.5).

PHS and NK: Paternal half-siblings and non-kin did not differ significantly
with respect to the percent of scans in which they played together (Wilcoxon Z =
0.0, n = 4, p = 0.5, Figure 3.5), nor did their association indices differ signiﬁcantly
(Wilcoxon Z = -0.845, n = 7, p = 0.199, Figure 3.5). However, paternal half-
siblings fed together more than did non-kin (Wilcoxon Z = -2.032, n = 11, p =
0.021, Figure 3.5). Paternal half-siblings formed coalitions at higher hourly rates
than did non-kin (Mann Whitney U = 4157, n = 53 PHS, n = 131 NK, p = 0.010,
Figure 3.3), but after Bonferroni adjustment this difference was not statistically
significant. Paternal half-siblings displayed significantly lower rates of dyadic
aggression than did non-kin (Mann Whitney U = 2519, n = 53 PHS, n = 131 NK,

p = 0.002).

Effects of variables other than kinship

Effects of differential body size were investigated by comparing behavior
of cohort members with that of individuals reared in different cohorts. Non-kin
cohort members were not statistically distinguishable from non-kin raised in
separate cohorts with respect to either playing (CHT >7 = .8% 1 1.5, NCH >1 =
1.6% 1 1.6, Wilcoxon Z = -1.153, n = 6, p = 0.125) or feeding together (CHT >7 =
0.8% 1 0.5, NCH >2 = .3% 1 0.3, Wilcoxon Z = -1.089, n = 3, p = 0.138). We also
found no differences between cohort and non-cohort animals with respect to

association patterns (CHT x = 0.039 1 0.007, NCH >‘< = 0.032 1 0.005, Wilcoxon

56

Z = -0.105, n = 6, p = 0.458), rates of coalition formation (CHT >7 = 0.008 1 0.005,
NCH >7 = 0.013 1 0.002, Mann Whitney U = 979, n = 16 CHT, n = 115 NCH, p =
0.318), or rates of dyadic aggression (CHT >7 = 0.059 1 0.015, NCH >7 = 0.068 1
0.006, Mann Whitney U = 967, n = 16 CHT, n = 115 NCH, p = 0.37).

We examined effects of kinship on coalition formation separately within
dyads of three different sex compositions: female-female, male-male, and mixed
sex. Effects of kin group were found within all three dyad types (female-female:
Kruskal-Wallis T = 19.201, d.f. = 4, p = 0.001; male-male: Kruskal-Wallis T =
7.352, d.f. = 4, p = 0.061; mixed sex: Kruskal-Wallis T = 18.095, d.f. = 4, p =
0.001). When data documenting rates of coalition formation were divided'up by
dyad composition within kinship groups, resulting sample sizes were too small to
permit all 8 possible comparisons (shown in Figure 3.3) within each dyad type.
However, where sample sizes allowed comparisons, rates of coalition formation
in all three dyad types showed the same pattern as those shown in Figure 3.3, in
which all dyad types are represented together. For example, the rate of coalition
formation in all three dyad types was higher for full-sibling littermates than for
half-sibling littermates, and paternal half-siblings always formed coalitions
together at higher rates than did non-kin. Thus the results shown in Figure 3.3
were not driven by the behavior of members of any one dyad type alone, as

members of all dyads behaved similarly.

57

DISCUSSION

Evidence that kinship affects hyena social behavior

Both kin selection theory (Hamilton 1964) and mate selection theory
(Bateson 1983) predict that kinship will inﬂuence social interactions among
conspeciﬁcs. Kin-differentiated behavior in gregarious mammals requires
significant social discrimination abilities (Sherman et al. 1997). Although earlier
studies (e.g. Holekamp et al. 1999) suggested that Crocuta could discriminate
maternal kin from non-kin, genetic data were not available until now to permit
analyses of kin recognition abilities among other kin classes, including paternal
kin. Full siblings, half-siblings, and non-kin each share different r-values yet all of
these kin classes overlap in time and space within spotted hyena clans. Thus, if
hyenas can discriminate among these relatedness classes, then they should
theoretically favor their most closely related kin. Indeed, our data documenting
affiliative behaviors, summarized in Table 3.3, indicate that Crocuta can
discriminate among several different groups of siblings, and that they can also
distinguish paternal kin from non-kin.

Although affiliative interactions varied here among sibling classes,
patterns of dyadic aggression showed little variation. Rates of dyadic aggression
were generally just as high among kin as non-kin. Thus, in this respect, spotted
hyenas resemble various cercopithecine primates in which it has been found that
kinship enhances cooperation but does not necessarily protect individuals from
aggression (Bernstein et al. 1986; Hunte et al. 1987; Widdig et al. 2002). The

only significant difference emerging in our analysis of dyadic aggression was that

58

paternal half-siblings received less dyadic aggression than did non-kin. This
result is interesting because we have found in a separate study (Van Horn et al.
2004) that young hyenas direct significantly less intense aggression at their sires
than at unrelated adult control males. Thus, whereas maternal kinship does not
necessarily protect hyenas from aggression, reducing the frequency or intensity
of aggression may represent one form of nepotism among paternal kin in
Crocuta. High frequencies of agonistic interaction with kin in some species might
be attributed to more frequent social interaction in general, and consequently to
increased opportunities to come into conﬂict with kin (Bernstein et al. 1986).
However, this cannot explain our results since we controlled for the amount of
time pairs spent together in our analysis of aggression rates.

In virtually all analyses represented here, sample sizes were small,
variance was great, and statistical power was low. Our sample sizes were
severely limited by availability of genetic data and by our efforts to carefully
match animals for comparison based on sex, age, and social status.
Nevertheless differential treatment of various kin classes clearly occurred among
our study animals. This differential treatment occurred in accordance with
predictions of kin selection theory, and could not be explained by effects of sex,
body size, or social rank. The robust differences we observed in afﬁliative
interactions among full-siblings, half siblings, and non-kin (Table 3.3) support
acceptance of the hypothesis that hyenas can discriminate among individuals

sharing different coefficients of relatedness.

59

Evidence supporting the familiarity hypothesis

Evidence of kin discrimination has been reported for a wide variety of
species (Waldman et al. 1979; Gouzoules 1984; Fletcher et al. 1987; Waldman
1988; Pfennig 1999; Silk 2002; van der Jeugd et al. 2002), but the mechanisms
by which kin recognition is mediated are known only for a small subset of these.
One possibility is that individuals identify relatives on the basis of familiarity
engendered by shared association with each other or with a common parent
(Walters 1987). Hyena cubs associate very closely with their mothers for the ﬁrst
several months of life (Holekamp et al. 1997). Furthermore, maternal kin
associate more closely than do non-kin (Holekamp et al. 1997), so hyena cubs
are often in proximity to older siblings and other maternal relatives. That spotted
hyenas base recognition of maternal kin on familiarity is suggested here by two
lines of evidence. First, although half-sibling littermates and maternal half-
siblings share the same coefﬁcient of relatedness, half-sibling littermates grow up
together at the den, whereas maternal half-siblings do not because they are born
in different years. Here half-sibling littermates associated more closely than did
maternal half-siblings, suggesting that familiarity cues experienced during
communal rearing affect patterns of affiliation among siblings once all these
animals are independent of the communal den.

Hyenas may also use familiarity cues to distinguish between maternal
half-siblings and paternal half-siblings, even though they share the same
relatedness coefficient with animals in both groups. Here, although we found no

differences between maternal half-siblings and paternal half-siblings that were

60

statistically significant, maternal half siblings nevertheless tended to be favored
over paternal half-siblings in all types of interactions measured except play
(Table 3.3). There is no paternal care in this species, females often mate with
multiple males, and paternal kin do not associate closely, so paternal half-
slblings have no access to shared social cues of relatedness. However, as also
occurs in baboons (Smith et al. 2003), maternal kin in hyenas can use social
cues based on shared experience with a common mother to govern their
affiliative behavior. Though our results suggest that Crocuta can recognize
paternal kin, maternal kinship may nonetheless be more important to hyenas
than paternal kinship. Maternal kinship explains a great deal of the variance in
social relationships among cercopithecine primates even when paternal

relationships are known (Smith et al. 2003).

Evidence supporting the phenotype matching hypothesis

Phenotype matching has been suggested as an important mechanism of
kin recognition in peacocks (Pavo cn'status, Petrie et al. 1999), beavers (Castor
canadensis, Sun et al. 1997), ground squirrels (Spermophilus beldingi, Sherman
1981; Holmes et al. 1982; Holmes et al. 1983; Holmes 1986; Holmes 1986),
macaques (Macaca mulatta, Widdig et al. 2001), and baboons (Papio
cynocephalus, Smith et al. 2003). Phenotype matching is especially likely when
multiple paternity prevents littermates from experiencing any obvious differences
with respect to familiarity cues on which to base discriminations between full-

siblings and half-siblings (Holmes et al. 1982). This appears to be the case in

61

Crocuta. Four lines of evidence suggest that hyenas allocate both afﬁliative and
aggressive behaviors according to kinship in the absence of social cues of
relatedness, suggesting self-referent phenotype matching as a mechanism for
kin discrimination.

First, although full- and half-sibling littermates share common pre-natal
and post-natal environments, full-sibling littermates showed more afﬁliative
behavior than did half-sibling littermates. In addition, rates of aggression in both
nursing and non-nursing contexts were higher between half-sibling littermates
than between full-sibling littermates. The consistent trends observed in afﬁliation
and aggressive behavior between full-sibling littermates and half-sibling '
littermates cannot be mediated by familiarity-based mechanisms, and instead
support an hypothesis invoking phenotype matching (Hauber et al. 2001).

Second, paternal half-siblings are more closely related than non-kin, but
neither have access to social cues of relatedness in Crocuta, thus making
paternal kin recognition through familiarity improbable. However, paternal half-
siblings were observed feeding together during a greater percent of scans,
formed coalitions together at higher rates, and were less frequently the targets of
dyadic aggression than were non-kin.

Third, although we observed directional trends suggesting greater
nepotism among maternal half-siblings than paternal half-siblings, we found no
significant differences between these groups of siblings. This similarity between
maternal half-siblings and paternal half-siblings is predicted by the phenotype

matching hypothesis but not by the familiarity hypothesis.

62

Finally, half-sibling littermates and maternal half-siblings in Crocuta share
the same coefficient of relatedness (r = 0.25) but differ with respect to the den
environments and social cues they experience. We observed no differences
between half-sibling littermates and maternal half-siblings with respect to playing
together, feeding together, rates of forming coalitions together, or rates of dyadic
aggression. The lack of difference in these behaviors between half-sibling
littermates and maternal half-siblings is more parsimoniously explained by the
phenotype matching hypothesis than by the familiarity hypothesis.

Familiarity-based and phenotype matching mechanisms of kin recognition
are not mutually exclusive, and more than one mechanism has been suggested
to operate in a variety of species, including ground squirrels (Sherman 1980;
Holmes et al. 1982; Holmes 1986; Schwagmeyer 1988), mice (Kareem et al.
1982), and various primates (Widdig et al. 2001; Silk 2002; Widdig et al. 2002).
Similarly both mechanisms appear to operate in spotted hyenas. Earlier
observations suggested that hyenas distinguish among individual conspeciﬁcs
based on vocalizations (Holekamp et al. 1999), odors (Hofer et al. 2001), and
visual cues (Kruuk 1972). Further study will be required to ascertain which of

these sensory modalities might modulate kin recognition in Crocuta.

63

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64

 

 

 

 

 

 

 

 

 

 

 

 

Familiarity Phenotype Matching
1. FSL>MHS 1. FSL>MHS

2. FSL > PHS 2. FSL > PHS

3. FSL > NK 3. FSL > NK

4. MHS > NK 4. MHS > NK

5. HSL > MHS 5. HSL = MHS

6. MHS > PHS 6. MHS = PHS

7. FSL = HSL 7. FSL > HSL

8. PHS = NK 8. PHS > NK

 

 

Table 3.2. Predictions for interactions among spotted hyenas generated by kin
selection theory (in regular font) and by hypotheses suggesting two possible
mechanisms of kin recognition (in bold font), familiarity-based recognition and
phenotype matching. “>” denotes the prediction that greater afﬁliation, higher
rates of coalition formation, and lower rates of dyadic aggression should be seen
in one group than the other if kin recognition occurs via that mechanism, whereas
“=” denotes a prediction that the two groups should treat each other similarly.
Predictions in bold face indicate those that differ between the familiarity
hypothesis and phenotype-matching hypothesis of kin recognition; in the
remaining (non-bolded) cases, predictions of both hypotheses are the same.

65

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66

Figure 3.1. Mean percent of scans in which individual hyenas were observed
playing and feeding together with a) full-sibling littermates and maternal half-
siblings, b) full-sibling littermates and paternal half-siblings, and c) full-sibling
littermates and non-kin. Mean association indices are also shown for each set of
animals. All pairs represented here were matched for sex, age, and relative
social rank. Sample sizes represent numbers of individuals. Statistically ‘
significant differences are indicated with an asterisk.

67

Figure 3.1

Fe rce nt sca n s

Percent scans

Percent scans

8)
14 -

12-

_l
O
l

1

men

 

 

.L
NAOQO

LL

 

I Full Sib Littermates

 

 

El Maternal Half-sibs

   

 

- 0.45

‘ 0.35

- 0.25

- 0.15

- 0.05

 

 

Playing together Feeding together Association Index

 

I Full Sib Littermates
Cl Patemal Half-sibs

 

 

 

 

- 0.5

-0.4

- 0.3

-02

Association index

- 0.1

 

Playing together Feeding together Association Index

I Full Sib Littermates

D Non- kin
Playing together Feeding together Association Index

68

0.5

0.45

0.4
0.35
0.3
0. 25

Association Index

0.15
0.1
0.05

Associatlon index

Figure 3.2. Mean percent of scans in which individual hyenas were observed
playing and feeding together with a) maternal half-siblings and non-kin, b)
maternal half-siblings and half-sibling littermates, c) maternal and paternal half-
siblings, and. Mean association indices between individual hyenas and members
of both comparison groups are also shown. All pairs represented here were
matched for sex, age, and relative social rank. Other notation is as in Figure 3.1.

69

Figure 3.2

Percent scans

Percent scans

Percent scans

a)
14 4

12“

A
m o
l I

 

b)
14 -
12 «

1o-

 

 

 

I Maternal Half-sibs
0 Non -kin

 

 

Playing together

 

 

 

 

 

I Maternal Half-sibs
0 Half Sib Littermates

 

 

5

 

Feeding Together

 

 

ﬁsh

 

C)
14

12«

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49

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Playing together

 

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. Cl Paternal Half-sibsI

 

 

11

.1.

 

- 0.45

- 0.35

' 0.25

- 0.15

' 0.05

 

I W 0

Association Index

 

~

 

 

 

 

 

T

Feeding Together

 

 

Feeding Together

70

Association Index

4

Association Index

j:

0.6 ‘

0.5

0.4

0.3

0.2

0.1

Assoclatlon Index

Association Index

0.5

' - 0.45

0.4

: 0.35

0.3

i- 0.25

0.2

0.15

0.1
0.05

Assoclatlon Index

 

 

Coalitions Ihour

 

Figure 3.3. Mean hourly rates at which coalitions formed within dyads composed
of full-sibling littermates, half-sibling littermates, maternal half-siblings, paternal
half-siblings, and non-kin. Sample sizes represent numbers of dyads. Statistically
significant differences are indicated with asterisks over brackets.

71

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. o

 

 

   

 

 

 

 

 

 

 

 

Playing together Feeding together Association Index

Figure 3.4. Mean percent of scans in which pairs of full- and half-sibling
littermates were observed playing and feeding together. Mean association
indices between full- and half-sibling littermates are also shown. Sample sizes
represent numbers of sibling dyads. Statistically signiﬁcant differences are
indicated with an asterisk.

72

14 a T 0.5

 

 

 

I Paternal Hal f-sibs 0 45

12 - D Non-kin '
- 0.4
10 1 - 0.35
- 0.3

' 0.25

11 *
6“ - 0.2
4 « - 0.15
4 11 7 7 - 0.1
2 _ 4
.44 i
O " I 1 II 0

Playing together Feeding Together Association Index

Percent scans
Assoclatlon Index

 

 

 

 

 

 

Figure 3.5. Mean percent of scans in which individual hyenas were observed
playing and feeding together with their paternal half-siblings and unrelated
animals. Mean association indices are also shown. All pairs represented here
were matched for sex, age, and relative social rank. Other notation is as in
Figure 3.1.

73

CHAPTER FOUR

FACTORS INFLUENCING SIBLING AGGRESSION IN THE SPOTTED
HYENA (CROCUTA CROCUTA)

INTRODUCTION

Inclusive fitness theory (Hamilton 1964) explains how costly altruistic
behaviors can increase in frequency within populations through compensatory
benefits received by kin. However, Hamilton’s rule also speciﬁes the
evolutionary conditions under which selfish behavior, including sibling rivalry, is
expected to occur among close kin (Mock et al. 1997). Intense aggression
directed at siblings is one form of sibling rivalry that is commonly observed in,
animals. Aggression among siblings is often severe and sometimes lethal. Kin
selection theory predicts that animals’ behavior should reﬂect a balance between
direct and indirect components of inclusive ﬁtness, and that this balance should
determine when, if ever, it might pay to attack or kill siblings to gain direct fitness
at the cost of reduced indirect ﬁtness.

Whereas siblicidal aggression is a common and well-documented
phenomenon in many birds (Mock 1984; Drummond et al. 1986; Mock et al.
1997; Loughhead et al. 1999), the topic has been little studied in mammals, with
its occurrence documented only among domestic pigs (Sus scrofa, Fraser et al.
1991) and inferred among spotted hyenas (Crocuta crocuta, Frank et al. 1991;
Hofer et al. 1997; Golla et al. 1999; Smale et al. 1999). Among domestic cats,
dogs, and pigs, poor nutrition during gestation can retard intrauterine growth in
the last offspring within a clutch or litter (Robinson et al. 1999), and the ‘runt’ of a

litter may lose out in post-natal sibling competition. Aggression among siblings

74

has been described in Arctic foxes (Alopex lagopus Macpherson 1969), red foxes
(Vulpes vulpes, Henry 1985; Henry 1985), coyotes (Canis Iatrans, Bekoff 1981 ),
and Galapagos fur seals (Arctocephalus galapagoensis, Trillmich 1986), but the
functional significance of this aggression remains unclear.

Sibling rivalry has been defined as “any features of animals or plants that
have the effect of promoting individual survival and/or reproduction at the
expense of current and future siblings (Mock et al. 1997, p. 8).” Siblicide
represents an extreme form of sibling rivalry in which sibling competition results
in death (Mock et al. 1990). Although siblicide may results from overt
aggression, fighting may not be the only form of siblingicompetition. That is,
siblicide can also occur when one offspring monopolizes resources, ensuring
mortality among its siblings. Mortality through non-aggressive siblicide is much
less certain than through overt aggression (Mock et al. 1997). The focus of this
chapter is on sibling rivalry among spotted hyena cubs expressed through overt
aggression, since aggression directed at siblings here represents a vivid and
easily quantifiable behavioral indicator of selﬁshness. We also hope to shed light
on the factors that inﬂuence this fighting among hyena siblings.

Spotted hyenas are precocial at birth (Pournelle 1965). Litter size in this
species is small, usually one or two cubs, and rarely three. Adult female Crocuta
usually have only 2 functional teats, so nursing more than two cubs concurrently
is generally impossible. In contrast to other neonatal carnivores, hyena cubs are
born with their eyes open, coordinated locomotor capabilities, and fully erupted

canine and incisor teeth (Frank et al. 1991). Among captive hyenas, intense

75

fighting between littermates begins within minutes of birth (Frank et al. 1991) and
this fighting continues for the next several days (Frank et al. 1991; Smale et al.
1995; Drea et al. 1996). In the wild, neonatal spotted hyenas spend most of their
time underground (East et al. 1989), making behavioral observations of neonatal
cubs there difficult and rare. Although ﬁghting is often observed in the wild
between littermates when they emerge from the den, direct observations of fatal
sibling aggression have never been made among wild hyenas. However, indirect
evidence suggests that intense early sibling aggression might function in nature
to kill siblings, resulting in either obligate (Frank et al. 1991; Frank 1996) or
facultative siblicide (Hofer et al. 1997; Golla et al. 1999; Smale et al. 1999;
Wachter et al. 2002). Siblicide is considered ‘obligate’ when aggression within a
brood or litter is almost always fatal to subordinates, as occurs in many avian
species such as eagles, herons, and egrets (reviewed in Mock et al. 1997). In
‘facultative’ siblicide, however, siblings adjust competition intensity as costs and
benefits of intrabrood aggression vary with current environmental conditions
(Mock et al. 1997). Facultative siblicide has been documented in blue-footed
boobies (Sula nebouxr), ospreys (Pandion haliaetus), cattle egrets (Bubulcus
ibis) and great blue herons(Ardea herodias fanninr) (reviewed in Mock et al.
1997)

Frank et al. (1991) invoked three lines of indirect evidence to infer the
occurrence of obligate siblicide among spotted hyena cubs. First, they observed
intense fighting among captive littermates and severe wounding and emaciation

among some wild-caught cubs from twin litters. Second, they found that litter

76

sizes observed in the wild were significantly smaller than those observed in
captivity, suggesting that litter reduction might routinely occur in the wild due to
siblicide. Although obligate siblicide is known to occur in several avian species
(Mock et al. 1997), obligate siblicide had not previously been suggested to occur
in any mammal. Third, Frank et al. (1991) observed signiﬁcantly more same-sex
twin litters than mixed-sex twin litters in the wild than expected based on chance
expectations, and they inferred based on this that siblicide was contingent on
litter sex composition. They also observed an excess of female singletons,
suggesting that these females were originally from all-female twin litters that were
reduced to singletons through siblicide. The sex-bias in the obligate model of
hyena siblicide proposed by Frank et al. (1991) made siblicidal aggression
among spotted hyenas unique in the animal kingdom, as frequency or intensity of
attacks on siblings are not known to vary with sibling sex in any other vertebrate
species. Frank et al. (1991) failed to clearly establish that siblicide was
responsible for these sex biases and small litter sizes, as they never conclusively
refuted alternative explanations for these patterns. Larger litter size in captive
than wild hyenas might be due to differences in prenatal factors (e.g., stress and
diet quality) or postnatal factors (e.g., predation in nature) rather than to obligate
siblicide. A bias towards production of mixed-sex litters might not be the result of
obligate siblicide in same-sex litters, but rather due to female manipulation of sex
ratios according to environmental conditions (Holekamp et al. 1995). In addition,
the function of intense early intra-litter aggression in hyenas might not serve to

eliminate a sibling, but rather to establish intra-litter rank relationships very early

77

in life, as these would strongly affect future competitive outcomes while still
maximizing inclusive ﬁtness. Furthermore, workers studying hyenas after Frank
et al. (1991) found no evidence for obligate siblicide among wild spotted hyenas,
and concluded that skewed ratios of litter sex compositions indicated only the
occurrence of facultative siblicide in this species (Hofer et al. 1997; Smale et al.
1999). Further support for the facultative siblicide hypothesis came from studies
examining rates of intra-litter aggression between hyena cubs (Smale et al. 1995;
Golla et al. 1999; Wachter et al. 2002). Here it was argued that, when
environmental conditions are poor, rates of intra-litter aggression are high and
the dominant sibling can monopolize milk from both the mother’s teats,
eventually causing the subordinate cub to starve.

Although the debate persists over whether overt sibling aggression in
spotted hyenas might result in obligate or facultative siblicide, all investigators
agree that early sibling aggression in this species is unusually intense and
frequent. The goals of the current study, were therefore to determine what
factors influence the occurrence and frequency of aggression among Crocuta
siblings. Specifically, using data on sibling aggression occurring upon
emergence from the den collected systematically in the wild over a 15 year
period, we asked how rates of sibling aggression were inﬂuenced by cub age,
litter composition, maternal rank, local prey abundance, identity of the target of

aggression, and the speciﬁc context in which aggression occurs.

78

METHODS

Study Site and Subjects

This study took place in the Talek region of the Masai Mara National
Reserve, Kenya, in the northern portion of the Serengeti ecosystem. This region
consists of open rolling grasslands grazed year-round by several different
ungulate species, the most numerous of which are Thompson’s gazelles (Gaze/la
thomsom), topi (Damaliscus kom'gum) and impala (Aepyceros melampus). Each
year the resident ungulate populations are joined for 3 or 4 months by large
migratory herds of wildebeest (Connochaetes taurinus) and zebra (Equus
burcheI/I). The migratory herds typically arrive in the Talek area in July or August
and depart in October or November. When both resident and migratory
ungulates are present, superabundant food resources are generally available to
Talek hyenas such that feeding competition is greatly relaxed among them
(Holekamp et al. 1996; Holekamp et al. 1999).

Social groups, or clans, of spotted hyenas contain multiple adult males
and several matrilines of adult female kin with offspring. Males disperse from
their natal groups after puberty, whereas females are usually philopatric (Frank
1986; Henschel et al. 1987; Mills 1990; Smale et al. 1997). Adults can be ranked
in a strict linear dominance hierarchy with members of the same matriline
occupying adjacent rank positions. Female Crocuta are dominant to immigrant
males, and offspring attain ranks just below those of their mothers (Holekamp et
al. 1991; Engh et al. 2000; Engh et al. 2003). Rank relations, particularly those

among females, remain stable for extended periods and across a variety of

79

contexts (Kruuk 1972; Tilson et al. 1984; Frank 1986; Smale et al. 1993). An
individual’s position in the group’s hierarchy strongly determines its priority of
access to food (Kruuk 1972; Frank 1986).

Throughout the year, female hyenas bear their litters in isolated natal dens
(East et al. 1989). When cubs reach 2 to 4 weeks of age, females transfer their
offspring to the clan’s communal den where several mothers maintain their cubs
together for 8 to 12 months (Kruuk 1972). Spotted hyena cubs typically leave the
communal den at approximately 8 months of age and begin traveling throughout
the home range and feeding at ungulate kills with adults. However, hyena cubs
remain dependent on their mothers for milk until weaning, which takes place, on
average in our study population, at 13 to 14 months of age (Holekamp et al.
1996)

Subjects here were members of one large Crocuta clan that usually
contained 60 to 80 hyenas who defend a group territory of approximately 65 km’.
All adult members of the study clan were identified by their unique spot patterns,
and young cubs that had not yet developed spot patterns were identified by
unique scarring, bald patches, ear notches, size differences, molt patterns, or a
combination of these features. Sex was determined from the dimorphic glans
morphology of the erect phallus (Frank et al. 1990). By two months of age, the
glans of the male’s phallus assumes a distinctly different shape from that of the
female (Drea et al. 1998). That is, the male’s phallus is pointed at its tip and has
a constriction above the glans whereas the shape of the female’s pseudopenis is

blunt at the tip and lacks a constriction. Cubs regularly develop erections during

80

greeting ceremonies, which occur virtually every time a new hyena arrives at the
den. Young hyenas were sexed here repeatedly by multiple observers, and sex
could be assigned with complete certainty by the time cubs were 2-3 months old.
However, on several occasions, cubs died before they could be sexed. Only
litters in which the sexes were known for all siblings were included in our dataset.
We estimated cub birth dates (to 1 7 days) by using their pelage, size, and
other aspects of their appearance and behavior when cubs were first observed
above ground (Holekamp et al. 1996). Mother-offspring relations were
established on the basis of regular nursing associations. Members of twin litters
may be sired by either one or two fathers, but monozygotic twins have never.
been documented in spotted hyenas (R. C. Van Horn, pers. comm.) Social
ranks were determined based on wins and losses In dyadic agonistic
interactions. Outcomes of these interactions were organized into a matrix from
which each individual hyena could be assigned a social rank in the clan’s
dominance hierarchy (Martin et al. 1988). lntra-litter ranks were determined
based on outcomes of dyadic aggression between littermates; when one cub
aggressed against its littermate, which responded by avoidance and submissive
behavior, we described the aggressor as dominating its littermate. By the time
twin litters emerge above ground in nature, sibling rank relationships are well-
established such that aggression within litters is exhibited almost exclusively by

the dominant cub.

81

Data Collection

Behavioral data and measures of prey abundance were collected between
June 1988 and September 2003. Throughout this period, observers were
present in the study area at least 23 days/month except for April 1991, when
observers were present for only 14 days. We observed hyenas daily from our
vehicles, which we used as mobile blinds, mainly between 0600 and 0900 h and
between 1700 and 1900 h. An observation session started when we found two or
more hyenas separated from other conspeciﬁcs. by at least 200m, and terminated
when we left that group. Observation sessions occurred at natal and communal
dens, at ungulate kills, and away from both dens and kills. Throughout each
observation session, we recorded the identities of all individual hyenas present at
20 to 30 minute intervals.

During the study period, we monitored behavioral interactions within 71
twin litters (18 all-female litters, 34 mixed-sex litters, and 19 all-male litters) in
which both members of the litter were present together during at least 25 hours
of observation during the co-existence of those two littermates. Data were
available during each monthly age interval throughout the first year of life for 24
of these 71 twin litters, including 7 all-female litters, 16 mixed-sex litters, and one
all-male litter. These 24 twin litters were used in analyses of how sibling
aggression varies with age, how shifts occur over time with respect to the
contexts in which aggression is observed, and in comparisons of aggression
directed at siblings and unrelated peers as this changes over time. Both

members of 46 of the 71 twin litters (11 all-female litters, 26 mixed-sex litters, and

82

9 all-male litters) were observed during the 1-2 month age interval for at least
150 min together, and these 46 litters were used in all analyses involving only the '
1-2 month age interval, which started at birth and ended at 2 months of age.
Throughout every observation session, we recorded all occurrences of
aggressive behavior as critical incidents (all occurrence sampling, Altmann
1974), and the identities of all aggressors and target animals were also recorded.
Although social play behavior can resemble aggressive behavior among cubs,
the former often involves play solicitation postures and never results in pain- or
fear-induced vocalizations. Occurrence of these vocalizations, or the active ﬂight.
of one opponent, was used here to distinguish true aggression from play-ﬁghting.
Aggressive behaviors included head wave, lunge, aggressive posture (i.e., ears
cocked fon/vard while the tail was bristled and raised), chase, displace, stand
over, bite, bite-shake and push. The speciﬁc context in which each aggressive
interaction occurred was classified as occurring either over “milk”, over “solid
foods” or in “other” contexts involving neither milk nor solid foods. Aggression
over milk and solid food was associated with conflicts between littermates over
access to the mother’s nipples during nursing or access to meat or bones,
respectively. Aggressive interactions occurring in contexts unrelated to ‘milk’ or
‘solid foods’ were often unprovoked, or occurred in response to affiliative
behavior directed by of one littermate towards the other. Dyadic aggression
involved only one aggressor and one target animal. Coalitionary aggression was
not included in the data set. Rates of aggression within pairs were calculated by

dividing the total number of aggressive interactions observed between two

83

animals during a particular age interval by the total number of hours in which
both members of that pair were observed concurrently during that age interval.
Rate data for each age interval were based on the following mean number of
hours of observation per litter: for 1-2 month age interval, 6.38 1 0.77 hours of
observation; for 3-4 month age interval, 20.95 1 1.62 hours of observation; for the
5-6 month age interval, 24.60 1 1.72 hours of observation; for the 7-8 month age
interval, 19.33 1 1.44 hours of observation; for the 9-10 month age interval, 13.74
1 1.21 hours of observation; and for the 11-12 month age interval, 9.14 1 1.04
hours of observation.

Local availability of food to Talek hyenas was estimated by counting all
prey animals found within 100m of 4 km-long transect lines in two different areas
of the Talek clan home range (Holekamp et al., 1999). Both transects were run
twice each month, between 0800 and 1000h. During any age interval, the
aggression rate calculated for any particular pair of siblings could be associated
with the average number of prey counted per census for all censuses performed
between the starting and ending dates of that age interval for that sibling pair.
On average 4.8 1 0.02 prey censuses were conducted during each 2 month age
interval. Monthly variation in prey counts has been described by Holekamp et al.
(1993). The number of prey animals counted per census ranged from 61 to 958,
with a mean of 353.17 1 24.45. Since births are not synchronized among female
Crocuta (Szykman 2001), cub age is not correlated with prey abundance in this

species.

84

Data Analysis

Rates of dyadic aggression were analyzed using the pair as the unit of
analysis, with each pair used only once in the entire data set. Since our data
were not normally distributed, we compared hourly rates of aggression between
sibling pairs using non-parametric statistics. Effects of age were examined by
partitioning age into 2-month intervals up to one year (1-2 months, 3-4 months, 5-
6 months, 7-8 months, 9-10 months and 11-12 months). Using the 24 twin litters
observed throughout the ﬁrst year of life, we employed a Friedman’s repeated-
measures ANOVA to determine how aggression rates varied with age. Post hoc
comparisons were performed using Wilcoxon matched-pairs signed-ranks tests.
The sequential Bonferroni adjustment was then used to correct for multiple
testing (Rice 1989).

To determine how age-related shifts occurred in the contexts in which we
observed intra-Iitter aggression, we divided age into 2 periods of 1-6 months and
7-12 months and compared the distribution of aggressive interactions between
each of the two age intervals within the contexts of ‘milk’, ‘solid foods’, and ‘other’
using a Wilcoxon matched-pairs signed-ranks tests. As in our analysis of age
effects, effects of the context in which aggression occurred were examined using
the 24 twin litters for which we had data throughout the first year of life.

We evaluated effects of composition of twin litters on rates of aggression
using a Kruskal-Wallis one-way ANOVA to compare all-female litters, mixed-sex
litters, and all-male litters, and a Mann-Whitney U-test to compare same-sex to

mixed-sex litters. We inquired how rates of aggression differed between same-

85

sex and mixed-sex sibling pairs within twin litters that were female-dominated
and male-dominated using a Mann-Whitney U-test.

In analyses examining effects of maternal rank on rates of aggression
between littermates, we assigned each litter the rank of its mother during the
year in which that litter was born. Since the total number of adult females
present in the clan varied over time, rank was standardized from 0 to 1, with 1
assigned to the highest-ranking, and 0 to the lowest-ranking sibling pair born
within each year. High-ranking littermates were deﬁned as those having a
standardized rank of 0.5 or greater, while low-ranking littermates had a
standardized rank less than 0.5. Effects of maternal rank on hourly rates of I
aggression were examined in two ways. First, we evaluated hourly rates of
aggression in relation to standardized rank using a Spearman’s Rank correlation.
Second, we assigned litters to high- and low-rank categories, and compared
hourly rates of aggression between high- and low-ranking litters using a Mann-
Whitney U test. Within high- and low-ranking litters, we compared aggression
rates observed between mixed-sex and same-sex littermates using Mann-
Whitney U-tests. Rates of aggression were evaluated in relation to prey
abundance using a Spearman’s Rank correlation. Differences between same
and mixed-sex litters in relation to levels of prey abundance were analyzed using
a Mann-Whitney U-test.

To determine how targeting of aggression varied during early ontogeny,
we used 21 of the 24 twin litters observed throughout the ﬁrst year of life and

employed a Friedman’s repeated-measures ANOVA to compare the percent of

86

aggressive acts cubs directed towards siblings among 2-month age intervals.
The same analysis was conducted with the percent of aggressive acts directed
towards unrelated cohort peers. Cohort peers were defined as unrelated animals
that spent at least 4 months living together concurrently at the clan’s communal
den. Whereas individual cubs may have only one twin littermate, they may have
up to 12 unrelated cohort peers with a mean of 3.52 1 0.58 peers per individual
cub. Post hoc comparisons were not made among age intervals since our
interest was in whether or not there was an ontogenetic shift in percent of
aggressions directed toward siblings and cohort peers. However, we did
compare the percent of aggressive acts a cub directed towards its siblings with
the percent of aggressive acts directed at unrelated peers during each 2-month
age interval using a Wilcoxon matched-pairs signed-ranks tests. Although
information about paternity was unavailable for many hyenas used as subjects in
this study, we defined unrelated animals as having coefﬁcients of relatedness (r,
Hamilton 1964) less than 0.125, calculated from matrilineal pedigrees as in
Holekamp et al. (1999). Differences between groups in all analyses were
considered significant when p _<_ 0.05. Throughout the paper, means (1 se) are

reported. All statistical tests were performed using Statistica 6.1 software.

RESULTS

Effects of Age
Rates of intra-litter aggression were highest and most variable during the
first 2 months of life, and aggression rates subsequently dropped dramatically

(Figure 4.1 ). A Friedman’s ANOVA on rates of aggression within the 24 litters in

87

which both cubs survived to 12 months revealed a significant effect of age (F523
= 16.41, P = 0.006). Rates of aggression dropped signiﬁcantly between the 1-2
and 3-4 month age intervals (Wilcoxon Z = 2.78, n = 24, P = 0.005), but there
was no significant difference in aggression rates between the 3-4 month and 5-6
month intervals (Wilcoxon Z = 1.35, n = 24, P = 0.177). By 5-6 months of age,
rates of aggression had stabilized at low levels and did not change again

significantly.

Effects of the context in which aggression occurs

Using the 24 twin pairs in which both siblings survived to 12 months, we
found that siblings engaged in a signiﬁcantly higher percentage of aggressions
while fighting over milk during the 1-6 month age interval than during the 7-12
month age interval (Figure 4.2; Wilcoxon Z = 3.41, n = 24, P < 0.001). However,
siblings engaged in a significantly higher percentage of aggressions over solid
food during the 7-12 month age interval than during the 1-6 month age interval
(Figure 4.2; Wilcoxon Z = 2.81, n = 24, P = 0.005). Aggression directed toward
siblings in ‘other’ contexts did not vary signiﬁcantly with age (Figure 4.2;

Wilcoxon Z = 1.94, n = 24, P = 0.06).

Effects of litter composition and sex of dominant cub
Since rates of aggression were highest and most variable during the 1-2
month age interval, we limited our subsequent analyses of factors affecting

variability in intra-litter aggression to this first age interval. Although mixed-sex

88

twins tended to exhibit higher rates of aggression than did either type of same-
sex twins during the 1-2 month age interval, rates of aggression did not vary
significantly with litter composition (Kruskal-Wallis T = 4.65, n = 11 all-female, 26
mixed-sex, and 9 all-male litter-mates, P = 0.098). However, when all-female
and all-male pairs were lumped together into the category of same-sexed twins,
we found that mixed-sex litter-mates had significantly higher rates of aggression
than did same-sex litter-mates during the 1-2 month age interval (Figure 4.3;
Mann-Whitney U = 178, n = 20 same-sex litter-mates, 26 mixed-sex litter-mates,
P = 0.05).

To evaluate the effects of the sex of the dominant sibling within each litter
during the 1-2 month age interval, we compared aggression rates from litters in
which a male was the dominant cub with litters in which a female dominated its
litter-mate. Within mixed-sex litters, there were no significant differences in rates
of aggression between litters in which females were the dominant cubs and those
in which males were dominant (Figure 4.3; Mann-Whitney U = 38, n = 22
dominant females, 4 dominant males, P = 0.67). Similarly, within same-sex
litters, aggression rates did not vary with the sex of the dominant cub (Figure 4.3;
Mann-Whitney U = 37, n = 11 dominant females, 9 dominant males, P = 0.28).
Within twin litters in which the dominant cub was male, we found no significant
difference between same-sex and mixed-sex litters in the rate of hourly
aggression during the 1-2 month age interval (Figure 4.3; Mann-Whitney U = 69,
n = 4 mixed-sex, 9 same-sexed litter-mates, P = 0.52). However, within twin

litters in which the dominant cub was female, early aggression rates were higher

89

within mixed than same-sex litters (Figure 4.3; Mann-Whitney U = 14, n = 22

mixed-sex, 11 same-sexed litter-mates, P = 0.035).

Effects of maternal rank

Variability in intra-litter aggression during the 1-2 month interval was not
correlated with maternal rank (Spearman rs = -0.0126, n = 46 pairs, P = 0.934).
The mean aggression rate within low-ranking litters was twice that within high-
ranking litters during the 1-2 month age interval, but this difference was not
statistically signiﬁcant (Mann-Whitney U = 263.5, n = 24 high-ranking litter-mates,
22 low-ranking litter-mates, P = 0.991 ). We also examined effects on rates of
intra-litter aggression of rank and litter composition together. Within high-ranking
litters, we found no difference in aggression rates between same-sexed and
mixed-sexed litters during the 1-2 month age interval (Figure 4.4; Mann-Whitney
U = 58, n = 10 same-sexed, 14 mixed-sex litter-mates, P = 0.46). However,
within low-ranking litters, aggression occurred at higher rates within mixed- than
same-sex litters during the 1-2 month interval (Figure 4.4; Mann-Whitney U = 33,

n = 10 same-sexed, 12 mixed-sexed litter-mates, P = 0.05).

Effects of prey abundance

Hourly rates of intra-litter aggression during the 1-2 month age interval
decreased as local prey abundance increased (Figure 4.5; Spearman rs = -0.294,
n = 46, P = 0.049). To determine whether local prey abundance differentially

influenced aggression rates among high and low-ranking litters, we also

90

evaluated the relationship between prey and rates of aggression for high and
low-ranking litter-mates separately. Rates of aggression among high-ranking
litter-mates did not vary significantly with prey abundance during the 1-2 month
age interval (Spearman rs = -0.128, n = 24, P = 0.56). Rates of aggression
among low—ranking litter-mates declined as prey abundance increased, but this
trend was only marginally significant (Spearman rs = -0.398, n = 22, P = 0.06).
To determine whether the higher rates of aggressions found in mixed-sex litters
was due to lower levels of prey abundance, we compared levels of prey
abundance during the 1-2 month age interval between same-sex and mixed-sex
litters and found there to be no signiﬁcant difference (Mann-Whitney U = 586, n =

37 same-sexed, 34 mixed-sex litter-mates, P = 0.62).

Sibling aggression compared with aggression toward unrelated peers

The percentage of all aggressive acts that hyenas directed towards
siblings decreased with age (Figure 4.6; F5,,2o = 22.68, P < 0.001). Despite the
fact that siblings associated with each other more closely than did unrelated
peers throughout the first year of life, hyenas directed a higher percentage of all
their aggressive acts towards their unrelated peers as they grew older (Figure
4.6; F5, 20 = 22.68, P < 0.001). Cubs directed a signiﬁcantly higher percentage of
their total aggressions toward their siblings than toward unrelated peers during
the 1-2 month age interval (Figure 4.6; Wilcoxon Z = 2.67, n = 21, P = 0.008) and
during the 3-4 month age interval (Figure 4.6; Wilcoxon Z = 2.79, n = 21, P =

0.005). Within the age intervals of 5-6 and 7-8 months, cubs did not direct

91

signiﬁcantly different proportions of their aggression towards litter-mates and
unrelated peers (5—6 months: Wilcoxon Z = 0.369, n = 21, P = 0.711; 7-8
months: Wilcoxon Z = 0.533, n = 21, P = 0.593). However, by 9-10 months,
hyenas directed significantly more aggression toward unrelated peers than their
litter-mates (Wilcoxon Z = 2.416, n = 21, P = 0.015). We found no signiﬁcant
difference in the percentage of aggressions directed towards litter-mates and
unrelated peers in the 11-12 month age interval (Wilcoxon Z = 0.254, n = 21, P =

0.798).

DISCUSSION

Variables affecting sibling aggression

Overall, we found that age, context of aggression, litter composition, local
prey abundance and the identity of the target of aggression all play important
roles in shaping patterns of intra-litter aggression among spotted hyena cubs.
Thus, we have replicated and extended results reported by Smale et al. (1995) in
that we observed the same patterns of ontogenetic variation as did these earlier
workers with respect to both hourly rates of intra-litter aggression and the
contexts in which intra-Iitter fighting occurs. The current study also showed that
rates of intra-litter aggression were affected by litter sex composition and local
prey abundance, variables not previously examined by Smale et al. (1995).

As in earlier studies of this species (Frank et al. 1991; Smale et al. 1995;
Drea et al. 1996; Golla et al. 1999), spotted hyena cubs in our study exhibited the

highest rates of aggression during the first 2 months of life, with aggression rates

92

declining thereafter. Infra-litter dominance determines priority of access to the
mother’s teats and the dominant cub can potentially monopolize the supply of
milk. Thus, the early establishment of intra-litter rank relations can confer
important benefits to dominant cubs, such as faster cub growth (Hofer et al.
1993). Frank et al. (1991) found that rates of intra-litter aggression decreased in
captivity once intra-litter dominance was established. In captivity, dominance
was established within the ﬁrst 8 days of life (Smale et al. 1995). All rank
relationships among spotted hyenas other than those between litter-mates are
determined by social variables such as maternal rank and immigration status,
and rank among non-sibling youngsters depends at ﬁrst on whether or not their
mothers and other conspecifics are present during ﬁghts (Frank 1986; Holekamp
et al. 1993; Smale et al. 1993). However, wild neonates establish rank
relationships with their siblings in isolated natal dens away from external
inﬂuences, so intra-litter rank relationships can only be determined by cubs’
relative fighting ability (Smale et al. 1995). The importance of early
establishment of dominance status, and the fact that this status can only be
determined by fighting suggests that the intense intra-Iitter aggression observed
during the 1-2 month age interval in this study represents an early struggle to
establish and maintain intra-litter dominance between siblings, rather than a
routine attempt to kill one’s litter-mate as suggested by Frank et al. (1991). The
intensity of early fighting observed between litter-mates in both the wild and
captivity reflects the huge fitness advantage the winner in these fights will enjoy if

environmental conditions deteriorate to the point at which the mother can only

93

provide enough milk to support a single cub. Dominant cubs can displace their
subordinate litter-mates from access to the mothers’ teats until weaning, and
from access to solid food indefinitely (Smale et al. 1995). Given that rates of
aggression are quite low in Talek hyenas after the first 2 months of life, we found
it surprising that Hofer and East (1997) observed siblicide in a litter already nine
months old (273 days). Perhaps the commuting system of Serengeti spotted
hyenas, in which mothers take extended foraging trips outside of the clan’s
territory, favors prolonged sibling aggression not seen in the Masai Mara.
lntra-litter aggression among spotted hyenas is primarily related to
competition among litter-mates over access to milk or solid food. During the ﬁrst
6 months of life, cubs in this study typically fought over access to the mother’s
nipples. However, by months 7-12, cubs fought primarily over solid food, even
though weaning in this population does not occur until ~ 13 months of age.
Smale et al. (1995) found that over 80% of intra-Iitter aggressions in spotted
hyena cubs occurred over competition for milk or food. Similarly, in this study,
over 65% of intra-litter aggression occurred in the context of competition over
access to milk or food, suggesting that rates of aggression might vary with
resource abundance. Indeed, we found that rates of aggression during the ﬁrst 2
months of life decreased as local prey abundance increased, and that this
relationship was more apparent in offspring of low- than high-ranking mothers.
Golla et al. (1999) found that levels of aggression between hyena siblings in the
wild decreased as maternal provisioning rates increased, further suggesting that

resource availability inﬂuences sibling competition. Wachter et al. (2002)

94

compared intra-litter aggression between populations of spotted hyenas
inhabiting prey-rich and prey-poor areas of Tanzania, and found that litter-mates
fought less in the population co-existing with abundant prey. All these data are
consistent with the hypothesis that prey scarcity may lead to deﬁciency in the
milk supply of the lactating female, enhancing rates and intensities of aggression
between her cubs for access to her teats.

Perhaps the best examples of food availability inﬂuencing sibling
aggression come from observations and ﬁeld experiments with birds. Avian
models of facultative siblicide predict that the amount of food supplied by the
parent should inﬂuence offspring aggression. This “food amount hypothesis”
(Mock et al. 1987) is supported by avian studies demonstrating a causal
relationship between food deprivation and sibling aggression. Observational
studies of birds have shown increased fighting during periods of low food
availability, increased attack rates during meals and decreased attack rates after
meals (reviewed in Mock et al. 1987; Drummond 2001). Field experiments
manipulating the feeding of blue-footed booby chicks have also found that rates
of aggression increased when chicks are food-deprived (Drummond et al. 1989;
Nunez et al. 1996). To date, the data from spotted hyenas suggest that, like
these avian species, their behavior conforms to predictions of Mock’s (1987)
“food amount hypothesis” rather than to the predictions of the obligate siblicide
hypothesis.

Given that local prey abundance inﬂuenced sibling aggression in the

current study, and that social rank determines priority of access to food in

95

Crocuta (Kruuk‘1972), we found it surprising that maternal rank did not
significantly inﬂuence sibling aggression here. Since high-ranking females are
usually able to provide sufficient milk to support both offspring in their twin litters,
the need for aggression between high-ranking litter-mates should be less than
that between low-ranking litter-mates. In this study, low-ranking litter-mates
demonstrated twice the mean aggression rates of high-ranking litters, yet this
difference was not statistically significant due to large variance and small sample
sizes. Furthermore, the negative relationship between prey abundance and rates
of intra-litter aggression was stronger within low-ranking than high-ranking litters.
Thus, trends in our data suggest that maternal rank might indeed inﬂuence intra-
litter aggression. Golla et al. (1999) and Smale et al. (1995) found that rates of
sibling aggression increased as maternal social status declined, suggesting that
lower rates of milk production among low-ranking mothers result in higher rates
of sibling aggression.

Both the Smale et al. (1995) study and the current study took place in the
Talek region of the Masai Mara National Reserve, Kenya, where prey are
generally abundant. Although the time periods of the two studies differed, the
same methods for estimating local prey abundance were used during both study
periods and mean levels of prey abundance between the two study periods did
not significantly differ (Mann-Whitney U = 15292, P = 0.35). Thus, the
relationship between intralitter aggression and maternal rank observed in the
Smale et al. (1995) could not be attributed to a lower mean abundance of local

prey than that recorded in the current study. Rate data from our study were

96

based on only half the number of hours of observation per litter as those used by
Smale et al. (1995). Therefore, another possibility is that our less-rigorous
criterion for time cubs needed to spend together to be included in the data set
might account for the difference in results between our studies. However, even
when we limited our data set to the six litters that were observed for the same
number of hours as were cubs observed by Smale et al. (1995), we still found no
significant relationship between rates of aggression and matem'al rank during the

1-2 month age interval (Spearman rs = -0.183, n = 14 pairs, P = 0.531 ).

Sex-biased siblicide

The obligate siblicide model proposed by Frank et al. (1991) assumes that
same-sexed hyena litters routinely ﬁght until one sibling dies because same-sex
twins are evenly matched in competitive ability, but that competition is relaxed
among mixed-sex litters. Although Hofer and East (1997) and Golla et al. (1999)
found no support for the obligate siblicide hypothesis in spotted hyenas, they
observed higher rates of aggression and/or facultative siblicide in same- than
mixed-sex litters, particularly among all-female litters. In the current study, we
found no significant difference in rates of aggression between all-female, mixed-
sex, and all-male litters and this same negative result was also obtained by
Smale et al. (1995) and Drea et al. (1996). However, we were surprised to ﬁnd
here that, when all-female and all-male litters were pooled, mixed-sex litters,
particularly those produced by low-ranking females, engaged in aggression at

higher rates than did same-sexed litters. In fact, the highest rates of aggression

97

during the 1-2 month age interval were observed in low-ranking, mixed-sex
litters, particularly when females rather than males were the dominant cubs. This
result contradicts predictions of an hypothesis suggesting that adult female
Crocuta might be producing mixed-sex twins to avoid competitive symmetries
and prolonged ﬁghting between same-sex twins (Smale et al. 1999). Since
higher rates of aggression in mixed-sex litters were not associated with lower
levels of prey abundance than those found in same-sex litters, this difference
could not be attributed to variation in prey abundance. Perhaps one reason that
previous studies in the Serengeti (Hofer and East 1997; Golla et al. 1999) found
higher rates of aggression or facultative siblicide in all-female litters was because
the Serengeti area is characterized by lower levels of prey abundance than in the
Masai Mara (current study). When levels of prey are low, competition between
siblings in all-female litters might be higher since females will remain in the natal
clan and grow up as competitors. However, where relatively abundant prey are
available throughout the year, such as in the Masai Mara, females might
compete more with their brothers than their sisters since their brothers will not
remain in the natal clan and become important allies for them.

Frank et al. (1991) suggested that, since females acquire their mother’s
rank in the social hierarchy and remain in the natal clan their entire lives,
elimination of a close-ranking competitor would confer selective advantages to
surviving cubs from all-female litters. However, to explain siblicidal aggression
within male-male litters, Frank et al. (1991) proposed a different adaptive

explanation, arguing that elimination of a close-ranking brother would result in

98

more rapid weight gain during the ﬁrst year of life, which in turn would improve a
male’s chance of survival during dispersal. Sex-biased siblicide among spotted
hyenas seems unlikely considering the lack of parsimony in the preceding
explanations, our observation here of higher aggression rates among same- than
mixed-sex twins, and the fact that sex-biased siblicide has not been recorded in
any other animal species to date. In addition, hyena litter-mates are often
tremendously helpful to each other regardless of their sex (Smale et al. 1995;
Wahaj et al. 2004), so routine killing of same-sex litter-mates would appear to be
highly maladaptive. The fitness benefits of having a living litter-mate appear to
be substantial. For example, spotted hyena siblings are each other’s closest
associates and most frequent partners during coalition formation (Smale et al.
1995; Wahaj et al. 2004). Thus, although same-sex siblings may be each other’s
closest-ranking competitors, they are also each other’s most important allies.
During the first 6 months of life, hyena litter-mates in this study engaged In
more aggressions over milk than in any other context, and during the ﬁrst 4
months of life they fought more with their litter—mates than with unrelated peers.
However, by 7-12 months of age, cubs began ﬁghting over access to solid food,
and by the 9th and 10th months of life, they directed more aggression toward
their peers than toward their litter-mates. After cubs leave the communal den at
approximately 8 months of age, both siblings and unrelated peers are potential
competitors over access to solid foods. Since intra-litter dominance is firmly
established by 7-12 months, cubs no longer need to fight with their siblings and

begin competing with other peers over access to carcasses. This ontogenetic

99

progression from fighting with siblings to ﬁghting with peers might correspond to
developmental changes in the need to establish rank relations with clan
members other than siblings (Drea et al. 1996).

In addition to the factors found in the current study, other variables that
appear to inﬂuence rates of sibling aggression are maternal hormone levels
during fetal development (Dloniak 2004) and genetic relatedness within twin
litters (Wahaj et al. 2004). Dloniak (2004) showed that high-ranking female
spotted hyenas have higher fecal androgen concentrations than do low-ranking
females during the second half of gestation, and that this variance in maternal
fecal androgen levels is related to offspring behavioral phenotype. Cubs born to
females excreting higher fecal androgen concentrations during late pregnancy
show higher rates of aggression toward unrelated peers than do cubs born to
females with lower fecal androgen concentrations. However, Dloniak (2004)
found no relationship between maternal androgen levels and intra-litter
aggression, so prenatal androgens do not appear to affect aggression rates
between siblings in spotted hyenas.

Relatedness between litter-mates also inﬂuences rates of intra-litter
aggression. Female spotted hyenas often mate with multiple partners and twin
litters may be sired by either one or two males, resulting in full-sibling and half-
sibling litter-mates (Engh et al. 2002; East et al. 2003). Wahaj et al. (2004) found
that rates of aggression during nursing between half-sibling littermates were nine
times higher than that between full-sibling litter-mates. Similarly, Hofer et al.

(2004) found that rates of aggression between half-sibling litter-mates were

100

higher than between full-sibling twins, and that this difference was substantially
exaggerated under conditions of limited access to resources. Perhaps variation
in mean relatedness within rank categories explains why Smale et al. (1995)
found higher rates of aggression in lower-ranking litters, but this study failed to

ﬁnd rank-related variation in intralitter aggression.

101

1.4 ~

1.2 -

1.0 ~

0.8 -

0.6 -

 

Aggressions per hour

0.4 ~

0.2 -

 

 

0.0 A . I . J 1 A
1-2 3-4 5-6 7-8 9-10 11-12

Age interval (months)

Figure 4.1. Mean hourly rates of intra-Iitter aggression during each two month
age interval in the first year of life. The sample represented by each data point
includes 24 litters in which both cubs survived to 12 months. Statistically
significant differences are denoted with an asterisk.

102

100 i

 

 

*
I I
I I - 1-6 months of age
IIIIIIII 7-12 months of age
30 . * ‘
I I
I I
8
:3
'5 60 -
8’
8
8
.9
8
g, 40-
8’
3
6'3
20 -
o llllllllllil IIIIIIIIII

 

 

 

milk solid foods other

Context of aggression

Figure 4.2. Mean percent of aggressive interactions between siblings during the
1-6 (black bars) and 7-12 (gray bars) month age intervals that we observed in the
contexts of ‘milk’, ‘solid foods’, and contexts ‘other’ than milk or solid foods. The
sample represented in each pair of bars is 24 litters in which both cubs survived
to 12 months. Statistically signiﬁcant differences are denoted with asterisks.

103

- Female littermate dominant
Male littermate dominant

 

Aggressions per hour during the 1-2 month age intenial

 

 

 

 

 

mixed-sex same-sex

Litter composition

Figure 4.3. Mean hourly rates of aggression during the 1-2 month age interval
within same and mixed-sex litters in which females (black bars) and males (gray
bars) were the dominant cubs. Sample sizes above bars represent number of
litters in each group. Other notations are as in Figure 4.2.

104

- Mixed-sex litters

 

 

 

5 . i Same-sex litters
_ 5 _
g a:
i I l
g I j
5
S 4 12
E
“J
I;
5
o: 3 -
I:
'C
3
U
5
2
a
Q
(I)
C
.9
U)
(D
9
O)
O)
<

 

 

 

 

 

   

Maternal rank

Figure 4.4. Mean hourly rates of aggression during the 1-2 month age interval
within same-sex (gray bars) and mixed-sex litters (black bars) born to mothers of
high and low rank. Other notations are as in Figure 4.3.

105

 

 

 

6 l
O High-ranking litters
O Low-ranking litters
O

5 .
E O
0.)
.E
0)
g 4
.C
”E O
O
E
‘1‘
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5 3 .
8’
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8
F 0
£8 1 . ° 0

O O O
O
0 e
0 - 00 W 09. 0 ° 0. . ° a.
O 200 400 600 800 1000

Local prey abundance

Figure 4.5. Hourly rates of intra-litter aggression during the 1-2 month age
interval as a function of local prey abundance. Sampled litters include 24 high-
ranking litters and 22 low-ranking litters.

106

1.4.

   

 

 

 

 

 

 

 

 

 

 

   

 

 

 

 

   

- Aggressions directed toward sibling
Aggressions directed toward unrelated peers
1.2 -
*
E 1.0 - * *
Q)
32'
... H
U)
m
g 0.8 -
U)
C
.9 -..
(D
09
9
8 0.6 .
(U ,.
° , "
E 35%
g 11“.. i:
g 0.4 ~ f 4__
1:.-
0.2 r ,
0.0 - - ' - -'
3-4 5-6 7-8 9-10 11-12

 

Age Intenlal (months)

Figure 4.6. Mean percent of all aggressive interactions during each two month
age interval in which hyenas directed aggression toward their litter-mates (black
bars) or towards unrelated peers within their cohorts (gray bars). The sample
here includes 21 litters in which both cubs within each twin litter survived to 12
months. Total aggressive interactions included 354 ﬁghts directed toward
siblings and 237 ﬁghts directed toward cohort peers during the ﬁrst 12 months of
life. Statistically significant differences within each age interval are indicated by
asterisks.

107

CHAPTER FIVE

USE OF ULTRASONOGRAPHY TO TEST OBLIGATE AND FACULTATIVE
MODELS OF SIBLICIDE IN THE SPOTTED HYENA (CROCUTA CROCUTA)

INTRODUCTION

Whereas siblicidal aggression is a common phenomenon in many birds
(Mock 1984; Drummond et al. 1986; Mock et al. 1997; Loughhead et al. 1999),
the topic has been little studied in mammals, with its occurrence documented
only among young pigs (Sus scrofa: Fraser et al. 1991) and inferred among
spotted hyenas (Crocuta crocuta: Frank et al. 1991; Hofer et al. 1997; Golla et al.
1999). In birds, sibling rivalry can be severe, and it is often lethal (Drummond
2001). Spotted hyenas have been described as a bizarre exception to the I
general rule that mammalian sibling rivalry is less deadly than sibling conﬂict
among birds (Mock et al. 1997). Modal litter size among spotted hyenas is two,
and vicious fighting among neonatal litter-mates has been documented by Frank
et al. (1991). These authors suggested that the function of this early sibling
aggression in hyenas is to kill one’s litter-mate. This suggestion has been widely
adopted, and is now presented as fact in various textbooks on animal behavior in
general (e.g. Alcock 2001; Goodenough et al. 2001), books on sibling rivalry in
particular (Mock et al. 1997), and also in a number of ﬁlms and articles in the
popular press (Sherman 1992; Stevens 1993; Slack 1999; McDonald 2001).

Siblicide is considered ‘obligate’ when aggression within a brood or litter is
almost always fatal to subordinates, as is true in many avian species (e.g.
eagles, herons, and egrets: reviewed in Mock et al. 1997). By contrast, in

‘facultative’ siblicide, siblings adjust the intensity of intrabrood aggression as

108

costs and beneﬁts of this aggression vary with current environmental conditions
(Mock et al. 1997). Here inclusive ﬁtness benefits of permitting sibling survival
generally outweigh direct ﬁtness costs of resource competition with siblings
except under environmental conditions so challenging that only a single offspring
has any chance of survival;

Female spotted hyenas give birth to one or two cubs, and rarely three.
Adult female hyenas usually have only two functional teats, so nursing more than
two'cubs concurrently is generally impossible. In the wild, female Crocuta bear
their litters in isolated natal dens or burrows (East et al. 1989) and transfer them
to the clan’s communal den when the cubs reach 2 to 4 weeks of age. Thesmall
diameter of both natal and communal den holes prevents adults from entering, so
dens are accessible only to the neonates. Although neonates usually come to
the mouth of the den to nurse, observers may not see them there for several
weeks because they remain hidden in the den entrance whenever the mother lies
there to suckle her young (East et al. 1989).

The difficulty of observing free-living neonatal spotted hyenas has made
direct observation of siblicide impossible in the wild. However, indirect evidence
for obligate siblicide in this species has emerged in the work of Frank et al.
(1991). These workers concluded that 25% of all same-sex hyena cubs born
routinely succumb to fatal sibling aggression. This conclusion was based on
three lines of indirect evidence. First, neonatal spotted hyenas are precocial and
born with fully erupted incisors and canines. Intense aggression between captive

littermates, involving the use of these weapons and occurring immediately after

109

birth, suggested that this early aggression might function to kill siblings (Frank et
al. 1991). Second, the litter sizes observed by Frank et al. (1991) in the wild
were significantly smaller than those they observed among captive hyenas,
suggesting that litter reduction must occur routinely in the wild. Speciﬁcally,
among litters born to multiparous captive females, the ratio of singletons: twins:
triplets was 1:10:2 at birth, and mean litter size was 2.08 (in 13 litters). By
contrast, the ratio of singletons: twins: triplets was 42:57:0 in the ﬁeld when cubs
were first brought from the natal den to the clan’s communal den at 2-4 weeks of
age, and mean litter size was 1.58 (in 99 litters; Frank et al. 1991). Third, same-
sex twin litters were rare in wild populations when compared to captive
populations. That is, the ratio of same-sex: mixed-sex twin litters was 5:5 in
captivity, but only 5:28 and 1:8 in wild populations in eastern Africa (Frank et al.
1991) and the Kalahari (Mills 1990), respectively. Frank et al. (1991) concluded
that this difference between captive and field observations resulted from selective
loss of cubs in the wild due to habitual siblicide within same-sex litters.
Specifically, they suggested the following: “Siblicide appears to kill nearly 25% of
spotted hyena offspring: at birth, 50% of litters are same-sex, and half of those
individuals succumb” (Frank et al. 1991, page 704). Such a sex-bias in siblicidal
behavior has not been observed or suggested to occur in any other animal
species studied to date.

Smale et al. (1999) found that sex ratios and litter sizes in free-living
Crocuta varied with environmental conditions, and argued that their results

conformed better to a facultative model of siblicide in spotted hyenas than to an

110

obligate model. However, their study could not address the question of why litter
sizes observed by Frank et al. (1991) appeared to differ between captive and
wild hyenas. In order to test the possibility that differences in litter sizes
observed in captive and field settings might be due to differing circumstances
before birth, rather than siblicide after birth, Smale et al. (1999) suggested using
ultrasonography in pregnant hyenas to obtain early estimates of litter size in wild
hyenas, combined with intensive monitoring of behavioral interactions among
den-dwelling cubs as soon as possible after birth. Wahaj and Holekamp (in prep)
adopted the latter suggestion and examined factors inﬂuencing sibling
aggression during the first two months of life in wild spotted hyena cubs. The
primary goal of the current study is to test predictions of obligate and facultative
models of siblicide using ultrasonography and observational data to compare
litter size, sex composition and litter reduction between captive and wild hyenas.
The obligate and facultative models of siblicide generate different suites of
predictions regarding what we should observe as we examine litters in wild and
captive populations of spotted hyenas. First, as noted by Frank et al. (1991), the
obligate model predicts that 25% of offspring die in the wild. However, if siblicide
is facultative, litter reduction should be far less common than the 25% predicted
by the obligate model. Second, Frank et al. (1991) argued that the few same-sex
litters observed in their earlier field work resulted from habitual siblicide within
triplet litters, and that singletons resulted from habitual siblicide within same-sex
twin litters. By contrast, the facultative model predicts that siblicide should only

occur routinely when a mother produces more offspring than she can support.

111

Thus, the facultative model indicates we should be more likely to observe
siblicide in prey-poor than prey-rich environments, and we should observe
siblicide frequently when a female produces a larger number of cubs that her
number of functional teats, such as when females give birth to triplet litters or
when females with only one intact teat give birth to twins. Both of these latter
types of cases are unusual, and in both mortality due to siblicide should occur
irrespective of offspring sex. Third, the sex-bias in the obligate model predicts
that sex ratios in singleton litters and sex compositions of twin litters should differ
from chance expectations due to litter reduction among same-sex twins, whereas
the facultative model predicts that litter reductions should occur within both
same- and mixed-sex litters, and result in offspring sex ratios and litter
compositions that do not differ from chance expectations. Fourth, according to
the obligate siblicide hypothesis, hyena litter sizes in captivity should be larger
than in wild populations since researchers and/or the mother (because she has
access to her cubs) can intervene in captivity to prevent litter reduction via
siblicidal aggression. Othewvise, however, litter sizes and frequencies of litter
reductions should be similar between captive and wild populations. In addition,
the facultative model predicts that intra-litter aggression in the wild should be
more intense during periods of resource scarcity than during periods of resource
abundance, whereas the obligate model predicts no such variation in the
intensity of this aggression. Finally, the obligate model of siblicide predicts that
cubs from mixed-sex litters should have higher survivorship than cubs from

same-sex litters, and that cubs whose same-sex litter-mates survive should have

112

lower survivorship than should cubs whose same-sex siblings die very young.
The facultative model predicts no difference in survivorship between cubs from
same- and mixed-sex litters or between cubs whose litter-mates survive and
those whose siblings die at an early age.

Although our primary goal here was to test predictions of obligate and
facultative models of siblicide in the spotted hyena, we also hoped to use
ultrasonography to inquire about potential mechanisms of litter reduction other
than siblicide, focusing on prenatal mechanisms in particular. Two obvious
possibilities are resorption of embryos in utero and stillbirths. Female spotted
hyenas are unique among mammals in having external genitalia that are highly
masculinized. That is, the clitoris is enlarged to form a fully erectile pseudopenis
and the vaginal labia are fused to form a structure that remarkably resembles the
scrotal sac of the male (Neaves et al. 1980). Because the female hyena gives
birth through her peniform clitoris, complications during the birth process may
result in fetal mortality (Frank et al. 1994; Frank et al. 1995). Females giving
birth for the first time, in particular, may experience unusually high mortality of
their neonates due to dystocia (Frank et al. 1995). Here, although we were
unable to evaluate stillbirths in free-living hyenas, resorptions could be observed
in both wild and captive females, and stillbirths could be evaluated in captive

females.

113

METHODS

Field Study

Field data were collected between July 1988 and May 2004 from one
large social group, or clan, of spotted hyenas inhabiting the Talek region of the
Masai Mara National Reserve, Kenya. Hyena clans contain multiple adult males
and several matrilines of adult female kin with their offspring. Members of both
sexes are capable of breeding at approximately 24 months of age, although most
individuals delay ﬁrst reproduction for several more months (Matthews 1939;
Holekamp et al. 1996). Males disperse from their natal groups after puberty,
whereas females are usually philopatric (Frank 1986; Henschel et al. 1987;.Mills
1990; Smale et al. 1997). Adults can be ranked in a strict linear dominance
hierarchy, with members of the same matriline occupying adjacent rank
positions. Female Crocuta are dominant to immigrant males, and offspring attain
ranks just below those of their mothers (Holekamp et al. 1991; Engh et al. 2000;
Engh et al. 2003). Rank relations, particularly those among females, remain
stable for extended periods and across a variety of contexts (Kruuk 1972; Tilson
et al. 1984; Frank 1986; Smale et al. 1993). An individual’s position in the
group’s hierarchy strongly determines its priority of access to food (Kruuk 1972;
Frank 1986).

Subjects here were members of a Crocuta clan that usually contained 60
to 80 hyenas, and defended a group territory of approximately 65 km’ (Boydston
et al. 2001). All adult members of the study clan were identiﬁed by their unique

spot patterns, and young cubs that had not yet developed spots were identified

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by unique scarring, bald patches, ear notches, size differences, molt patterns, or
a combination of these features. Sex was determined from the dimorphic glans
morphology of the erect phallus (Frank et al. 1990). By two months of age, the
glans of the male’s phallus assumes a distinctly different shape from that of the
female (Drea et al. 1998). That is, the male’s phallus is pointed at its tip and has
a constriction above the glans whereas the female’s pseudopenis is blunt at the
tip and lacks a constriction. Cubs regularly develop erections during greeting
ceremonies, which occur virtually every time a new hyena arrives at the den.
Young hyenas were sexed here repeatedly by multiple independent observers,
and sex could be assigned with complete certainty by the time cubs were 2-3
months old. However, on several occasions, cubs died before they could be
sexed. A disappearance date for each cub was assigned as the date on which it
was last seen if it did not survive to adulthood.

Spotted hyenas breed throughout the year with the gestation period
lasting 110 days (Schneider 1926; Kruuk 1972). We estimated cub birth dates
(to 1 7 days) by using their pelage, size, and other aspects of their appearance
and behavior when cubs were first observed above ground (Holekamp et al.
1996). We assigned the date on which a cub was first seen above ground as its
‘date first seen’, although it’s actual date of birth might have been several weeks
earlier.

Mother-offspring relations were established on the basis of regular nursing
associations. Females that had given birth at least once (multiparous females)

could be distinguished from nulliparous females (who had never previously given

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birth) based on the presence of pink scar tissue on the posterior surface of the
erect phallus (Frank et al. 1994). This scarring results from tearing of the phallus
at ﬁrst parturition, and it remains visible throughout the lifetime of the animal.
Social ranks were determined based on wins and losses in dyadic agonistic
interactions. Outcomes of these interactions were organized into a matrix from
which each female hyena could be assigned a social rank in the clan's
dominance hierarchy (Martin et al. 1988).

Since very little is known about the length or timing of the estrous cycle in
female spotted hyenas, and since pregnancy cannot be identiﬁed through
assessment of the female’s physical state in this species, we relied on the abrupt
cessation of male courtship behavior to provide behavioral indicators as to when
females became pregnant. That is, females were usually followed by an
entourage of adult males for some weeks before estrus, but this entourage
abruptly disappeared when a female conceived (Szykman 2001). Once a female
was considered pregnant, she was immobilized with an intramuscular injection of
Telazol (6.5mg/kg) delivered from a COz-powered rifle in a lightweight plastic
syringe. When anaesthetized, females underwent a transabdominal ultrasound
using a real-time HITACHI EUB-405 scanner with a 5 MHz curved-array
transducer. Animals were scanned while lying on their backs in the supine
position after we removed their fur from the lower abdomen with electric clippers.
Ultrasound data were collected in the field from August 1999 through May 2004.
Multiple ultrasounds within a single pregnancy were not possible in wild hyenas

due to both the difficulty of darting any particular female repeatedly within a

116

narrow window of time, and our reluctance to stress pregnant females with
multiple dartings.

Fetuses and their heartbeats were identified using methods described by
Place et al. (2002). Brieﬂy, using the bladder as a landmark, we located the
bifurcation of the uterine body and followed each of the two horns anteriorly to
search for the presence of fetuses. Fetuses were recognized during early
pregnancy by the presence of a gestational sac within a thickened endometrial
cavity (Figure 5.1a). Fetal cardiac activity can be clearly discerned as a rapid
fluttering within the fetus as early as 24 days post-mating (M. Weldele and N.
Place — pers. communication). Thirty days after mating, development of spine,
cranium, and long bones begin, and skeletal elements can be easily discerned
on sonographic images (Figure 5.1 b). Circumference of the gestational sac (in
young fetuses) and fetal femur lengths (in older fetuses) were measured to
estimate gestational age (Place et al. 2002), which later allowed us to intensify
monitoring of pregnant females during a narrow window of time around the
expected date of parturition. All immobilized females were radio collared
(Telonics lnc., Mesa, AZ) and tracked daily to facilitate discovery and observation
of neonatal cubs. Two different sets of litter size data from wild female hyenas
are reported in this chapter: a) the subset of female hyenas that were examined
via ultrasonography, and b) all female hyenas, including those with litters that
were and were not observed in utero with ultrasound.

Detailed demographic records for the Talek hyena clan were collected

throughout the study period and have been maintained since early 1988.

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Demographic data were used to calculate survivorship tables during the first two
years of life for individuals in a) litters of varying size, b) twin litters of varying sex
compositions and 0) twin litters in which one sibling died before three months of
age compared to those in which both siblings lived at least three months. Data

for survivorship tables were not censored.

Captive Study

Pregnant spotted hyenas were studied at the Field Station for the Study of
Behavior, Ecology, and Reproduction at the University of California, Berkeley
from October 1987 through March 2003. A description of the Berkeley hyena
colony is presented in Frank et al. (1989) and captive husbandry is described in
Berger et al. (1992). Pregnancies in captivity were monitored by transabdominal
ultrasonography using a real-time Aloka SSD-500 scanner with a 5 MHz curved-
array transducer. Prior to each examination, animals were immobilized with an
intramuscular injection of Ketaset (4 — 6 mg/kg) and xylazine (1 mg/kg)
administered via blow-dart. Detection of fetuses was as in ﬁeld studies, although
captive hyenas often undenrvent multiple (mean = 1.96 1 0.15) ultrasounds per
pregnancy, whereas wild hyenas underwent only one. For cases in which more
than one ultrasound was conducted during a particular captive pregnancy, but
the number of fetuses observed varied among examinations, the ultrasound
showing the greatest number of fetuses was used in calculating litter size in
utero. Exact dates on which conception occurred were often known for captive

females because mating usually occurred in the presence of human observers.

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In addition, gestational age could straightforwardly be estimated based on femur
length measurements made on fetuses via ultrasonography (Place et al. 2002).
Staff members are almost always present during captive births to aid or intervene
in the event of birth complications. Therefore, in contrast to the situation in the
field study, neonatal litter sizes presented for captive hyenas were true litter sizes
at birth as there was no time or opportunity for mortality to reduce litters after
parturition. Captive mothers give birth in pens (2 X 2 m) with straw bedding and
a plastic 200-litre barrel. Mothers are accessible to the infants 24 h a day, which
is not the case in nature. Although severe fighting between sibling neonates has
been observed in captivity, siblicide has never been observed there because
cubs are always separated before they can inﬂict mortal injury on one another.
Long-term goals of the Berkeley hyena project include experimental
treatments of pregnant spotted hyenas with anti-androgens and letrazole (an
aromatase inhibitor) as well as performing fetectomies (early caesarian sections)
to study development of the external genitalia. Females born to mothers that had
been treated with anti-androgens were not considered at all in our dataset. In
order to determine which captive pregnancies should be included in our
comparisons with those in wild hyenas, we compared litter size at birth in
multiparous females that had never received any sort of treatment (n = 12) with
litter size at birth from each of the following groups: females who were
themselves treated during pregnancy with anti-androgens or letrozole (n = 12),
females that had previously had a fetectomy performed on them during an earlier

pregnancy (n = 13), and females on which an amniocentesis procedure was

119

performed during the current pregnancy (n = 5). Mean litter size in all but the last
of these groups was significantly smaller than in untreated females (F3, 39 = 3.6, P
= 0.04, followed by Tukey’s posthoc pain/vise comparisons), so all these other
treatment groups were excluded from all further analyses. Together, females
receiving no treatment and females on which amniocentesis was performed were

referred to as “untreated" captive females, and their litters comprised our dataset.

Terminology

The number of fetuses observed “in utero” refers to the number of fetuses
detected via ultrasonography during pregnancy in both captive and wild hyenas.
The term “neonatal” refers to the post-partum number of neonates in captivity,
but in the wild this term refers to the number of cubs present when a litter was
first seen above ground. In both cases, “neonatal” litter size indicates the
number of cubs observed alive as soon after parturition as possible. Resorptions
of fetuses were detected when either a second ultrasound during a particular
pregnancy confirmed a reduction in the number of fetuses in utero (captive study
only) or a second or third trimester fetus lacked a heartbeat (both captive and
wild studies). Stillbirths could only be positively identified in captive hyenas,
because sources of early mortality are difficult to identify in the field. In both wild
and captive studies, “litter reduction” was defined as a decrease in litter size from
the number of fetuses observed in utero to the number of living “neonatal” cubs

observed.

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Data Analysis

Results are reported for both primiparous and multiparous females.
However, to make our results comparable to those of Frank et al. (1991), in some
analyses we limited our dataset to only multiparous females. Sample sizes of
litters observed in utero and those observed as neonates sometimes differed in
the wild because some ultrasounded females kept their litters so well hidden that
we never had opportunities to. observe these cubs as neonates. In addition,
some captive litters were born to females that were never ultrasounded.
Independent sample t-tests were used to compare litter sizes between captive
and wild populations, and between primiparous and multiparous females. Chi-
square tests were used to compare litter compositions, and these were adjusted
for small sample sizes as necessary using Yate’s correction. Litter reductions
were assessed by matched comparison of number of fetuses observed in utero
to the number of cubs observed alive at the end of the same pregnancy either at
parturition (captivity) or when cubs ﬁrst emerged above ground (ﬁeld study) at
approximately six weeks of age (mean = 42.9 1 6.8 days, n = 27 cubs in the
wild). For these matched comparisons we used dependent sample t-tests. We
used a Spearman’s Rank correlation to assess the relationship between mean
litter sizes born to females in the wild and the social ranks of those females. A
one-way ANOVA was used to determine whether litter size varied with age at
which litters were first seen above ground. Binomial tests were used to

determine whether observed sex ratios differed from those based on chance

121

expectations. In survivorship analyses, proportions of individuals surviving were
compared among multiple groups using a multiple-sample test, in which a score
was assigned to each survival time using Mantel's procedure (Mantel 1967), and
then a Chi-square value was computed based on the sum of these scores for
each group. Cox’s F tests were used in survivorship analyses to compare
survival between only two groups. Despite small sample sizes and low statistical
power, differences between groups were considered significant when P 5 0.05.
Throughout the paper, means (1 se) are reported. All statistical tests were two-

tailed and performed using Statistica 6.1 software.

RESULTS

Sample Sizes

Field Studv: Twenty-two females were immobilized and ultrasounded
during pregnancy in the wild, including 2 primiparous and 20 multiparous
females. For 18 of these 22 females, we were able to observe their litters above
ground within the first few weeks of life, but four ultrasounded females
maintained their litters for extended periods in dense thickets or otherwise made
it impossible for us to observe their cubs as neonates. Of the 18 observable
females, 2 were primiparous and 16 were multiparous. In the larger sample of all
wild females for which litter size was known (including both those who were
ultrasounded and those who were not), we had 241 litters, of which 44 were from
primiparous females and 192 from multiparous females. For mothers of ﬁve of

these 241 litters, parity was not known.

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Captive Study: Twenty-seven “untreated” females were immobilized and
ultrasounded during pregnancy, including 11 primiparous and 16 multiparous
captive females. Thirty-two litters were born in the captive colony, but mothers of
five of these litters were not ultrasounded prior to birth. Of these 32 captive

litters, 15 were born to primiparous females and 17 to multiparous females.

Litter Composition and Litter Size
Litter composition in utero did not differ overall between captive and wild

hyenas (Figure 5.2; Yate's x 2 = 0.265, d.f. = 2, P > 0.8), nor did it differ when we

compared only captive and wild hyenas that had been examined during
pregnancy with ultrasonography (Figure 5.2; Yate’s X 2 = 0.884, d.f. = 2, P S 0.5).
When we compared the ratios of singleton: twin: triplet litters at birth between
untreated captive females (litter composition at birth was 11:1 1 :3) and our larger
sample of all wild hyenas (litter composition at emergence was 123:126:2), we

found a signiﬁcant difference between these litter compositions (Yate’s x 2 =

11.78, d.f. = 2, P < 0.01 ). However, when triplet litters were eliminated from the
neonatal dataset, we found no difference between captive and wild hyenas with
respect to the proportions of singletons and twin litters observed (Yate’s X 2 =
0.03, d.f. = 1, P > 0.98). These data suggest that perhaps captive hyenas have
disproportionately large numbers of triplet litters compared to wild hyenas. We
observed no difference in composition between litters observed in utero and

those observed again later as neonates in either captive (Figure 5.2a; Yate’s X 2

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= 1.84, d.f. = 2, P > 0.30) or wild hyenas (Figure 5.2b; Yate’s x 2 = 0.39, d.f. = 2,

P > 0.80).

Considering both primiparous and multiparous females together that were
examined via ultrasonography, we found no difference between captive and wild
hyenas in mean size of litters in utero (captive: n = 27, mean = 1.93 1 0.12; wild:
n = 22, mean = 1.91 1 0.11; t = 0.102, P = 0.92), or in mean size of neonatal
litters (captive: n = 32, mean = 1.31 1 0.16; wild: n = 18, mean = 1.50 1 0.20; t = -
0.702, P = 0.49). In order to fairly compare neonatal litter size between captive
and wild hyenas that were never examined via ultrasonography, we limited the
dataset of captive hyenas to only those 25 cases in which litter size was greater
than zero (i.e., cases were excluded in which ultrasonography indicated
occurrence of stillbirths or resorptions such that no cubs were born alive) since
litters in which all cubs are stillborn cannot be detected in wild litters not observed
with ultrasound. Mean neonatal litter size in captive females here did not differ
significantly from that observed in the larger sample of all wild females (captive: n
= 25, mean ‘= 1.68 1 0.14; wild: n = 251, mean = 1.52 1 0.03; t = 1.34, P = 0.18).
Mean neonatal litter size also did not differ between wild females that were
ultrasounded and wild females that were not ultrasounded (wild ultrasounded
litters: n = 18, mean = 1.50 1 0.20; all wild litters: n = 241, mean = 1.52 1 0.03; t
= 0.09, P = 0.92). Since the age at which cubs are ﬁrst observed differs between
captive and wild hyenas, we also compared mean neonatal litter size born to the
25 captive hyenas with that observed in a subset of 25 wild hyenas whose cubs

were seen soonest after birth (i.e., the earliest dates first seen), but we found no

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difference (mean age ﬁrst seen in the wild for this subset was 4.12 1 0.52 days,

mean litter size for both wild and captive populations was 1.68, t = 0.0, P = 1.0).

Litter Composition and Litter Size among Multiparous Females

We next restricted our analyses only to multiparous females to compare
our findings with those reported by Frank et al. (1991). Here again we found no
difference in litter composition between captive and wild hyenas either in utero
(captive litter composition = 2:1 1 :3, wild litter composition = 2:16:2; Yate’s x 2 =
0.185, d.f. = 2, P > 0.9) or among neonates (captive litter composition = 4:8:3,
wild litter composition = 2:10:1; Yate’s x 2 = 0.60, d.f. = 2, P > 0.7). When only
multiparous females were considered, litter composition differed between
captives and our larger sample of all wild hyenas (captive litter composition =
4:8:3, wild litter composition = 87210312; Yate’s x 2 = 16.93, d.f. = 1, P < 0.001),
but again this difference vanished when triplets were excluded from the dataset

(Yate’s X 2 = 0.29, d.f. = 2, P > 0.8). We found no difference in litter composition

between uterine and neonatal observations of multiparous females either in
captivity (Yate’s x 2 = 0.57, d.f. = 2, P > 0.70) or in the wild (Yate’s x 2 = 0.31, d.f.
= 2, P > 0.80).

Among ultrasounded females, we also failed to find any significant
difference between captive and wild hyenas in mean litter sizes observed either
in utero (captive: n = 16, mean = 2.06 1 0.13; wild: n = 20, mean = 2.00 1 0.10; t
= 0.36, P = 0.72) or as neonates (captive: n = 17, mean = 1.61 1 0.23; wild: n =

16, mean = 1.5 1 0.22; t = 0.45, P = 0.65). Thus, our results here differed from

125

those obtained earlier by Frank et al. (1991). However, when we compared
multiparous captive females with our larger sample of wild multiparous females
that were not ultrasounded, we found neonatal litter size to be significantly larger
in captivity than in the wild (Table 5.1; t =2-2.63, P = 0.009). Thus, these results

were the same as those reported earlier by Frank et al. (1991).

Litter Reduction

Significantly more fetuses were observed in utero than as neonates
among captive females (Figure 5.3; t = 2.8, n = 27, P = 0.01). Speciﬁcally, nine
of 27 litters were reduced in captive females. Among captive multiparous .
females, five of 16 litters were reduced, and here again we observed signiﬁcantly
more fetuses in utero than living neonates (t = 2.41, n = 16 pairs, P = 0.03).
Thus, roughly one third of captive litters were reduced, and none of those
reductions were due to siblicide.

When we compared the number of fetuses observed in utero in the wild to
the number of cubs in litters observed later as neonates, we found that ﬁve of 18
litters were reduced. Because siblicide could not account for reductions in either
singleton litters or in litters from which all cubs disappeared, only two of the five
cases of litter reduction we observed in ultrasounded wild hyenas could have
possibly been attributable to siblicide. In both of these cases, twin litters in utero
appeared above ground as singletons. Thus, as in captivity, we found that
significantly more fetuses were observed in utero than as neonates in the wild

(Figure 5.3; t = 2.36, n = 18, P = 0.03). Although siblicide is not permitted in

126

captivity, the proportion of litters in which litter reduction occurred did not differ

between captive and wild hyenas (Yate’s x ’- = 0.004, d.f. = 1, P > 0.95). Among

wild multiparous females, ﬁve of 18 litters were reduced and more fetuses were

observed than neonates within pregnancies (t = 2.41, n = 16 pairs, P = 0.03).

Possible Causes of Litter Reduction

In captivity, 80% of litter reductions were due to stillbirths and 20% were
due to resorptions. Of 32 captive pregnancies, 9 (28%) produced at least one
stillborn cub, and fetal resorptions occurred in 2 (6.3%) of the 32 pregnancies.

In wild spotted hyenas, litter reductions might have been due to stillbirths,
resorptions, predation, disease, infanticide or siblicide. Although it was
impossible for us to detect stillbirths in nature, we did observe one fetus being
resorbed in a wild female. There was substantial variation in the age at which
cubs were first observed above ground, and the longer it took us to see wild
litters, the smaller they tended to be (Figure 5.4; F2, 215 = 3.18, P = 0.04).
Singleton litters were first observed above ground substantially later than twin
(LSD post-hoc test, P = 0.04) or triplet litters, though the small sample of triplet
litters failed to yield signiﬁcant differences in age at first sighting from those of
smaller litters (LSD post-hoc test, P = 0.09 for singleton vs. triplet and P = 0.19
for twin vs. triplet).

In our large sample of wild females, we observed 32 cases of litter
reduction from twin to singleton litters in 102 twin litters and half of these 32

cases occurred before the first three months of life. Six of these reductions were

127

most likely due to siblicide. For example, each of two adult females in our study
population sustained severe damage to one of her teats during fights, leaving
only one functional teat intact. Each time either of these females produced twins
(three times for each female), the subordinate cub was viciously attacked by the
dominant whenever it attempted to nurse. These subordinate cubs exhibited
many wounds and scars, grew far more slowly than their dominant siblings and
inevitably disappeared within the first few months of life (mean age at death for
these six cubs was 118.4 1 39.8 days). In both triplet litters born in the wild, the
third-ranking cub disappeared at a very young age (at 4 and 29 days after birth,

respectively), after being severely attacked by both its dominant litter-mates.

Effects of Maternal Parity and Social Rank

In captivity, litter size in utero did not vary signiﬁcantly with parity (t =
1.50, P = 0.15), but neonatal litter sizes were larger among multiparous females
than among primiparous females (Figure 5.5; t = 2.48, P = 0.02). Among
primiparous females in captivity, seven of 15 pregnancies produced stillborn
cubs. Among captive multiparous females, 2 stillbirths and 2 resorptions were
observed in 17 pregnancies. Although primiparous females tended to have more
stillbirths and resorptions than multiparous females, this difference was not

significant among captive females (Yate’s x 2 = 1.0, d.f. = 1, P > 0.7).

Only two primiparous females were ultrasounded in the wild and each
contained only one fetus in utero, whereas mean litter size in utero for

multiparous females was 2.0 1 0.10 (n = 20 females). Among ultrasounded wild

128

hyenas, these same two primiparous females had neonatal litter sizes of only
one cub while mean neonatal litter size from multiparous females was 1.92 1
0.14 (n = 13 females). Because only two primiparous females were ultrasounded
in the wild, it was impossible to use statistical tests to fairly compare mean litter
size in utero between primiparous females in the wild and captivity. However,
among our larger sample of 236 wild hyenas, we observed no signiﬁcant
difference in neonatal litter sizes between primiparous and multiparous females
(Figure 5.5; t = 1.46, P = 0.147). Thus, it appears that litter sizes in the two wild
primiparous females in which we observed singletons fetuses in utero were not
representative of litter sizes in other primiparous females in the natural habitat.
We found no relationship between mean litter size and maternal social rank
among our large sample of wild female hyenas (E23219 = 0.65, Spearman rs =

0.033, n = 24 ranks, P = 0.875).

Sex Ratios

We observed no significant difference between proportion of male and
female cubs produced in all litters considered together, in singletons considered
alone, or in twin litters considered alone among either captive or wild hyenas
(Table 5.2). The ratio of all-male:mixed-sexzaIl-female twin litters born in captivity

was 325:4 and this did not differ from chance expectations (Yate’s X 2 = 0.21, d.f.

= 1, P > 0.5). Similarly, ratios in twin litters born to wild hyenas did not differ from

chance expectations (Figure 5.6a; Yate’s x 2 = 0.95, d.f. = 1, P > 0.5), nor did

129

they differ from these ratios observed in captive hyenas (Yate's x 2 = 0.55, d.f. =

2, P > 0.7).
Within 33 twin litters born to multiparous females, Frank et al. (1991)
observed a ratio of 422821 (all-male:mixed-sexzall-female), which differed

signiﬁcantly from chance expectations (Yate’s x 2 = 14.56, d.f. = 1, P < 0.001).

Among multiparous females from the current study, we observed a ratio of

17:43:22 at emergence, which did not differ from chance expectations (Yate's x 2

= 0.54, d.f. = 1, P > 0.3), but was signiﬁcantly different from the ratio observed by

Frank et al. (1991) (Figure 5.6b; Yate’s x 2 = 9.56, d.f. = 2, P < 0.01).

Survivorship Among Wild Hyena Cubs

Among wild hyenas, we observed significant differences in the proportion
of individuals surviving to reproductive maturity (24 mo. of age) among 112
singleton cubs, 208 cubs from twin litters, and 6 cubs from triplet litters (Figure

5.73; X 2 = 13.34, d.f. = 3, P = 0.001). Cubs from twin litters experienced higher

survivorship than those from singleton (Cox’s F224_ 415 = 1.29, P = 0.01) or triplet
litters (Cox’s F12. 415 = 7.33, P < 0.001), and cubs born as singletons also
survived better than did cubs from triplet litters (Cox’s F224, 12 = 4.10, P = 0.009).
Of 146 cubs from twin litters in which the sex of both siblings could be
determined, we found no significant variation in survivorship among individuals
from all-female, mixed-sex, and all-male litters (Figure 5.7b; n = 26 cubs from all-

female litters, 84 cubs from mixed-sex litters, 36 cubs from all-male litters; x 2 =

1.59, d.f. = 3, P = 0.45). Within twin litters, individuals experienced better

130

survivorship when their siblings survived to at least three months of age than
when their siblings disappeared before three months of age (Figure 5.7c; n = 142
individuals whose siblings survived longer than 3 months, n = 32 individuals
'whose siblings disappeared before 3 months of age, Cox’s F284. 64 = 2.11, P <
0.001). These data strongly suggest habitual siblicide would be maladaptive in

these animals.

DISCUSSION

Several lines of evidence presented here are inconsistent with predictions
of the obligate siblicide hypothesis. First, possible siblicide in the wild could
account at most for reduction of cub number in only 2 of 18 (11.1%) ultrasounded
litters. This is considerably less than the 25% predicted by the obligate siblicide
model, especially considering that 37% of litters in captivity were reduced strictly
due to stillbirths and resorptions. We observed resorption in one of 18 wild
litters, which is the same proportion (6%) as that observed among captive litters
(2 of 32). Stillbirths occurred in 28% of 30 captive litters. If rates of stillbirth were
similar in captivity and the wild, we would have expected reductions due to
stillbirths in five of 17 wild litters. In fact, four wild litters were smaller when
observed as neonates above ground than when observed in utero. Thus, if
indeed rates at which stillbirths occur are roughly the same in the wild and in
captivity, then further litter reduction due to siblicide must be extremely rare in

our wild population at the present time.

131

Second, frequency of litter reductions in captivity, where siblicide could not
occur, did not differ from that in our wild study population. Third, habitual
siblicide did not reduce triplets to same-sex twins as suggested by Frank et al.
(1991), since all members of both wild triplet litters observed here died before
five months of age. Fourth, the lack of sex bias in compositions of twin or
singleton litters in either the wild or captivity suggests that litter reductions here
were not occurring exclusively within same-sex litters in the wild. In addition,
probability of survival among members of twin litters did not vary with sex
composition of these litters. Finally, habitual siblicide could not be adaptive in
spotted hyenas since, not only did cubs from twin litters experience better ‘
survivorship than those from singleton or triplet litters, but also twins whose
siblings died early experienced signiﬁcantly worse survivorship than did those
whose siblings survived for at least three months. These results unambiguously
contradict predictions of the obligate siblicide hypothesis.

On the other hand, a large body of evidence now exists that facultative
siblicide does occur among free-living spotted hyenas. Hofer and East (1997)
inferred that facultative siblicide might be occurring in all-female twin litters based
on occurrence of significantly fewer all-female litters than expected by chance,
and a female bias within singleton litters. Golla et al. (1999) found support for the
facultative siblicide hypothesis by demonstrating that rates of aggression
between litter-mates increased as maternal rank and cub growth rates
decreased. Similarly, Smale et al. (1995) observed that rates of aggression

within twin litters increased as maternal rank decreased. Smale et al. (1999)

132

found that offspring sex ratios varied as environmental conditions changed over a
10 year study period, but that mean litter size remained constant, a result
consistent with the facultative model of siblicide. Most recently, Wahaj and
Holekamp (in prep) observed that sibling aggression increased as local prey
abundance declined. Thus, several lines of evidence from a number of different
researchers indicate that siblicide may occur facultatively within hyena litters.

We agree with the assertion made by Frank et al. (1991).that fighting
between neonatal litter-mates is unusually intense in spotted hyenas relative to
sibling fighting observed in most other mammals. However, we disagree with
Frank et al. (1991) regarding the function of this early aggression. Whereas
Frank et al. (1991) argued that neonatal ﬁghting functions to kill siblings within
same-sex litters, we agree with the alternative suggestion put forward by Smale
et al. (1995), that the function of neonatal ﬁghting is simply to establish a rank
relationship between litter-mates. Once this rank relationship has been
established, there is little need for further aggression unless the mother simply
cannot support all the cubs to which she has given birth, as frequently occurs in
triplet litters. Even in captivity, medical treatment of sibling-inﬂicted wounds was
only required for members of triplet litters (Frank et al. 1991).

Frank et al. (1991) observed larger neonatal litters among multiparous
captive females than litter sizes at emergence in wild Crocuta. Data from the
current study replicate that earlier result. However, litters were ﬁrst observed on
the day of birth in captivity in both the current study and that of Frank et al.

(1991), and some weeks after birth in the wild, where mortality might have

133

occurred that was due to a number of sources other than siblicide. We found
here that the longer it took us to ﬁrst observe litters in the wild, the Iikelier it was
that we would observe singletons. We saw triplet litters unusually early in life
because these cubs were typically so hungry that, even at very young ages, they
followed their mothers some meters away from den holes as they attempted to
continue nursing. Siblicide did appear to reduce triplet litters, and litters born to
mothers possessing only one functional teat. But aside from these cases, we
have no more reason to believe cub disappearances were due to siblicide than to
predation, disease or a number of other mortality sources.

Between 1979 and 1984, Frank et al. (1991) observed four cases of early
litter reduction due to siblicide in the ﬁeld, from twins to singletons. Between
1988 and 2003, we observed 32 cases in which cubs originally seen as twins
were reduced to singletons within the ﬁrst three months of life. In addition, all
triplet litters we observed in the field died early. Among ultrasounded wild
hyenas, 28% of litters observed in utero were reduced. In captivity, 33% of litters
observed in utero were reduced by the end of the parturition process. Thus, litter
reduction occurs commonly in both captive and wild hyenas. In captivity,
siblicide cannot account for any litter reduction at all, and it also appears that
very few cases of litter reduction could be attributed to siblicide in our wild study
population during the current study period. Birth complications, especially among
primiparous spotted hyenas, appear to be a common cause of litter reduction
(Frank et al. 1995). In a zoo in Amsterdam, 35% (18 of 51) of cubs were stillborn

or died immediately after birth from cases other than siblicide (Kranendonk et al.

134

1982). In the captive Berkeley colony, Frank et al. (1995) reported that eleven of
18 neonates (61%) born to primiparous females were stillborn and four of 11
(36.4%) primiparous females experienced dystocia (difﬁcult parturition), whereas
only two of 30 (7%) multiparous females had stillbirths. In another study, ﬁve of
eight (63%) primiparous female Crocuta experienced birth complications (Frank
et al. 1994). In addition to giving birth through a narrow penile clitoris, female
spotted hyenas possess abnormally long birth canals and fetuses have short
umbilical cords, so infants not born immediately after placental detachment will
die of anoxia in the birth canal (Frank et al. 1995). This risk of oxygen
deprivation appears to be greater in primiparous females where labour takes
longer since the clitoris must stretch for the ﬁrst time to accommodate the fetus
(Frank et al. 1994). Thus, litter reductions appear to be caused more commonly
by dystocia than by siblicide in Crocuta, especially among primiparous females.
We failed to observe parity inﬂuencing litter sizes among our larger sample of
wild females and perhaps this was because other sources of mortality in the wild
(such as predation and disease) were diluting any effects of parity.

Frank et al. (1991, page 704) claimed a “marked difference in survival
[occurred] between same- and mixed-sex litters,” whereas our survival analysis
showed that mixed-sex litters survive no better than same-sex litters of either
type. Frank et al. (1991) clearly observed a bias towards mixed-sex twin litters,
and they attributed this finding to obligate siblicide within same-sex litters. If
siblicide is truly sex-biased and independent of local environmental conditions,

than sex composition of twin litters in hyena populations should deviate from

135

binomial expectations, yielding an overabundance of mixed-sex litters and too
few same-sex litters. However, our long-term study failed to ﬁnd a sex bias in
twin litters, and our ratios of the various types of twin litters differed signiﬁcantly
from those reported by Frank et al. (1991). Secondary sex ratios in Crocuta can
apparently be adjusted according to ecological conditions (Holekamp et al. 1995;
Smale et al. 1999). Studies conducted in areas where hyenas are challenged by
relatively low prey abundance, have found a bias towards production of mixed-
sex twins (Mills 1990; Hofer et al. 1997). By contrast, siblicide and sex biases
within twin litters were absent in spotted hyenas from Ngorongoro Crater, an area
characterized by year-round abundant prey (Wachter et al. 2002). Thus, one
hypothesis to account for the difference in composition in twin litters between the
current study and that of Frank et al. (1991) is that perhaps a combination of low
prey availability and large clan size accounted for the bias towards mixed-sex
twin litters during the study period of Frank el al. (1991). Whereas clan size
hovered around the local carrying capacity throughout the study period of Frank
et al. (1991), clan size was well below carrying capacity just as often as it was at
or above carrying capacity during our own extended study period in the same
population (Boydston 2000). On the other hand, as S. E. Glickman (pers.
comm.) has pointed out, although physiological mechanisms are known by which
offspring sex ratios can be biased either towards males or towards females (e.g.
alteration of vaginal PH, etc.), no mechanism is currently known by which adult
females might increase the probability of producing mixed-sex twins. Unless a

female Crocuta can separately adjust conditions within the two horns of her

136

bicornuate uterus to promote the occurrence of mixed-sex twins, it remains
possible that the peculiar sex compositions in twin litters observed in Frank et al.
(1991) were caused by frequent occurrence of facultative siblicide within same-
sex litters during their earlier study period.

The intensive fighting that occurs between neonatal spotted hyena siblings
has received a great deal of attention from the media, and the lay public now
generally believe that hyena cubs routinely behave like Cain and Abel. This view
adversely affects our ability to protect these and other members of the family
Hyaenidae (East et al. 1998). Our data convincingly show that the normal
function of early sibling aggression in this species cannot be to kill one’s litter-
mate. We therefore hope our data will change public attitudes towards these

much maligned animals, and facilitate their conservation.

137

 

 

 

 

 

 

Population Mean Litter Size 1 se N
Frank et al. (1991) - captive 2.081 0.14 13
Frank et al. Q991L- ﬁeld 1.58 1 0.05 99
This study - captive 1.93 1 0.18 15
This study - ﬁeld 1.56 1 0.04 192

 

 

Table 5.1. Neonatal litter sizes born to multiparous females that were directly
observed in Chapter 5 compared to those observed earlier by Frank et al. (1991),
who used only multiparous females in their analysis. “N” indicates the number of
litters born.

 

 

 

 

 

Population # Males # Females N P (binomial test)
Wild (overall) 140 128 268 0.25
Captive (overall) 21 20 41 0.50
Wild (in singleton litters) 38 43 81 0.66
Captive (in singleton litters) 5 4 9 0.50
Wild (in twin litters) 89 97 186 0.61
Captive (in twin litters) 11 13 24 0.42

 

Table 5.2. Sex ratios among litters born to wild and captive hyenas.

138

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Figure 5.1. Sonographic images of a) early pregnancy (gestational age here was
43 days) indicated by the presence of a gestational sac and thickened
endometrial cavity. The gray donut-shaped outer circle is the endometrial wall of
the uterine horn and the dark hypoechoic center represents the amniotic ﬂuid and
the developing fetus, b) late pregnancy (gestational age here was 97 days)
indicated by skeletal development as well as an observable heartbeat. The
vertebrae and ribs of the fetus are indicated by the hyperechoic white bands
across the screen. The arrow points to the fluttering cardiac region.

139

a) 1 00%
90%
30%
70%

50%
40%
30%
20%
1 0%

0%

Percent of litters

b) 100%
90%
80%
70%
60%
50%
40%
30%
20%
1 0%

0%

Percent of litters

 

.1»... I

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11

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twins

 

I in utero i
D neonatal 1

 

 

triplets

Litter composition In captive hyenas

 

 

 

 

singletons

 

twins
Litter composition In wild hyenas

 

lin utero ;

D neonatal 1

 

 

triplets

Figure 5.2. Percent of all litters that contained one, two or three cubs when
observed in utero and again as neonates in a) captive and b) wild hyenas
examined during pregnancy with ultrasonography. Numbers above bars
represent numbers of litters of each type.

140

3.0 -

- in utero

. neonatal

2.5 ~

2.0 -

 

Litter Size

 

 

0.5 ~

 

 

 

0.0

 

captive

Figure 5.3. Matched pairs comparisons within pregnancies of litter size before
and after birth in captive and wild hyena populations. Numbers above bars
represent numbers of pregnant females examined via ultrasonography.
Significant differences are indicated with asterisks.

141

50»

 

 

 

 

 

101 *

4° ' 116
E 30 t
C
a)
o
In
E
I:
o
O)
< 20 .

10 ~

0 L

singleton twin triplet
Litter size

Figure 5.4. Mean age at which cubs were observed above ground in wild litters
for which we had an opportunity to see cubs. Numbers above bars represent
litters in each group. Signiﬁcant differences are noted with an asterisk.

142

 

 

 

 

 

 

 

 

 

 

 

multiparous

Figure 5.5. Mean litter sizes before and after birth compared between
primiparous and multiparous hyenas in captivity and in the wild. Neonatal litter
sizes are reported for both ultrasounded and non-ultrasounded hyenas.
Numbers above bars represent litters in each group. Signiﬁcant differences are
indicated with asterisks.

143

a) 100% 1
90% J
80% -
70% a
60%
50%
40% 1
30%
20%
10% 1
0%

 

I observed
0 expected

 

 

 

19 23.25

Percent of twin litters

 

 

 

 

 

 

male-male male-female female-female

Sex composition

b)

100% A;
90%
80%
70%
60% .
50%
40%
30% ;
20% ‘
10%
0%

 

I Frank et al. (1991);
D Current study

 

 

22

 

Percent of twin litters

 

 

 

 

 

male-male male-female female-female

Sex composition

Figure 5.6. Percent of wild twin litters of each type born to a) both multiparous
and primiparous females in the current study compared to expectations based on
a binomial distribution and b) multiparous females from the current study
compared to those monitored by Frank et al. (1991). Sample sizes above bars
represent number of litters of each type observed.

144

Figure 5.7. Survivorship of a) 112 singleton cubs, 208 cubs from twin litters, and
6 cubs from triplet litters; b) 26 cubs from all-female litters, 84 cubs from mixed-
sex litters, and 36 cubs from all-male litters, and c) 142 individuals from twin
litters whose litter-mate lived longer than 3 months and 32 individuals whose twin
died before 3 months of age.

145

a)

1.200 1

Survivorship (Lx)

1.000 ~ 3
0.800 4 '
0.600 -
0.400 —,

 

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—-a——-Twins 1

...... Triplets j

 

 

 

 

0.200 1

0.000%.4‘ .91..

Survivorship (Lx)

Survivorship (Lx)

 

 

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.600 1
0 + Sib lived > 3mos

 

 

 

 

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Age (months)

146

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