Behavioral Ecology Vol. 12 No. 5: 558-568
© 2001 International Society for Behavioral Ecology
Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females
a Institute of Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315 Berlin, Germany b Max-Planck-Institut für Verhaltensphysiologie, Postfach 1564, D-82305 Seewiesen, Germany
Address correspondence to M.L. East at the Institute of Zoo and Wildlife Research. E-mail: east{at}izw-berlin.de .
Received 27 August 2000; revised 11 November 2000; accepted 17 November 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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A long-term study of immigrant male spotted hyenas (Crocuta crocuta) living in large multimale/multifemale groups (clans) demonstrated that males acquire social status by queuing. Maximum likelihood estimates of parameters of a stochastic queuing model that assessed queuing discipline confirmed that immigrant males respected the convention that their positions in a queue of typically 15 or more individuals was determined by their sequence of arrival. Levels of aggression among males were low; males did not attempt to improve their social status through physical contests. Size and body mass did not influence male social status. The stability of queues was insured by an increase in the rate at which males formed coalitions against other males as they rose in social status and by coalitions between high-ranked males and dominant females. High-ranked, long-tenured males chiefly consorted with ("shadowed") and focused their affiliative behavior on females of high reproductive value and disrupted attempts by subordinate males to associate with these females. High-ranked males also supported females against lower-ranked males that harassed them. In contrast, lower-ranked, short-tenured males focused their affiliative behavior on young adult females and rarely shadowed or defended females. Males that did not disperse from their natal clan (nondispersers) quickly acquired top rank in the male social hierarchy. Irrespective of the social status acquired from their mother when young, nondisperser adult males submitted to all adult females.
Key words: aggression, Crocuta crocuta, queuing, social status, spotted hyenas.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Competition among males for access to mates can be intense and can result in high variance in male reproductive success, particularly in polygynous species. Sexual selection favors male traits that are attractive to females and that increase competitive ability. For example, costly sexual advertisement (Borgia, 1985
;
Hamilton and Zuk, 1982;
Zahavi, 1975) and symmetry in
body characters (Møller and
Hoglund, 1991) have been viewed as signals of male quality. Large
males prevent physically inferior males from gaining access to females
(Clutton-Brock, 1989;
Emlen and Oring, 1977) and
reduce the cost incurred by females due to harassment by marginal males
(Cassini, 1999;
Clutton-Brock et al., 1993;
Modig, 1996;
Nefdt, 1995;
Poole 1989;
Wikelski et al., 1996). Small
males use different tactics that utilize their greater agility
(Arak, 1988;
Steele and Partridge, 1988).
Older males may be better able to provide resources for their offspring and
mates
(Côté
and Hunte, 1993; Kokko,
1997), and old age may be an indicator of viability
(Kokko and
Lindström, 1996).
In a variety of species, males queue or "stand in line" to gain
access to mates. Male thirteen-lined ground squirrels (Spermophilus
tridecemlineatus) form queues of short duration
(Schwagmeyer and Parker,
1987), and much longer-term queues have been described in many
cooperative breeding species (Wiley and
Rabenold, 1984), in oystercatchers (Haematospus
ostralegu; Ens et al.,
1995), and in several lekking species of birds, such as
long-tailed manakins (Chiroxiphia linearis;
McDonald, 1989) and black
grouse (Tetrao tetrix; Kokko et
al., 1998).
Queues may operate according to a strict convention in that access to mates
is determined by the sequence in which males join queues. Alternatively,
movement to the head of a queue may be influenced by both the sequence in
which individuals joined the queue and the characteristics of queuing
individuals (Kokko et al.,
1998). Unlike conventional contests where there are winners and
losers (Maynard Smith, 1982),
queuing males that survive for a sufficiently long period can eventually
expect to gain access to mates. Differences in survivorship, however, will
influence the reproductive success of males that have to queue for long
periods before acquiring mates. Late arrivals to queues might be expected to
try to "jump the queue" if they are likely to gain more immediate
access to females by such action. If queue jumpers frequently obtain mates
before males that respect queuing conventions, then queuing would not be an
evolutionarily stable convention
(Schwagmeyer and Parker,
1987). Maynard Smith
(1983) suggested that queues
are likely to be stable if the value of the contested resource was low in
relation to the cost of violating the queuing convention and if early arrivals
in the queue have a greater resource holding potential (RHP) than late
arrivals. He also suggested that in human queues cooperation between waiting
individuals could provide stability.
We have proposed that in large, stable social groups of spotted hyenas
(Crocuta crocuta), immigrant males queue for social status in a
linear dominance hierarchy, and while doing so they cultivate relationships
with the more dominant female members of the group
(East and Hofer, 1991). Close
relationships with females are essential because of the unusual reproductive
anatomy of females (East et al.,
1993). Female spotted hyenas have a peniform clitoris that is
positioned between their hind legs, with the opening to the reproductive tract
at the tip of the clitoris that points forward. Although the peniform clitoris
is not erected during copulation (East et
al., 1993), its position and structure ensures that males can only
copulate successfully with the complete cooperation of the female
(East et al., 1993;
Kruuk, 1972). To secure such
cooperation, males need to develop close relationships with females over a
period of time (East and Hofer,
1991; East et al.,
1993; Hofer and East,
1995b). In this respect, males with long tenure have an advantage
over more recent immigrants because of their longer term relationships with
females. We have argued that aggression among queuing males is low because a
close relationship with a female is a nontransferable resource and cannot be
acquired through physical contests (East
and Hofer, 1991; East et al.,
1993). Thus, we consider that female control over mating in
spotted hyenas has favored the submission of males to females and the lack of
selection for physical contests among males
(East et al., 1993;
Hofer and East, 1995b).
In this study we used long-term data from individually known spotted hyenas from three social groups in the Serengeti National Park, Tanzania, to demonstrate that male social status is linked to tenure and is not influenced by phenotypic traits such as body size. We applied a stochastic queuing model to establish that males acquire social status by queuing. We then considered factors that contribute to the stability of the male social queue. We propose that the most important resource that immigrant males acquire by queuing is mating opportunities, and we predict that immigrant males with high social status should be better able to compete for access to females than males of lower social status.
Queue jumping should be most strongly discouraged by males that have
invested most time in queuing and those that stand to lose benefits associated
with high status. Thus, we predict that males with high rank and long tenure
should enforce queuing conventions more vigorously than low-ranked, recent
immigrants. As cooperation among queuing males is likely to be more effective
in preventing queue jumping than the actions of individuals
(Maynard Smith, 1983), we
predict that male coalitions may play a role in the stability of the male
social queue. If so, high-ranked males should form coalitions against other
males more often than more subordinate males, and individual males should not
attempt to jump the queue. However, coalitions of queue jumpers may succeed if
they challenge an individual or smaller coalition ahead of them in the
queue.
If females are more likely to mate with males that have developed long-term relationships with them, then we would expect males and females that have associated for long periods of time to have stronger relationships than those that have associated for short periods. We also predict that short-tenured males should seek to diminish this asymmetry by developing relationships with young females that have short reproductive associations with all males. By primarily developing relationships with older females, males with long-term tenure would avoid inbreeding with their female offspring.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study population
In the Serengeti National Park, Tanzania, spotted hyenas live in large, stable social groups or clans that contain approximately the same number of adult males and females (Hofer and East, 1993a
,
1995a). Data used in this
study were obtained from three clans that were studied for approximately 12
years (May 1987—June 1999), 9 years (November 1989—June 1999), and
8 years (August 1990—June 1999), respectively. Clan members were
individually known (Hofer and East,
1993a,
1995a). Females remain in
their natal clan, and all adult females breed
(Hofer and East, 1993c).
During the study period, a total of 60, 59, and 61 adult females were observed
in the three study clans, respectively. Females were aged on the basis of
their known birth dates. Previously it has been reported that male spotted
hyenas disperse from their natal group, and breeding males in a clan are
immigrant males (Frank, 1986;
Kruuk, 1972;
Mills, 1990). The average
annual rate of mortality for immigrant males was 15.6%
(Hofer et al., 1993). During
the study period, a total of 42, 42 and 41 immigrant males were observed in
the three study clans, respectively. In addition, one natal male from each of
two study clans and two natal males from the third clan did not disperse and
became part of the male dominance hierarchy in their natal clan. We refer to
natal males that did not disperse as "nondispersers." When
discussing both immigrant males and nondisperser natal males, we refer to
"postdispersal" males. Behavioral data from
"predispersal" males that operate within the social system of
their natal clan as offspring of their mother were not included in this
study.
Social status
We determined social status of males chiefly from submissive acts (retreat,
displacement, cower, tail between legs, ears back, head bobbing, head upside
down) and occasionally from aggressive acts (direct approach, push, stand
over, lunge, chase, bite) in dyadic interactions recorded ad libitum and
during focal observations of individuals. The death or disappearance of males
and the immigration of males altered the male dominance hierarchy. When such
changes occurred, we determined a new rank for all postdispersal male clan
members from dyadic interactions.
Postdispersal males and adult females were assigned a standardized rank for comparison of ranks across clans. This measure distributed ranks evenly between the highest rank (standardized rank +1) and the lowest rank (standardized rank -1), with the median rank being scored as 0. Individuals with standardized ranks within the top, middle, and lower third of the total range of values were then classified as high-, mid-, or low-ranked.
Body size parameters
We compared body size parameters from 10 immigrant males with the rate at
which these males increased in social status. Body size parameters were
obtained from anesthetized animals following the procedure described by Hofer
and East (1993a). Body length
was measured from the back of the skull to the tail root and thus excluded
head and tail length. Because spotted hyenas have the ability to consume large
amounts of food, body mass can be influenced by the amount of food in the
digestive system (Kruuk,
1972). For this reason, measures of body mass used in this study
were only from males with "normal" belly scores. We calculated the
rate at which males increased in status by dividing the number of rank
positions by which they advanced in status by the duration of the period
between the date of the first status increase to the date on which the highest
lifetime status was acquired.
Male tenure
We calculated the total tenure of an immigrant male as the period between
the date on which the male was first observed in the new clan territory and
the date of the last sighting or death of the male. Tenures of males were also
calculated for particular events as the period from the date on which the male
was first observed in the clan territory until the date of the event in
question. When the position of males in a social queue changed due to death,
disappearance, or immigration of another male, we recalculated the tenure and
social status of males in the queue. A minimum (censored) period of tenure was
calculated for immigrant males that were already established in a clan when
the study commenced and for those that joined a clan during the study and were
alive when the study ended. The tenure of males that remained in their natal
clan to breed was calculated to begin at the age at which males attained
adulthood (2 years of age).
To investigate whether the tenure of a male influenced his behavior toward
adult females of different age, we classified the behavior of males that
approached to within 5 m of a female as "affiliative" if he
greeted (East et al., 1993)
the female, groomed the female, or rubbed his body or head against that of the
female, or "other" if the male approached the female without
displaying affiliative behavior. Males were categorized as those with no more
than 3 years tenure and those with tenure longer than 3 years. Adult females
were divided into two age classes, those no more than 5 years of age (i.e.,
females within 3 years of reaching adulthood), and those older than 5 years of
age. The former group consisted mainly of first-time breeders; the latter
consisted mainly of experienced breeders. Male-female interaction data were
obtained from focal samples of males observed chiefly at the clan communal den
or recorded and libitum during encounters between males and females. The mean
duration of 151 focal samples from 57 males was 41 ± 38 min. To avoid
pseudoreplication in behavioral data, we included only one interaction by a
specific male with a specific female in analyses of behavioral data. If more
than one interaction between a particular male-female combination occurred in
the behavioral data, then a single interaction was selected at random.
We used the same categories of females and males to examine the response of young and older females to the approach of shorter or longer tenured males. The response of females to males were defined as (1) directly aggressive if the female chased or bit the male, (2) threatening if the female glared, got to her feet, approached with her tail raised, pushed or lunged without making contact with the male, or (3) other, which were chiefly neutral responses in which the female did not react to the male or (rarely) affiliative responses (grooming, greeting).
Coalitions
Immigrant males were considered to have formed a coalition with other
postdispersal males or adult female clan members if they joined an on-going
conflict by siding with one of the opponents. In addition, they participated
in display coalitions in which two or more animals "walk parallel"
(Kruuk, 1972) without
directing this display toward another clan member. When parallel walking, one
or both partners often raised their tails, groaned, and investigated scent
marks. Display coalitions may signal an intention to cooperate with other
members of the coalition and advertise the existence of the coalition to other
group members. Male coalitions mostly involved coalition partners walking or
running toward the target male that then retreated. Male coalitions that
challenged females, a behavior termed "female baiting"
(Kruuk, 1972), involved males
approaching a female with an aggressive posture and occasionally biting the
female.
Shadowing
Frank (1986: 1520) stated
that courtship in spotted hyenas consists of two levels of attendance
behavior:
The first is "following," the male trailing behind a walking female, stopping when she does and lying near her when she enters a day bed. The second is "consortship," the same male being seen with a given female on two or more consecutive sightings of the female. Eventually, one or more males form a more lasting association, attending her closely for days or weeks, the highest ranking male staying closest to her and occasionally threatening others that approach her too closely.
We have not applied these definitions because we consider following
behavior and consortship to be essentially the same behavior. Instead, we
apply the term "shadowing"
(East and Hofer, 1991) for
males that actively follow a female, regardless of how many days the male
follows the female. Some shadowing males excluded more subordinate males from
close proximity (0-20 m) of the female they followed, and males that were not
shadowing also excluded subordinate males from close proximity with particular
females or groups of females. Exclusion was typically achieved by low-level
approach and displacement interactions. By excluding subordinate males from
females, dominant males defended their priority of access to females and
disrupted attempts by other males to develop relationships with females.
We recorded the identities of the male(s) and female involved in shadowing associations when this behavior was observed. Only one record per day for a specific shadowing association was included in the analysis. The rate at which a male shadowed females was calculated by dividing the total number of shadowing cases for each male by his tenure in the clan. Only males with tenure of at least 6 months were included in the analysis. We calculated the rate at which each female was shadowed by dividing the number of instances she was shadowed by her tenure as an adult clan member. Females were considered independent and adult at 2 years of age; all have their first estrous cycle and most give birth during the 2 years following independence. Calculation of the rate at which females were shadowed was thus restricted to females that were observed for at least 2 years after independence.
Estrus and conception dates
To assess whether shadowing was linked to estrus, we required an estimate
of the likely estrous period for females. For females that were shadowed, we
calculated the conception date of their litters from the birth date of the
litter, based on a 110-day gestation period
(Matthews, 1939). Birth dates
for litters were either known or estimated from the pelage and locomotory
abilities of cubs and are likely to be accurate ± 7 days
(Hofer and East, 1993c).
Schneider (1952) quoted an
estrous period of 1 day. As it is possible that estrus may last for several
days, we estimated two periods during which estrus was likely to occur; one
spanning a period of 7 days before and after the estimated conception date,
and another spanning 15 days before and after the estimated conception
date.
Queuing discipline
We assessed the degree to which males observed the queuing convention
(queuing discipline) in a number of ways. First, for all immigrant males with
at least six changes in social status, Wilcoxon signed-rank tests were used to
investigate whether successive changes in rank position for each male involved
an increase in social status. Rank changes due to nondispersing natal males
joining the male dominance hierarchy were excluded. Second, for each clan we
calculated maximum likelihood estimates for a quantitative measure of queuing
discipline, a pair of indices introduced in a stochastic queuing model by
Kokko et al. (1998). Kokko et
al. (1998) distinguished two
processes that affect the position within a queue: the integration of
newcomers, represented by the newcomer priority index, P, and the
strictness by which established males adhere to the queuing convention,
reflected by the rank priority index, Q. Briefly, P
describes the disadvantage of a newcomer to move to a position of high social
status when trying to join a clan compared to the chances of the average
established male already present in the hierarchy. At P = 0, no
newcomer could bypass an established male in the hierarchy (i.e., the newcomer
always joins at the bottom). At P = 1, the chances of newcomers and
established males are equal, and if P > 1 newcomers would benefit
from not having previously been a member of the queue. If Q = 0, then
the current social status would be irrelevant for arranging the ranks among
all males once the newcomers joined, whereas Q = 1 describes a strict
and impartial "first in, first to the top" queuing convention.
Thus, the null hypothesis of random order and lack of queuing discipline is
equivalent to the pair of values (P, Q) = (1, 0), and the
log-likelihood ratio test G can be used to test whether empirical
estimates of (P, Q) for a given queue significantly deviate from the
null hypothesis. Further details on how empirical estimates for (P,
Q) are computed can be found in Kokko et al.
(1998).
Statistics
Statistical and graphical analyses were performed using SYS-TAT 9.0
(Wilkinson, 1999). All
statistical tests are two-tailed. Means are given ± SDs. Immigrant
males that were members of study clans at the start of the study and immigrant
males that were alive at the end of the study provided censored data on
tenure. We calculated the significance of Spearman rank correlations according
to Siegel (1956).
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RESULTS |
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Male immigration
The age at which 14 known natal males joined a new clan was 4.12 ± 1.31 years. There was no significant effect of maternal rank on the age at immigration (Spearman rank correlation, n = 13,
= 0.423).
Tenure and rank
When males first immigrated into a clan, they were submissive to all clan
members and thus acquired a dominance rank at the bottom of the social
hierarchy. On five occasions, coalitions of immigrant males below median rank
chased males that were in the process of immigrating into the clan for
distances of at least 100 m. These long chases were unlike the interactions
among established immigrant males that involved displacements by only a few
meters. These observations suggest that males below median rank are more
aggressive to new immigrants than to established immigrants, and this may
ensure that new males join the bottom of the hierarchy.
During the study immigrant males died or disappeared, and new immigrants
joined clans. Figure 1 plots
the change in social status in relation to tenure for two males from each of
the three study clans. These data show that immigrant males gradually
increased in social status as their tenure increased and as those above them
in the hierarchy died or disappeared. When immigrant males acquired a new
rank, their social position altered by only one or two rank positions. Sudden,
large changes in social status were not observed among immigrant males. For
all (n = 68) immigrant males with at least six changes in social
status, the majority (78%, n = 53) showed that new ranks were
significantly more likely to be of a higher status than the previous rank.
Thus, more males than expected by chance increased their social status in a
manner consistent with a strict queuing convention (
2 = 21.24,
df = 1, p <.00001). This was particularly true of immigrant males
in the largest clan (Mamba), where the hierarchy consisted of at least 20
males at any point in time during the study. Here, 26 out of a total of 28
(93%) immigrant males showed a consistent, steady improvement in social status
whenever their rank changed. In the two smaller clans (Pool and Isiaka) with
between 10 and 15 immigrant male members at any one time, a smaller proportion
of rank changes conformed to a strict queuing convention. In the Isiaka clan
13 (68.4%) of 19 males and in the Pool clan 14 (67%) of 21 showed a
significant, consistent increase in social status. In the minority of cases
when an immigrant male's social status declined, the mean rank change was
small (1.2 ± 0.5 rank positions, n = 47 males). Such
incidences mainly occurred when immigrant males had not been clan members for
a long period (mean tenure 332 ± 61 days) and had low social status
(highest social status of males suffering a decline in social status had a
mean rank = 12.0 ± 5.7, when the alpha male had a rank of 1).
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The center panel in Figure 1 illustrates an example of a strict queue in the Mamba clan after the death of the top-ranked male and the advancement of the second-ranked male to the top rank. The lower panel in Figure 1 illustrates a less strict queue in the Pool clan.
During this study, 13 snapshots of male queues, like that plotted in the upper panel of Figure 1, could be taken after the acquisition of the alpha position by a male. Excluding individuals with censored data on tenure and nondisperser natal males, results from linear regressions indicate that the longer the male queue, the more years an immigrant male takes to reach the alpha position. In the large Mamba clan, males required between 7 and 8 years to become the alpha male, whereas in the smaller Pool and Isiaka clans males required between 4 and 5 years.
In contrast to immigrant males, nondisperser males that remained in their natal clans to breed did not follow the queuing convention and acquired a high rank in the male dominance hierarchy when they ceased to socially operate as an offspring of their mother and began to behave like an immigrant male (see below).
Queuing discipline
A quantitative measure of queuing discipline is provided by the newcomer
priority index, P, and the rank priority parameter, Q.
Maximum likelihood estimates for the parameter pair (P, Q) over the
entire study period were the value pairs (0.01, 0.74) for the Isiaka clan,
(0.01, 0.72) for the Mamba clan, and (0.01, 0.74) for the Pool clan. Each of
the three pairs of values were highly significantly different (p
<.000001) from the null model.
Male—female relationships
Does the length of an association between a male and female influence their
behavior toward each other? Considering only one randomly chosen interaction
by a specific male with a specific female, we found that long-tenured males
(with more than 3 years tenure) were equally likely to show affiliative
behavior to both young (18 affiliative acts in 127 approaches) and older
females more than 5 years of age (6 affiliative acts in 67 approaches,
2 = 1.102, df = 1, p =.30). In contrast,
short-tenured males (with no more than 3 years tenure) showed a higher
incidence of affiliative behavior toward younger females no more than 5 years
of age (5 affiliative acts in 40 approaches) than older females (0 affiliative
acts in 62 approaches, 2 = 8.149, df = 1, p
=.004).
Does the length of their association influence the response of a female to
the approach of a male? The response of young females to short-tenured males
was different from their response to males with longer tenure
(2 = 9.975, df = 2, p =.007;
Figure 2). Young females were
more frequently directly aggressive to approaches by long-tenured males than
they were to more recent immigrants. In contrast, young females showed less
direct aggression to short-tenured males, but frequently gave low-level
threats to such males when they approached.
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The response of older, experienced females to approaches by recent and
longer tenured males also differed (2 = 7.825, df = 2,
p =.02; Figure 3).
Older females threatened both recent and longer tenured males; however, they
were more frequently directly aggressive to shorter tenured males than to
longer tenured males.
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One case of a coalition of 10 females attacking a mid-ranked male was observed. The reason for the attack was unknown. The male was not observed for more than a month after the attack. He reappeared in the territory for a few days and then was not seen again. This incident demonstrated that females directly influence membership of the male queue.
Natal males
One hundred twenty-eight natal males from the three study clans survived
beyond the age of 16 months and thus were potential dispersers
(Hofer and East, 1995a). Of
these, four natal males in three study clans did not disperse. These
nondisperser males were sons of mid- and low-ranked females. They acquired
alpha status within a period of months after they ceased to operate as the
offspring of their mothers and started to behave toward adult females in a
manner similar to that of immigrant males
(Figure 1). They were then able
to exclude all immigrant males from close proximity with females they
defended. Nondisperser natal males habitually submitted to all females,
including females that they dominated when young and associated with their
mother's social status.
Body size and social status
The rate at which males increased in social status was not correlated with
their body mass ( = 0.575, n = 8), body length ( = 0.050,
n = 9), chest girth ( = 0.485, n = 10), or shoulder
height ( = -0.250, n = 10).
Shadowing
Immigrant males rarely shadowed females when they first joined a clan. The
mean interval between immigration and the first case of shadowing behavior was
1.6 ± 1.0 years (n = 64 males). Females were shadowed mostly
by a solitary male (92%, n = 994), occasionally by two males (7%),
and rarely (1%) by larger groups of three to eight males. High-ranked females
were shadowed at a higher rate than lower-ranked females
(Figure 4) and some mid- and
low-ranked females were rarely if ever shadowed by males.
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The rate at which high-ranked males shadowed females was higher than that of lower-ranked males, and some males were rarely if ever observed shadowing females (Figure 5). High-ranked males shadowed a larger number of individual females than lower-ranked males (Figure 6), but they did not shadow all female clan members. Instead, shadowing effort was focused on a few specific females. For example, the male in each study clan that held the alpha position for the longest periods (censored tenures of 5.3, 7.0, and 9.0 years, respectively) only shadowed 10 of 37, 10 of 52, and 8 of 61 of available females, respectively, during the years they were alpha males. All three alpha males focused their shadowing effort on a few high-ranked females (75% of shadowing effort on two females, 69% on three females, and 70% on two females, respectively).
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The duration of shadowing associations varied (range 1-119 days), with most associations (89%) persisting 1-3 days and only rarely (11% of 806 associations) for longer periods. Only 11 of 105 males shadowed a specific female for 14 days or more (14-43 days); 5 of these were alpha males and all 11 males were above median rank. In one case a nondisperser natal alpha male shadowed a female for 119 days.
Of 1171 shadowing associations for which the conception date for a female's next litter was known, only 5% occurred within the 2-week period spanning the calculated conception date, and only 10% occurred within the month spanning the calculated conception data (15 days before and 15 days after the conception date). These results indicate that males frequently shadowed females that were not in estrus.
In the Serengeti, spotted hyenas regularly commute to feed on migratory
herbivores up to 70 km from their territory (Hofer and East,
1993a,b).
Males were observed following commuting females when they departed from or
returned to their territory. Males that shadowed particular females inside
their territory were relocated within days in association with the same female
long distances away from the territory. These observations indicate that males
shadow females even when they commute.
Defense of females
Males that shadowed females and males associating with females in the
vicinity of the den or at resting sites prevented lower-ranked males from
approaching the females. Exclusion was mostly achieved by approach-and-retreat
interactions. Figure 7 shows
that males below median rank rarely defended females in this way, but males
above median rank frequently did so and mostly defended females that were
above median rank. Considering those males observed interacting with females,
we compared the number of males recorded defending females (22 males above and
0 males below median rank) with those that were never seen defending females
(19 males above and 42 below median rank) and found that males below median
rank never defended females, while those above median rank frequently did so
(2 = 30.665, df = 1, p <.000001).
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Males with short tenure rarely attempted to defend females, but when they did so, they defended young females that had recently become adults (Figure 8). Males with longer tenure chiefly defended adult females with longer tenure (Figure 8).
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Coalitions among males
We predicted that high-ranked, long-tenured males should form coalitions
more often than lower ranked males. For the following analysis, we used data
from all males that progressed from low to middle status and ultimately
obtained high social status during the study (n = 30 males). For each
male we calculated the rate at which he joined coalitions during the period he
held low, middle, or high rank. Monthly rates at which males participated in
coalitions against other males increased as they rose in rank from low through
middle to high status (Friedman ANOVA = 6.067, df = 2, p =.048).
Despite long-term observations of three clans for 8, 9, and 12 years, we observed only one incidence of severe aggression among males. This involved a coalition of two immigrant males (ranked 4 and 7) briefly attacking another immigrant male ranked 3 and inflicting deep wounds. The tenures of the males ranked 3, 4, and 7 on the day of the attack were 3.5 years, 2.9 years, and 2.7 years, respectively.
Coalitions between males and females
Coalitions between postdispersal males and adult female hyenas were rare.
Of a total of 129 postdispersal males, only 19 males, all high-ranked (mean
standardized rank 0.8 ± 0.2) were observed in 27 coalitions with
females. The targets of male—female coalitions were always males with a
lower rank than the supporting male. Males chiefly formed coalitions with high
(59%) and mid-ranked (30%) females. We found no evidence that low-ranked males
attempted to increase their social status by forming coalitions with females
when these females challenged higher-ranked males.
Harassment of females
Although females are dominant to males, males harass females. Single males
harass single females by stalking them or approaching them in an aggressive
manner, then lunging and occasionally biting them on their legs or rump. Of
501 interactions with females that involved a single male, 6% involved this
form of harassment. Most of this harassment was from mid-ranked males (55%).
Harassment by low-ranked (24%) or high-ranked males was less common (21%).
Females that were bitten by males on their legs often limped for several days,
which may have impeded their ability to hunt.
Groups (two to seven individuals) of males occasionally aggressively harassed or "baited" females. Of 348 male coalitions, 28% were formed to bait females. When baited, females were often supported by other females, and on seven occasions they were supported by high-ranked males.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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This long-term study demonstrated that the social status of immigrant male spotted hyenas increased with their length of tenure in a clan (Figure 1). Physical contests were not used to improve social status, and the rate at which males increased in rank was not related to body mass or body size. The hierarchy among immigrant males can be described as a social queue, and we have shown that hyena males observe strict queuing conventions. A benefit linked to high male social status was increased access to female clan members (Figures 5 and 7).
Male social queues
Immigrant males observed a queuing convention whereby successively arriving
individuals waited their turn to rise in social status, and males did not use
aggressive contests to improve their status. Both quantitative measures of
queuing discipline introduced by Kokko et al.
(1998), the newcomer priority
index (P) and the rank priority index (Q), confirm this. The
low value of P (0.01) for all three study clans implies that males
almost always join at the bottom of the hierarchy, and this value was
substantially lower than that (0.28) reported for queues of a similar length
at black grouse leks (Kokko et al.,
1998). The values of Q of between 0.72 and 0.74 were
substantially higher than the overall value for black grouse of 0.53 and
indicated that male spotted hyenas show a far more strict queuing discipline
than black grouse. We found no evidence that phenotypic characteristics such
as skeletal size (body length, chest girth, shoulder height) or body mass
influenced the rate at which males progress along the queue.
Queue stability
In the thirteen-lined ground squirrel, queuing conventions collapse when
more than two males form a queue
(Schwagmeyer and Parker,
1987). In contrast, queues that involved numerous male spotted
hyenas were stable throughout this long-term study, and males in queues of
more than 20 animals observed queuing conventions
(Figure 1).
Maynard Smith (1983)
suggested that queues may be stable if the value of the contested resource is
low in relation to the cost of violating the queuing convention. We showed
that experienced breeding females are more tolerant of high-ranked males with
longer tenure than they are of recent immigrants. This suggests that if
short-tenured males attempt to mate with such females, they are likely to be
aggressively rejected, and thus such females are of low value to them.
It has been argued that queues may be stable if early arrivals in queues
have a greater resource holding potential (RHP) than later arrivals
(Maynard Smith, 1983). Because
the rate of status increase by males is not related to measures of body size
or mass, RHP does not appear to be a simple phenotypic property. We found that
when males achieved high status, they formed coalitions with other queuing
males more often than when they were mid- or low-ranked. Our results therefore
suggest that coalitions among high-ranked males may increase the RHP of early
arrivals. The importance of such cooperation was acknowledged by Maynard Smith
(1983) in his discussion of
the stability of human queues.
High-ranked males supported adult females that challenged lower-ranked males. High-ranked males also supported females that were harassed or baited by groups of lower-ranked males. Coalitions with socially dominant females probably reinforce the stability of the male hierarchy and may also strengthen bonds between high-ranked males and females.
One successful case of aggressive queue jumping was observed that involved a coalition of two immigrant males. The asymmetry in tenure and rank between the attacking coalition and victim was modest, and the victim was successfully evicted from the male queue. This observation suggests that male coalitions may be more effective than individuals in successfully jumping the queue, but coalitions are rarely formed to achieve this rise in status.
Greeting ceremonies are used by spotted hyenas to signal acceptance of
their social status to more dominant individuals. As greetings among immigrant
males chiefly involve individuals of similar social status
(East et al., 1993), greeting
ceremonies probably confirm relative status between males of adjacent rank
and, by doing so, may help to maintain the stability of queues.
Male—female behavior
Shadowing was not restricted to the estrous period of the female, so this
behavior may help males to strengthen relationships with females. If so,
high-ranked males invested more in fostering relationships with females than
did more subordinate males (Figures
5 and
6), and top-ranked males
focused their shadowing effort on a few high-ranked females.
Long-tenured males displayed more affiliative behavior to older than to
younger females, and older females responded with less direct aggression to
long-tenured than to short-tenured males. These results suggest that
long-tenured males seek mating opportunities with older females with breeding
experience and that young females are less desirable mating partners. This may
be because first-time breeders are more likely than experienced breeders to
produce no surviving cub or a surviving singleton rather than a twin litter
(Hofer H and East ML, unpublished data). High-ranked females are also valuable
mating partners because the reproductive success of Serengeti females
increases with social status, and their cubs grow at a faster rate and have a
higher survival than cubs of low-ranked mothers
(Golla et al., 1999;
Hofer and East, 1996).
Our results indicate that high-ranked males chiefly competed for
high-ranked and older females, thus leaving low-ranked recent immigrants the
possibility of associating and mating with reproductively less valuable
females. This suggestion is supported by observations of mating between
short-tenured males and young females (East ML, Hofer H, and Wilhelm K,
unpublished data). Thus it is possible that there are two parts to a male
queue, with recent immigrants queuing for status and attempting to encourage
younger, low-ranked females to mate with them, and males with long-term tenure
and high rank competing for reproductively more valuable females. As matings
are not entirely monopolized by high-ranked males, the possibility that mid-
and low-ranked males can obtain mating opportunities may help stabilize long
queues (Kokko and Johnstone,
1999).
A unique aspect of Serengeti clans is that group members regularly leave
their territory on long-distance foraging trips to areas containing large
numbers of migratory herbivores (Hofer and East,
1993a,b).
As high-ranked females dominate access to food resources within the clan
territory, they commute less often than females with lower social status
(Hofer and East, 1993c).
Similarly, immigrant males with high social status are more often inside the
clan territory than lower-ranked males
(East and Hofer, 1991). As a
result, high-ranked males and females encounter each other more often in the
clan territory than lower-ranked animals of the opposite sex, and this may in
part explain why high-ranked females are shadowed more often than more
subordinate females (Figure 4).
High-ranked females are also more valuable mating partners than lower-ranked
females (Golla et al., 1999;
Hofer and East, 1996).
High-ranked males may shadow the female of their choice and exclude
lower-ranked males from approaching her, but these actions may not be
sufficient to ensure that she will chose him as her mate. Thus, a male's
reproductive success may not be directly linked to his investment in building
relationships and female defense, but rather to female mate choice
(East et al., 1993). The
strength of the bond developed between a female and a male is likely to be a
factor influencing female mate choice, but other factors such as genetic
quality may also be involved. The social status of immigrant males was an
indicator of longevity, and thus it may be used by females as a reliable
signal of male viability.
Even though Serengeti hyenas breed throughout the year, the pool of
potential mates available in the clan territory is limited and constantly
changing during periods when clan members commute (Hofer and East,
1993b,c).
For this reason, patterns of mate choice by Serengeti males and females may be
different from those in more strictly territorial populations.
Harassment
Recently, much attention has been focused on the impact of male harassment
on female mate choice. It has been shown that when harassment is costly to
females, females may chose mates that provide protection against harassment
(Cassini, 1999;
Clutton-Brock et al., 1993;
Modig, 1996;
Nefdt, 1995;
Poole, 1989;
Wikelski et al., 1996).
Although female spotted hyenas are dominant to males, some male—female
interactions might be viewed as harassment by males. Our results show that
mid-ranked males often harassed females and that high-ranked males not only
excluded subordinate males from females but that high-ranked males also formed
coalitions with females to stop harassment by subordinate males. Thus it is
possible that females that are shadowed or defended by high-ranked males
rarely suffered harassment by subordinate males. Male harassment of females
may be a form of male display that focuses the attention of the female on the
male. Mid-ranked males are more likely to require attention from females than
high-ranked males that have established, long-term relationships with
females.
Choosing a queue
Immigrant males advertise their social status by producing a loud call or
whoop (East and Hofer, 1991).
High-ranked males produce more whooping bouts and longer bouts of whoops than
subordinates, and as males increase in social status the rate at which they
whoop increases. Thus whoops probably advertise a male's position in the
social hierarchy, and potential immigrants may use whooping behavior to assess
the lengths of queues in different clans
(East and Hofer, 1991).
Immigrant males required several years of tenure before they acquired the
alpha position. The number of years required to obtain the alpha position was
greater in larger clans with longer queues than in smaller clans with shorter
queues. If mating opportunities within a clan are chiefly monopolized by the
alpha male, as suggested by Frank
(1986), then it might be
expected that immigrant males should seek to join the clan with the shortest
male queue. If, however, the alpha male does not monopolize matings, the
dispersing males should not only consider the length of queues in the clans
they may join, but also the number of female clan members (i.e., potential
mates). A model by Kokko and Sutherland
(1998) shows that it pays to
join a longer queue when the amount of resource awaiting is greater than that
associated with a shorter queue.
If the difference in the responses of young and old females to short- and
long-tenured males reflected mating opportunities, then the number of young
females that recently entered the breeding population rather than the total
number of females might be the relevant measure for a dispersing male
assessing which queue to join. If dispersing males focus on the number of
young females per clan and distribute themselves in an ideal free manner
(Sutherland, 1996), male
immigration would track female recruitment and lead to a balanced adult sex
ratio, as seen in Serengeti clans (Hofer
and East, 1993a). Male choice of queue would then regulate the
adult sex ratio in clans.
Inbreeding
If males with long tenure chiefly mate with experienced females, they are
less likely to mate with their own offspring. Alternatively, if males can
identify their female offspring, then older males might be expected to
associate with female cubs that they have not sired, with the view to
developing associations with possible future breeding partners. Because
high-ranked males are more tolerated by clan females close to the communal den
(East and Hofer, 1991) and
high-ranked males often greet and associate with female cubs and subadults at
the den (East et al., 1993),
high-ranked males appear to have a better opportunity to foster associations
with female cubs and subadults than lower-ranked males.
Natal nondisperser males
Prior to this study it was thought that male spotted hyenas always disperse
from their natal groups (Frank,
1986; Kruuk, 1972;
Mills, 1990). However, in all
three study clans there were natal males that did not disperse, suggesting
that this was a rare but not unusual phenomenon in the Serengeti population.
In contrast to immigrant males, such nondisperser males acquired top rank in
the male social hierarchy when they began to compete with immigrant males for
access to females. The fact that relatively young nondispersers acquired high
rank suggests that queue stability is not maintained by age asymmetries among
males. Genetic analysis of paternity has demonstrated that natal nondisperser
males fathered cubs (East et al., unpublished data); thus a lack of dispersal
did not prevent successful reproduction. It is probable that natal
nondisperser males gain immediate high rank in the male hierarchy due to the
social dominance they acquire from their mother over all immigrant males
during their development. Even though predispersal natal males are dominant to
female clan members ranked below their mothers, these males are socially
subordinate to such females when they become nondisperser males.
During this study, sons of mid- and low-ranked females became nondispersers, whereas all sons of high-ranked females dispersed. As mentioned previously, males compete for mating opportunities with high-ranked females, probably because they are the most valuable mating partners. It may be that to avoid inbreeding, high-ranked females are unlikely to mate with male relatives, but will mate with nonrelated natal males. If so, sons of high-ranked females that want to mate with high-ranked females must disperse from their natal clan.
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ACKNOWLEDGEMENTS |
|---|
We are grateful to the Tanzania Commission of Science and Technology for permission to conduct the study and to the director generals of the Tanzania Wildlife Research Institute and Tanzania National Parks for cooperation and support; the Fritz-Thyssen-Stiftung, the Stifterverband der deutschen Wissenschaft, the Max-Planck-Gesellschaft, and the Institute for Zoo and Wildlife Research Berlin for financial assistance; to A. Francis, W. Golla, R. Klein, B. Knauer, C. Trout, L. Trout, A. Türk, W. Wickler, and K. Wilhelm for assistance and support, and to W. Goymann, O. Höner, H. Kokko, W.J. Sutherland, B. Wachter, and an anonymous reviewer for their helpful comments.
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