AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 129:584–590 (2006)
Early Sexual Maturity in Male Hamadryas Baboons
(Papio hamadryas hamadryas) and Its
Reproductive Implications
Dietmar Zinner,1* Ellen Krebs,2 Annette Schrod,3 and Werner Kaumanns2
1
Forschergruppe Kognitive Ethologie, Deutsches Primatenzentrum, D-37077 Göttingen, Germany
2
Arbeitsgruppe Primatologie, Zoologischer Garten, D-50735 Cologne, Germany
3
Abteilung Reproduktionsbiologie, Deutsches Primatenzentrum, D-37077 Göttingen, Germany
KEY WORDS hamadryas baboon; life history; sexual maturity; male; mating system
ABSTRACT We present data on sexual maturity in
young hamadryas baboon males (Papio hamadryas hama-
dryas) and its reproductive consequences in a large cap-
tive baboon colony. Hamadryas baboons live in a multi-
level social system, with one-male units (OMUs) as the
smallest social entity. Male leaders of OMUs are believed
to monopolize matings within their OMUs; hence mating
is believed to be polygynous and monandrous. In a cap-
tive colony of hamadryas baboons, we found evidence that
young males less than 4 years old fathered at least 2.5%
of 121 offspring born subsequent to vasectomy of all adult
males, and males aged 4–5 years fathered at least 16.5%
of the offspring. Additional evidence that these young
Social systems consist of three distinct elements (Kap-
peler and van Schaik, 2002): the social organization
(e.g., group composition and spatiotemporal cohesion),
the social structure (e.g., social interactions and relation-
ships), and the mating system (e.g., who mates with
whom, and what are the genetic consequences). How-
ever, these elements are not necessarily congruent, e.g.,
a particular social organization does not necessarily
reflect the logically corresponding mating system (Cords,
1988, 2000).
The multilevel social system of hamadryas baboons
(Papio hamadryas hamadryas) is unique among pri-
mates (Stammbach, 1987). The basic unit of hamadryas
social organization is the one-male unit (OMU), which
usually consists of an adult male (the ‘‘OMU leader
male’’) and a number of reproductive females and their
young offspring (Kummer, 1968a; Stammbach, 1987). At
higher levels of hamadryas social organization, individu-
als are members of clans, bands, and troops. Clans are
groups of 2 or 3 OMUs who associate closely, and
because of male philopatry, OMU leader males within
clans are thought to be related (Abegglen, 1984). Several
OMUs or clans group together to form a band. A band
numbers about 60–150 (with up to 220) baboons (Zinner
et al., 2001; Swedell, 2002), and is believed to be the
equivalent to the multimale, multifemale group of sav-
anna baboons. Bands travel together, and sometimes
fight each other as units. They are the autonomous ‘‘eco-
logical’’ unit, whereas the OMU is the ‘‘reproductive’’
unit (Kummer, 1968a). Within OMUs, the leader male
prevents females from interacting or mating with other
adult males, and it is assumed that reproduction is
C 2005
V WILEY-LISS, INC.
males are able to sire offspring came from a morphologi-
cal comparison of sperm from hamadryas males of differ-
ent ages. The sperm of a 48-month-old hamadryas baboon
were morphologically indistinguishable from viable sperm
from adult males, whereas sperm from a 45-month-old
male showed some aberrations. If successful copulations
by adolescent males constitute a regular pattern even in
free-ranging hamadryas baboons, a hamadryas male’s
chances to reproduce would not be limited to his role as
an OMU leader as previously assumed, and a male’s
reproductive career would consist of two phases: the ado-
lescent phase, and the OMU leader male phase. Am J
Phys Anthropol 129:584–590, 2006. V 2005 Wiley-Liss, Inc.
C
monopolized by the OMU leader. Thus, in hamadryas
baboons, the mating system seems to correspond to the
social organization and social structure, and can be clas-
sified as polygynous and monandrous (Kummer, 1968b;
Kummer et al., 1970; Stammbach, 1987).
However, testing this assumption is only possible
using molecular genetic markers to determine paternity,
or using demographic data from OMUs where the OMU
leader males are infertile. Females conceiving and giving
birth in such OMUs would be strong evidence that the
reproductive monopoly of OMU leader males is not as
strict as previously thought.
To date, one molecular study of captive (Smith et al.,
1999) and two of wild (Yamane et al., 2003; Hammond et
al., in press) Arabian hamadryas baboons have been per-
formed, with contradictory results. Smith et al. (1999)
and Yamane et al. (2003) showed that OMU leader males
did not father the majority of infants and juveniles
within their OMUs, but in the study of Hammond et al.
(in press), at least 92% of infants were sired by the
respective OMU leader males. Based on these results,
extra-unit copulations and extra-unit paternities in ham-
*Correspondence to: Dietmar Zinner, Deutsches Primatenzen-
trum, Kellnerweg 4, D-37077 Göttingen, Germany.
E-mail: dzinner@gwdg.de
Received 17 September 2004; accepted 6 May 2005
DOI 10.1002/ajpa.20344
Published online 5 December 2005 in Wiley InterScience
(www.interscience.wiley.com).
 MATURITY IN MALE HAMADRYAS BABOONS
adryas baboons cannot be excluded. On the other hand,
Kummer et al. (1974) showed that established bisexual
pair bonds are usually not threatened by other adult
males, and that OMU leader males aggressively herd
their females away from other adult males. Hence,
chances in females for extra-unit copulations with other
adult males seem to be low (Sigg et al., 1982), but copu-
lations between juvenile males and estrous females were
observed in the wild (Kummer, 1968a; Sigg et al., 1982;
Swedell, 2005) and in captivity (Kaumanns, 1983). Such
copulations might result in pregnancies if older juvenile
or adolescent hamadryas males are sexually mature, and
thus might explain some of the extra-unit paternities in
the Saudi Arabian population.
In fact, Jolly and Phillips-Conroy (2003) presented
data concerning an earlier start of testicular enlarge-
ment in hamadryas baboons compared to olive baboons,
which would fit the picture of reproductively active ado-
lescent males. However, data concerning gametic devel-
opment are missing, as well as data on the reproductive
and demographic consequences of early maturity in
hamadryas baboon males. Here, we test the hypothesis
that 4-year-old hamadryas baboon males are capable of
producing viable sperm, and that males of this age class
(48–60 months) are reproductively active before reaching
adulthood and were responsible for a number of infants
born in a captive colony.
MATERIALS AND METHODS
This study is based on demographic data from the
hamadryas baboon colony of the Cologne Zoo. These
data, as well as data concerning the social structure of
the colony, such as size and composition of OMUs, have
been recorded systematically since 1989. For our study,
the relevant time period lasted from January 1994–July
2004.
At the Cologne Zoo, hamadryas baboons are kept in a
naturalistic outdoor enclosure (‘‘baboon rock’’), with a
total area of approximately 450 m2. The rock is almost
10 m high, and is surrounded by water. All adult mem-
bers of the colony could be identified individually, al-
though this was not possible for all infants, juveniles,
and subadults. Age and sex classes could be determined
in every case. Therefore, the exact number of males and
their respective age class were available for any given
month in the study period, including months when
births and conceptions occurred.
Vasectomy
Between January 1989–June 1994, the baboon popula-
tion at the Cologne Zoo doubled in size (from 70 to 141
individuals, within 9 OMUs). To limit population expan-
sion, adult males were vasectomized. For surgery, males
were anesthetized, the spermatic duct was cut, and an
approximately 1-cm-long portion was removed. Surgery
was conducted by experienced veterinarians of the
Cologne Zoo. Vasectomies were carried out in June 1994,
October 1996, November 1998, September 2001, and
July 2004. In 1994, all 19 males of the colony who were
older than 5 years at the time underwent surgery, with
the exception of one senescent OMU leader. Four fe-
males of his OMU conceived and gave birth after June
1994. We eliminated these data from our sample. After
July 1995, no more females conceived in this particular
OMU, and the male died in April 1998. The number and
American Journal of Physical Anthropology—DOI 10.1002/ajpa
585
1
TABLE 1. Number and age of vasectomized males
Vasectomy 36–48 m 48–60 m 60–72 m >72 m Total
June 1994 0 0 11 8 192
October 1996 0 1 5 0 6
November 1998 0 0 3 2 5
September 2001 0 0 4 5 9
July 2004 4 1 3 2 10
1
m, months.
2
One additional senescent OMU leader was not vasectomized.
age of males vasectomized in the following years are
listed in Table 1.
As expected, the effect of vasectomy on adult males
was a decrease in number of births in the colony, from
20.7 per year in the 6 years prior to the first set of vasec-
tomies in June 1994, to 9.2 per year in the 6 years after
the first vasectomies, although the number of females
was not reduced. Furthermore, after vasectomies, we
observed births in 14 out of 18 OMUs, and females of all
age classes were affected, suggesting that it was not a
single adult OMU leader whose surgery failed and who
sired all the infants in several other OMUs. A further
detailed description of consequences of the birth-control
measurements for the demographic development of the
colony and the management implications are described
elsewhere (Krebs and Kaumanns, 2002).
Conceptions
Conception dates were calculated retrospectively from
dates of birth. Average gestation length in captive hama-
dryas baboons is about 181 days (Kaumanns et al., 1989;
Zinner et al., 1993); hence, date of conception was de-
fined as date of birth minus 181 days. Whether any con-
ceptions occurred subsequent to the last vasectomy in
July 2004, when for the first time males between 3–4
years of age were vasectomized, is not clear at the mo-
ment (January 2005).
Paternity
No genetic data are available to determine paternity.
For our research question, however, it was only necessary
to know which age classes of males were in the colony in
the months when conceptions occurred. Since postvasec-
tomy no adult male should be able to sire an infant,
infants who were nevertheless born in the colony must
have been sired by younger, nonvasectomized males.
Testicular size and sperm morphology
Data on testicular volume and sperm morphology were
obtained from two juvenile males (aged 45 and 48
months) from the baboon colony of the German Primate
Center (DPZ). The two males were castrated as part of
population management measures. After removal of the
testes and accessory tissues from the scrotum, sperm
were washed from the spermatic duct for subsequent
morphological analyses (Schrod, 2002). Testes were
weighed and measured with a caliper (mm), whereby the
longest dimension refers to length, and the largest
dimension orthogonal to length was width. These meas-
urements refer to testes only without epididymis and
scrotum tissues. We calculated testicular volume (in cm3)
according to Glander et al. (1992) as: 10
3 3 (testicular
width/2)2 3 (testicular length/2) 3 4p/3. Relative testicu-
586 D. ZINNER ET AL.
TABLE 2. Testes measurements of juvenile hamadryas baboons
Age Body Mass right Vol. right Rel. vol. right Mass left Vol. left Rel. vol. left
Male (months) mass (kg) testis (g) testis (cm3) testis (cm3/kg) testis (g) testis (cm3) testis (cm3/kg)
Zorro 45 10.4 2.61 1.86 0.179 2.65 1.58 0.152
Steve 48 13.9 4.02 3.22 0.232 3.49 2.16 0.155

lar volume was expressed as testicular volume (cm3)/

body mass (kg).
For comparison of sperm morphology and morphome-
try, we used ejaculates from six adult hamadryas baboon
males (>10 years old) from the colonies in Berlin Zoo
and Safari Beekse Bergen (The Netherlands). These
sperm were obtained in the course of a comparative
study (Schrod, 2002) using electroejaculation (e.g., Mar-
tin, 1978). Two hundred spermatozoa from each male
were measured according to standard sperm morphomet-
ric methods (Hobson Sperm Tracker System, Hobson,
Ltd., Sheffield, UK). Measurements were then pooled for
each male, and the resulting individual means were used
in further statistical comparisons. For morphological
classification of sperm, we analyzed 200 spermatozoa
from each male microscopically for head and tail aberra-
tions, such as amorphic heads, head and tail deforma-
tion, coiled tails, broken tails, double tails, and cytoplas-
matic droplets (Leidl et al., 1971; Weitze, 2001; Schrod,
2002).

Ethical note
Vasectomy and castration of male hamadryas baboons
were applied as birth-control measures in the captive
populations in Cologne Zoo and the DPZ. They were not
been initiated or caused by our study. Hamadryas ba-
boons reproduce well under captive conditions (Kaumanns
et al., 1989; Krebs and Kaumanns, 2002), and a decelera-
tion of reproduction is often required to avoid the nega-
tive effects of crowding. Vasectomy, castration, and elec-
troejaculation were carried out by veterinarians while
animals were sedated.

RESULTS
Maturation in male hamadryas baboons
Age, body mass, testicular mass, and absolute and rel-
ative testicular volumes of the two young hamadryas
males from the DPZ colony are given in Table 2. The
body mass of the two DPZ juveniles is greater than the
body mass of juvenile males of the same age from
another captive colony (Crawford and Handelsman,
1996; n ¼ 5, mean ¼ 8.4 kg, SD ¼ 2.4 kg; range, 6.2–
12.0 kg) and most likely also greater than that of wild
male hamadryas baboons of a comparative age class
(Jolly and Phillips-Conroy, 2003; n ¼ 6, mean ¼ 6.1 kg,
SD ¼ 1.76 kg for age class 2; estimated age, 24–50 Fig. 1. Hamadryas baboon spermatozoa. a: Viable, morpho-
months). Absolute volume of the left testis of the same logically normal, homogenous sperm from adult male (>10 years
six wild hamadryas males (24–50 months) was 1.25 cm3, old; diluted sample, obtained through electroejaculation). b:
and relative testicular volume was 0.20 cm3/kg (Jolly Sperm from juvenile male (48 months old; from spermatic duct).
and Phillips-Conroy, 2003). These data are comparable Morphology and homogeneity similar to sperm from adult male.
with data from the two young DPZ males. c: Sperm from juvenile male (45 months old; from spermatic
duct). Sperm are inhomogeneous, at mostly premature stages,
Mature sperm that were morphologically indistin- but with some mature.
guishable from sperm of adult hamadryas baboons were
found in the spermatic duct of the older and heavier of
the two juvenile males (Steve) (Fig. 1). In contrast, Morphometric comparison of spermatozoa of adult
sperm from the younger and lighter male showed vari- hamadryas baboons and the 48-month-old male revealed
ous morphological forms, but also included some mature no difference in any of the variables examined (Table 3).
spermatozoa. Furthermore, spermatozoa of the 48-month-old male did

American Journal of Physical Anthropology—DOI 10.1002/ajpa

 MATURITY IN MALE HAMADRYAS BABOONS
TABLE 3. Morphometrical comparison of sperm of six adult hamadryas baboons and sperm of 48- and 45-month-old male
adult mean (n ¼ 6) SD
Head length (lm) 5.3 0.9
Head width (lm) 3.4 1.1
Head length/width 1.4 0.1
Tail length (lm) 70.0 2.4
Total length (lm) 75.5 2.7
1
Two hundred spermatozoa from each male were measured for head length and width, ratio of head length and width, tail length,
and total length (single mean test).
Fig. 2. Temporal pattern of vasectomies and conceptions
(per month) in hamadryas baboon colony of Cologne Zoo be-
tween January 1994–July 2004. Arrows indicate dates of va-
sectomies. *Four conceptions occurred in OMU of only nonva-
sectomized senescent OMU leader.
not show a higher proportion of aberrant spermatozoa
than in adult males (17.5%; adults, 16.8%). The sperma-
tozoa of the 45-month-old male, however, showed signifi-
cant aberrations in ratio of head length and width, tail
length, and total length compared to spermatozoa of
adult males. Sperm density and motility could not be
compared due to the different methods to obtain sperm,
i.e., washing the spermatic duct after castration and
electroejaculation.
Reproductive impact of juvenile male
hamadryas baboons
The temporal pattern of vasectomies and conceptions
(as inferred from birth dates 6 months later) of the ham-
adryas baboon colony of the Cologne Zoo is shown in
Figure 2. No conceptions occurred for 10 months after
the 1994 vasectomies of all adult and subadult males
(with the exception of two conceptions in the OMU of
the only nonvasectomized adult OMU leader), 5 months
after the 1996 vasectomies, 3 months after the 1998 va-
sectomies, and 3 months after the 2001 vasectomies.
During subsequent months, conceptions occurred, fol-
lowed by births, despite the virtual absence of fertile
adult males.
Within our 121-month study period (vasectomies from
June 1994 until July 2004), 121 conceptions occurred,
resulting in deliveries 6 months later (plus four deliv-
eries in the OMU of the nonvasectomized senescent
male). Based on the presence and absence of males of
various age classes in months when conceptions oc-
587
1
48 months (n ¼ 1) P 45 months (n ¼ 1) P
5.1 0.723 5.7 0.325
3.5 0.847 3.3 0.796
1.5 0.519 1.7 0.003
68.9 0.302 56.9 0.001
74.0 0.230 62.6 0.001
curred, we conclude that in at least three cases (2.5%),
the putative sires must have been males aged 36–48
months, because in the respective months, these males
were the oldest nonvasectomized males in the colony
(Table 4). In another 20 cases (16.5%), only males be-
tween 48–60 months old could be considered putative
sires. Furthermore, in 65 cases (53.7%), only males be-
tween 60–72 months old, and in 33 cases, only males
aged between 72–84 months comprised the oldest nonva-
sectomized age class present in the colony at times of
conceptions. None of the males aged less than 7 years
was an OMU leader at the time of conceptions.
Characteristics of females who conceived
In hamadryas baboons, all adult reproducing females
are normally members of OMUs. Within our study
period, all females, except for five nulliparous females,
could be clearly recognized as members of OMUs. The
identification of the five nulliparous females was uncer-
tain, and we therefore could not be sure which of these
females were attached to an OMU and which were possi-
bly ‘‘floaters.’’ (Floaters are not closely attached to a cer-
tain OMU, but ‘‘float’’ from one male to another, includ-
ing subadults.) However, in the course of the study, these
five females contributed only five births (7.8%) to the
number of births that occurred in periods subsequent to
vasectomies. After their first births (all stillbirths), all
five of these females became members of OMUs.
Our data strongly suggest that not only young and
floating females, but also older females who were clearly
members of an OMU and were decidedly attached to an
individual vasectomized adult male, conceived during
periods following the vasectomies.
One-male units
Before the first vasectomies (1989–1994), the colony
consisted of nine OMUs with an average of 4.1 (63.7)
females in each. During the period after the first vasec-
tomies (1995–2000), the number of OMUs increased to
18, with 3.1 (62.1) females on average. All of the older
OMUs lost females to younger adult males in the period
from 1995–2000 (Krebs, 2000; Krebs and Kaumanns,
2002). Within the study period, births occurred in 5 of
the 9 older OMUs, and in all nine OMUs that were
established after the first vasectomy. Since infants were
born after vasectomies in 14 out of 18 OMUs, it seems
unlikely that vasectomy failed in all males. Conceptions
by juvenile and subadult males were not characteristic
of only one or a few OMUs.
DISCUSSION
In hamadryas baboons, receptive females interact fre-
quently with adolescent males in the wild and in captiv-
American Journal of Physical Anthropology—DOI 10.1002/ajpa
588 D. ZINNER ET AL.
TABLE 4. Number of conceptions while certain male age class was oldest, nonvasectomized male age class present in colony, and
average number of males of respective classes that were present1
36–48
Number of conceptions 3.0
% conceptions 2.5
Number of males (mean 6 SD) 4.7 6 0.6
1
Total number of conceptions ¼ 121 (100%). Additionally, there were four conceptions in one OMU with nonvasectomized, senescent
OMU leader male. This male was present in the colony from June 1994 to April 1998. Further, during the whole study period, 19 to
38 older but vasectomized males have been present in the colony.
ity and copulations occur, mostly initiated by the female
(Kummer, 1968a, 1995; Sigg et al., 1982; Kaumanns,
1983; Swedell, 2005). Kummer (1968a) assumed that
copulations with younger males may seldom result in
pregnancy, because 1) it was thought that hamadryas
baboon males are multiple mounters and that a long ser-
ies of mountings resulting in ejaculation is almost impos-
sible in the vicinity of the unit leader, and 2) these
young males are probably not yet sexually mature. Mul-
tiple mounts, however, are not necessary for ejaculation
(personal observations; Nystrom, 1992), and males may
be capable of inseminating females when they are not
yet 4 years old.
In our study, we found strong evidence that captive
hamadryas baboon males aged less than 4 years are also
capable of producing viable sperm, and that they fa-
thered at least 2.5% of infants born after all adult males
were vasectomized. An additional 16.5% of infants born
after vasectomies were most likely fathered by males
aged only 4–5 years. These males are only 50–60% of the
adult body mass, and do not show the attributes of adult
male hamadryas baboons, such as the long shoulder
mane. None of these young males were OMU leaders at
times of conception, and they are possibly best character-
ized as adolescents according to the definition by Setch-
ell and Lee (2004).
In contrast, Biquand et al. (1994) did not find any evi-
dence for further reproduction in an isolated band of
free-ranging Arabian hamadryas baboons after the male
leaders had been vasectomized. However, no data are
available as to whether any adolescent males were
present in the OMUs during the 3.5-year study period.
Biquand et al. (1994) mentioned only one subadult male
who lived in the band but died 18 months after the adult
males had been vasectomized.
Puberty in male primates is signaled by enlargement
of the testes, which coincides with the production of via-
ble sperm (Alberts and Altmann, 1995). In rhesus ma-
caques (Macaca mulatta), it was shown that these
pubescent males are physically capable of fathering off-
spring (van Wagenen and Catchpole, 1956; Erwin and
Mitchell, 1975). However, under natural conditions, this
reproductive potential is normally not realized, because
of competition with full-grown adult males (Alberts and
Altmann, 1995).
Kummer (1968a) also reported that in hamadryas
baboons, some adult OMU leaders interfered with and
threatened or attacked their females when copulating
with younger males, but other OMU leaders did not. The
potential of young males to interact sexually with recep-
tive females seems to be higher in the hamadryas mat-
ing system than in other baboon taxa, although juvenile
males also appear in the mating records of receptive yel-
low baboon females, taking advantage of the temporary
American Journal of Physical Anthropology—DOI 10.1002/ajpa
Oldest, nonvasectomized male class (months)
48–60 60–72 72–84
20.0 65.0 33.0
16.5 53.7 27.3
3.9 6 0.6 3.5 6 1.5 2.5 6 1.4
absence of consort males to copulate with the female. In
such situations, juveniles, but not subadults, are toler-
ated by the adult male (Hausfater, 1975). In yellow
baboons, however, it seems unlikely that these young
males are already able to inseminate a female (Altmann
et al., 1981).
The operational sex ratio is normally more female-
biased in hamadryas OMUs than in multimale groups of
olive, yellow, or chacma baboons. If a hamadryas female
comes into estrus, there is only one adult male mating
partner available, whereas in other baboon taxa, there
are more potential adult mating partners in the group.
Other adult males will not be competitors of young ham-
adryas males, because the OMU leader will keep his
females away from them, and adult males may be inhib-
ited from interacting with females belonging to other
males (Kummer et al., 1974). Second, in hamadryas
baboons, it is more likely that an OMU leader and a
young male competitor are genetically related than in
other baboon taxa, due to a lack of male migration. This
may lead to a certain degree of tolerance of adolescent
males by OMU leaders, and in particular when they do
not yet show the morphological attributes of maturity.
Proximate mechanisms enhancing juvenile
male copulations
Certain demographic conditions may facilitate sexual
interaction among receptive females and adolescent
males, such as large OMUs or synchronously cycling fe-
males. Since fewer females became pregnant after the
vasectomies, the number of cycling females, as deter-
mined by the number of females with swelling, increased
(Krebs, 2000; Krebs and Kaumanns, 2002). Accordingly,
the number of days when there was more than one
female with swelling increased, and the operational sex
ratio within OMUs and within the colony became more
female-biased. A higher degree of synchrony among fe-
males within an OMU causes problems for the leader
male, because he cannot control and monopolize all his
females to the same degree. As in other species, this
may enhance reproductive opportunities for subordinate
males (Altman, 1962). In hamadryas baboons, these are
possibly sexually precocious younger males, e.g., Kum-
mer (1968a) observed copulations with nonleader males
in particular during times when a large percentage of
the troop’s females were in estrus.
If the females within an OMU show synchronized
cycles, then the leader male not only requires more time
and energy to monopolize his females, but he may also
temporarily deplete his sperm reservoir when mating
with high frequency (Small, 1988). As a result, the prob-
ability of conception for each female declines with in-
creasing numbers of synchronous females (Zinner et al.,
 MATURITY IN MALE HAMADRYAS BABOONS
1994). In such a situation, it is in the females’ own re-
productive interests to look for alternative mates, and
possibly adolescent males. Therefore, larger OMUs with
a higher degree of female synchrony may increase the
chances of young males to copulate successfully. This
may be an additional argument to explain the low pater-
nity probability of Arabian OMU leader males in the
study of Yamane et al. (2003). Arabian OMUs are rela-
tively large and female-biased (Kummer et al., 1985; Zin-
ner et al., 2001).
Young males may also have greater chances to copu-
late during times when the swelling of females is not at
its maximum, but when there is still a small chance for
an ovulation to occur (Saayman, 1970; Nunn, 1999).
CONCLUSIONS
Under captive conditions and when adult OMU lead-
ers were not able to inseminate their females because
of vasectomies, successful copulations by young males
were relatively frequent. Under natural conditions, the
success of adolescent males will most likely be much
smaller, particularly if OMUs contain only one or two
females who cycle asynchronously. However, if successful
copulations by adolescent males constitute a regular pat-
tern even in free-ranging hamadryas baboons, a male’s
chances to reproduce would not be limited to his role
as an OMU leader, as previously assumed (Kummer,
1968a). Studies of the genetic relationships within and
among hamadryas OMUs, and in particular patterns of
paternity, are necessary to examine male reproductive
strategies in this species, in particular from populations
that are not commensal such as those in Arabia.
ACKNOWLEDGMENTS
We thank Prof. G. Nogge for his generous support of
research at the Cologne Zoo, and Susanne Rensing for
veterinary assistance at the German Primate Center. We
are grateful to J. Setchell, Peter M. Kappeler, Eckhard
W. Heymann, M. Heistermann, and two anonymous re-
viewers for useful comments on the manuscript. We also
thank the Zoological Garden Berlin, the Safari Beekse
Bergen, and the German Primate Center for their co-
operation.
LITERATURE CITED
Abegglen JJ. 1984. On socialization in hamadryas baboons.
Lewisburg, PA: Bucknell University Press.
Alberts SC, Altmann J. 1995. Preparation and activation: deter-
minants of age at reproductive maturity in male baboons.
Behav Ecol Sociobiol 36:397–406.
Altman SA. 1962. A field study on the sociobiology of rhesus
monkeys (Macaca mulatta). Ann NY Acad Sci 102:338–435.
Altmann J, Altmann S, Hausfater G. 1981. Physical maturation
and age estimates of yellow baboons, Papio cynocephalus, in
Amboseli National Park, Kenya. Am J Primatol 1:389–399.
Biquand S, Boug A, Biquand-Guyot V, Gauthier JP. 1994. Man-
agement of commensal baboons in Saudi Arabia. Rev Ecol
(Terre Vie) 49:213–222.
Cords M. 1988. mating systems of forest guenons: a preliminary
review. In: Gauthier-Hion A, Bourlière F, Gauthier J-P, King-
don J, editors. A primate radiation: evolutionary biology of
the African guenons. Cambridge: Cambridge University Press.
p 323–339.
Cords M. 2000. The number of males in guenon groups. In: Kap-
peler PM, editor. Primate males. Cambridge: Cambridge Uni-
versity Press. p 84–96.
American Journal of Physical Anthropology—DOI 10.1002/ajpa
589
Crawford BA, Handelsman DJ. 1996. Androgens regulate circu-
lating levels of insulin-like growth factor (IGF)-I and IGF
binding protein-3 during puberty in male baboons. J Clin
Endocrinol Metab 81:65–72.
Erwin J, Mitchel G. 1975. Initial heterosexual behavior of ado-
lescent rhesus monkeys (Macaca mulatta). Arch Sex Behav 4:
97–104.
Glander KE, Wright PC, Daniels PS, Merelender AM. 1992.
Morphometrics and testicle size of rain forest lemur species
from southeastern Madagascar. J Hum Evol 22:1–18.
Hammond RL, Winney BJ, Macasero W, Flores B, Boug A,
Scheffrahn W, Biquand V, Biquand S, Bruford MW. In press.
Kin structure in Arabian hamadryas baboons, Papio hama-
dryas hamadryas.
Hausfater G. 1975. Dominance and reproduction in baboons
(Papio cynocephalus). A quantitative analysis. Contrib Primatol
7:1–150.
Jolly CJ, Phillips-Conroy JE. 2003. Testicular size, mating sys-
tem, and maturation schedules in wild anubis and hamadryas
baboons. Int J Primatol 24:125–142.
Kappeler PM, van Schaik CP. 2002. Evolution of primate social
systems. Int J Primatol 23:707–740.
Kaumanns W. 1983. Soziale Strukturen bei einer Zookolonie
von Mantelpavianen (Papio hamadryas). Ph.D. thesis, Univer-
sität Konstanz, Konstanz, Germany.
Kaumanns W, Rohrhuber B, Zinner D. 1989. Reproductive
parameters in a newly established colony of hamadryas
baboons (Papio hamadryas). Primate Rep 24:25–33.
Krebs E. 2000. Soziale Beziehungen unter Mantelpavianweib-
chen (Papio hamadryas) unter Berücksichtigung der Konkur-
renz. Ph.D. thesis, Universität Köln, Cologne, Germany.
Krebs E, Kaumanns W. 2002. Management und Geburtenkon-
trolle bei Mantelpavianen (Papio hamadryas) im Kölner Zoo.
Zool Garten NF 72:424–441.
Kummer H. 1968a. Social organization of hamadryas baboons.
A field study. Chicago: University of Chicago Press.
Kummer H. 1968b. Two variations in the social organization of
baboons. In: Jay PC, editor. Primates. Studies in adaptation and
variability. New York: Holt, Rinehart and Winston. p 293–312.
Kummer H. 1995. In quest of the sacred baboon. A scientist’s
journey. Princeton: Princeton University Press.
Kummer H, Goetz W, Angst W. 1970. Cross-species modifica-
tions of social behavior in baboons. In: Napier JR, Napier PH,
editors. Old World monkeys. Evolution, systematics and be-
havior. New York: Academic Press. p 351–363.
Kummer H, Götz W, Angst W. 1974. Triadic differentiation: an
inhibitory process protecting pair bonds in baboons. Behav-
iour 49:62–87.
Kummer H, Banaja AA, Abo-Khatwa AN, Ghandour AM. 1985.
Differences in social behaviour between Ethiopian and Ara-
bian hamadryas baboons. Folia Primatol (Basel) 45:1–8.
Leidl W, Schefels W, Stolla R, Metzger E. 1971. Differenzierun-
gen und Befruchtungsvermögen pathologischer Spermien.
Dtsch Tierarztl Wochenschr 78:129–134.
Martin ICA. 1978. The principles and practice of electroejacula-
tion of mammals. Symp Zool Soc Lond 43:127–152.
Nunn CL. 1999. The evolution of exaggerated sexual swellings
in primates and the graded-signal hypothesis. Anim Behav
58:229–246.
Nystrom PDA. 1992. Mating success of hamadryas, anubis and
hybrid male baboons in a ‘‘mixed’’ social group in the Awash
National Park, Ethiopia. Ph.D. thesis, Washington University,
St. Louis, MO.
Saayman GS. 1970. The menstrual cycle and sexual behaviour
in a troop of free ranging chacma baboons (Papio ursinus).
Folia Primatol (Basel) 12:81–110.
Schrod A. 2002. Vergleichende Analysen der Spermienmotilität,
-morphologie und -morphometrie bei Primaten mit unter-
schiedlichen Paarungssystemen. Ph.D. thesis, TiHo Hannover,
Germany.
Setchell JM, Lee PC. 2004. Development and sexual selection in
primates. In: Kappeler PM, van Schaik CP, editors. Sexual
selection in primates: new and comparative perspectives.
Cambridge: Cambridge University Press. p 175–195.
590 D. ZINNER ET AL.
Sigg H, Stolba A, Abegglen JJ, Dasser V. 1982. Life history of
hamadryas baboons: physical development, infant mortality,
reproductive parameters and family relationships. Primates
23:473–487.
Small MF. 1988. Female primate sexual behavior and conception.
Are there really sperm to spare? Curr Anthropol 29:81–100.
Smith DG, Kanthaswamy S, Disbrow M, Wagner JL. 1999. Re-
construction of parentage in a band of captive hamadryas
baboons. Int J Primatol 20:415–429.
Stammbach E. 1987. Desert, forest and montane baboons: multi-
level societies. In: Smuts BB, Cheney DL, Seyfarth RM,
Wrangham RW, Struhsaker TT, editors. Primate societies.
Chicago: University of Chacago Press. p 112–120.
Swedell L. 2002. Ranging behavior, group size and behavioral
flexibility in Ethiopian hamadryas baboons (Papio hamadryas
hamadryas). Folia Primatol (Basel) 73:95–103.
Swedell L. 2005. Strategies of sex and survival in hamadryas
baboons. Through a female lens. Upper Saddle River, NJ:
Pearson, Prentice Hall.
American Journal of Physical Anthropology—DOI 10.1002/ajpa
van Wagenen G, Catchpole HR. 1956. Physical growth of the
rhesus monkey (Macaca mulatta). Am J Phys Anthropol 14:
245–273.
Weitze KF. 2001. Spermatologische Untersuchungen. In: Busch
W, Holzmann A, editors. Veterinärmedizinische Andrologie.
Stuttgart: Schattauer Verlag. p 87–109.
Yamane A, Shotake T, Mori A, Boug A, Iwamoto T. 2003. Extra-
unit paternity of hamadryas baboons (Papio hamadryas) in
Saudi Arabia. Ethol Ecol Evol 15:379–387.
Zinner D, Kaumanns W, Rohrhuber B. 1993. Infant mortality in
captive hamadryas baboons (Papio hamadryas). Primate Rep
36:97–113.
Zinner D, Schwibbe M, Kaumanns W. 1994. Cycle synchrony
and probability of conception in female hamadryas baboons
Papio hamadryas. Behav Ecol Sociobiol 35:175–183.
Zinner D, Peláez F, Torkler F. 2001. Group composition and
adult sex-ratio of hamadryas baboons (Papio hamadryas ham-
adryas) in central Eritrea. Int J Primatol 22:415–429.