American Journal of Primatology 71:1–12 (2009)
RESEARCH ARTICLE
Living on the Edge: Life-History of Olive Baboons at Gashaka-Gumti National
Park, Nigeria
JAMES P. HIGHAM1,2, YMKE WARREN1, JEREMIAH ADANU2,3, BUBA N. UMARU2,3, ANN M. MACLARNON1,
VOLKER SOMMER2,4, AND CAROLINE ROSS1,2
1
Centre for Research in Evolutionary Anthropology, Roehampton University, London, United Kingdom
2
Gashaka Primate Project, Serti, Taraba State, Nigeria
3
Department of Forestry and Wildlife Management, Federal University of Technology, Yola, Adamawa State, Nigeria
4
Department of Anthropology, University College London, London, United Kingdom
Baboons are the most successful and ubiquitous African primates, renowned for their behavioral and
reproductive flexibility, which enable them to inhabit a wide variety of habitat types. Owing to a
number of long-term field studies, comparative behavioral, developmental, demographic, and lifehistory data are available from several populations, but study sites show a heavy bias toward South and
East African savannahs, with little research in West or Central Africa. Life-history data from such areas
are important if we are fully to understand the nature of the environmental factors that limit baboon
distribution. Here, we present demographic data for olive baboons at Gashaka-Gumti National Park
(GGNP), Nigeria, collected from December 2000–February 2006, and use these data to test comparative
models of baboon life-history. The GGNP habitat, which includes large areas of rainforest, is an
environment in which baboons are little studied, and rainfall is much higher than at previous study
sites. GGNP troop size data are presented from censuses, as well as life-history data for two troops, one
of which is within the park and wild-feeding (Kwano troop), whereas the other dwells at the park edge,
and supplements its diet by crop-raiding (Gamgam troop). Troop sizes at GGNP are small compared
with other field sites, but fit within previously suggested ranges for baboons under these climatic
conditions. Inter-birth intervals in Kwano troop were long compared with most studied populations,
and values were not as predicted by comparative models. Consistent with known effects of food
enhancement, Gamgam troop experienced shorter inter-birth intervals and lower infant mortality
than Kwano troop. We indicate some possible factors that exclude baboons from true rainforest, and
suggest that the clearing of forests in Central and West Africa for agricultural land may allow baboons
to extend their range into regions from which they are currently excluded. Am. J. Primatol. 71:1–12,
2009.
r 2009 Wiley-Liss, Inc.
Key words: life-history; reproduction; mortality; comparative; crop-raiding
INTRODUCTION
The baboon (Papio hamadryas) is one of the best
studied of all primates, with a number of long-term
study sites established across Africa. These have led
to a plethora of long-term comparative behavioral,
developmental, demographic, and life-history data
[e.g. Altmann et al., 1977; Bentley-Condit & Smith,
1997; Cheney et al., 2004; Lycett et al., 1999; Sigg
et al., 1982; Smuts & Nicolson, 1989], allowing
comparison between populations with a wide range
of habitats and climates, and modeling of the
ecological correlates of life-history variables, behavior, and group sizes [Barrett et al., 2006; Dunbar,
1992; Dunbar, 1996; Hill et al., 2000; Hill & Dunbar,
2002; Williamson & Dunbar, 1999]. However, baboon
study sites have shown a heavy bias toward southern
Africa [e.g. De Hoop, Hill, 1999; Drakensberg, Henzi
et al., 1992; Lycett et al., 1999; Moremi, Cheney
r 2009 Wiley-Liss, Inc.
et al., 2004] and East Africa [Amboseli, Altmann,
1980; Gilgil, Strum & Western, 1982], with few
published studies from West Africa, [Comoé, Kunz
and Linsenmair, 2008; Mt Assirik, Sharman, 1981;
Contract grant sponsors: Roehampton University; The Leakey
Trust; Primate Society of Great Britain; NUMICO Research
B.V.; British Federation of Women Graduates; The International
Federation of Animal Welfare.
Correspondence to: James P. Higham, Institute for Mind and
Biology, University of Chicago, 940 East 57th Street, Chicago, IL
60637. E-mail: jhigham@uchicago.edu
Received 2 April 2008; revised 12 November 2008; revision
accepted 13 November 2008
Current address: James P. Higham, Institute for Mind and
Biology, University of Chicago, 940 East 57th Street, Chicago,
IL 60637.
DOI 10.1002/ajp.20651
Published online in Wiley InterScience (www.interscience.
wiley.com).
2 / Higham et al.
Shai hills, Depew, 1983] and none from central
Africa. As a consequence, baboons are well studied in
savannah grasslands, whereas relatively little is
known about baboon ecology in some other habitats,
particularly forest, into which baboons penetrate to
various extents at the edges of their distribution.
Here, we present life-history and group size estimates for wild olive baboons (P. hamadryas anubis)
[Rogers, 2000] at Gashaka-Gumti National Park
(GGNP), Nigeria, and set these data in the context
of comparative baboon socio-ecology. This site is a
geographical, habitat and climatic outlier compared
with other baboon sites, and as such our data are of
particular interest for understanding the role of the
environment in influencing subspecific variation in
baboon ecology.
Comparative studies that investigate variation
in baboon life-history and group size tend to focus on
variation in a few key climatic variables, such as
average temperature, mean annual rainfall, and
rainfall seasonality [Barrett et al., 2006; Dunbar
1992, 1996; Hill et al., 2000; Williamson & Dunbar,
1999]. Rainfall is a reliable indicator of plant
productivity, and therefore of resource availability,
in both tropical [Deshmukh, 1984] and temperate
[Knapp & Smith, 2001] grasslands, and may be key
in indirectly determining female condition, and
hence fertility [e.g. orang-utans, Knott, 2005]. Consistent with this, Lycett et al. [1999] showed that
patterns of rainfall correlate positively with the
likelihood of conception in baboons at Drakensberg,
and suggested that food availability mediates this
link via female condition, although seasonal changes
in temperature may also be important. There is also
evidence that periods of drought reduce the likelihood of conception and increase the likelihood of
fetal loss at Amboseli [Beehner et al., 2006], and food
scarcity has been linked to increases in infant and
juvenile mortality at Amboseli [Altmann et al., 1985],
and De Hoop [Barrett & Henzi, 2000].
The first major comparative analyses of baboon
ecology came from Dunbar [1992, 1996; Williamson &
Dunbar, 1999] who used annual temperature, rainfall,
and rainfall diversity to explain likely minimum
feeding and traveling requirements in different environments, and then used the constraints posed by
these to investigate the maximum group sizes that
could be maintained when the available time is
directed toward social relationships. These comparative analyses of group size and activity were followed
by a comparative model of inter-birth intervals. Hill
et al. [2000] used data from 14 field sites (of which 13
were in East or southern Africa), and showed that the
number of group females and mean annual temperature explain 84% of the variance in inter-birth
intervals across baboon populations, with number of
females showing a significant quadratic relationship
with rainfall. However, this inter-site analysis found
no relationship between inter-birth interval and
Am. J. Primatol.
absolute measures of rainfall. In a separate comparative analysis, Barrett et al. [2006], taking data from
ten East and southern African sites, correlated
inter-birth intervals and infant mortality with an
index of habitat productivity and seasonality.
They argued that in less productive, but more
seasonal habitats, baboon populations are more likely
to have seasonal birth peaks, reducing the likelihood
that infant weaning occurs at a difficult time for
infants to sustain independence [Barrett et al., 2006].
Thus, rainfall is an important correlate of life-history
in baboons, but seasonality of rainfall may be as
important as total annual rainfall.
Although there are a large number of baboon
field sites from which long-term data are available
for forming and testing comparative models, there
are few such studies from wet, forested sites. Olive
baboons are the most common type found in forests,
although this may be a temporary expansion
[Kingdon, 1997], and all baboons appear to be
excluded from most of the wet, closed forests of
Central and West Africa. Kingdon [1997] speculated
that ecological pressures, such as disease and
competition, may limit the success of baboons in
these environments, and some authors have suggested that the opening up of forests for agriculture
[Tappen, 1960; Greenhood, 1971], may have enabled
baboons to extend their range into areas from which
they would otherwise have been excluded. However,
an understanding of the factors that may limit the
distribution of baboons in the equatorial forest zone
is currently lacking. Our study helps fill this need, by
presenting the first life-history and group size data
for forest baboons in west-central Africa. We provide
data for two troops at GGNP, one of which is wildfeeding (Kwano troop), whereas the other (Gamgam
troop) supplements its diet via crop-raiding [Warren
et al., 2007]. Many studies have demonstrated that
the consumption of anthropogenic foodstuffs can
have major effects on life-history parameters and
demography in primates [e.g. chimpanzees, Goodall,
1983; Japanese macaques, Mori et al., 1997; Sugiyama and Oshawa; Indian langurs, Borries et al., 1991;
Barbary macaques, Fa, 1984; baboons, Altmann
et al., 1978; Strum, 1991], and we look for such
relationships here. In setting data from the wildfeeding Kwano troop into context, we investigate
whether our data fit with predictions from baboon
models and comparative relationships suggested by
Dunbar [1992, 1996], Hill et al. [2000], and Barrett
et al. [2006].
METHODS
Study Site
GGNP is on the eastern border of
to the southern edge of western
P. hamadrayas anubis distribution
habituated two troops, one (Kwano
Nigeria, close
extension of
(Fig. 1). We
troop) inside
Life-History of Wild Olive Baboons / 3
the park at the Gashaka Primate Project field station
at Kwano [Sommer et al., 2004], and the other 10 km
away on the edge of the park, close to the village of
Gashaka, along the banks of the river Gam Gam
(Gamgam troop). Both sites lie in the forest–grassland transition zone, and hence contain some
elements of both habitat types. However, Kwano
troop home range has substantially more lowland
and gallery rainforest (65%) than guinea savannah
woodland (35%), whereas the reverse is true for
Gamgam troop [15% forest, 70% guinea savannah
woodland, 15% crop-land and elephant grass;
Warren, 2003]. Gamgam troop’s home range is
consequently much more open than Kwano troop’s,
receives much greater and more intense grass
burning during the dry season, and is also heavily
grazed by the cattle of nomadic Fulani at certain
times of year. In addition to these habitat differences, Gamgam troop regularly supplements its diet
with maize and a variety of other crops taken directly
from farms along the banks of the river [Warren
et al., 2007].
Among baboon field sites, GGNP is an extreme
outlier with regards to rainfall, and Kwano represents the wettest of all baboon study sites to date.
Average
annual
rainfall
(x ¼ 2022 mm
for
2001–2006, data from Gashaka Primate Project
weather station) is around 3.5 SDs above the mean
of the 14 baboon sites listed in Hill et al. [2000]
(x ¼ 693 mm,
SD 5 399).
Kwano’s
mean
temperature, 26.41C, is also high, being greater than
1 SD above the mean in Hill et al. [2000] (x ¼ 22:1 C,
Fig. 1. Position of Gashaka-Gumti National Park (GGNP,
square) with respect to 31 other baboon field sites (circles) used
by Dunbar [1992] to develop his model of baboon behavior.
Adapted from Dunbar [1992], with approximate olive baboon
range (gray shading) added from Kingdon [1997]. The olive
baboon range is bounded in the North-East and South-East by
the presence of hamadryas and yellow baboons respectively, in
the North by the sahara, in the West by the presence of guinea
baboons, and in the South and South-West by high rainfall and
associated closed forests. GGNP is close to the southern edge of
the western extension of the olive baboon range.
SD 5 3.8). The habitat of GGNP, especially the large
closed forests in Kwano troop’s home range, is also
unusual for baboons, which are found more commonly in savannah habitats, and are certainly much
better studied in such environments.
Troop Sizes
Censusing was undertaken to obtain data on
baboon troop sizes at GGNP between March and July
2006 [as in Altmann et al., 1985; Samuels and
Altmann, 1991]. Censusing of troops (total n 5 22)
by an experienced field assistant took place around
the Kwano, Gashaka, and Selbe areas. Three counts
of individuals in age–sex classes in each troop were
taken, each separated by a minimum of 30 min.
Home range areas and distinguishing features of
individuals in troops were noted to prevent accidental
re-sampling.
Monitoring and Measuring Life-History
We started habituation of the two study troops
in 2000, and the first birth dates used in our analysis
come from December 2000. At the start of the study
period, modal Kwano troop size was 28, whereas
modal Gamgam troop size was 14. At the start of full
data collection in March 2001, all adult troop
members were known individually, as were many
juveniles and infants. From March 2001 until May
2002, field assistants followed rotating focal individuals from both troops for 8 days a month. From May
2002 until November 2003, field assistants followed
focal individuals for 20 days a month in Kwano troop,
but there was no regular work undertaken with
Gamgam troop, and only an occasional census used
to ascertain whether all group members were still
present, and whether new infants had been born.
Since December 2003, field assistants have attempted to follow focal individuals in both troops
for a minimum of 20 days a month, and for up to 26
days a month. As such, records are completely
continuous for Kwano troop, but there is less
continuity for Gamgam troop. Data collected include
the presence or absence of troop members, details of
age–sex classes, births, deaths, signs of illness,
wounds and female reproductive state according to
the following scheme [Higham et al., 2007; 2008]:
Lactating—suckling an infant; Pregnant—not cycling and showing the pregnancy signs [Altmann,
1973]; S0—cycling with no swelling; S1—cycling
with a small swelling of the ano-genital area
(AGA); S2—cycling with a medium–large swelling
of the AGA and a small swelling of the Para-Callosal
Skin (PCS); S3—cycling with a large swelling of the
AGA and full swelling of the PCS.
For both troops, a number of life-history parameters were estimated (Table I). Owing to less
continuity in data collection for Gamgam troop
compared with Kwano troop, (see above) there is
Am. J. Primatol.
4 / Higham et al.
TABLE I. Definitions of Life-History Parameters
Parameter
Unit
Definition
Length of postpartum amenorrhea (PPA)
Length of post infant death amenorrhea (PIDA)
Duration of cycling (when infant survived) (DC)
Post infant death duration of cycling (PIDDC)
Gestation length (G)
Months
Months
Months
Months
Days
Cycle length
Days
Observed inter-birth interval
Months
Observed inter-birth interval post infant death
Months
Inter-birth interval
Infant mortality
Months
%
Group size
No.
Time from birth until the first day of sexual swelling
Time from infant death until the first day of sexual swelling
Duration of cycling from end of PPA to conception
Duration of cycling from end of PIDA to conception
Using measures of fecal hormones to estimate ovulation date
(Higham et al. 2008), time from date of probable conceptive
ovulation to birth date
Using measures of fecal hormones to estimate ovulation date
(Higham et al. 2008), time between successive estimated
ovulation dates
Inter-birth interval when two consecutive birth dates for a given
female are known, and where the first infant survived and was
successfully weaned
Inter-birth interval when two consecutive birth dates for a given
female are known and the former infant died o12 months. For
other sites, this figure was calculated by (PIDA1PIDDC1G).
When PIDDC was not available, DC was used
(PPA1DC1G)
Births resulting in death o12 months old as a percentage
of all births
Modal group size of the troop.
less confidence in some of the data. Data are not
presented where there is uncertainty about their
accuracy; thus sample sizes for Gamgam troop are
lower. Age specific mortality was calculated [following Altmann et al., 1977] for infants up to 12 months
old only as, for several years of the study, individual
identification of juveniles in the two troops was
incomplete. We document birth seasonality in both
troops, and present a number of other life-history
parameters, which focus on the inter-birth interval.
Inter-birth intervals have been estimated in very
different ways across studies. Altmann et al. [1977]
calculated the inter-birth interval by adding together
the mean values of each of its constituent parts
(length of postpartum amenorrhea, duration of
cycling to conception, and gestation length). Other
researchers [e.g. Bentley-Condit & Smith, 1997; Sigg
et al., 1982] used observed inter-birth intervals only,
i.e. the interval between consecutive births, with
successful rearing and weaning of the first infant.
Lycett et al. [1998] estimated the inter-birth interval
by multiplying the number of adult females by the
number of monitored years and then dividing by the
number of births. Although we follow Altmann et al.
[1977], we report the observed inter-birth interval
additionally. Estimates are provided of gestation and
cycle lengths using ovulation dates estimated from
fecal hormones measures [Higham et al., 2008],
which are likely to be more accurate than estimates
made from observation of sexual swellings. We aimed
to collect fecal samples every 1–2 days from individual females for the measurement of fecal estrogen
and progestogen levels, and these two hormone
metabolite measures were combined to estimate
Am. J. Primatol.
ovulation dates in individual cycles [see Higham
et al., 2008].
When presenting our data, we also give previously published values from several sites that have
presented similar and directly comparable data.
These sites are Amboseli, Kenya [Altmann et al.,
1977; Altmann, 1980]; Mchelelo, Kenya [BentleyCondit & Smith, 1997]; Gilgil, Kenya [Smuts &
Nicholson, 1989]; and Erer, Ethiopia [Sigg et al.,
1982]. As this sample represents a relatively limited
range of the available comparative data, we compare
our values for GGNP group sizes and inter-birth
intervals from the wild-feeding Kwano troop statistically with multi-group datasets published by Hill
et al. [2000] and Barrett et al. [2006], using onesample t-tests (SPSS 15). We then use our data to
test previously suggested comparative baboon models and relationships [Barrett et al., 2006; Dunbar,
1992, 1996; Hill et al., 2000].
Comparison of Kwano and Gamgam troop LifeHistory
Where sample sizes were sufficient to enable
statistical analyses, independent sample t-tests
(SPSS 14.0) were used to compare life-history
parameters between Kwano and Gamgam troops.
We also compare birth-seasonality in the two troops.
Testing Comparative Relationships
As we estimate infant mortality up to 12 months
only (compared with the more common 24 months,
see above), and infant deaths in Kwano troop were
clustered during the study period, suggesting that
Life-History of Wild Olive Baboons / 5
our estimates of mortality may need revision in the
future, we do not use our mortality data to test
suggested comparative relationships of baboon mortality. In addition, we do not use data from the foodenhanced Gamgam troop in such comparisons.
Instead, we focus on testing comparative relationships using inter-birth interval data from the wildfeeding Kwano troop, and troop size data obtained
during the census.
Dunbar [1992, 1996] and Williamson and
Dunbar [1999] published models of baboon behavior
that predict maximum ecologically tolerable and
minimum ecologically permissible troop sizes for
areas with different mean ambient temperatures and
mean annual rainfall. We used the published tables
of these predictions in Dunbar [1996] to see whether
the troop sizes measured in our census fit within
Dunbar’s suggested range. We used the points in the
table that most closely approximated the climate at
Kwano, which were a mean annual rainfall of
2100 mm (compared with 2022 mm for Kwano over
the study period), and a mean annual temperature of
251C (compared with 26.41C for Kwano over the
study period).
We compared our estimates of inter-birth interval with predicted values for our study population
derived from Hill et al. [2000], who showed that
inter-birth intervals in baboon populations could be
predicted by mean temperature and number of troop
females, with the relationship described by the
following regression equation:
lnðIBIÞ ¼ 20:736 2:914 lnðFÞ þ 0:553½lnðFÞ2
8:953 lnðTÞ þ 1:452½lnðTÞ2
where T is the mean annual temperature, and F the
mean number of troop females.
We used the Kwano mean temperature (26.41C),
and the mean number of troop females measured in
our GGNP census. We tested the model additionally
using mean number of troop females in the Kwano
area only.
Finally, we looked at the relationship proposed
by Barrett et al. [2006] between inter-birth intervals
and a measure of habitat productivity, P42t [from le
Houréau, 1984 cited in Barrett et al., 2006], which
represents the number of months in which precipitation (in mm) is greater than twice the mean annual
temperature (in 1C). For Kwano this figure is 7.
Barrett et al. [2006] suggested that this index can be
related to the inter-birth interval, with a close to
significant positive relationship between inter-birth
intervals and P42t when the outlying Drakensberg
population is removed from the analysis. We investigate whether data from Gashaka are consistent
with this proposed relationship or whether, like
Drakensberg, Gashaka does not appear to fit this
pattern.
Research Ethics
All research protocols followed were assessed
and approved by Roehampton University’s Research
Degrees Board, which included ethical approval, and
adhered to all legal requirements of both Nigeria and
the UK.
RESULTS
Troop sizes for GGNP are presented in Table II.
The mean GGNP troop size is significantly smaller
than troop sizes at 14 other study sites [Hill et al.,
2000] (t 5 6.22, df 5 13, Po0.001)
Table III presents data on life-history of Kwano
and Gamgam troops; here we focus on the lifehistory of the wild-feeding Kwano troop.
Kwano Life-History
Inter-birth intervals at Kwano (29.9 months,
calculated from constituent means, see Table I) are
long, being significantly longer than the sample of 11
sites given in Barrett et al. [2006] (t 5 3.0, df 5 10,
P 5 0.013), and higher than all sites yet studied bar
the outlying Drakensberg [38.5, Lycett et al., 1998;
Barrett et al., 2006]. Inter-birth intervals are
reduced in Kwano troop following infant death
(t 5 2.8, df 5 5, P 5 0.036), even given wide variation in the age at which infants died (0–9 months).
This reduction comes from a reduction in duration of
cycling (t 5 6.2, df 5 10, Po0.001). The observed
inter-birth interval of 25.0 months is based on just
two observations, owing to high infant mortality in
Kwano, and hence few cases in which females with a
surviving infant went on to have second offspring,
with both birth dates accurately known.
Kwano troop suffered high infant mortality
compared with other sites (Fig. 2), and most of the
nine infant deaths were clustered in time. Four
infants died in October 2004, at the peak of the
wettest rainy season recorded to date, with 2337 mm,
around 16% higher than the Kwano average
(x ¼ 2022 mm). We also recorded two infant deaths
in January 2003, shortly after a group takeover, in
which an immigrant male chased and harassed group
females before becoming the new dominant male.
TABLE II. Mean Troop Sizes in Three Different
Areas of GGNP
Troop size
Area
Kwano
Gashaka
Selbe
Overall
Number of females
Mean
SD
Mean
SD
No. of troops 5
22.3
21.2
19.4
20.7
6.5
3.6
6.5
5.1
5.4
4.5
5.6
5.0
1.0
1.4
0.9
1.2
7
5
10
22
Am. J. Primatol.
Am. J. Primatol.
4.0
3.5
2.8
5.1
n/a
n/a
n/a
185.3
42.3
25.0
13.8
29.9
47%
27d
anubis
Type
180–188
39–46
23-27
8–21b
n/a
n/a
26–28
7–17
0–4
10–16
1–8
Range
4
3
2
5
n/a
19c
n/a
7
8
5
7
n
1.5
9.3
anubis
188–192
42.3
16.0
–
16.5
6.3%
14–21
–
–
Mean
n/a
2.3
1.2
–
n/a
n/a
n/a
1.0
–
0.7
–
SD
n/a
41–45
15–17
–
n/a
n/a
14–21
8–10
–
12
–
Range
Gamgam troop
Data converted from days to months where appropriate. N values given are incidences not females.
a
Median cycle length.
b
Wide range owing to variation in age at which infants died.
c
Total number of known births.
d
Modal group size throughout study period.
e
Mean derived from Table II in Altmann (1980).
f
Mean of three bands that made up Cone Rock Troop in 1974 (236/3).
References
4.8
1.5
2.3
2.6
SD
11.3
1.4
12.4
3.4
Mean
Postpartum amenorrhea
Post infant death amenorrhea
Duration of cycling
Post infant death duration
of cycling
Gestation length
Cycle length
Observed inter-birth interval
Post infant death
Inter-birth interval
Infant mortality
Group size
Parameter
Kwano troop
1
3
4
–
n/a
16c
n/a
4
–
2
–
n
[Altmann et al.,
1977; Altmann, 1980]
cynocephalus
175
32–34
21
10.9
22
33%
45e
12
0.8
4
–
Mean
Amboseli
(Alto’s troop)
[Bentley-Condit
& Smith, 1997]
cynocephalus
181.5
38.9
27.9
12.8
24.5
12%
79.6
14.6
1.9
4.9
–
Mean
Mchelelo
TABLE III. Life-History Parameter Estimates of Kwano and Gamgam Troops, Compared With Some Other Sites
[Smuts &
Nicolson, 1989]
anubis
180.2
42a
25.0
11.8
24.9
22%
115–135
13.4
1.0
5.6
4.9
Mean
Gilgil
[Sigg et al.,
1982]
hamadryas
–
–
24
–
–
18%
78.7f
14
1
–
3.5
Mean
Erer
6 / Higham et al.
7
7
3
6
1
0
3
3
0
4
3
19
21
4
5
0
No data
0
0
4
4
14
2000–2002
2002–2003
2003–2005
2005–2006
Neither gestation length (t 5 1.1, df 5 3,
P 5 0.367) nor cycle length (t5 5 0.2, P 5 0.988)
differed between the two troops. Inter-birth intervals
were shorter in Gamgam than in Kwano (t 5 6.0,
df 5 4, P 5 0.004). Although length of postpartum
amenorrhea was shorter in Gamgam compared with
Kwano, this was not significant (t 5 0.8, df 5 9,
P 5 0.429), and instead, reduced inter-birth intervals
were largely the result of reduced duration of cycling
(t 5 6.3, df 5 5, P 5 0.002). Although Gamgam troop
is smaller than Kwano troop it increased in size by
50% between 2000 and 2006, whereas Kwano troop
size remained static (Table IV). Infant mortality in
Kwano was high compared with Gamgam (Fig. 2),
where the only known infant death o12 months was
that of a twin. No adult females have died or
disappeared in Gamgam troop since fieldwork began
in 2000, though one known adult male death
occurred in Gamgam troop in 2005, after a farmer
inflicted serious wounds on the individual during
crop-raiding.
Y. Warren
J. Adanu
J. Higham
E. Ey
Comparison of Kwano and Gamgam Troops
TABLE IV. Change in Modal Troop Size and Composition Over Four Fieldwork Phases
Both of these infant deaths occurred during or after
chases of the mothers.
Four adult females disappeared in Kwano,
including one during the 2004 heavy rains. Disappearances all occurred after females were seen
struggling with obvious and debilitating disease
symptoms, which included visible external growths
on the abdomen, and severe loss of fur. Other
females have been observed with symptoms such as
heavy fur loss during the study period, but have
recovered. On one female disappearance, her infant
also vanished, whereas on another, an infant died
before the mother disappeared, and on a third a
female was heavily pregnant when she disappeared.
Adult
males
Fig. 2. Survivorship curve for Kwano and Gamgam troops,
presented with published data from Amboseli [Altmann, 1980],
and Mchelelo [Bentley-Condit & Smith, 1997]. The only known
infant death o12 months of age in Gamgam was a twin (born
19th August 2004) that died; the other survived.
8
8
4
5
12
Gamgam
troop size
10
Subadult
females Juvenile Infant
8
Adult Subadult
females
males
6
Age in months
Adult
males
4
Kwano
troop size
2
Fieldwork
years
0
5
4
3
6
0.0
2
1
5
3
Amboseli (Alto's Troop)
Mchelelo
Gamgam Troop
Kwano Troop
0.2
0
1
2
2
Adult Subadult
females
males
0.4
7
7
6
7
0.6
Study
Survivorship
0.8
6
6
6
3
1.0
28
27
26
26
Subadult
females Juvenile Infant
Life-History of Wild Olive Baboons / 7
Am. J. Primatol.
8 / Higham et al.
There is no clear evidence of birth seasonality in
Kwano troop with births observed in all months
except April (Fig. 3a), but Gamgam troop possibly
shows a birth peak 6 months (approximate gestation
length) after wet season crop-raiding (Fig. 3b),
although sample sizes are too small to test for the
significance of this pattern.
Testing Comparative Relationships
The models developed by Dunbar [1996, following Dunbar, 1992], produce estimates of maximum
ecologically tolerable and minimum ecologically
permissible troop sizes of 53 and 13 respectively for
baboons living in an area with rainfall at 2100 mm
per year and a mean ambient temperature of 251C.
The troop sizes observed in our census (Table II), as
well as our study troop sizes, fall within, but toward
the lower end of, the range suggested by Dunbar’s
[1996] model.
Hill et al.’s [2000] regression model predicts an
inter-birth interval of 41.7 months for GGNP
baboons, and 38.1 months for Kwano baboons
5
400
Kwano Rainfall
Kwano Births
Rainfall (mm)
3
200
2
100
Number of known births
4
300
Apr
May
Jun
Jul
(a)
Aug
Sep
Oct
Nov
Dec
Jan
0
Feb
Month
500
5
4
300
3
200
2
100
1
0
Mar
Apr
May
(b)
Jun
Jul
Aug
Sep
Oct
Nov
Dec
Jan
Number of known births
Rainfall (mm)
Crop raiding
Gamgam Rainfall
Gamgam Births
400
0
Feb
Month
Fig. 3. Birth seasonality and rainfall, 2001–2006 for Kwano troop
(a) and 2000–2006 for Gamgam troop (b), with periods of cropraiding indicated for the latter. Data are orientated such that the
X-axis starts at the beginning of the wet season and ends at the
close of the dry season.
Am. J. Primatol.
DISCUSSION
The geographic, habitat, and climatic characteristics of GGNP make troop size and life-history data
particularly important for understanding interpopulation differences in baboon life-history. A
number of features of GGNP baboons, such as long
durations of cycling to conception and small group
sizes, differ from characteristics of East and southern African baboon populations. In addition, values
for Kwano and Gamgam troops differ, reflecting
effects of food enhancement.
Troop Sizes
Troop sizes at GGNP are significantly smaller
than at most other sites studied to date. However,
other populations have shown similarly small group
sizes, including Drakensberg [x ¼ 22:5, n 5 61; Henzi
and Lycett, 1995], Mulu [22, Dunbar, 1992] and Bole
[19, Dunbar, 1992], while recent data from Comoé,
Côte d’Ivoire, also show small troop sizes [average 15
individuals, Kunz & Linsenmair, 2008].
Kwano Life-History
1
0
Mar
specifically; much longer than the 29.9 months
actually found.
Barrett et al. [2006] found a relationship
between inter-birth interval and P42t that was
non-significant when Drakensberg is included
(P 5 0.658), but close to significance when it is not
(P 5 0.059). When Kwano is added to this dataset,
this relationship is not significant, whether Drakensberg is included (r2 5 0.025, F1,9 5 0.230, P 5 0.643)
or not (r2 5 0.239, F1,8 5 2.511, P 5 0.152).
Kwano inter-birth intervals are longer than
those at all other sites bar the outlying seasonally
breeding Drakensberg population [Barrett et al.,
2006; Lycett et al., 1998]. The long duration of
cycling observed in Kwano troop is curious, as
females apparently exhibit swellings for significant
periods without conceiving, and it is unclear why
females should do this when instead they could
extend the period of postpartum amenorrhea and
avoid the costs of exhibiting swellings. A similar
phenomenon, in which females apparently exhibit
swellings for long periods before conception, has
been documented in, for example, hamadryas baboons [Colmenares & Gomendio, 1988], mandrills
[Hadidian & Bernstein, 1979], and macaques [e.g.
pig-tailed, Hadidian & Bernstein, 1979]. The function of swellings in such circumstances has often
been related to infanticide avoidance; by exhibiting
swellings, a female may reduce the probability of a
male committing infanticide to hasten estrus. Indeed, captive hamadryas baboon females shorten the
length of postpartum amenorrhea when faced with a
new alpha male following a takeover [Zinner &
Life-History of Wild Olive Baboons / 9
Deschner, 2000], indicating that swellings may help
avert infanticide by offering incoming males mating
opportunities. Similar observations have also been
made in gelada, in which females exhibit swelling
sooner in the presence of unfamiliar males [Dunbar,
1980]. In these scenarios it is usually assumed that
cycles are ‘deceptive’ [Takahata et al., 1996], falsely
advertising ovulation when the female is actually
anovulatory. From observational data it is impossible
to tell whether swellings are always associated with
ovulation. However, hormonal analyses of Kwano
troop female cycles have always detected ovulation
when sampling frequency was sufficient [Higham,
2006], although we have not targeted the first
swelling following postpartum amenorrhea for study,
leaving open the possibility that they are anovulatory. Additionally, it is interesting to note that
differences in duration of cycling between GGNP
baboons and East African populations mirror patterns in chimpanzees, with West African chimpanzees having significantly longer durations of cycling
before conception than East African [Deschner &
Boesch, 2007]. It is also possible that long durations
of cycling in some West African primates are more
related to environmental factors than to social
factors such as infanticide prevention. For example,
we found that consumption of one specific food type,
Vitex doniana, can interfere with cycling function,
and prevent swelling expression [Higham et al.,
2007].
Infant mortality under 12 months was high in
Kwano troop, even higher than the 38% seen at
Moremi, where infanticide and predation risks are
severe [Cheney et al., 2004]. The occurrence of both a
dominant male takeover (2003), and a wet season of
exceptionally high rainfall (2004), may help to
explain why recorded infant mortality was especially
high during the study period.
Comparison of Kwano and Gamgam Troops
We found a number of significant differences
between Kwano and Gamgam troops that can be
linked to food enhancement. Gamgam troop had
significantly shorter intervals than Kwano troop, not
derived from a shorter length of postpartum amenorrhea, but rather a reduced duration of cycling.
This contrasts with a study of captive olive baboons,
in which inter-birth intervals were reduced by 60%
compared with the wild, yet mean duration of cycling
was 4.16 months, similar to that seen in the wild for
many baboon populations [Garcia et al., 2006]. Interbirth intervals were instead short owing to a reduced
period of postpartum amenorrhea [x ¼ 4:77 months;
Garcia et al., 2006].
Infant mortality in Kwano troop was much
higher than in Gamgam troop. The only death
recorded in the first 12 months of life in Gamgam
troop was that of a twin. Twins born on 18th August
2004 are one of the only sets of twins ever recorded in
wild baboons, and the survival of both individuals
was never likely [Alberts & Altmann, 2006]. Lower
mortality in Gamgam troop may be related not only
to the nutritional advantages of crop-raiding by this
troop, but also to lower rainfall, which was, on
average, 5% higher in Kwano than Gamgam. Moreover, in the year of very high rainfall (2004), which
was associated with multiple infant deaths in Kwano
troop, Kwano rainfall was some 570 mm (32%)
higher than that of Gamgam.
Kwano troop did not show evidence of birth
seasonality despite highly seasonal patterns of rainfall that are both consistent in volume and reliable in
timing. Seasonal birth peaks in baboon populations
are often linked to rainfall and consequent patterns
of food availability. For example, at Amboseli, a peak
occurs in June–July [Altmann, 1980], whereas at
Mchelelo, peaks are seen in September–October and
January–February [Bentley-Condit & Smith, 1997].
At Moremi, although births occur throughout the
year, 76% are between July and December [Cheney
et al., 2004], whereas at Drakensberg, 86% occur
during the rains [October–March; Lycett et al.,
1999]. In the wet forests of Kwano, productivity is
relatively high all year round, perhaps weakening
the link between rainfall and food availability that is
critical to these relationships between food availability and seasonality. If females are most likely to
conceive during periods of plentiful food [as
suggested by, e.g. Beehner et al., 2006; Cheney
et al., 2004; Lycett et al., 1999], then seasonal cropraiding may induce seasonal breeding in Gamgam
troop (Fig. 3).
Testing Comparative Relationships
Our data fit with some of the comparative
relationships suggested by some authors, but not
others. Firstly, our troop size data are within the
range of group sizes suggested by Dunbar’s comparative behavior-based model [1992, 1996], but this
model predicts a maximum ecologically tolerable
group size of around 53—far in excess of any troops
seen in the region. Dunbar’s [1992, 1996] model is
based on the premise that time is a ‘‘hidden
constraint’’ on baboons, and that the amount of
time available to service social relationships after the
necessary requirements of foraging and traveling
time constrains group size. It is perhaps worth
considering whether high rainfall may provide an
additional constraint on available time. As the
Kwano troop do not travel or forage during heavy
rain, and as there are days during the wet season
when heavy rain occurs for the majority of the day,
this reduces substantially the amount of total time
available i.e. the effective day length. A necessary
consequence of this is that available time for serving
social relationships is also reduced substantially, and
Am. J. Primatol.
10 / Higham et al.
potential to reduce available foraging time substantially, and increase the potential for disease, creates
its own risk for infants that are making the
transition to independence.
In summary, previously published models do not
always adequately predict the life-history of West
African forest baboons. A combination of high rainfall and high fruit productivity in wet forests may
mean that the constraints on this population are not
always those assumed to be operating on baboons
living in drier and more open habitats. More detailed
studies of the effects of high rainfall and greater
levels of frugivory on baboon life-histories will help
us to understand better the environmental constraints acting on such populations.
hence the maximum group sizes that can be
sustained. Consideration of rainfall as a constraint
on time may also help explain why predictive models
of baboon distribution tend to predict that baboons
should be present in areas of high rainfall where they
actually are absent.
Hill et al.’s [2000] regression model does not
appear to predict inter-birth intervals accurately at
GGNP. This could be because the climatic conditions
found at GGNP are well outside the values for which
the model was parameterized. More recent comparative models being developed to estimate baboon
inter-birth intervals from climatic data apparently
do substantially better in predicting GGNP interbirth intervals accurately (Caroline Bettridge, personal communication). Barrett et al. [2006] argued that
the index of habitat productivity P42t may be
positively correlated with inter-birth intervals, with
longer inter-birth intervals as habitat productivity
increases and seasonality decreases, owing to increasing risk for infants in the transition to
independence in less seasonal habitats. Our study
does not appear to provide support for this suggestion, as the addition of data from the Kwano
population makes this comparative relationship
nonsignificant, even in the absence of data from
Drakensberg. We give two nonmutually exclusive
possible explanations for this. Firstly, owing to the
presence of large forests within their home range,
the Kwano troop have access to relatively high plant
productivity all year round, even given strong
seasonality in rainfall. In more arid habitats, there
is likely to be a closer link between rainfall and
productivity than is found at GGNP, such that
seasonality of rainfall is more important in proximately determining productivity in different months
of the year. Secondly, perhaps high rainfall, with its
Life-History and the Changing GGNP
Environment
Our data provide insight into the life-history of
baboons in an environment in which they are little
studied. High rainfall and closed forests found in
Kwano are associated with small group sizes, long
inter-birth intervals, and high infant mortality.
Together, these data are consistent with a population
living in an environment toward the edge of its
distributional limits. Possible factors contributing to
such limits include the increased disease risks
associated with wet and humid closed-canopy forests,
as well as competition from specialized forest
primates such as guenons, mangabeys, and apes,
and the reduced effective day length caused by high
rainfall (see above). The detected differences in lifehistory parameters between Kwano troop and Gamgam troop are pronounced, and can be linked to
environmental differences between Gamgam and
Kwano troop home ranges, including lower rainfall
TABLE V. Infant Survivorship Table for Kwano (K) and Gamgam (G) Troops
Age interval in
months x, x11
At birth
0, 1
1, 2
2, 3
3, 4
4, 5
5, 6
6, 7
7, 8
8, 9
9, 10
10, 11
11, 12
Sample size Nx
Mortality rate qx
Survival rate Px 5 1qx
Survival from full-term pregnancy to x11
K
G
K
G
K
G
K
G
19
18
16
14
14
12
12
12
12
11
10
10
10
16
16
15
15
15
15
15
15
15
15
15
15
15
0.05
0.11
0.13
0.00
0.14
0.00
0.00
0.00
0.08
0.09
0.00
0.00
0.00
0.00
0.06
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.95
0.89
0.87
1.00
0.86
1.00
1.00
1.00
0.92
0.91
1.00
1.00
1.00
1.00
0.94
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
0.95
0.84
0.74
0.74
0.68
0.68
0.68
0.68
0.63
0.53
0.53
0.53
0.53
1.00
0.94
0.94
0.94
0.94
0.94
0.94
0.94
0.94
0.94
0.94
0.94
0.94
Age interval represents month x to month x11. Sample size represents number of individuals at start of each month x. Mortality rate qx was calculated as
the number of individuals who died during that interval as a proportion of the number of individuals in the sample for that interval. Survival rate is 1—the
mortality rate.
Am. J. Primatol.
Life-History of Wild Olive Baboons / 11
in Gamgam troop range, reduced forest cover and
greater predominance of savannah, and the presence
of agricultural land. Although Gashaka is in the
forest–savannah transition zone, much of the savannah may be derived as a result of anthropogenic
impact. As such, human habitat modification at
Gashaka, largely related to the removal of forests,
increase in the regularity and intensity of grass
burning, and the planting of crops, appears to have
beneficial consequences for baboons. Environments
such as those found in Gamgam troop’s range are
becoming more common in the region, as in all West
and central Africa. The effects of this are twofold.
Firstly, the closed forests in which baboons are
absent are being opened up and/or destroyed,
changing habitat conditions such that they are more
similar to those seen in other parts of the baboon
distribution. Secondly, crops may significantly improve local food resources available to baboons.
These factors together may change the environmental pressures, that currently restrict baboon distribution in West and central Africa in ways that are
beneficial for baboons. This suggests that, should the
clearing of forests in these regions for agricultural
land continue, it may enable baboons to extend their
range into regions from which they are currently
excluded.
ACKNOWLEDGMENTS
Fieldwork benefited from a permit by the
Nigerian National Parks Service to the Gashaka
Primate Project, which receives its core funding from
the Chester Zoo Nigeria Biodiversity Programme.
NCF/WWF-UK provided logistical support. Bobbo
Buba, Halidu Ilyusu, Buba Bello, Nuhu Husseini,
Haruna, Elodie Ey, Helen Cross, and Alejandra
Pascual Garrido helped to collect data in the field.
Martin Evans assisted with preparation of Figure 1,
and Stuart Semple, Anthony Di Fiore, Peter Henzi,
and one anonymous reviewer gave valuable
comments on a previous version of the manuscript.
Funding came from Roehampton University, with
additional funding from The Leakey Trust, Primate
Society of Great Britain, NUMICO Research B.V.,
British Federation of Women Graduates and
the International Federation of Animal Welfare.
Research complied with all applicable animal care
regulations and laws, including the ethical guidelines
for the treatment of animals of the American Society
of Primatologists, and the UK Home Office Animals
(Scientific Procedures) Act 1986. This is GPP
publication number 68.
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