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Physical maturation life-history classes and age estimates of free-ranging western gorillasЧinsights from Mbeli Bai Republic of Congo.

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American Journal of Primatology 71:106–119 (2009)
RESEARCH ARTICLE
Physical Maturation, Life-History Classes and Age Estimates of Free-Ranging
Western Gorillas—Insights From Mbeli Bai, Republic of Congo
THOMAS BREUER1,2, MIREILLE BREUER-NDOUNDOU HOCKEMBA2, CLAUDIA OLEJNICZAK3,
RICHARD J. PARNELL4, AND EMMA J. STOKES4
1
Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
2
Mbeli Bai Study, Wildlife Conservation Society—Congo Program, Brazzaville, Republic of Congo
3
Department of Anthropology, Washington University, St. Louis, Missouri
4
Wildlife Conservation Society, Bronx, New York
Physical maturation and life-history parameters are seen as evolutionary adaptations to different
ecological and social conditions. Comparison of life-history patterns of closely related species living in
diverse environments helps to evaluate the validity of these assumptions but empirical data are lacking.
The two gorilla species exhibit substantial differences in their environment, which allows investigation
into the role of increased frugivory in shaping western gorilla life histories. We present behavioral and
morphological data on western gorilla physical maturation and life-history parameters from a 12.5-year
study at Mbeli Bai, a forest clearing in the Nouabalé-Ndoki National Park in northern Congo. We assign
photographs of known individuals to different life-history classes and propose new age boundaries for lifehistory classes in western gorillas, which can be used and tested at other western gorilla research sites.
Our results show that western gorillas are weaned at a later age compared with mountain gorillas and
indicate slower physical maturation of immatures. These findings support the risk-aversion hypothesis
for more frugivorous species. However, our methods need to be applied and tested with other gorilla
populations. The slow life histories of western gorillas could have major consequences for social structure,
mortality patterns and population growth rates that will affect recovery from population crashes of this
critically endangered species. We emphasize that long-term studies can provide crucial demographic and
life-history data that improve our understanding of life-history evolution and adaptation and help to
refine conservation strategies. Am. J. Primatol. 71:106–119, 2009.
r 2008 Wiley-Liss, Inc.
Key words: age estimation; development; western gorilla; life-history classes; long-term studies
INTRODUCTION
Life-history traits and physical maturation are
assumed to be the result of evolutionary adaptations
to various socioecological factors and are shaped by
differences in substrate use, body or brain size and
diet [e.g. Kappeler & Pereira, 2003; Leigh, 1994a,
2004; Ross & Jones, 1999; van Schaik & Deaner, 2003;
Walker et al., 2006]. Nutrition is an obvious factor
affecting primate life-history pace. For example, rates
of maturation and reproduction of wild animals are
considerably slower than those of animals under foodprovisioned conditions [e.g. Altmann & Alberts, 2005;
Leigh, 1994b; Sigg et al., 1982; Strum, 1991; Zihlman
et al., 2007]. Spreading the metabolic needs for
juvenile (JUV) maturation over a longer period
(growth at a slow rate) in environments with poorer
and unstable or unpredictable food availability will
help to reduce the risks of starvation, primarily
resulting from intraspecific feeding competition [Janson & van Schaik, 1993]. Hence this ‘‘risk-aversion’’
hypothesis assumes that feeding on seasonally available resources, such as ripe fruit, will result in
prolonged periods of JUV maturation, and feeding
r 2008 Wiley-Liss, Inc.
on leaves that are assumed to be an abundant and
predictable resource is expected to speed up the
life-history pace of primates.
Empirical evidence for the risk-aversion hypothesis
has been equivocal [Leigh, 1994a; Ross & Jones, 1999;
Wich et al., 2004, 2007]. For example, Leigh [1994a]
demonstrated that more folivorous anthropoid primates
Contract grant sponsors: Brevard Zoo; Chicago Zoological
Society; Columbus Zoo and Aquarium; Cincinnati Zoo and
Botanical Garden; Sea World and Busch Gardens Conservation
Fund; Toronto Zoo; Wildlife Conservation Society; Woodland
Park Zoo; Little Rock Zoo; Lincoln Park Zoo; Zoological Society
of Milwaukee County Global Environmental Facility CongoPROGEAP; Louis Leakey Foundation; Wenner-Gren Foundation; German Academic Exchange Service (DAAD); Max Planck
Society.
Correspondence to: Thomas Breuer, Department of Primatology, Max Planck Institute for Evolutionary Anthropology,
Deutscher Platz 6, D-04103 Leipzig, Germany.
E-mail: breuer@eva.mpg.de
Received 18 March 2008; revised 15 September 2008; revision
accepted 17 September 2008
DOI 10.1002/ajp.20628
Published online 10 November 2008 in Wiley InterScience (www.
interscience.wiley.com).
Western Gorilla Maturation and Life History Classes / 107
have rapid growth rates in the earlier stages of ontogeny
and cease growth earlier than nonfolivorous species and
postulated a relationship between life-history pace and
digestive system. Similarly, Godfrey et al. [2003] found
that folivorous primate species exhibit faster dental
development. In contrast the risk-aversion hypothesis
does not predict patterns of ontogenetic diversity in
small-bodied New World monkeys [Garber & Leigh,
1997] and folivorous indriids mature more slowly than
like-sized frugivorous lemurids [Godfrey et al., 2004].
Most of our knowledge about primate life-history
evolution has been gained through broad-scale interspecific studies [e.g. Lee, 1999; Ross & Jones, 1999].
However, some life-history traits (e.g. weaning age,
age at first reproduction or age at full body size) of a
given species also vary according to the ecological
conditions (phenotypic plasticity) [Lee & Kappeler,
2003]. Therefore, comparisons of closely related species
or populations living in different environments would
help to clarify the role of ecological factors in shaping
life-history parameters. However, with a few exceptions
[e.g. Altmann & Alberts, 2005; Barrett et al., 2006;
Borries et al., 2001], empirical data from closely
related species or populations of the same species are
missing. In this study we provide life-history data on
western gorillas (Gorilla gorilla) in order to investigate
whether increased frugivory can lead to differences in
life-history pace between closely related species within a
single genus.
Great apes mature slowly and have long life spans,
making it difficult to obtain life-history data from wild
populations [Knott, 2001] as most ape studies are too
short to cover all stages of the life cycle. Long-term
studies are therefore needed to provide detailed ape
life-history data for addressing such evolutionary and
ecological questions. Furthermore, population parameters and life-history data have important conservation implications in the light of the crisis now facing
great apes [Tutin et al., 2005].
Gorillas are the largest living primates and
they are primarily herbivores [Doran-Sheehy et al.,
2006; Robbins, 2007; Rogers et al., 2004]. According to the risk-aversion model, they are assumed to
mature much faster than other, more frugivorous
apes and an ontogenetic analysis of captive African
apes supports this assumption [Leigh & Shea,
1996]. Moreover, comparison of some life-history
parameters with free-ranging chimpanzees (Pan
troglodytes) and orangutans (Pongo spp.) supports
the hypothesis of faster maturation of species with
a more folivorous diet [Hill et al., 2001; Knott,
2001; Wich et al., 2004]. Our current knowledge
about gorilla life-history patterns comes predominantly from one high-altitude mountain gorilla
population and long-term study site (Karisoke
Research Center) located at the extreme range of
gorilla distribution in the Virunga Volcanoes
[summarized in Robbins, 2007]—with preliminary
data available on Grauer’s gorillas [Yamagiwa &
Kahekwa, 2001]. However, western gorilla habitat
differs from that of mountain gorillas: in lowland
forests terrestrial herbaceous vegetation occurs at
lower densities and is more patchily distributed
[e.g. Rogers et al., 2004]. Western gorillas are more
frugivorous than mountain gorillas with fruiting
trees being more abundant but showing large
seasonal variation in fruit availability [Masi,
2007; Rogers et al., 2004]. Differences in resource
availability combined with reduced folivory could
have direct effects on western gorilla development
leading to slower life histories [Doran & McNeilage, 2001] and particularly to a later weaning age.
If such differences in life-history patterns between western and mountain gorillas occur, then age
boundaries delimiting life-history classes (infants
(INF), juvenile (JUV), subadults (SAD), adults) should
consequently differ between the two gorilla species.
However, western gorilla researchers have typically
adopted age boundaries from mountain gorillas
(see Table I). This is simply owing to a lack of longterm field studies spanning a full generation meaning
that previous studies of western gorillas could only
accurately age immature gorillas that had been seen
since birth, e.g. those of 1–2 years (yr) (or gorillas of up
to 6 yr of age at Mbeli Bai) [Gatti et al., 2004;
Magliocca et al., 1999; Parnell, 2002a; Stokes et al.,
2003]. Moreover, in the early years of western gorilla
studies, researchers aged wild gorillas by making
comparisons with captive individuals, potentially leading to an underestimation of true age. Long-term
demographic data on known individuals provide the
ages associated with external and behavioral criteria
that demark the boundaries of life-history classes [e.g.
Altmann et al., 1981].
Here, we investigate whether the physical
maturation of western gorillas supports the riskaversion hypothesis and is slower than that of
mountain gorillas. Secondly, we aim to assign the
age boundaries for western gorilla life-history
classes, which have previously been impossible to
accurately define owing to the lack of long-term
studies, and introduce techniques that will help to
compare physical maturation between different
gorilla populations. Finally, we discuss the implications of our findings for the social structure,
population growth and conservation of western
lowland gorillas.
METHODS
Observations were made at Mbeli Bai, a 12.9 ha
large swampy clearing (‘‘bai’’ in the local language)
in the Nouabalé-Ndoki National Park, Republic of
Congo [see also Parnell, 2002a; Stokes et al., 2003].
This pristine protected area has never been logged
and no illegal human activities have been recorded in
the study area since the start of the Mbeli Bai study
in 1995 (following pilot studies in 1993 and 1994). We
Am. J. Primatol.
Am. J. Primatol.
Subadult
Juvenile
Infant
Age
category
Gorilla
beringei
beringei
Gorilla
beringei
graueri
Gorilla
gorilla
Gorilla gorilla
Gorilla
gorilla
An infant is carried
by a female for
prolonged periods and
remains closely
attached to the female
Schaller [1963],
Harcourt et al. [1980]
and Watts [1990]
Subadults have more A subadult is
slender bodies,
advanced beyond the
starting to show
juvenile period
secondary sexual
characteristics and
A juvenile is weaned No morphological
and more
description provided
independent but with in the references
a plump morphology,
remaining close to the
mother and carried
dorsally under
stressful situations
An infant is still
suckling and carried
by the mother
Gatti et al. [2004]a
Behavioral and morphological and life-history markers
This study This study
Harcourt
Watts [1990] Yamagiwa Magliocca Parnell [2002a],
et al. [1980]
and
et al.
Stokes et al. [2003],
and Harcourt
Kahekwa
[1999] Gatti et al. [2004]a
and Robbins et al.
and Stewart
[2001]
[2004]
[2007]
0–4 yr
0–4 yr
0–3 yr
0–3 yr
0–4 yr
An infant is an
0–3b yr
unweaned gorilla, still
suckling and riding
ventrally or dorsally.
Infants are
nutritionally
dependent on their
mother and do not
survive maternal
death. White
buttock tufts of
infants are very
obvious. Infants have
large heads in
relation to the
torso and possess
very dark hair
3–6 yr
4 yr to age at
4–7 yr
3–6 yr
3–6 yr
4–7.5 yr
Juveniles are weaned
first
gorillas that can
copulation
survive the death of
the mother but they
are occasionally seen
suckling but
predominantly
feeding on their own.
Juveniles are
occasionally riding
dorsally on the
mother’s back and are
often staying in close
proximity to the
mother
6–8 yr
7–10 yr
6–8 yr
6–8 yr
7.5–10 yr Subadult gorillas still
for
have slender
females
bodies and are much
7.5–11 yr smaller than adult
for males size but are mainly
Gorilla
beringei
beringei
TABLE I. Comparison of Age Boundaries of Life-History Classes and the Markers (Morphological Markers in Bold) Used for Those Classes in Wild
Western and Mountain Gorillas
108 / Breuer et al.
48 yr
Young
12–15c yr
silverback
Blackback 8–12 yr
Adult
female
10–13 yr
Over 13 yr –
Age at first
10–13 yr
copulation to
approximately
11–13 yr
Age at first
Over 10 yr Over 8 yr
labial swelling
(6–7 yr)
12–15 yr
8–12 yr
Over 8 yr
14–18 yr
11–14 yr
Over
10 yr
behavioral traits,
such as independence
from their group and
aggression (in the
case of males)
Nulliparous females An adult female has An adult female is
are slightly smaller
obvious nipples and persistently
than parous females developed breasts
transporting infant,
and can show small
has a round body and
sexual swellings. A
smooth curves,
parous female has
sagging breasts with
obvious elongated
long nipples
nipples and
developed breast
A blackback male is A blackback is similar A blackback is a
reaching or larger
in size or larger than female-sized gorilla
than the size of
an adult female, but with angular and
parous females.
with more developed muscular body with
Blackback males
musculature and red- conspicuous
(start to) show signs brownish backs
pectoralis major
of secondary sexual
muscle over which the
characters, such as
skin is usually taut
longer arm hair
and red-brownish
saddle and strong
neck muscles, but
these signs are not
yet fully developed
Young silverbacks are A silverback’s saddle A young silverback is
clearly larger than turns silver
silvering but not yet
parous females and
fully grown
reach adult male
body length.
However, their
secondary sexual
characters are
incompletely
developed. The
brownish saddle is
gray but not fully
silver and the
saddle hair is much
shorter than that
of adult females.
Their sagittal crest is
not yet fully
developed and they
are lacking a
silverline. Young
independent of the
mother. Females can
be seen with small
labial swellings
Western Gorilla Maturation and Life History Classes / 109
Am. J. Primatol.
Am. J. Primatol.
414 yr
Gorilla
beringei
beringei
Gorilla
beringei
graueri
Over
13 yr
Gorilla
gorilla
Over 15 yr
Gorilla gorilla
A silverback is very
large sized with
prominent sagittal
crest, muscular and
angular build, with
the pelage of the
saddle and sometimes
legs, neck and sides
gray to silver in color;
in fully mature males;
hair of the lumbar
region turns silver
Behavioral and morphological and life-history markers
silverbacks often
range on their own
Over 18 yr An adult silverback is
a fully grown male
with fully
developed
secondary sexual
characters. He often
has a peaked
sagittal crest and
his saddle
coloration is gray
to silver
(sometimes also
the legs). They can
also develop a very
bright silverline
that is running along
the belly. Adult
silverbacks can have
one or more females
Gorilla
gorilla
The definitions used to assign the photographs are listed in the column ‘‘This study.’’
a
No young silverback class, silverbacks are considered as males older than 12 yr.
b
The boundary of the infant class is occasionally set at an age of 3.5 yr, particularly in census studies, indicating that infants do not build sleeping nests [Weber & Vedder, 1983].
c
Males over 12 yr are occasionally classified as silverbacks [e.g. Robbins, 2007; Williamson & Gerald-Steklis, 2001].
d
Watts and Pusey [1993] consider male gorillas at the age of 15–16 yr to be fully grown, but can mate exclusively with fertile females at 14 yr when they should be called silverbacks; juveniles are defined as
males between 4 yr and age at first copulation and adolescents are between age at first copulation and approximately 11–13 yr.
Silverback Over 15d yr
Gorilla
beringei
beringei
TABLE I. Continued
110 / Breuer et al.
Western Gorilla Maturation and Life History Classes / 111
collected data during nearly continuous monitoring
by four principal investigators and assistants from
February 1995 until July 2007 on 303 different
gorillas living in 61 social units (groups or solitary
males). We made observations with 15–45 telescopes from a platform overlooking the clearing.
Gorillas were habituated to the presence of observers
on the platform and were individually identified from
features such as size, pelage, shape of ears and brow
ridge and nose prints [Parnell, 2002b]. One advantage of studying gorillas at forest clearings lies in the
accumulation of demographic and life-history data of
many different gorilla groups compared with only
one or two groups followed in the forest. Limitations
of bai studies include the gaps between visits of
certain gorilla groups, which may in some cases span
several months. These observational gaps can limit
the accurate assessment of developmental processes,
exact birth dates, and hinder our ability to distinguish ‘‘death’’ vs. ‘‘dispersal’’ away from the population in individuals that disappear from a group.
However, it was often possible to limit the error in
birth date estimates to just a few weeks (see below).
Of the 303 gorillas monitored, 59 were parous
females and 32 were adult males (silverbacks) when
first observed (parous females and adult silverbacks
(ASB) not considered in this study), whereas 110
offspring were born during the study. The remaining
102 gorillas were not fully adult when observed for
the first time, and their birth date was estimated
according to the procedure outlined below.
Age Estimation
Given the long period of immaturity in gorillas, a
study duration of 12.5 yr is too short to track
individuals longitudinally from birth to adulthood,
and to provide exact ages for mature gorillas. We
therefore used a combination of (1) the assignment of
a reliable birth date based on observations of the first
appearance of a newborn to a known female
(n 5 110), or the first sighting of a newborn in a
previously unknown group (carried ventrally, pink
coloration; n 5 9), and (2) retrospective assignment
of age to immatures of unknown birth date by
comparing their physical maturation with individuals of known age. For INF born during the study,
age was estimated based on morphology and size of
the INF, their behavior and that of their mother at
first observation of the newborn [Nowell, 2005;
Nowell & Fletcher, 2007; Parnell, 2002b]. We
compiled a good record of the physical maturation
and behavior of INF of known age and could
therefore improve the precision of estimated birth
dates, even for groups that were absent from the
clearing for several months. In the second case, we
did not have accurate records of age, because the
immature gorillas were either born before the study
began or transferred into the population. We therefore
assigned a birth date retrospectively using both
external morphology (e.g. body size, hair color, body
proportions) and behavior (e.g. suckling behavior,
proximity to and dependence on the mother) compared
with gorillas of known age. This was not possible in the
first 5 yr of the study, because we did not have any
gorillas of known birth date for comparison. We
therefore retrospectively aged all nonadult gorillas
(n 5 93), identified both at the start of the study and
those that immigrated into the population, using
supplementary data (e.g. field notes on physical
maturation, photographs, 4200 hr of video footage).
Retrospective classification will produce a degree of
error in age estimates owing to individual variation,
and certain biological questions such as age at first
parturition can only be answered with data from
gorillas of known birth date. However, we argue that,
given the objective of dividing a continuum of development into biologically meaningful classes, our
methodology for assigning age boundaries to lifehistory classes is justified.
Life-History Classes and Their Age Boundaries
To define the boundaries of life-history classes
we first used morphological and behavioral criteria
and also assigned photographs of known individuals
to the different classes (see below). Some class
boundaries are easier to recognize in some animals
than in others and there is much variation between
individuals [e.g. Strum, 1991]. Our definition of lifehistory classes follows Setchell and Lee [2004] and
has been adopted by various primatologists for a
number of different species. We did not distinguish
between males and females before females were
considered adult (the blackback/female separation)
(BB/AF) (Table II) because determining the sex of
gorillas at Mbeli Bai is almost impossible once
gorillas are no longer riding dorsal on the mother.
The developmental stages of wild western gorillas
have been assumed to mirror that of mountain gorillas
[Nowell, 2005] and our criteria represent a summary of
previous definitions of life-history classes and the
morphological and behavioral markers used in different
gorilla studies (Table I). Infancy ends when an animal
can survive maternal death. Although there are large
individual differences (see ‘‘Results’’), the INF/JUV
transition is best described by life-history parameters,
such as lactational weaning, which can be identified by
field observations. Between November 2002 and July
2007 we noted every suckling event and assigned
weaning age as the mid-point of visits before and after
suckling termination [see also Nowell & Fletcher,
2007]. We furthermore provide information on the
minimum age of survival after the disappearance of a
mother and the minimum age of dispersal. The JUV
period ends when puberty (SAD class) starts; however,
that is difficult to determine without hormonal data
unless external signs, such as sexual swelling in
Am. J. Primatol.
112 / Breuer et al.
TABLE II. Mean Estimated Ages of Western Gorillas That Were Assigned, Using 201 Photographs, to Different
Life-History Stages by Two Judges
LifeNumber Sample
Known history
of
size
year of
class
different (] of
Judge birth assigned gorillas photos)
1
2
1
2
1
2
1
2
1
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
2
Yes
1
Yes
2
Yes
1
Yes
2
Yes
1
2
1
2
1
2
1
No
No
No
No
No
No
No
2
No
1
No
2
No
Infant
Infant
Juvenile
Juvenile
Subadult
Subadult
Blackback
Blackback
Young
silverback
Young
silverback
Adult
female
Adult
female
Adult
female/
blackback
Adult
female/
blackback
Juvenile
Juvenile
Subadult
Subadult
Blackback
Blackback
Young
silverback
Young
silverback
Adult
silverback
Adult
silverback
Mean age (yr)
of gorillas
Minimum age
Maximum age
P-values of
assigned to Standard (yr) of gorillas
(yr) of gorillas Mann–Whitney Ulife-history
error
assigned to life- assigned to life- test of differences
class
(yr)
history class
history class
between judgesa
6
7
15
14
5
9
2
2
1
11
14
34
32
20
25
16
11
3
2.2
2.6
5.2
5.4
9.0
9.6
12.8
13.4
15.3
0.4
0.4
0.2
0.2
0.2
0.3
0.2
0.2
0
0.5
0.5
4.0
4.1
7.9
7.9
11.4
11.4
15.3
3.6
4.2
9.4
9.0
10.9
11.9
13.8
13.8
15.3
1
3
15.3
0
15.3
15.3
1
1
12.2
–
12.2
12.2
1
1
12.225
0
12.225
12.225
1
6
12.086
0.457
9.802
12.611
1
5
12.543
0.017
12.517
12.611
1
2
4
4
10
11
6
1
3
10
13
34
28
23
6.5
7.5
9.7
10.4
11.8
12.1
16.2
–
0.3
0.5
0.3
0.2
0.2
0.2
6.5
7.1
7.1
6.5
10.7
10.7
14.8
6.5
8.0
10.9
11.5
14.6
14.8
18.2
7
33
16.4
0.3
12.2
18.3
6
42
20.0
0.3
17.4
23.6
5
33
20.7
0.3
17.6
23.6
0.358
0.441
0.199
0.226
–
–
0.751
–
0.659
0.218
0.382
0.159
Photos were assigned according to external appearance of examples given in Figure 1 and morphological markers described in Table I and correspondingly
number of gorillas assigned to life-history classes varied between two judges. P-values indicate if there were any significant differences between judges in
their ratings of gorillas (using the estimated age as a measure of this). The data set is split by whether or not the year of birth is a known variable to the
study.
a
Mann–Whitney U (MWU) exact test only applied when sample size was larger than three.
females (albeit small in gorillas) or ejaculation of
semen in males, can be observed [Setchell & Lee,
2004]. Puberty is considered to have ended once an
individual attains reproductive competence. In
mountain gorillas, nulliparous females go through a
2-yr period of adolescent sterility [Harcourt et al.,
1980]. Thus the AF class used for mountain
gorillas includes nulliparous females because first
parturition occurs at a median age of 10 yr (range
8.7–12.8) [Harcourt et al., 1981; Watts, 1991]. For
female gorillas born during our study, we noted when
we first saw the small labial swellings and age at first
Am. J. Primatol.
birth, to determine the boundary between SAD/AF
accordingly.
Delayed male maturation is the result of sexual
dimorphism in gorillas [Leigh & Shea, 1995]. Therefore, gorilla researchers define additional classes for
males that are fertile but are not yet fully grown. We
defined the SAD/BB boundary as the same cut-off
point as for SAD/AF. To support this assignment, we
also determined when males reached approximately
the body length of an AF, which is one criterion for
BB classification [Schaller, 1963]; however, this
criteria from the early years at Karisoke has never
Western Gorilla Maturation and Life History Classes / 113
been properly tested and others have grouped JUV
and SAD into an old JUV class [Watts & Pusey,
1993]. We used digital photogrammetry to measure
the body length of nonadult males and fully grown
female gorillas [Breuer et al., 2007]. Between
January 2004 and July 2007 we took digital photographs of gorillas standing perpendicular to the
gorilla–camera axis and simultaneously measured
the distance between gorilla and camera with a laser
range finder, and then calculated body length as the
product of distance and pixel length [Breuer et al.,
2007]. Young silverbacks (YSB) are larger and more
muscular than AF and start to develop a silver saddle
and strong gluteal and nuchal muscles; however,
their secondary sexual characteristics (e.g. silvering
of saddle, development of sagittal crest) are not fully
developed and this process of maturation takes
several years. YSB in western gorillas become
increasingly peripheral to a group and eventually
leave to become solitary males [Parnell, 2002a;
Robbins et al., 2004]. We therefore provide the
earliest age at male emigration. Similar to other
sexually dimorphic primate species [e.g. Altmann
et al., 1981; Sigg et al., 1982; Watts, 1985], male
gorillas are considered adult (ASB) with cessation of
their growth in both body size and full development
of secondary sexual characteristics (see details in
Table I). Achievement of full body size in western
gorillas reflects competitive ability to acquire females
and we therefore also provide the earliest age when
harems are formed.
However, it should be noted that in the absence
of morphological data on body size (which are
difficult to obtain noninvasively) any comparison
between gorilla species should be treated as preliminary and we propose ways that will help to make
such comparisons.
Photographic Assignment of Age Boundaries
We used photographs (taken between 16th April
2004 and 16th August 2007) to improve the definition of boundaries between classes that did not show
morphological discontinuity (INF/JUV, JUV/SAD,
SAD/BB, BB/YSB, YSB/ASB). We assigned 201
photographs of 53 different gorillas (covering approximately all ages from 6 months (mo) to approximately 24 yr) to life-history classes described above
(see Fig. 1 and Table I). We only used photographs of
gorillas standing quadrupedal and perpendicular to
the gorilla–camera axis to avoid effect of body
posture on appearance of coloration [Breuer et al.,
2007]. This assignment was done on the basis of
external appearance using different morphological
cues such as body proportions, muscle developments
(gluteal and neck muscles) or the development of
secondary sexual characters (arm hair, saddle coloration, sagittal crest). This assignment procedure was
carried out independently by two of the authors
Fig. 1. Photos showing side profiles of gorillas of different lifehistory classes. The two photos in each row present a typical
example of the life-history classes used in this study (from top:
infant (INF), juvenile (JUV), subadult (SAD), blackback (BB),
young silverback (YSB) and adult female (AF)/adult silverback
(ASB)).
(T. B. and M. B.-N. H.). We compared our results
with those of two independent experienced gorilla
observers who were not familiar with the age of the
study animals to verify that our assignment was not
biased by knowledge of the identity and age of the
gorillas. All judges were familiar with the criteria
describing gorilla life-history classes and we found
that definitions of life-history stages were equal
among all four judges (Table I and Fig. 1). We
calculated the boundaries between life-history classes
using binary logistical regression, with life-history
Am. J. Primatol.
114 / Breuer et al.
class of one of two neighboring classes as the
dependent variable and age as the covariate. Age
boundaries were then calculated by solving the
eaxþb
following equation: y ¼ ð1þe
axþb Þ where x is the age
boundary and a and b are estimated by maximum
likelihood using SPSS 13 for Windows (SPSS Inc.,
Chicago, IL). We set y 5 0.5 as the cut-off point when a
gorilla should be assigned to the older class and round
results to the nearest half year.
We found no statistical difference between the
assignments of the independent and the authors’
judgement, and thus took the average value of the age
boundary sets of both results (Table II). Gorillas that
were photographed multiple times generally showed
high consistency in class assignment when photos
were made within a short time interval. For those
cases with a large interval between two photographs,
we often assigned nonadult gorillas to a different
category. Assignment of life-history classes by all four
judges was very similar showing that it was generally
easy to assign gorillas to different classes based solely
on their external appearance (average k: K 5 0.658;
range: 0.593–0.779, all Po0.001, n 5 201 photos;
Spearman rank correlations: average: rS 5 0.939,
range: 0.913–0.968, all Po0.001, n 5 192 photos not
assigned as AF or AF/BB (sex of gorillas unknown)).
Hereafter we use only assignments by T. B. and M. B.N. H. We present results of the INF/JUV, JUV/SAD,
SAD/BB boundaries for gorillas for which we knew
the year of birth (n 5 91 photos). Despite monitoring
many immature females, we had only one female
whose age we knew at first parturition, because most
SAD and nulliparous females emigrated out of the
study population (Mbeli Bai study, long-term data).
Given the lack of data on accurate ages of AF, and the
correspondingly small sample size, we could not apply
logistic regression to define the age of the SAD/AF
boundary, and the results on this particular age-class
boundary should be treated with caution.
Unless otherwise stated we present results as yr
and mo to the nearest month. All research, protocols
reported in this study were reviewed and approved
by the Congolese Ministry of Forest Economy and
Environment and the Nouabalé-Ndoki Project of the
Wildlife Conservation Society. We also confirm that
all research reported in this article adhered to the
American Society of Primatologists Principles for the
Ethical Treatment of Non-Human Primates and no
animal handling was involved in the study.
RESULTS
The youngest immature that survived the dispersal or death of the mother was 4 yr old. There
were three events in which a female transferred with
her offspring following the death of the group’s
silverback and the mothers (n 5 2; one mother
transferred two times) remained with their offspring
until these were 4 yr 11 mo and 5 yr 6 mo. Similarly,
Am. J. Primatol.
the youngest gorilla seen to transfer alone was 4 yr;
he was also the youngest when last seen suckling.
Immature gorillas were last seen to suckle at an
average age of 4 yr 9 mo (n 5 25) (median: 4 yr 9 mo,
range 3 yr 1 mo–6 yr 1 mo), which is significantly
later than that for mountain gorillas (average: 3 yr
5 mo (n 5 11), median: 3 yr 7 mo, range 2 yr 8 mo–5 yr
2 mo) [Fletcher, 1994; Stewart, 1981] (U 5 37,
z 5 3.452, P 5 0.001) [see also Nowell & Fletcher,
2007]. We assigned photos of gorillas up to a
maximum age of 4 yr 3 mo to INF and the
youngest gorilla we assigned as JUV was 4 yr old
(Table II). The INF/JUV boundary was best set at
4 yr (summarized in Table III). Therefore, we
propose an age boundary for INF/JUV in western
gorillas of 4 yr.
Boundaries to SAD were solely described by
photo assignment. We found substantial overlap
between the JUV and SAD classes for both judges
(Table II). We determined a boundary of 7 yr 7 mo
and proposed 7.5 yr as the JUV/SAD boundary in
western gorillas (Table III). The female of known age
was seen three times with labial swellings between
9 yr 6 mo and 10 yr 3 mo, which is 2 yr later than in
mountain gorillas (7–7.5 yr) [Harcourt et al., 1980].
She had her first baby at 11 yr 5 mo. This age of first
parturition falls within the upper range for mountain gorillas (average: 10 yr 3 mo, range 8 yr
8 mo–12 yr 10 mo) [Gerald, 1995]. Two females of
known age did not have offspring when they
transferred out of the population at the ages of 9 yr
3 mo and 9 yr 11 mo. On the basis of these field
observations, we tentatively suggest the designation
of the SAD/AF boundary as 10 yr.
The youngest male to attain the approximate
body length of an AF was 10 yr 8 mo old (Fig. 2).
Photo assignment showed that there was almost no
overlap between SAD and BB; thus, the boundary
between the two classes was estimated to be 11 yr
7 mo (Table III). We therefore designate the SAD/BB
boundary at an age of 11 yr.
The minimum age (estimated retrospectively) of
a BB was 10 yr 8 mo and the maximum was 14 yr
10 mo. Photographs of males ranging from 12 yr 2 mo
to 18 yr 4 mo of age were assigned to the YSB class.
We calculated a boundary of 14 yr 6 mo (Table III)
between BB/YSB. The youngest male that was
first seen making visits to Mbeli Bai without his
former group had an estimated age of 13 yr 7 mo
and we propose that YSB class starts at age 14 yr but
also realize that there are large interindividual
differences when males become silver. The youngest
male classified as fully grown was estimated to be
17 yr 5 mo old. We estimated the YSB/ASB boundary
as 18 yr 2 mo (Table III). Therefore, we propose that
the ASB class begins at age 18 yr (compared with
15 yr in mountain gorillas) as this corresponds to the
estimated age a male can acquire a female [Breuer,
unpublished data].
Western Gorilla Maturation and Life History Classes / 115
TABLE III. Results From Logistic Regression of Photo Assignment to Reveal Age Boundaries Between Different
Life-History Classes
Judge
Life-history
boundary
Estimated age of
boundary
Number of
photos
Variable
B
SE
Wald
df
Sig.
87.764
336.107
13.421
54.946
2.327
17.458
2.014
15.430
58.578
652.110
3.116
37.838
166.724
6191.397
23921.980
7.454
30.835
0.754
5.909
0.623
4.993
5530.692
61604.160
1.466
17.421
4644.687
0.000
0.000
3.242
3.175
9.516
8.731
10.454
9.550
0.000
0.000
4.517
4.718
0.001
1
1
1
1
1
1
1
1
1
1
1
1
1
0.989
0.989
0.072
0.075
0.002
0.003
0.001
0.002
0.992
0.992
0.034
0.030
0.971
1
Infant/juvenile
3.8
46
2
Infant/juvenile
4.1
49
1
Juvenile/subadult
7.5
54
2
Juvenile/subadult
7.7
57
1
Subadult/blackback
11.1
36
2
Subadult/blackback
12.1
36
1
Blackback/young
silverback
14.7
82
Age
Constant
Age
Constant
Age
Constant
Age
Constant
Age
Constant
Age
Constant
Age
2
Blackback/young
silverback
14.4
75
Constant
Age
2451.006
1.592
68335.566
0.360
0.001
19.581
1
1
0.971
0.000
1
Young/adult silverback
18.0
68
2
Young/adult silverback
18.3
69
Constant
Age
Constant
Age
Constant
22.871
3.364
60.703
2.596
47.586
5.179
1.251
22.562
0.853
15.565
19.503
7.237
7.239
9.264
9.347
1
1
1
1
1
0.000
0.007
0.007
0.002
0.002
Fig. 2. Body length growth of male western gorillas. The
horizontal graded bar indicates the range of adult female body
length (range: 72.3–74.8 cm) also measured by photogrammetry
[Breuer et al., 2007]. Data points are from males with known
birth dates and in the cases of gorillas older than 12 yr of known
year of birth. The same individual can contribute multiple data
points.
DISCUSSION
Reassigning Age Boundaries of Western
Gorilla Life-History Classes
Estimating age in free-ranging primates improves with observer experience and duration of the
study, and age boundaries of life-history classes have
often been re-assessed and refined when knowledge
of the physical maturation of wild primates improved
[Altmann et al., 1977, 1981; Sigg et al., 1982].
Here, we have revised the age boundaries of lifehistory classes in western gorillas using long-term
demographic data from Mbeli Bai (Table I and Fig.
3). Therefore, we propose that these new age
boundaries can be tested at other field studies using
similar behavioral and morphological criteria. However, these boundaries should not always be considered as clear cut-off points between age classes
but rather an estimated age around which a transition occurs (e.g. JUV/SAD, BB/YSB, etc.). It is
possible that the development may be faster at sites
that are more similar to the habitat of mountain
gorillas (e.g. secondary forests with higher herb
density). However, our site constitutes a large
swampy clearing with superabundant aquatic herbs,
and so perhaps already presents a representative
assessment of life-history boundaries for western
gorillas.
Assigning Photographs to Different LifeHistory Classes
Currently we have empirical data on individuals
of known age ranging from 1 to 12.5 yr. Our
procedure allowed us to assign age to gorillas older
than 12.5 yr and we have used retrospective aging to
assign an age boundary to silverbacks. In spite of
practical difficulties in accurately assessing and
comparing gorilla sizes owing to different distances
of the gorillas from the observer, photo assignment
showed interobserver reliability between judges
familiar or unfamiliar with the identity and age of
the study animals. This method can reliably be used
Am. J. Primatol.
116 / Breuer et al.
Fig. 3. Developmental stages (life-history classes) in the life cycle of mountain gorillas (MG) and western gorillas (WG).
to assign gorillas of unknown ages to different lifehistory classes. However, when morphology changes
gradually, the application of photogrammetry to
measure body length can provide more precise
estimates of age than other physical characteristics—body length is difficult to take into account
when assigning photos to life-history classes. Such
continuous monitoring of known-aged gorillas will
also help identifying growth spurts and modes of
development [e.g. Leigh & Bernstein, 2006].
Owing to the fact that some criteria (e.g. age
when males reach AF size) for the different boundaries for mountain gorillas have never been tested, it
would be important to apply photogrammetry and
photo assignment to the Virunga gorillas (albeit this
might be difficult owing to the dense vegetation),
who have been monitored for several decades, to see
how well such assignment fits with the currently
used age boundaries in mountain gorillas. Also the
application of video images might help make the
classification of gorillas and other primates into
different life stages easier. Such comparative studies
of different gorilla populations would test our
conclusions on the slower development of western
gorillas. In addition, there is little consensus in the
use of life-history classes in the well-studied mountain gorillas and some classes have been poorly
defined. For example, although some consider all
males over 12 yr of age to be adult or silverbacks [e.g.
Robbins, 2007; Williamson & Gerald-Steklis, 2001],
others make the distinction between YSB and
mature silverbacks that are not fully grown until
15 yr of age [Watts, 1990; Watts & Pusey, 1993].
These caveats should be recognized in the light of
our comparison with western gorillas and we urge
future studies on both species to follow standardized
age-class definitions such as that we have presented
here to facilitate comparative analyses.
Comparison Between Western and Mountain
Gorillas
The later weaning age in western gorillas
compared with mountain gorillas is supported by
an average increase of 16 mo in the duration of
suckling. The results presented here and during an
Am. J. Primatol.
earlier investigation show that western gorilla INF
are not weaned before the age of 4 yr, when
termination of suckling bouts by the mother peaks
[Nowell & Fletcher, 2007]. The INF/JUV boundary
determined by our photo assignment was similar to
the weaning age and the minimum age we observed a
gorilla to survive the death of its mother. Although
the cessation of suckling is a more obvious milestone
that delimits a life-history class, we confirm that
other boundaries, particularly during adolescence
(e.g. JUV/SAD boundary), are more fluid [Setchell &
Lee, 2004]. Correspondingly, JUV and SAD mountain gorillas have been pooled as adolescents for
some data analyses [Watts & Pusey, 1993]. We
therefore need more behavioral data to confirm our
estimate of the JUV/SAD boundary that is currently
based solely on the photo assignment. We assigned
the age of the SAD/BB boundary to 11 yr and found
that males attain AF size at around 11 yr of age.
Similarly, males do not attain the size of AF until
they are at least 10 yr old in Bwindi [Robbins,
personal communication] where mountain gorillas
consume more fruits than in the Virungas [Robbins,
2007]. Although the body length criterion remains to
be tested for mountain gorillas, the development of
secondary sexual characters (e.g. longer arm hairs of
males) is not obvious before the age of 11 yr in
western gorillas. This event is assumed to happen
much earlier in life in mountain gorillas (Table I).
The slower maturation in known-aged males up to
the BB age suggests that this likely leads to a later
age of growth cessation in western gorilla silverbacks
compared with mountain gorillas. Males become
solitary when they are considered YSB and appear
not to be fully grown until the age of approximately
18 yr when they are able to acquire females,
compared with mountain gorillas that are considered
fully grown at 15–16 yr [Watts, 1990]. Also gorillas in
Bwindi Impenetrable National Park, Uganda, appear
to develop more slowly than mountain gorillas
monitored in the Virunga Volcanoes [Robbins, personal communication]. Continuous monitoring is
needed to assess the accuracy of this age boundary
for ASB. Our limited data on age at parturition of AF
and age of visible sexual swellings suggest a later age
at parturition (although it is possible that we may
Western Gorilla Maturation and Life History Classes / 117
have missed the first appearance of these small
sexual swellings and a miscarriage owing to the
observation gaps of groups). However, more data are
needed from SAD and AF of known age in order to
confirm the age boundary of 10 yr proposed here.
Implications for Life-History Theory, Social
Organization and Conservation
Our findings provide support for the ‘‘risk-aversion’’ hypothesis and the prediction of slower development of western gorillas owing to greater frugivory,
stronger seasonality in the habitat, lower herb density
or the rarity of weaning foods [Doran & McNeilage,
2001; Nowell & Fletcher, 2008]. Although slower
immature growth and later weaning age do not
necessarily lead to later age at parturition or age at
maturity (owing to different modes of life histories)
[Leigh & Bernstein, 2006], our data indicate that this
may be the case in our population. Other aspects of
western gorilla biology such as arboreality, large daily
ranges [Doran-Sheehy et al., 2004; Remis, 1995] and
increased foraging complexity (including cognitive
skills for locating ripe fruits) can potentially reduce
the allocation of energy to physical maturation [van
Schaik & Deaner, 2003; Walker et al., 2006; Zihlman
et al., 2007]. Detailed studies on energy gains and
overall energy balance are currently under way that
will help to explicitly test these predictions [Masi,
unpublished manuscript].
In addition, primates that face increased predation risk are assumed to grow faster because smaller
individuals are considered at higher risk [Janson &
van Schaik, 1993]. In contrast to mountain gorillas,
western gorillas face leopard predation risks but the
exact degree is unknown [Robbins et al., 2004].
Current life history of mountain gorillas could also
reflect adaptation to predation pressures in the past
so that we were not able to test whether western
gorilla life history has evolved under increasing
predation risk.
A slower life history and longer period of
dependency of immature western gorillas could have
important consequences for other aspects of western
gorilla biology. A minimum tenure of 18 yr is
required for the son of the group’s silverback (who
will then be around 36 yr) to reach maturity. Given
high levels of male–male competition and the
subsequent impacts on male longevity and tenure
length, slower life history will impact on the
probability of father–son multimale group forming.
If male tenure length is shorter than a male’s age to
mature, age-graded groups are unlikely to develop.
This scenario could provide an alternative explanation for the lack of multimale (kin) groups in western
gorillas compared with mountain gorillas [see alternative explanation in Harcourt & Stewart, 2007].
The later weaning age (higher ratio of lactation
to gestation) and the predominance of one-male
groups in western gorillas could signal increased
infanticide risk because INF in multimale mountain
gorilla groups face lower risks of being killed by a
silverback than do one-male groups [Robbins et al.,
2007]. Infanticide and predation risk (and other
factors such as fallen from trees) can cause the
observed high INF mortality rates [more than 50% to
weaning age: Breuer, unpublished results; Robbins
et al., 2004] of western gorillas at Mbeli Bai.
Recently, western gorillas have been re-classified from endangered to critically endangered on the
IUCN Red List, in response to the escalating rates of
decline owing to Ebola and commercial hunting
across much of their range in the last two decades
[Tutin et al., 2005]. Slower development and the
potential for higher mortality compared with mountain gorillas will negatively affect their intrinsic rate
of increase and their potential for recovery from
population crashes. These are therefore important
variables to incorporate into models of population
dynamics and species-level conservation strategies.
This study has provided insights into the potential
implications of slower life history for western
gorillas, emphasizing the importance of long-term
studies in providing accurate baseline demographic
and life-history data of undisturbed primate populations in assessing the vulnerability of populations to
these threats.
ACKNOWLEDGMENTS
Our sincere thanks go to the Ministère de
l’Économie Forestière et de l’Environnement for
permission to work in the Nouabalé-Ndoki National
Park and the staff of Wildlife Conservation Society’s
Congo Program for crucial logistical and administrative support. We are grateful to many different
research assistants who helped to collect data at
Mbeli and to Roger Mundry for the statistical advice.
We thank Damien Caillaud and Shelly Masi for the
assignment of gorilla photos and Shelly Masi, Martha
Robbins, Olaf Thalmann and Liz Williamson for
their helpful comments on an earlier version of this
manuscript. Thanks to Andrew Robbins for the help
with the demographic database. This research
project was reviewed and approved by the Congolese
government and the Nouabalé-Ndoki Project of the
Wildlife Conservation Society.
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