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Captive and wild orangutan (Pongo sp.) survivorship a comparison and the influence of management

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American Journal of Primatology 71:680–686 (2009)
RESEARCH ARTICLE
Captive and Wild Orangutan (Pongo sp.) Survivorship: A Comparison and the
Influence of Management
S.A. WICH1, R.W. SHUMAKER1, L. PERKINS2, AND H. DE VRIES3
1
Great Ape Trust of Iowa, Des Moines, Iowa
2
Zoo Atlanta, Atlanta, Georgia
3
Research Group Behavioural Biology, Utrecht University, Utrecht, The Netherlands
For managers of captive populations it is important to know whether their management provides a
species with the physical and social environment that maximizes its survivorship. To determine this,
survivorship comparisons with wild populations and long-term evaluations of captive populations are
important. Here we provide both for orangutans. We show that survivorship has increased during the
past 60 years for captive orangutan populations in zoos. In addition, we show that survivorship of
captive orangutans in the past used to be lower than for wild orangutans, but that for recently born
(1986–2005) orangutans survivorship is not significantly different from the wild. This indicates that
captive management in the past was suboptimal for orangutan survivorship, but that modern
management of captive orangutans has increased their survivorship. We discuss the possible factors
of modern management that could have influenced this. Am. J. Primatol. 71:680–686, 2009.
r 2009
Wiley-Liss, Inc.
Key words: life history; Pongo; mortality; survival; great apes
INTRODUCTION
Life history analyses of captive animals are
scientifically interesting and practically important
because they provide information on the flexibility of
a species’ life history and the factors that influence
such flexibility. In captivity, the more stable and
mostly higher food availability in combination with
proper medical care, improved hygienic circumstance
and lack of predation generally are found to reduce
age of first reproduction [Parga & Lessnau, 2005;
Shumaker et al., 2008; Sugiyama & Ohsawa, 1982];
reduce interbirth intervals [Hill et al., 2001; Parga &
Lessnau, 2005; Wich et al., 2009]; reduce mortality
and increase survivorship compared with wild
populations [Bronikowski et al., 2002; Courtenay &
Santow, 1989; Debyser, 1995; Hill et al., 2001; Parga
& Lessnau, 2005; Sugiyama & Ohsawa, 1982]. But
other factors such as improper hygienic situations,
improper diet, diseases, obesity, injuries from exhibits, poor adaptation to a zoo’s climate, spread
of infections, inbreeding and social stress [de Wit,
1995; Gozalo & Montoya, 1990; Karstad & Sileo,
1971; Taylor & Poole, 1998; Ward et al., 2003;
Wielebnowski, 1996] might actually increase mortality in captivity. For managers of captive populations,
it is important to know how management practices
can be improved to reduce factors that influence
mortality in such populations [e.g., Leong et al.,
r 2009 Wiley-Liss, Inc.
2004]. The effect of captivity on mortality differs
between species and can lead to higher survival in
one species, but to lower survival in another species
[Cui et al., 2006; Savage et al., 1996]. For instance, a
potentially more stable food supply in captivity than
in the wild has led to higher survival of black-andwhite snub-nosed monkeys (Rhinopithecus bieti) in
captivity [Cui et al., 2006]. The opposite has been
reported for cotton-top tamarins (Saguinus oedipus)
where a lack of experienced individuals to provide
infant care in captivity has led to higher mortality in
captivity than in the wild [Savage et al., 1996].
Orangutans in captivity follow several of the
expected trends for animals in captivity. Their age at
first reproduction in captivity is lower than in the
wild [Markham, 1995; Shumaker et al., 2008], and
interbirth intervals are shorter than those reported
from the wild [Anderson et al., 2008; Markham,
1995; Wich et al., 2009]. Nevertheless, it has also
been observed that immature mortality is very high
Correspondence to: Serge A. Wich, Great Ape Trust, 4200 SE
44th Ave., Des Moines, IA, 50320.
E-mail: swich@greatapetrust.org
Received 20 November 2008; revised 10 April 2009; revision
accepted 14 April 2009
DOI 10.1002/ajp.20704
Published online 11 May 2008 in Wiley InterScience (www.
interscience.wiley.com).
Captive and Wild Orangutan Survivorship / 681
[Anderson et al., 2008; Markham, 1995], and that
captive infant mortality is even higher than that of
some wild populations [Anderson et al., 2008].
Markham [1995], however, acknowledges that the
studbook data included in her analysis contains data
from the global captive population, in which management standards might differ among regions and
includes data from more than 50 years ago when
standards of management were different from those
at present. Management practices, such as veterinary care, balanced diet, opportunities for locomotion,
have improved since the start of the studbook
records until the present time, and we hypothesize
that this will be reflected in improved survivorship.
This has probably led to the large variation in
mortality age that is contained in the studbook.
Anderson et al. [2008], however, write ‘‘can it really
be true that despite provisioning and veterinary
supervision, captive animals have decreased survivorship?’’ Subsequently they suggest that higher
mortality in captivity than the wild is a result of wild
data underestimating mortality, even though they
use the complete global studbook from its inception
for their analyses and hence include a large variation
in the quality of management in their analyses.
Underestimating wild orangutan mortality did,
however, not occur because Wich et al. [2004] used
conservative methodologies and therefore overestimated mortality.
The aim of this paper is therefore twofold. First,
we will examine survivorship data for captive
individuals born during three periods; 1946–1965,
1966–1985 and 1986–2005, to determine whether
survivorship in a selected number of zoos have
actually changed over time. These periods are somewhat arbitrary, but 1985 is the year that the
Association of Zoos and Aquariums (AZA) decided
to start emphasizing and sharing husbandry standards, which should have benefited management
from 1986 onwards. Since the current studbook
contains data until 2005 we decided to use 20-year
blocks to keep the time periods comparable. Second,
we compare survivorship data from the wild with
those from captivity for a selected number of zoos to
determine whether captive survivorship differs from
that in the wild.
METHODS
Wild Orangutans
Life history data from wild orangutans were
collected at the Ketambe research station (31410 N,
971390 E) in the Gunung Leuser National Park,
Leuser Ecosystem, Sumatra, Indonesia. This is the
only wild population that has been studied for a
sufficient duration to provide long-term demographic
data. The research area is mostly covered by pristine
rainforest from the alluvial lowlands at ca. 350 m
above sea level up to higher altitudes around 1,000 m
above sea level [Rijksen, 1978; Schaik & Mirmanto,
1985]. Orangutan research at the site started in 1971
when Dr. Herman Rijksen established the research
station and continues until the present day. Details
on data collection and life history calculations have
been published in Wich et al. [2004, 2009], but the
most important aspects are summarized here. For a
total of 65 individual orangutans we had either birth
records (n 5 35) or were able to estimate their age
(n 5 30). Age estimates were based on long-term
photographic records of individuals with known ages
and this enabled us to estimate ages without a large
age interval. All researchers that have been conducting long-term research in Ketambe have been carefully sharing photos and information with SW to
achieve these age estimates.
Captive Orangutans
Data from captive orangutans were obtained
from the international studbook database. The
studbook provides data on birth dates, death dates,
sex and species from all registered captive orangutans. We excluded hybrid orangutans for all analyses
in this paper and conducted analyses separately for
each sex. As earlier analyses showed no differences in
survival rates for captive Sumatran and Bornean
orangutans [Wich et al., 2009], we lumped the two
species. For wild-born orangutans the birth dates
were estimated by the facilities at which the
orangutans first entered captivity. Since orangutans
were mostly under 2–3 years old when arriving at the
facilities, age estimates will rarely be off by more
than 2–3 years and as such will affect our analyses
only by slightly overestimating survivorship. We
excluded any birth dates that could not be verified.
Because this procedure mostly affected the oldest
birth records, the analysis for captive orangutans
presented here underestimates their survivorship in
captivity. All stillbirths were excluded from the
analyses, as these would complicate comparisons to
wild data for which stillbirths are hard to determine.
To try to control for differences in management
styles we included only North American, European
and Australian facilities, and excluded breeding
facilities. The overall number of individuals included
was 1,199, of which 578 (292 females and 286 males)
were Bornean and 621 (329 females and 292 males)
were Sumatran.
A significant challenge for life history analyses
with studbook data is that they are a mixture of wildand captive-born individuals and therefore contain
left-censored data (wild-born individuals brought
into captivity when young). As a result, survivorship
will be overestimated and the extent of this effect
depends on how large the number of wild-born
individuals is compared with the number of
captive-born individuals. We examined the extent
of this effect by comparing the complete dataset as
Am. J. Primatol.
682 / Wich et al.
described above (i.e., containing left-censored data)
with a dataset that only contained captive-born
individuals (i.e., without left-censored data). For
equal ages (i.e., 0–40 years) these two datasets did
not differ significantly. Therefore, we decided to use
the mixed dataset for the first comparison with wild
orangutans.
For the comparison between the 20-year periods
we only used captive born individuals and only used
the years an individual was alive in the 20-year block
in which an individual was born to avoid overlapping
datasets.
vorship was also lower during the 1966–1985 than
the 1986–2005 period (Table I).
Survivorship for males shows a similar pattern
with a significant difference in survival rates
between the three examined periods (Wilcoxon–
Gehan statistic 5 6.94, df 5 2, P 5 0.03, Fig. 2).
Survivorship was lower during the 1946–1965 period
(Median survival time 5 2.0 years, n 5 22), than the
1966–1985 period (Median survival time 5 12.7
years, n 5 149, Table I), and the 1986–2005 period
(Median survival time420.0 years, n 5 152, Table I).
But survivorship did not differ significantly between
the 1966–1985 and 1986–2005 period (Table I).
Life Tables
Standard discrete time measures were used for
the life-table analysis [e.g., Hill et al., 2001]. Yearly
mortality rate (qx) was used to calculate yearly
survival rate px ( 5 1qx). The probability of surviving from birth to age x (lx, or survivorship) is
calculated as the product of all px values from age 0
to age x1. Life tables were generated with SPSS
from the international studbook data.
All research was in compliance with animal care
regulations and applicable national laws from the
countries where the research was conducted.
RESULTS
Captive Orangutan Survival
To assess the effect management has on orangutan survival, we examined only orangutans that
had been born in captivity during one of the three
periods (females: n 5 358; males: n 5 323). For
female orangutans there was a significant difference
in survivorship between the three examined periods
(Wilcoxon–Gehan 5 18.61, df 5 2, Po0.001, Fig. 1).
Survivorship tended to be lower during the
1946–1965 period (Median survival time 5 6.8 years,
n 5 20) than the 1966–1985 period (Median survival
time420.0 years, n 5 186, Table I), and was significantly lower than the 1986–2005 period (Median
survival time420.0 years, n 5 152, Table I). Survi-
Captive and Wild Orangutan Survival
Compared
We first compared wild male orangutan survivorship with that of captive male orangutans. Even
though previous analyses indicated no differences in
survivorship of captive Sumatran and Bornean
orangutans of both sexes [Anderson et al., 2008;
Cocks, 2007; Wich et al., 2009], we decided to conduct
the current analyses only for the Sumatran orangutans to avoid potential confounds. The survivorship
of wild Sumatran orangutan males (Median survival
time 5 41.4 years, n 5 37) was found to be significantly higher than that of captive Sumatran orangutan males (Median survival time 5 16.7 years:
Wilcoxon–Gehan 5 8.34, df 5 1, P 5 0.004, n 5 292).
TABLE I. The three periods for captive orangutans
compared
Wilcoxon–Gehan
df
P
vs. 1966–1985
vs. 1986–2005
vs. 1986–2005
3.38
16.0
11.07
1
1
1
0.07
o0.001
0.001
vs. 1966–1985
vs. 1986–2005
vs. 1986–2005
4.01
6.93
1.09
1
1
1
0.05
0.008
0.3
Period
Females
1946–1965
1946–1965
1966–1985
Males
1946–1965
1946–1965
1966–1985
Fig. 1. Cumulative female survival for the three periods in captivity and wild orangutans from age 0 to 20 years.
Am. J. Primatol.
Captive and Wild Orangutan Survivorship / 683
Fig. 2. Cumulative male survival for the three periods in captivity and wild orangutans from age 0 to 20 years.
TABLE II. Captive and
orangutans compared
male
and
female
Wilcoxon–Gehan
df
P
vs. wild
vs. wild
vs. wild
6.67
1.62
0.06
1
1
1
0.01
0.2
0.81
vs. wild
vs. wild
vs. wild
8.54
7.0
3.9
1
1
1
0.03
0.008
0.05
Period
Females
1946–1965
1966–1985
1986–2005
Males
1946–1965
1966–1985
1986–2005
wild
For females such an effect was not found and
survivorship was not significantly different for wild
(Median survival time 5 29.3 years, n 5 28) and
captive Sumatran orangutan females (Median survival time 5 24.6 years: Wilcoxon–Gehan 5 0.755,
df 5 1, P 5 0.38, n 5 329).
As both the male and female captive datasets
contain data from the start of the studbook during
which management techniques might have been less
sophisticated than they are today, we conducted
additional comparisons in which we compared wild
survivorship between ages 0 and 20 years with the
three 20-year periods of captive survivorship. For
female orangutans there was a significant difference
in survivorship (Wilcoxon–Gehan 5 17.11, df 5 3,
P 5 0.001, Fig. 1). Survivorship of wild female
orangutans (Median survival time420 years,
n 5 17) was significantly higher than captive females
during the 1946–1965 (Median survival time 5 6.0
years, n 5 14, Table II). Wild survivorship did not
differ significantly from 1966 to 1985 (Median
survival time420 years, n 5 112, Table II), and
1986–2005 period (Median survival time420 years,
n 5 82, Table II).
For male orangutans there was also a significant
difference in survivorship (Wilcoxon–Gehan 5 9.62,
df 5 3, P 5 0.02, Fig. 2). Survivorship of wild male
orangutans (Median survival time420 years, n 5 18)
was significantly higher than captive males from
1946 to 1965 (Median survival time 5 3.81 years,
n 5 16, Table II). Wild survivorship did also differ
significantly from the 1966 to 1985 period (Median
survival time412.05 years, n 5 89, Table II). Wild
male survivorship was not significantly higher than
captive males during the 1986–2005 period (Median
survival time420 years, n 5 77, Table II).
DISCUSSION
Ideally, managers of captive animals would have
data available to evaluate the success of their
management strategies on the survivorship of the
species under consideration. In reality, it is not
simple to evaluate the success of captive management; for many species, survivorship data from the
wild are not available and it is therefore not possible
to determine whether captivity has led to changes in
survivorship compared with the wild. In addition to
comparing captive survivorship to that in the wild, it
would be valuable to managers to be able to
determine whether longevity of captive species
changes over time. The latter is be expected given
the improvements in health care, nutrition, and
facilities that have been made by zoos over the years
for many of the species they house [e.g., apes: Brent,
2001; Hutchins et al., 2001]. There seem to be very
few studies that analyze life history trends over time
in captivity, but there are data that suggest that
longevity for elephants has increased in captivity
over time [Wiese & Willis, 2004], which the authors
attribute to modern management practices. The
elephant data also indicate that survivorship for
captive elephants is lower than that for wild
elephants [Clubb & Mason, 2002; Wiese & Willis,
2004]. Unfortunately, for apes no formal analyses
appear to exist that examine survivorship changes
since apes have been in captivity. Jones [1982],
however, provides an overview indicating that
orangutan survivorship has increased from the late
1800s until the late 1970s. He concludes that while
Am. J. Primatol.
684 / Wich et al.
the earliest orangutans brought into captivity (from
1776 to 1925) only lived for a few years at most, those
arriving after 1946 had a maximum lifespan in zoos
of 30–40 years. The current studbook indicates that
males can live up to 50 and females can live to more
than 50 years [Shumaker et al., 2008], which is
similar to that found in the wild [Wich et al., 2004].
This indicates an increase in survivorship in captivity with improved management.
As an addition to these earlier assessments of
orangutan survivorship, we provided a preliminary
answer to the questions of how orangutan survivorship in captivity compares to the wild, and whether
management changes over the past 60 years have
had an impact on captive orangutan survivorship.
Our analyses clearly indicate that survivorship
increased from 1946 up until 2005 for both orangutan males and females. Thus to answer Anderson
et al.’s question ‘‘can it really be true that despite
provisioning and veterinary supervision, captive
animals have decreased survivorship?’’ we can now
reply: ‘‘yes, in the past captive orangutans had a
lower survivorship because captive management
was not optimal and only recently has it reached
standards that have increased orangutan survivorship to equal and above that of wild orangutans’’.
Thus, comparisons that use the complete studbook
[e.g., Anderson et al., 2008], that includes data from
times in which management was less well-developed
and also include data from zoos where management
might still be of lesser quality, may lead to
comparisons in which captive data show poorer
survivorship than wild data. However, it is important
to note that survivorship between the ages of 0–2
remains low in captivity, which is a pattern common
for primates, but improvement in captivity might be
possible. There is another drop in survivorship
between the ages of 11–14, but this is not related to
any management issues that we can determine.
The increase in survivorship is very likely the
result of a range of factors that have changed in zoo
management. These changes have been stimulated
by the development of husbandry manuals for the
various great ape species [Fulk & Garland, 1992;
Mills et al., 1997; Ogden & Wharton, 1997; Sodaro,
1997]. Husbandry manuals provide a multi-disciplinary overview of the best management practices of a
species ranging from topics such as veterinary care to
housing design. Although it is not yet possible to
determine which factors have been most critical for
the increased orangutan survival, there are several
factors that might have been important.
Improved housing [Coe et al., 2001; Seidensticker
& Doherty, 1996] in several species has been linked to
decreased mortality rates [e.g., Courtenay & Santow,
1989; Glatston et al., 1984] or increased reproduction
[e.g., Carlstead et al., 1999]. Changes include the
enlargement of the enclosure; equipping the enclosure
with affordances that stimulate more natural locomo-
Am. J. Primatol.
tion [Glatston et al., 1984; Maple, 1980]; changes that
might reduce the risk of disease transmission between
people and orangutans [Maple, 1980]; and hygienic
improvements that led to a reduction in disease and
disease transmission [Lee & Guhad, 2001].
Like many other primates, orangutans have
diets consisting of items, such as fruits, leaves, inner
bark, from many dozens or even hundreds of plant
species, complemented with invertebrates and in
some cases meat, soils, honey and more [Russon
et al., 2009]. Often these items are eaten in different
quantities during the year or over the years as a
result of fluctuating availability [Wich et al., 2006].
The bulk of many diets in captivity consist of
relatively few items that are not likely to show much
intra-annual variation [Nijboer & Dierenfeld, 1996;
Oftedal & Allen, 1996; Pruetz & McGrew, 2001]. In
the past there were no strict guidelines for diets in
captivity and partly as a result many orangtuans
became obese [Jones, 1982]. Being overweight has
been linked to increased mortality through diabetes,
heart disease, high blood pressure and other diseases
in humans [Hensrud, 2002]. Although it is not
possible to determine how much of the increased
survival has been the result of dietary changes, in
other species it has been suggested that an appropriate diet has led to an increase in longevity [e.g.,
Wen Yang et al., 2007].
An important aspect of the health of any zoo
animal is its physical health. There is now more
known about the medical aspects of orangutan
management and clear medical guidelines have been
developed that include voluntary blood draws to
reduce the need for total sedation [Lee & Guhad,
2001; McManamon, 2007]. Although it is not possible
to infer any direct correlations between health care
and improved survival, it seems likely that the
improved care and guidelines have contributed to
the increased survivorship.
Stress is another factor that is important to
consider as it might have effects on the health of an
individual. Probably the most harmful form of stress
is long-term distress that is the result of the physical
properties of housing or imposed by the vicinity or
behavior of visitors [e.g., Moberg & Mench, 2000] or
of cagemates. Although the health consequences of
long-term stressors are not well understood in detail,
they are considered to have negative health consequences and can in extreme cases even lead to the
death of an individual [McEwen, 1998; Schreck,
2000]. The improvements that have been made in
the physical aspect of housing conditions in combination with the more appropriate social settings that
orangutans are housed in might have reduced stress
and improved health and increased survival. Negative stress (distress) has probably decreased as a
result of enabling orangutans to escape public view,
enlarging the enclosures to increase inter-individual
distances, improving diet and so forth. Both these
Captive and Wild Orangutan Survivorship / 685
aspects of stress are fruitful terrain for future
research.
In conclusion it seems that improved management of captive orangutans has increased their
survivorship and similar to that in the wild.
Although the exact contribution of each possible
factor that might have led to this increased survivorship is not known, we hope that this paper leads to
continuing efforts to improve management in
orangutans and other species.
ACKNOWLEDGMENTS
We acknowledge the participation of zoos worldwide that have contributed data to the international
orangutan studbook. All research was in compliance
with animal care regulations and applicable national
laws from the countries where the research was
conducted. Three anonymous reviewers provided
valuable suggestions to an earlier version of this
paper.
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