Captive and wild orangutan (Pongo sp.) survivorship a comparison and the influence of managementкод для вставкиСкачать
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: email@example.com 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 , 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. , 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.  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 , 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. 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