Why Do Animals Live Shorter in Captivity

Abstract

While it is normally believed that animals live longer in zoos than in the wild, this assumption has rarely been tested. We compared 4 survival metrics (longevity, baseline mortality, onset of senescence and rate of senescence) between both sexes of complimentary-ranging and zoo populations of more than 50 mammal species. Nosotros found that mammals from zoo populations generally lived longer than their wild counterparts (84% of species). The event was most notable in species with a faster pace of life (i.due east. a short life bridge, high reproductive charge per unit and high mortality in the wild) considering zoos evidently offering protection against a number of relevant weather condition like predation, intraspecific competition and diseases. Species with a slower stride of life (i.east. a long life span, low reproduction rate and depression mortality in the wild) benefit less from captivity in terms of longevity; in such species, there is probably less potential for a reduction in mortality. These findings provide a beginning general explanation about the dissimilar magnitude of zoo environs benefits amid mammalian species, and thereby highlight the effort that is needed to improve captive weather condition for tedious-living species that are particularly susceptible to extinction in the wild.

Introduction

Zoological gardens represent artificial environments in which animals are maintained, bred and displayed. By doing so, zoos achieve a diversity of goals across their visitors' recreation: basic zoological and conservation didactics reaches 700 meg visitors per twelvemonth all over the world^one. Continuing research and expertise building by many thousands of zoo staff worldwide continuously improves knowledge of animal, population and ecosystem management. Zoos also aim to maintain viable ex situ insurance populations of endangered species that can be used for re-introduction to the wild^2,iii. Zoo staff manages and generates funding for in situ conservation projects^one,4. Finally, zoos facilitate opportunities for researchers to increase expertise in a big variety of areas, from basic zoology to applied husbandry and molecular biological science.

When assessing the justification of holding nondomestic species in zoos, the welfare of the individual animals housed in captivity is a critical ethical upshot that has to be weighed against these aims^v. There is no unmarried proxy to mensurate the welfare of animals. Indicators typically employed include measures of survival (such as longevity, annual survival, or ageing rate), reproduction (such as fertility or litter size), physiology (such as stress hormones or the occurrence of specific diseases) and behavior (such as stereotypies)^5,6. It is typically believed that zoo animals live longer than their costless-ranging conspecifics due to the consequent provision of food, water, and shelter from harsh climates, the absence of predation and management to minimize vehement intraspecific encounters and accidents, equally well equally veterinary prophylactic and therapeutic intervention. Still, zoo animals may exist subject to behavioral deficits⁶. While an increasing number of comparative studies accept demonstrated species-specific differences in the response to zoo-conditions^7,eight,ix, and a few species-specific comparisons of survival metrics betwixt free-ranging and captive specimens have been published^10,11, big-calibration inter-specific comparisons of captive and free-ranging populations have not even so been performed. Indeed, information technology is probably difficult to gather accurate demographic estimates in these two contrasted environments for a large range of species. In mammals, comparisons between wild and zoo populations published then far were based on a small number of species (consistently less than 25) and did not command for confounding furnishings of phylogeny^12,13 or were restricted to a narrow taxonomic range (east.g. the mammalian guild Artiodactyla¹⁴). In improver, these studies have led to conflicting results because they both failed^12,thirteen and succeeded¹⁴ to detect the expected lower actuarial senescence rate (i.eastward. the rate of subtract in annual survival with increasing age) in zoos. Lastly, none of these studies included survival metrics other than senescence charge per unit, such as longevity or age at the onset of senescence. Therefore, whether the mutual belief that mammals in zoos outlast their wild counterparts holds true remains unknown.

To address this question, we compared a ready of survival metrics derived from life tables available from the literature for males and females of costless-ranging populations of 59 mammalian species (including viii dissimilar orders, see Supplementary Effigy S1) to those derived from the data on convict specimens of the same species from the Species360 database^thirteen,15 (formerly named International Species Information System database, ISIS). Based on these sex-specific life tables, four metrics describing the survival pattern of each species were calculated: longevity, baseline annual mortality, age at the onset of senescence and rate of senescence (Fig. 1). Nosotros compared these metrics between gratis-ranging and convict populations using linear models and controlled for phylogenetic relatedness among species using a mammal super-tree¹⁶. An expected higher longevity in zoos can originate from a lower baseline bloodshed, a later onset of senescence, a lower rate of senescence, or any combination of these measures (Fig. 1).

Results

In 84% of species we analyzed (85% for males and 83% for females, including all carnivores), longevity was higher in zoos than in the wild for both sexes (Figs 2 and 3A). The positive human relationship between longevity in the zoo and in the wild had a slope less than i (Table 1), indicating that brusk-lived species benefited from living in zoos to a higher extent than long-lived ones (Fig. 3A). In well-nigh 69% of the species (76% for males and 63% for females), the age at the onset of senescence was identical or delayed in zoos compared to the wild (Fig. 3B). The positive relationship betwixt zoo and wild data of onset of senescence too had a gradient less than 1 (Table 1), once more indicating that species with an early onset of actuarial senescence delayed this onset in captivity to a larger extent than species with a late onset of actuarial senescence. For these latter species, often no difference in response to captivity occurred, and some species even displayed an before onset of senescence in zoos (Supplementary Figure S2). The slopes of the human relationship between the baseline mortality (Fig. 3C) or the rates of actuarial senescence (Fig. 3D) at the zoo and in the wild were close to cypher (Table 1), indicating that these metrics did non strongly covary between zoo and wild populations. While the baseline bloodshed was lower in zoos for near 62% of the species (61% for males and 64% for females) and the rate of senescence was lower in zoos for nigh 73% of the species (76% for males and 71% for females), the nearly horizontal slopes underline the importance of the species' pace of life for these two metrics: species with a loftier baseline mortality and high rate of senescence in the wild (i.due east. species with a faster pace of life) typically had lower values at the zoo. In contrast, species with a low baseline mortality and a low rate of senescence in the wild (i.east. species with a slower stride of life) typically had higher values at the zoo. Notably, mammals in zoos displayed less variation in both baseline mortality and rate of senescence than in the wild (Fig. 3), indicating more standardized conditions in zoos. All these patterns were remarkably like for both sexes (Fig. three).

Tabular array 1 Parameter estimates (with 95% conviction interval) of linear regressions (on the log-calibration) linking the species-specific metrics obtained in zoo and free-ranging populations.

Full size table

Discussion

Our findings indicate that, in general, a life in zoos allows mammals to live longer. However, our data suggest that the species-specific stride of life influences the extent to which a given species may benefit from captivity. Species with a faster footstep of life typically suffer from high levels of environmentally-driven mortality in the wild including predation¹⁷, and zoos offer good protection against such causes of mortality. Mammals with a slower stride of life, however, are typically characterized by a later on age at showtime reproduction, a longer gestation menstruum, lower reproductive rates and lower annual mortality¹⁸. They do not do good equally much from living in zoos in terms of survivorship, or fifty-fifty take a slightly reduced longevity and college senescence rates, which might be attributable to an before onset of breeding in these species in a zoo setting^19,20. Thus, our broad-scale study supports previous piece of work reporting that both Asian and African elephant females live longer in the wild than in zoos¹⁰ (Fig. 3) and provides a first general explanation why unlike species may benefit with different magnitudes from captivity. Data for the common hippopotamus²¹, included in Fig. three for a visual comparison alongside the elephant species, corroborate this estimation. These findings emphasize that husbandry efforts to optimize the longevity of species with a slower pace of life should be intensified.

To what extent improvement of captive conditions has already occurred in zoos cannot be evaluated with our data. For long-lived species, we cannot include animals born in recent years considering of the demand to include only extinct cohorts to avoid overestimating historic period-specific bloodshed rates (i.e. just dead individuals tin can be included in life tables). If we assume that historic period-specific mortality decreases over fourth dimension in zoos thanks to improved husbandry weather, especially in recent years and independently of a species' pace of life, then the absence of contempo cohorts for long-lived species in our analyses might business relationship at least partly for our finding that the survival do good of living in zoos was less pronounced in long- than in brusque-lived species. Nosotros might expect improved living conditions in zoos to have delayed positive effects in long-lived species. For instance, at that place has been tremendous effort in building new elephant enclosures in a great number of zoos in the last decade (DWHM and MC, pers. obs.) and large-scale studies have been performed on the potential to increase captive elephant welfare²². However, the benefits of such efforts on survival measures will non be detectable before many years from now. In this respect, it should be kept in mind that our findings, specially concerning the longer-lived species, mostly reverberate past husbandry practices that are not necessarily representative any longer.

Our report refutes previous conclusions that the rate of actuarial senescence of vertebrates is not influenced past captivity^xiii. When accounting for differences in the footstep of life among species, we clearly demonstrate that faster-living species senesce at a lower rate in zoos than in the wild. In addition, we show that both males and females respond similarly to convict conditions. Such a discovery provides indirect evidence that the genuine sex activity differences in survival patterns in mammalian species subjected to high sexual choice²³ involve physiological mechanisms and cannot but be explained by higher susceptibility of males to environmental atmospheric condition.

Carnivores bear witness enhanced survival in zoos in our report, merely are more than susceptible to behavioral abnormalities⁷, highlighting the need for husbandry techniques to reduce these abnormalities while simultaneously maintaining the survival benefits. Although zoos offering simplified environments, social interactions might be equally circuitous and challenging every bit in the wild, considering the loftier frequency of non-combative contacts with humans and other species. Do animals, even when born and raised in zoos, perceive their enclosures as a spatial constraint in terms of compressed dwelling house ranges, or equally an actual restriction of freedom in terms of a limitation of their own choices? Alternatively, do animals perceive zoos as a safe habitat where potential predators, food scarcity, or extreme climatic conditions are absent, allowing them to drastically reduce vigilance²⁴? Our mere comparing of survival metrics between wild and captive populations should non be interpreted as a conclusive ethical judgment. Our findings should rather be considered equally bear witness that zoos generally raise the longevity of mammals, except in species where in that location is picayune potential for such an enhancement because of their slower footstep of life, which is already linked to both a low mortality and a high longevity in the wild. Because species with a slow pace of life are particularly threatened by extinction²⁵, maintaining ex situ insurance populations of such threatened species remains a crucial conservation strategy.

Methods

Life tables

Zoo and wild population life tables were compiled from the Species360 database and literature, respectively (run across Lemaître et al. ^xiv for more details). Concerning free-ranging populations, publications containing life-tables from semi-captive populations were excluded to let a strict comparing between convict and free-ranging populations. For 25 species, nosotros nerveless several life tables from the same or different populations. When available, we gave preference to life tables obtained from longitudinal data. When several life tables of a given quality were available, nosotros averaged them. When life tables were given in months or non with an integer of years, a standardization was made to obtain the survival at each integer historic period. For 9 species, the total number of individuals followed or considered was non given in the focal report. In such cases, we arbitrarily causeless that 100 individuals were considered per sex (close to the median value of the number of individuals live at 1 year of age in the life tables nosotros used). For wild life tables with a known total number of individuals (N = 50 species), the lowest was found for females of Mustela vison for which the life table only included xxx individuals, and the highest is observed for males of Oryctolagus cuniculus with a full of ix,020 individuals (Supplementary Table S1). For captive populations, we only used extinct cohorts of animals for which the sexual activity and both nascence and death dates were known, implying that animals were born in captivity. Extinct cohorts were defined as all cohorts born before a given year, which is determined as 2013 minus three quarters of the maximum longevity recorded for the species (Supplementary Tabular array S1). As in captivity the sexual activity ratio could be biased due to the culling of some young males during the starting time twelvemonth for management issues (mostly in ruminants), we only computed parameters when at least 25 individuals for each sex of each species were alive at 1 year of historic period to get accurate estimates of age-specific survival. Nosotros finally obtained a dataset of 52 species for which data for both females and males were available, with ane additional species with male person-only data (leading to 53 species in males) and 6 additional species with female-only data (leading to 58 species in females) (Supplementary Table S1). For both captive and wild populations, we fabricated the same calculations to obtain exactly comparable life tables. For visual comparison only, we included data from females of the 2 elephant species^26,27 and sex-combined data from the mutual hippopotamus²¹ in the resulting data plots but did not include them in the analyses, as their data did not stand for to the data pick criteria stated above.

Metrics of survival

To measure species- and sexual activity-specific patterns of survival and actuarial senescence in captive and complimentary-ranging populations, nosotros used four distinct but complementary metrics: the longevity, the baseline almanac mortality, the age at the onset of actuarial senescence and the rate of actuarial senescence (come across Fig. i. for a graphical display of these metrics). The longevity was extracted from species-specific life tables for both males and females and for both convict and wild populations (Supplementary Tabular array S1). Nosotros divers longevity equally the age at which 90% of individuals from the initial cohort (alive at i year of age) had died (Fig. 1). This allows avoiding spurious estimates due to the exceptionally long life of a few individuals¹⁵. However, this trait (called 'longevity' futurity) is non a direct measure of senescence because it does not include any explicit information about age-dependent pass up in survival. For other metrics, we first measured the logit-transformed age-specific mortality from a given life table. We thus constrained survival of 1 to be equal to 0.99, and nosotros fitted a Generalized Additive Model to obtain the historic period-specific bloodshed curve. Since both theoretical and empirical evidence reveal that actuarial senescence does not offset prior to the age of sexual maturity^28,29, the onset of actuarial senescence was defined as the age at which the annual mortality charge per unit was the lowest betwixt the age at sexual maturity and the historic period at which ninety% of individuals from the initial cohort have died (Fig. 1, Supplementary Table S1). The age at sexual maturity (in years) was collected for each sexual activity and each species from a specific literature survey (Supplementary Table S2). The baseline mortality for each sex of each species and for both captive and gratis-ranging conditions was defined equally the annual bloodshed observed at the historic period respective to the onset of senescence (Fig. 1, Supplementary Tabular array S1). The baseline mortality at the onset of actuarial senescence corresponds to the lowest mortality observed for a given sexual practice, species, and surroundings (i.e. wild or convict) betwixt the age at sexual maturity and the historic period at which 90% of individuals from the initial cohort have died. The rate of senescence was measured as the slope of the linear regression of survival (on a log scale) on age computed between the age at the onset of senescence and the historic period at which xc% of individuals from the initial cohort accept died (i.east. our measure of longevity)³⁰ (Fig. 1, Supplementary Tabular array S1). For brusk-lived species and life tables with a small sample size, we used the age at which at least v individuals of a given sex activity were still alive instead of the age at which 90% of the initial cohort was dead, both to achieve unbiased estimates due to the too few years lived past brusque-lived species, and to avert estimating survival from less than 5 individuals. All estimates are reported in Supplementary Table S1 and displayed on Fig. 2 and Supplementary Figures S2–S4.

Comparative analysis

To avoid biased assessment of the variation in survival patterns between convict and free-ranging populations, we controlled all the analyses for the non-independence betwixt species due to shared ancestry using 'Phylogenetic Generalized Least-Squares' (PGLS) models³¹. A phylogeny was built for the 59 species (Supplementary Figure S1) using the phylogenetic super-tree of mammals published by Bininda-Emonds et al. ^16,32. Survival and senescence metrics were compared between free-ranging and captive males and females using linear models. Longevity and the onset and rate of actuarial senescence metrics were log-transformed, while baseline annual bloodshed was logit-transformed prior to any analysis. In a first part, the results of which are displayed in the chief text, nosotros analyzed the relationship between the metric measured in zoos (dependent variable) and the corresponding metric measured in wild populations (independent variable). A college (for longevity and onset of senescence) or a lower (for baseline mortality and charge per unit of senescence) value in captivity indicates that the focal species performs better in zoos. In a 2d part, we tested whether the quality of demographic estimates in the wild (i.eastward. measured from longitudinal or transversal studies) and species body mass (log-transformed) influenced the relationships between captive and wild metrics. Survival and senescence patterns are strongly associated with body mass³³. Typically, larger species live longer^xviii and show a lower rate of senescence³⁴ compared to small species, and have a slower pace of life³⁵. To appraise whether the patterns we report held when accounting for size differences amidst species, nosotros included log-transformed body mass equally a covariate in our models in a secondary assay. We collected data well-nigh sex-specific hateful adult torso mass from the literature for each species analyzed (Supplementary Table S2). Therefore, for each of the four survival or senescence metrics in zoos and for a given sex activity, the full model included the corresponding wild metric and mean developed trunk mass as covariates, and the two-way interaction between the wild metric and data quality (equally a fixed factor using longitudinal data as the reference). We then reduced the model by testing nested models by likelihood-ratio tests (LRT) so that the terminal model only included variables with statistically significant furnishings. A total of 3 nested models were tested for each of the metrics analyzed (Supplementary Table S3). A Yard-exam was performed in each case. Models including the interaction between information quality and the wild estimates were never selected, whatever the survival or actuarial senescence metric considered (Supplementary Table S3). This suggests that quality of the wild demographic estimates did not influence the relationship between zoo and wild metrics. Moreover, we observed that trunk mass influenced zoo metrics in the same direction as the pace of life (Supplementary Tabular array S4), leaving the patterns unchanged, whether including torso mass in the models or not. All of these results are provided in Supplementary data (Supplementary Tables S3 and S4). For ruminant species, information technology has been shown that grazer species (whose natural nutrition consists mainly of grass) perform better than browser species (whose natural nutrition consists mainly of leaves or twigs) in captivity, in terms of survival and actuarial senescence^9,xiv. In a complementary analysis, we therefore took this pattern into business relationship and corrected the four survival and senescence metrics by including the percentage of grass in the natural diet of each ruminant species in the model. For all ruminant species, survival and senescence metrics were and then adjusted for 60% (median, N = 27) of grass in the natural diet. However, results remained remarkably similar with or without this correction (Supplementary Table S5). All analyses were performed with R version ii.14.0³⁶ and parameter estimates are given with the 95% confidence interval.

Additional Information

How to cite this article: Tidière, Thousand. et al. Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos beyond mammals. Sci. Rep. 6, 36361; doi: ten.1038/srep36361 (2016).

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Acknowledgements

Data reported in this paper originate from Species360 for convict life tables and from literature for costless-ranging life tables, and are bachelor in the Supplementary Materials (Tables S1 and S2). M.T. is funded past the French Ministry of Education and Enquiry. We thank Jeanne Peter Zocher of the Vetsuisse Faculty (Zurich) for the permission to utilize her images of hippopotamus, elephants and lion. We besides give thanks Jean-Michel Hatt, Sandra Wenger and Stamos Tahas for comments on the manuscript.

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Affiliations

Université de Lyon, F-69000, Lyon; Université Lyon 1; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622, Villeurbanne, France

Morgane Tidière, Jean-Michel Gaillard, Vérane Berger & Jean-François Lemaître
Zoologischer Garten Halle GmbH, Fasanenstr. 5a, 06114, Halle (Saale), Germany

Dennis W. H. Müller
World Clan of Zoos and Aquariums (WAZA), Gland, Switzerland

Laurie Bingaman Lackey
UMR 5175, Centre d'Ecologie Fonctionnelle et Evolutive, campus CNRS, 1919 route de Mende, 34293, Montpellier Cedex five, French republic

Olivier Gimenez
Clinic for Zoo Animals, Exotic Pets and Wild animals, Vetsuisse Kinesthesia, University of Zurich, Winterthurerstr. 260, 8057, Zurich, Switzerland

Marcus Clauss

Contributions

J.M.G., D.Westward.H.Thou., G.C. and J.F.50. designed the study; G.T., J.M.Yard., V.B., D.W.H.Grand., L.B.L., M.C. and J.F.Fifty. collated the data; M.T., J.M.Yard., V.B., O.Thousand., M.C. and J.F.L. analyzed the data; M.T. and M.C. wrote the first typhoon of the manuscript that then received input from all other authors.

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Tidière, M., Gaillard, JM., Berger, V. et al. Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals. Sci Rep 6, 36361 (2016). https://doi.org/10.1038/srep36361

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Received: 10 June 2016
Accustomed: 30 September 2016
Published: 07 Nov 2016
DOI : https://doi.org/10.1038/srep36361

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