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The Role of Sunlight, Artificial UV Radiation and Diet on Bone Health in Zoo Animals

It was the kind of breakthrough for which Shawn and I sometimes had to wait months. I thought of how Ezra could barely sit at the cafeteria table and how he endured karate lessons only while asking the instructor every two minutes when the hour would be up. As I watched him smile with delight I felt a deep sense of hope mixed with sadness—hope that he was taking pleasure in something, sadness that it was not with other people. For those relationships, unfortunately, remained unfulfilling. We enrolled him in special education programs for kids with autism and later a school focused on teaching social skills to kids like him, but Ezra is a loner.

When we inquired of his doctor, a talented autism specialist, about this, she assured us that Ezra will have close friends—someday. Fortunately he has his brothers, who play and fight with him as if he were any typical sibling. Ami, 12, and a social magnet at school, could not be more different but goes to any length to defend Ezra. Noam, 9, used to naturally draw Ezra into silly games.

Now he guides him to an online chat room where kids can log on and pretend to be penguins. For his 10th birthday, he received a page animal encyclopedia that became his constant companion. He pored over it in synagogue as if it were the Torah itself. On the school bus, while other kids played with their Game Boys, Ezra inhaled data about habitats and extinction rates. Not long after that, on a trip to the zoo in Portland, my father pointed out what he thought was a monkey.

Ezra corrected him. He had a remarkable recall for his interactions with them. When a school reading assignment mentioned a woodpecker, I asked if he had seen a woodpecker. It was a Friday. Rather than let him build a storehouse of animal trivia all alone, Shawn and I try to make his interest in animals a point of social connection.

At a conference Shawn met Temple Grandin, a well-known autistic author. Of course learning to live among real Homo sapiens is a more complex proposition. One Sunday at the zoo, a woman approached us. Carnivores show enhanced survival in zoos in our study, but are more susceptible to behavioral abnormalities 7 , highlighting the need for husbandry techniques to reduce these abnormalities while simultaneously maintaining the survival benefits. Although zoos offer simplified environments, social interactions might be as complex and challenging as in the wild, considering the high frequency of non-antagonistic 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 home ranges, or as 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 vigilance 24?

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Our mere comparison of survival metrics between wild and captive populations should not be interpreted as a conclusive ethical judgment. Our findings should rather be considered as evidence that zoos generally enhance the longevity of mammals, except in species where there is little potential for such an enhancement because of their slower pace 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 extinction 25 , maintaining ex situ insurance populations of such threatened species remains a crucial conservation strategy.

Concerning free-ranging populations, publications containing life-tables from semi-captive populations were excluded to allow a strict comparison between captive and free-ranging populations. For 25 species, we collected several life tables from the same or different populations. When available, we gave preference to life tables obtained from longitudinal data.

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When several life tables of a given quality were available, we averaged them. When life tables were given in months or not with an integer of years, a standardization was made to obtain the survival at each integer age. For 9 species, the total number of individuals followed or considered was not given in the focal study. In such cases, we arbitrarily assumed that individuals were considered per sex close to the median value of the number of individuals alive at 1 year of age in the life tables we used.

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For captive populations, we only used extinct cohorts of animals for which the sex and both birth 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 minus three quarters of the maximum longevity recorded for the species Supplementary Table S1. As in captivity the sex ratio could be biased due to the culling of some young males during the first year 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 age to get accurate estimates of age-specific survival.

We finally obtained a dataset of 52 species for which data for both females and males were available, with one additional species with male-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 made the same calculations to obtain exactly comparable life tables. For visual comparison only, we included data from females of the two elephant species 26 , 27 and sex-combined data from the common hippopotamus 21 in the resulting data plots but did not include them in the analyses, as their data did not correspond to the data selection criteria stated above.

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To measure species- and sex-specific patterns of survival and actuarial senescence in captive and free-ranging populations, we used four distinct but complementary metrics: the longevity, the baseline annual mortality, the age at the onset of actuarial senescence and the rate of actuarial senescence see Fig. The longevity was extracted from species-specific life tables for both males and females and for both captive and wild populations Supplementary Table S1. This allows avoiding spurious estimates due to the exceptionally long life of a few individuals 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. The age at sexual maturity in years was collected for each sex 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 free-ranging conditions was defined as the annual mortality observed at the age corresponding to the onset of senescence Fig.

The baseline mortality at the onset of actuarial senescence corresponds to the lowest mortality observed for a given sex, species, and environment i. All estimates are reported in Supplementary Table S1 and displayed on Fig. A phylogeny was built for the 59 species Supplementary Figure S1 using the phylogenetic super-tree of mammals published by Bininda-Emonds et al. 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 mortality was logit-transformed prior to any analysis. In a first part, the results of which are displayed in the main text, we analyzed the relationship between the metric measured in zoos dependent variable and the corresponding metric measured in wild populations independent variable. A higher for longevity and onset of senescence or a lower for baseline mortality and rate of senescence value in captivity indicates that the focal species performs better in zoos.


In a second part, we tested whether the quality of demographic estimates in the wild i. Survival and senescence patterns are strongly associated with body mass Typically, larger species live longer 18 and show a lower rate of senescence 34 compared to small species, and have a slower pace of life To assess whether the patterns we report held when accounting for size differences among species, we included log-transformed body mass as a covariate in our models in a secondary analysis.

We collected information about sex-specific mean adult body 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, the full model included the corresponding wild metric and mean adult body mass as covariates, and the two-way interaction between the wild metric and data quality as 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 final model only included variables with statistically significant effects. A total of 3 nested models were tested for each of the metrics analyzed Supplementary Table S3. A G-test was performed in each case. Models including the interaction between data 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 body mass influenced zoo metrics in the same direction as the pace of life Supplementary Table S4 , leaving the patterns unchanged, whether including body mass in the models or not. For ruminant species, it has been shown that grazer species whose natural diet consists mainly of grass perform better than browser species whose natural diet consists mainly of leaves or twigs in captivity, in terms of survival and actuarial senescence 9 , In a complementary analysis, we therefore took this pattern into account 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.

However, results remained remarkably similar with or without this correction Supplementary Table S5. All analyses were performed with R version 2. Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals.

Gusset, M. The global reach of zoos and aquariums in visitor numbers and conservation expenditures.

ECRP. Vol 3 No 1. A Trip to the Zoo: Children's Words and Photographs

Zoo Biol. Hoffmann, M. Science , — Conde, D. An emerging role of zoos to conserve biodiversity. Tribe, A. Assessing the role of zoos in wildlife conservation. Wildlfe 8 , 65—74 Hosey, G. Zoo Animals: Behaviour, Management, and Welfare. OUP Oxford, Mason, G. Species differences in responses to captivity: stress, welfare and the comparative method.

Trends Ecol. Clubb, R. Animal welfare: captivity effects on wide-ranging carnivores. Nature , — Why and how should we use environmental enrichment to tackle stereotypic behaviour? Mating system, feeding type and ex situ conservation effort determine life expectancy in captive ruminants.

B Biol. Compromised survivorship in zoo elephants. Science , Survey of Techniques. Email or Customer ID. Forgot password? Old Password.

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