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and rate of senescence than in the wild (Fig. 3), indicating more standardized conditions in zoos. All these patterns were remarkably similar for both sexes (Fig. 3). Discussion Our findings indicate that, in general, a life in zoos allows mammals to live longer. However, our data suggest that the species-specific pace of life influences the extent to which a given species may benefit from captivity. Species with a faster pace 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 pace of life, however, are typically characterized by a later age at first reproduction, a longer gestation period, lower reproductive rates and lower annual mortality18. They do not benefit as much from living in zoos in terms of survivorship, or even have a slightly reduced longevity and higher senescence rates, which might be attributable to an earlier onset of breeding in these species in a zoo setting19,20. Thus, our broad-scale study supports previous 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 different species may benefit with different magnitudes from captivity. Data for the common hippopotamus21, included in Fig. 3 for a visual comparison alongside the elephant species, corroborate this interpretation. These findings emphasize that husbandry efforts to optimize the longevity of species with a slower pace of life should be intensified. Figure 3. Comparison of (A) longevity, (B) age at the onset of senescence, (C) baseline annual mortality, and (D) rate of senescence (for males and females, respectively) between zoo and wild populations of 59 mammalian species. Points represent raw data, full lines represent the relationship between captive and wild estimates (on a log scale with 95% confidence interval of the model in grey) and the grey dashed line represents the equation y=x. For females, African (Loxodonta africana) and Asian (Elephas maximus) elephants and hippopotamus (Hippopotamus amphibius) were added for illustrative purposes, but were not included in the analysis. Longevity Baseline mortality Onset of senescence Rate of senescence slope intercept slope intercept slope intercept slope intercept Males 53 species 51 species 51 species 45 species 0.330 (0.191; 0.469) 6.432 (4.461; 8.403) −0.010 (−0.053; 0.033) 0.143 (0.113; 0.174) 0.538 (0.330; 0.746) 2.200 (1.122; 3.279) 0.186 (0.001; 0.372) 0.113 (0.092; 0.135) Females 58 species 56 species 56 species 48 species 0.351 (0.246; 0.456) 6.621 (4.410; 8.833) −0.010 (−0.080; 0.061) 0.115 (0.102; 0.128) 0.327 (0.123; 0.532) 2.413 (0.878; 3.947) 0.005 (−0.178; 0.188) 0.073 (0.055; 0.091) Table 1. Parameter estimates (with 95% confidence interval) of linear regressions (on the log-scale) linking the species-specific metrics obtained in zoo and free-ranging populations. Estimates were obtained from Linear Models when the phylogenetic signal λ was statistically not different from zero (i.e. for longevity, age at the onset of senescence and rate of senescence) and from Phylogenetic Generalized Least-Squares models when λ statistically differed from zero (for baseline mortality). www.nature.com/scientificreports/ Scientific Reports | 6:36361 | DOI: 10.1038/srep36361 5 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 because of the need to include only extinct cohorts to avoid overestimating age-specific mortality rates (i.e. only dead individuals can be included in life tables). If we assume that age-specific mortality decreases over time in zoos thanks to improved husbandry conditions, especially in recent years and independently of a species’ pace of life, then the absence of recent cohorts for long-lived species in our analyses might account at least partly for our finding that the survival benefit of living in zoos was less pronounced in long- than in short-lived species. We might expect improved living conditions in zoos to have delayed positive effects in long-lived species. For example, there 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 not be detectable before many years from now. In this respect, it should be kept in mind that our findings, especially concerning the longer-lived species, mostly reflect past husbandry practices that are not necessarily representative any longer. Our study refutes previous conclusions that the rate of actuarial senescence of vertebrates is not influenced by captivity13. When accounting for differences in the pace 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 captive conditions. Such a discovery provides indirect evidence that the genuine sex differences in survival patterns in mammalian species subjected to high sexual selection23 involve physiological mechanisms and cannot only
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