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Zoos need to evaluate their aim of high husbandry standards. One way of approaching this is to use the demographic data that has been collected by participating zoos for decades, assessing historical change over time to identify the presence or absence of progress. Using the example of carnivores, with data covering seven decades (1950–2019), 13 carnivore families, and 95 species, we show that juvenile mortality has decreased, and adult longevity increased, over this interval. While no reason for complacency, the results indicate that the commitment of zoos to continuously improve is having measurable consequences.

Seasonal reproduction is common in mammals. Whereas specific conditions triggering a seasonal response can only be identified in controlled experiments, large-scale comparisons of reproduction in natural habitats and zoos can advance knowledge for taxa unavailable for experimentation. We outline how such a comparison can identify species whose seasonal physiology is linked to photoperiodic triggers, and those whose perceived seasonality in the wild is the consequence of fluctuating resources without a photoperiodic trigger. This concept groups species into those that do not change their aseasonal pattern between natural habitats and zoos because they are not constrained by resources in the wild, those that do not change a seasonal pattern between natural habitats and zoos because they are triggered by photoperiod irrespective of resources, and those that change from a more seasonal pattern in the natural habitat to an aseasonal pattern in zoos because the zoo environment alleviates resource limitations experienced in the wild. We explain how detailed comparisons of mating season timing in both environments can provide clues whether a specific daylength or a specific number of days after an equinox or solstice is the likely phototrigger for a taxon. We outline relationships between life history strategies and seasonality, with special focus on relative shortening of gestation periods in more seasonal mammals. Irrespective of whether such shortening results from the adaptive value of fitting a reproductive cycle within one seasonal cycle (minimizing ‘lost opportunity’), or from benefits deriving from separating birth and mating (to optimize resource use, or to reduce infanticide), reproductive seasonality may emerge as a relevant driver of life history acceleration. Comparisons of data from natural habitats and zoos will facilitate testing some of the resulting hypotheses.

International audience; A large part of the diversity of longevity and actuarial senescence (i.e., the progressive decline of survival probabilities with age) across vertebrates can be related to body size, phylogeny, and the species' position on the slow-fast continuum of life histories. However, differences in mortality patterns between ecologically similar species, such as bovids and equids, remain poorly understood. Equids are commonly understood to outlive bovid species relative to their body mass, despite very similar feeding niches. Comparing survival patterns of 13 bovid and ten equid sub-species, our findings confirm that equids outlive bovid species, with a higher adult survival rate and a delayed onset of senescence for equids, but no difference of rate of actuarial senescence. These differences are associated with a slower generation time and longer inter-birth interval, due to a longer gestation period, for equids compared to bovids. Finally, our results suggest that all biological times (i.e., all life history traits expressed in time units) have evolved synchronously in bovids, whereas in equids gestation time and inter-birth interval either were never in synchrony with, or have slowed down relative to other biological times. Our findings suggest the existence of different selection pressures, or different constraints, on specific time-related traits between these two mammalian families.

1. Animals in seasonal environments often rely on photoperiodicity to time their reproduction. Elephants have a gestation length of approximately two years and a historical geographic distribution including higher latitudes than at present, so the evolution of a seasonal breeding pattern cued by photoperiodicity and timed to the long-day period is a theoretical option in both species. 2. We reviewed literature on reproductive patterns in free-ranging, semi-captive and captive Asian and African elephants, photoperiodic cueing, seasonal variation of body condition and other factors influencing their reproduction, as well as data from zoological collections on the timing of births. 3. Most of the free-ranging and all the semi-captive and captive elephant populations showed a moderate yet distinct seasonal breeding pattern. 4. Peak breeding activity of free-ranging Asian elephants took place in either the dry or the wet season, with no preference for short-day or long-day breeding at low latitudes (close to the equator) but a preference for long-day breeding at higher latitudes. Semi-captive Asian elephants mainly bred in the dry season when body condition was lowest and day-lengths were increasing. Peak conception often occurred in the wet season in free-ranging African elephants when body condition was highest, with no evident preference for short-day or long-day breeding at low latitudes but preference for long-day breeding at higher latitudes. 5. Asian and African elephants in zoos at latitudes from 43 to 53°N tended to conceive more often during spring and summer, i.e. when day-lengths were increasing. Body condition was not reported to vary significantly throughout the year and was rather high compared to in the wild. 6. We hypothesise that elephants are ‘long-day breeders’ in which the photoperiodic timing of conception can be influenced by many additional factors. Strategies to encourage natural conception in captive populations should include measures aimed at increasing breeding incentives in the northern hemisphere spring.

Primates, like other mammals, exhibit an annual reproductive pattern that ranges from strictly seasonal breeding to giving birth in all months of the year, but factors mediating this variation are not fully understood. We applied both a categorical description and quantitative measures of the birth peak breadth based on daily observations in zoos to characterise reproductive seasonality in 141 primate species with an average of 941 birth events per species. Absolute day length at the beginning of the mating season in seasonally reproducing species was not correlated between populations from natural habitats and zoos. The mid-point of latitudinal range was a major factor associated with reproductive seasonality, indicating a correlation with photoperiod. Gestation length, annual mean temperature, natural diet and Malagasy origin were other important factors associated with reproductive seasonality. Birth seasons were shorter with increasing latitude of geographical origin, corresponding to the decreasing length of the favourable season. Species with longer gestation periods were less seasonal than species with shorter ones, possibly because shorter gestation periods more easily facilitate the synchronisation of reproductive activity with annual cycles. Habitat conditions with higher mean annual temperature were also linked to less-seasonal reproduction, independently of the latitude effect. Species with a high percentage of leaves in their natural diet were generally non-seasonal, potentially because the availability of mature leaves is comparatively independent of seasons. Malagasy primates were more seasonal in their births than species from other regions. This might be due to the low resting metabolism of Malagasy primates, the comparatively high degree of temporal predictability of Malagasy ecosystems, or historical constraints peculiar to Malagasy primates. Latitudinal range showed a weaker but also significant association with reproductive seasonality. Amongst species with seasonal reproduction in their natural habitats, smaller primate species were more likely than larger species to shift to non-seasonal breeding in captivity. The percentage of species that changed their breeding pattern in zoos was higher in primates (30%) than in previous studies on Carnivora and Ruminantia (13 and 10%, respectively), reflecting a higher concentration of primate species in the tropics. When comparing only species that showed seasonal reproduction in natural habitats at absolute latitudes ≤11.75°, primates did not differ significantly from these two other taxa in the proportion of species that changed to a less-seasonal pattern in zoos. However, in this latitude range, natural populations of primates and Carnivora had a significantly higher proportion of seasonally reproducing species than Ruminantia, suggesting that in spite of their generally more flexible diets, both primates and Carnivora are more exposed to resource fluctuation than ruminants.

While seasonality has often been investigated with respect to reproduction, seasonality of mortality has received less attention. We investigated whether a seasonal signal of mortality exists in wild ruminants kept in zoos, using data from 60,591 individuals of 88 species. We quantified the mortality in the 3 consecutive months with the highest above-baseline mortality (3 MM). 3 MM was not related to relative life expectancy of species, indicating that seasonal mortality does not necessarily impact husbandry success. Although 3 MM was mainly observed in autumn/winter months, there was no evidence for an expected negative relationship with the latitude of the species' natural habitat and no positive relationship between 3 MM and the mean temperature in that habitat, indicating no evidence for species from lower latitudes/warmer climates being more susceptible to seasonal mortality under zoo conditions. 3 MM was related to reproductive biology, with seasonally reproducing species also displaying more seasonal mortality. This pattern differed between groups: In cervids, the onset of seasonal mortality appeared linked to the onset of rut in both sexes. This was less evident in bovids, where in a number of species (especially caprids), the onset of female seasonal mortality was linked to the lambing period. While showing that the origin of a species from warmer climate zones does not constrain husbandry success in ruminants in terms of an increased seasonal mortality, the results suggest that husbandry measures aimed at protecting females from rutting males are important, especially in cervids. Zoo Biol. 36:74–86, 2017. © 2016 Wiley Periodicals, Inc.

Life in zoological gardens provides a number of benefits to captive animals, resulting in an artificial reduction of the “struggle for life” compared to their free-ranging counterparts. These advantages should result in a higher chance of surviving from 1 year to the next, and thus in longer average life expectancies for captive animals, given that the biological requirements of the species are adequately met. Here, we compare the life expectancy of captive and free-ranging populations of three deer species (reindeer Rangifer tarandus, red deer Cervus elaphus, and roe deer Capreolus capreolus). Whereas captive reindeer and red deer had life expectancies equal to or longer than free-ranging individuals, the life expectancy of captive roe deer was shorter than that of free-ranging animals. These results support the impression that roe deer are difficult to keep in zoos, whereas reindeer and red deer perform well under human care. We suggest that the mean life expectancy of captive populations relative to that of corresponding free-ranging populations is a reliable indicator to evaluate the husbandry success of a species in captivity.

Supplementary Material, Supplementary_material for Geographical Origin, Delayed Implantation, and Induced Ovulation Explain Reproductive Seasonality in the Carnivora by Sandra A. Heldstab, Dennis W. H. Müller, Sereina M. Graber, Laurie Bingaman Lackey, Eberhard Rensch, Jean-Michel Hatt, Philipp Zerbe and Marcus Clauss in Journal of Biological Rhythms

The captive cheetah ( Acinonyx jubatus ) population is an important component in conservation planning. Cheetahs have been recorded in zoos since 1829 in Europe. Since then the global captive population has grown to 1722 in 2014, due to a combination of collection from the wild and increasingly successful captive breeding efforts. Between 1956 and 2014, 33% of the 563 total facilities holding cheetah reported reproduction, and 15% of the total captive population bred. The International Cheetah Studbook, established in 1988 within the World Association of Zoos and Aquariums, aims to record all captive cheetahs worldwide, in both zoological and private facilities. Since the studbook’s establishment the effective population size (the proportion of living breeders in the current captive population) has increased from 11.9% in 1988 to 16.4% in 2014; however, this remains lower than necessary for retention of genetic diversity. Successful cooperative breeding programs have the goal of making the captive population self-sustaining and maintaining genetic diversity.

Patterns of reproductive seasonality in the Carnivora are difficult to study comparatively, due to limited numbers of species for which information is available. Long-term databases of captive populations could overcome this difficulty. We apply a categorical description and a quantitative high-resolution measure (birth peak breadth, the number of days in which 80% of all births occur) based on daily observations in captivity to characterize the degree of reproductive seasonality in the Carnivora for 114 species with on average 1357 births per species. We find that the majority of species retained the birth seasonality displayed in the wild. Latitude of natural origin, delayed implantation, and induced ovulation were the main factors influencing reproductive seasonality. Most species were short-day breeders, but there was no evidence of an absolute photoperiodic signal for the timing of mating or conception. The length of the gestation period (corrected for body mass) generally decreased with birth seasonality but increased in species with delayed implantation. Birth seasons become shorter with increasing latitude of geographical origin, likely because the length of the favorable season declines with increasing latitude, exerting a strong selective pressure on fitting both the reproductive cycle and the interval offspring needs for growth following the termination of parental care into the short time window of optimal environmental conditions. Species with induced ovulation exhibit a less seasonal reproductive pattern, potentially because mates do not have to meet during a short time window of a fixed ovulation. Seasonal species of Carnivora shorten their gestation period so reproduction can occur during the short time window of optimal environmental conditions. Alternatively, other Carnivora species lengthen their gestation periods in order to bridge long winters. Interestingly, this occurs not by decelerating intrauterine growth but by delaying implantation.

In most mammals, both sexes display different survival patterns, often involving faster senescence in males. Being under intense sexual competition to secure mating opportunities, males of polygynous species allocate resources to costly behaviors and conspicuous sexual traits, which might explain these observed differences in longevity and senescence patterns. However, comparative studies performed to date have led to conflicting results. We aimed to resolve this problem by first reviewing case studies of the relationship between the strength of sexual selection and age-specific survival metrics. Then, we performed a comprehensive comparative analysis to test whether such relationships exist among species of captive ruminants. We found that the strength of sexual selection negatively influenced the onset of actuarial senescence in males, with males senescing earlier in polygynous than in monogamous species, which led to reduced male longevity in polygynous species. Moreover, males of territorial species senesced earlier but slower, and have a shorter longevity than males of species displaying other mating tactics. We detected little influence of the strength of sexual selection on the rate of actuarial senescence. Our findings demonstrate that the onset of actuarial senescence, rather than its rate, is a side effect of physiological mechanisms linked to sexual selection, and potentially accounts for observed differences in longevity.

There persist two widely held but mutually inconsistent views on the evolution of post-fertile lifespan of human females. The first, prevalent within anthropology, sees post-fertile lifespan (PFLS) in the light of adaptive processes, focusing on the social and economic habits of humans that selected for a lengthy PFLS.[1-3] This view rests on the assumption that human PFLS is distinct from that of other species, and focuses on quantifying the selective causes and consequences of that difference. The second view, prevalent within gerontology and comparative biology, emphasizes that PFLS is a phylogenetically widespread trait[4-6] or that human PFLS is predictable based on life-history allometries.[7] In this view, human PFLS is part of a broad cross-species pattern and its genesis cannot, therefore, rely on human-specific traits. Those who advocate the second view have questioned the “special pleading” for human specific explanations of PFLS,[4] and have argued that human PFLS is quantitatively greater but not qualitatively different than PFLS in many other animals.[5, 8] Papers asking whether human PFLS is explained by the importance of mothers more than grandmothers, whether paternal or maternal grandparents have more of an effect on child survival, or who is providing the excess calories are associated with the first view that assumes the need to explain the existence of human PFLS on the basis of a uniquely human socioecology. Anthropologists largely see human PFLS as derived, while comparative gerontologists point to evidence that it is one instance of a ubiquitous cross-species pattern. The two groups generally occupy non-overlapping research circles, in terms of conferences and journals, and therefore interact little enough to largely avoid the need to reconcile their views, allowing the persistence of misconceptions in each field. Our goal is to identify and address the most important of these misconceptions and thereby make clear that both of these seemingly incongruent views contain valid points. We argue that two distinct but related traits have been lumped together under the same concept of “post-reproductive lifespan,” one (post-fertile viability) that is tremendously widespread and another (a post-fertile life stage) that is derived to hominins, and that the differences and connections between these two traits are necessary for understanding human life-history evolution.

While it is commonly believed that animals live longer in zoos than in the wild, this assumption has rarely been tested. We compared four survival metrics (longevity, baseline mortality, onset of senescence and rate of senescence) between both sexes of free-ranging and zoo populations of more than 50 mammal species. We found that mammals from zoo populations generally lived longer than their wild counterparts (84% of species). The effect was most notable in species with a faster pace of life (i.e. a short life span, high reproductive rate and high mortality in the wild) because zoos evidently offer protection against a number of relevant conditions like predation, intraspecific competition and diseases. Species with a slower pace of life (i.e. a long life span, low reproduction rate and low 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 first general explanation about the different magnitude of zoo environment benefits among mammalian species, and thereby highlight the effort that is needed to improve captive conditions for slow-living species that are particularly susceptible to extinction in the wild.

While seasonality has often been investigated with respect to reproduction, seasonality of mortality has received less attention. We investigated whether a seasonal signal of mortality exists in wild ruminants kept in zoos, using data from 60,591 individuals of 88 species. We quantified the mortality in the 3 consecutive months with the highest above-baseline mortality (3 MM). 3 MM was not related to relative life expectancy of species, indicating that seasonal mortality does not necessarily impact husbandry success. Although 3 MM was mainly observed in autumn/winter months, there was no evidence for an expected negative relationship with the latitude of the species' natural habitat and no positive relationship between 3 MM and the mean temperature in that habitat, indicating no evidence for species from lower latitudes/warmer climates being more susceptible to seasonal mortality under zoo conditions. 3 MM was related to reproductive biology, with seasonally reproducing species also displaying more seasonal mortality. This pattern differed between groups: In cervids, the onset of seasonal mortality appeared linked to the onset of rut in both sexes. This was less evident in bovids, where in a number of species (especially caprids), the onset of female seasonal mortality was linked to the lambing period. While showing that the origin of a species from warmer climate zones does not constrain husbandry success in ruminants in terms of an increased seasonal mortality, the results suggest that husbandry measures aimed at protecting females from rutting males are important, especially in cervids. Zoo Biol. 36:74-86, 2017. © 2016 Wiley Periodicals, Inc.