Laurie Bingaman Lackey

Reproductive seasonality in captive wild ruminants: implications for biogeographical adaptation, photoperiodic control, and life history.

Many ruminant species show seasonal patterns of reproduction. Causes for this are widely debated, and include adaptations to seasonal availability of resources (with cues either from body condition in more tropical, or from photoperiodism in higher latitude habitats) and/or defence strategies against predators. Conclusions so far are limited to datasets with less than 30 species. Here, we use a dataset on 110 wild ruminant species kept in captivity in temperate‐zone zoos to describe their reproductive patterns quantitatively [determining the birth peak breadth (BPB) as the number of days in which 80% of all births occur]; then we link this pattern to various biological characteristics [latitude of origin, mother‐young‐relationship (hider/follower), proportion of grass in the natural diet (grazer/browser), sexual size dimorphism/mating system], and compare it with reports for free‐ranging animals. When comparing taxonomic subgroups, variance in BPB is highly correlated to the minimum, but not the maximum BPB, suggesting that a high BPB (i.e. an aseasonal reproductive pattern) is the plesiomorphic character in ruminants. Globally, latitude of natural origin is highly correlated to the BPB observed in captivity, supporting an overruling impact of photoperiodism on ruminant reproduction. Feeding type has no additional influence; the hider/follower dichotomy, associated with the anti‐predator strategy of ‘swamping’, has additional influence in the subset of African species only. Sexual size dimorphism and mating system are marginally associated with the BPB, potentially indicating a facilitation of polygamy under seasonal conditions. The difference in the calculated Julian date of conception between captive populations and that reported for free‐ranging ones corresponds to the one expected if absolute day length was the main trigger in highly seasonal species: calculated day length at the time of conception between free‐ranging and captive populations followed a y = x relationship. Only 11 species (all originating from lower latitudes) were considered to change their reproductive pattern distinctively between the wild and captivity, with 10 becoming less seasonal (but not aseasonal) in human care, indicating that seasonality observed in the wild was partly resource‐associated. Only one species (Antidorcas marsupialis) became more seasonal in captivity, presumably because resource availability in the wild overrules the innate photoperiodic response. Reproductive seasonality explains additional variance in the body mass–gestation period relationship, with more seasonal species having shorter gestation periods for their body size. We conclude that photoperiodism, and in particular absolute day length, are genetically fixed triggers for reproduction that may be malleable to some extent by body condition, and that plasticity in gestation length is an important facilitator that may partly explain the success of ruminant radiation to high latitudes. Evidence for an anti‐predator strategy involving seasonal reproduction is limited to African species. Reproductive seasonality following rainfall patterns may not be an adaptation to give birth in periods of high resource availability but an adaptation to allow conception only at times of good body condition.

Does sexual selection shape sex differences in longevity and senescence patterns across vertebrates? A review and new insights from captive ruminants

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.

Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals

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.

Relevance of management and feeding regimens on life expectancy in captive deer

OBJECTIVE To establish a demographic approach to facilitate the comparison of husbandry success for deer species in zoos and to test for factors that influence the performance of deer species in captivity. SAMPLE POPULATION Data collected from 45,736 zoo-kept deer that comprised 31 species. PROCEDURES Data had been collected by the International Species Information System during the last 3 decades on zoo-kept deer around the world. The relative life expectancy (rLE) of a species (ie, mean life expectancy as a proportion of the maximum recorded life span for that species) was used to describe zoo populations. The rLE (values between 0 and 1) was used to reflect the husbandry success of a species. RESULTS A significant positive correlation was found between the rLE of a species and the percentage of grass in the natural diet of the species, suggesting that there are more problems in the husbandry of browsing than of grazing species. The 4 species for which a studbook (ie, record of the lineage of wild animals bred in captivity) was maintained had a high rLE, potentially indicating the positive effect of intensive breeding management. CONCLUSION AND CLINICAL RELEVANCE The rLE facilitated the comparison of husbandry success for various species and may offer the possibility of correlating this quotient with other biological variables. Ultimately, identifying reasons for a low husbandry success in certain species may form the basis for further improvements of animal welfare in captivity.

Geographical Origin, Delayed Implantation, and Induced Ovulation Explain Reproductive Seasonality in the Carnivora:

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.

Seasonality of reproduction in Asian elephants Elephas maximus and African elephants Loxodonta africana: underlying photoperiodic cueing?

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.