Effects of summer microclimates on behavior of lions and tigers in zoos

The surrounding thermal environment has a direct influence on the well-being of an animal. However, few studies have investigated the microclimatic conditions that result from outdoor zoo enclosure designs and whether this affects where animals choose to spend time. Two African lions (Panthera leo) and two Siberian/Amur tigers (Panthera tigris altaica) were observed for a total of 18 full days during the summer and fall of 2009. Their activities and locations were recorded to the nearest minute of each test day. Simultaneous on-site microclimate measurements were taken of air temperature, relative humidity, solar radiation, and wind. Observations indicated that the locations where the animals chose to spend time were influenced by the microclimatic conditions. All subjects spent more time in the shade on their sunny warm days than on other days and differed from one another in their choice of shade source on all days. Temperature-comparable sunny and cloudy days showed a greater use of sun on the cloudy days. Species-specific differences between the lions (whose native habitat is hot) and the tigers (whose native habitat is temperate with cold winters) were observed with the tigers displaying more cooling behaviors than the lions in terms of solar radiation input and evaporative heat loss. The tigers were also more active than the lions. The results of this study provide new insight into how lions and tigers respond to microclimatic conditions in a captive environment.     

Past and present distribution of the North African–Asian lion subgroup: a review

• 1 The North African–Asian lion subgroup, which is composed of two subspecies, the Barbary lion, Panthera leo leo, and the Asian lion, P. l. persica, was nearly exterminated during the last centuries. The remaining free‐ranging population of Asian lions consists of c. 350 animals in India. The Barbary lion subsists as captive animals in zoos or circuses, all of which originate from the Moroccan Royal Collection. There have been multiple genetic hybridizations with sub‐Saharan lions.
• 2 Several incomplete distribution maps of the past occupation of lions were proposed in the literature. I examine the distribution of these lions with the help of a larger database, extracted from zoological, archaeological and historical reports. Some records are however not completely reliable. Data were collected over a long period of time (from the Epipaleolithic to the modern times) in Eurasia, North Africa and the Arabian Peninsula.
• 3 Dispersal took place in latitudes as far south as 15°N (Yemen) to 18°N (Mali; Chad) and as far north as 45–48°N (Bulgaria); and to longitudes as far west as 5.57°W (Morocco) and as far east as 84°E (India). Expansion was probably constrained by natural ecological factors northwards (higher seasonality, harsher winters) and southwards (extension of aridity after 3000 BP). At latitudes between 40 and 43°N, lions seem to have become a permanent part of the fauna during 6–8 millennia.
• 4 Lions were brought to extinction by humans through hunting, captures for exhibition in zoos and by the associated natural fragmentation of wild populations. The dates at which extinction took place varied greatly according to the geographical sites: 3000 BC for temperate Europe; 1000 BC in the south of Greece; 12–13th century in the Near East, Arabian Peninsula, Trans‐Caucasia or north of Afghanistan; and 19–20th century for North Africa, the Middle East and India.

     

Journey from Wilderness: Facing Dilemmas of Wild Animal Exhibits

Wild animal trade, including capture and transport of animals from faraway lands to European and American markets for public exhibition, became a well-established business by the nineteenth century. Journey by animals to the destination in rudimentary conditions caused high mortality. This is an area in history that receives scant attention today. Also, husbandry technology in zoos was in dire need of improvement in earlier years. It is easy for us to condemn the work of yesteryear by using today's prism, an act called “Presentism”. Instead, we should review the deed of our predecessors in historical perspective; judging them by today's moral standard will not get us anywhere. In early day America, traveling menageries first introduced the public to captive wild animals before zoos developed as civic institutions in increasingly urban societies. During the era, the division of circuses, menageries and zoos often blurred. This essay attempts to present a holistic review of wild animal exhibition operations including traveling menageries, circuses and zoos, focusing on selected topics from the eighteenth century through the middle of the last century. Today, even with tremendous contributions having been made, zoos still face considerable challenges in terms of wildlife conservation.     

Wild Animal Training: A Glance at Circuses and Hediger's Viewpoint

Historically, zoos have shared common features with circuses despite recent animosity toward them: Exhibition of wild animals in captivity. Experienced circus professionals can provide insight into the nature of wild animals from their sensitivity to man-made environmental components, potentially dangerous human errors, to animal escapes. These are told in numerous behind-the-scenes episodes. Zoos and circuses also have common needs such as improved animal husbandry and breeding. Moreover, both institutions face the public's naivete about animal life, and accusation about alleged cruelty to animals, often focusing on animal training. Professor Heini Hediger explained animal training from a scientific viewpoint. We can learn from his wisdom, for instance, the theoretical basis on training. Although traditional animal training has received adverse responses in recent years, accomplishments by trainers from the earlier era must be given a proper historical recognition.     

Where Are Zoos Going—or Are They Gone?

ABSTRACT

To some, zoos are prisons exploiting animals. In reality zoos range from bad to better. I make this distinction: A bad zoo makes animals work for it; a good zoo works for animals. Good zoos do effective conservation work and continually strive to improve exhibits, relevance to conservation, and inspiring public engagement for wildlife. Many zoos have improved enormously; the better ones being crucial in saving species that would have otherwise gone extinct. Nonetheless, for some people the mere word “zoo” carries impressions of old zoos, bad zoos, circuses, and theme-park shows that many find distasteful. Good zoos know they must innovate forward. As society grows increasingly estranged from nature and continues driving broad declines of wildlife, wild lands, and natural systems, the goal of zoos and every organization concerned with animal welfare should not be to separate humans from other animals, but to entangle all humans in nonhuman lives. Zoos of the next decades must become the first stage in bringing young people into life-long, engaged caring about animals. They could carry on that mission in their communities, in schools, in wild lands, as well as inside their gates. Without a strong public constituency, wild animals will not withstand continued human proliferation. Zoos and aquariums must innovate toward being a crucial force abetting the continued existence of wildness on Earth. Zoos of the future must become uplifting places of respect, rescue, enhancement, conservation, and public engagement.     

Characterization of Ovarian Steroid Patterns in Female African Lions (Panthera leo), and the Effects of Contraception on Reproductive Function

Because of poor reproduction after the lifting of an 8-year breeding moratorium, a biomedical survey of female lions in U.S. zoos was initiated in 2007. Fecal estrogen (FEM), progestagen (FPM) and glucocorticoid (FGM) metabolites were analyzed in samples collected 3–4 times per wk from 28 lions at 17 facilities (0.9–13.8 yr of age) for 4 mo—3.5 yr and body weights were obtained ~monthly from 17 animals at eight facilities (0.0–3.0 yr of age). Based on FEM, estrous cycle length averaged 17.5 ± 0.4 d in duration, with estrus lasting 4.4 ± 0.2 d. All but one female exhibited waves of estrogenic activity indicative of follicular activity; however, not all females expressed estrous behaviors (73%), suggesting silent estrus was common. Female lions experienced puberty earlier than expected; waves of estrogenic activity were observed as young as 1.1 yr of age, which may be related to a faster growth rate of captive vs. wild lions. Mean gestation length was 109.5 ± 1.0 d, whereas the non-pregnant luteal phase was less than half (46.0 ± 1.2 d). Non-mating induced increases in FPM were observed in 33% of females housed without a male, consistent with spontaneous ovulation. A number of study animals had been contracepted, and the return to cyclicity after treatment withdrawal, while variable, was ~4.0 yr and longer than the 1-yr expected efficacy, especially for those implanted with Suprelorin. For FGM, there were no differences in overall, baseline or peak mean concentrations among the age groups or across seasons, nor were there any relationships between reproductive parameters and FGM concentrations. Overall, results suggest that poor reproduction in lions after the breeding moratorium was not related to altered adrenal or ovarian steroid activity, but for some females may have been a consequence of individual institutions’ management decisions.     

华南虎现状及谱系分析

华南虎目前处于极危状态。野生个体已极为少见,只有中国一些动物园内饲养着 53只。按其亲缘关系分为上海系和贵阳系,上海系的华南虎携带优秀的多子基因,但其子代的生活力不强;而贵阳系的虎虽然产子率不高,但子代的生活力很强,现存的6只贵阳系华南虎具有极高的基因保存与基因研究价值,应建立基因库。这些虎分散饲养于22个单位,大大降低了适龄虎的交配繁殖机会,浪费了本已有限的珍贵资源,是抑制其种群发展的最主要因素。目前其种群的年龄结构非常合理,育龄虎占种群的62.3％,幼龄虎为28.3％,高龄虎很少,仅为9.4％,今后种群的发展乐观。     

Visitors' effects on the welfare of animals in the zoo: a review

Since the 1970s, research about zoo visitors' effects on the welfare of nonhuman animals in captivity has intensified. Numerous studies have shown that characteristics such as visitor presence, density, activity, size, and position are associated with animal behavioral and—to alesser extent physiological—changes. Studies usually interpret these changes as negative (undesirable) or positive (enriching), but it remains unclear whether they significantly impinge on animal welfare. To make confident conclusions about visitors' effects necessitates more studies using (a) a wider range of animal groupings, (b) measures of stress, (c) visitor-animal variables, and (d) other methodological improvements In the meantime, in addition to further research, individual zoos need to emphasize (a) monitoring the stress indicators of their captive animals, (b) observing visitor behavior, and (c) ensuring that staffs are aware of the “visitor effect” concept.     

Maintaining the genetic health of putative Barbary lions in captivity: an analysis of Moroccan Royal Lions

The last representatives of the Barbary lion (Panthera leo leo), once numerous in North Africa but exterminated from the wild by the 1940s, are believed to be the captive lions descended from the Moroccan Royal Collection, numbering less than 90 animals in zoos worldwide. The genetic fitness of these captive “Royal Lions” may now be under threat since, although most zoos have avoided hybridisation with animals of other origin, no formal breeding programme currently exists and several institutions have halted breeding activities. This situation has arisen since the distinctiveness of Barbary lions and the representative status of Royal Lions remain inconclusive and definitive molecular studies have yet to be completed. Previously, in the 1970s, morphological and phenotypic traits were used to match Royal Lions and the historic Barbary lion and an ex situ breeding programme was initiated involving a number of selected “founder” animals. This paper outlines the status of the descendent population within zoos in Morocco and Europe, including all known pure-bred descendents from the Royal Palace collection. Founder representation is shown to be greater across European collections than the Moroccan collection. Breeding exchanges are recommended between institutions in order to improve genetic diversity and maintain the genetic health of the population and a studbook for European zoo animals has been developed to support this action. This analysis serves as a benchmark for guiding effective maintenance of the captive population, thereby allowing time to clarify the conservation value of Royal Lions and their relevance to North African ecology.     

Environmental effects on the behavior of zoo-housed lions and tigers, with a case study of the effects of a visual barrier on pacing

Tigers and lions in the wild are nocturnal nonhuman animals who may hunt and mate opportunistically during daylight hours. In captivity, they spend most time on exhibit sleeping or pacing. To better understand their activity budget, this study examined the daily behavior patterns of 2 Sumatran tigers and 3 African lions in different housings. The proportion of scans the large felids spent engaged in stereotypic pacing varied by time of day and environment. The tigers spent different amounts of time pacing when housed in different exhibits; the lions paced more in off-exhibit housing than when on exhibit. These differences suggest changes to the cats' immediate housing environment may decrease pacing but provide little insight into altering specifics. Carnivores' pacing relates to their inability to control sensory access to social partners. Both environments with increased pacing contained chain-link fencing. allowing uncontrolled sensory contact. Where the tigers paced, the study placed a visual barrier between one female and keepers' or conspecifics' cues. This did not significantly decrease pacing. However, the study suggests considering sensory access and environmental variables when designing environments for captive carnivores.     

Comparative Skull Analysis Suggests Species-Specific Captivity-Related Malformation in Lions (Panthera leo)

Lion (Panthera leo) populations have dramatically decreased worldwide with a surviving population estimated at 32,000 across the African savannah. Lions have been kept in captivity for centuries and, although they reproduce well, high rates of stillbirths as well as morbidity and mortality of neonate and young lions are reported. Many of these cases are associated with bone malformations, including foramen magnum (FM) stenosis and thickened tentorium cerebelli. The precise causes of these malformations and whether they are unique to captive lions remain unclear. To test whether captivity is associated with FM stenosis, we evaluated 575 lion skulls of wild (N = 512) and captive (N = 63) origin. Tiger skulls (N = 276; 56 captive, 220 wild) were measured for comparison. While no differences were found between males and females or between subadults and adults in FM height (FMH), FMH of captive lions (17.36±3.20 mm) was significantly smaller and with greater variability when compared to that in wild lions (19.77±2.11 mm). There was no difference between wild (18.47±1.26 mm) and captive (18.56±1.64 mm) tigers in FMH. Birth origin (wild vs. captive) as a factor for FMH remained significant in lions even after controlling for age and sex. Whereas only 20/473 wild lions (4.2%) had FMH equal to or smaller than the 5^th percentile of the wild population (16.60 mm), this was evident in 40.4% (23/57) of captive lion skulls. Similar comparison for tigers found no differences between the captive and wild populations. Lions with FMH equal to or smaller than the 5^th percentile had wider skulls with smaller cranial volume. Cranial volume remained smaller in both male and female captive lions when controlled for skull size. These findings suggest species- and captivity-related predisposition for the pathology in lions.     

Seroepidemiology of Toxoplasma gondii in zoo animals in selected zoos in the midwestern United States

Toxoplasma gondii infections in zoo animals are of interest because many captive animals die of clinical toxoplasmosis and because of the potential risk of exposure of children and elderly to T. gondii oocysts excreted by cats in the zoos. Seroprevalence of T. gondii antibodies in wild zoo felids, highly susceptible zoo species, and feral cats from 8 zoos of the midwestern United States was determined by using the modified agglutination test (MAT). A titer of 1:25 was considered indicative of T. gondii exposure. Among wild felids, antibodies to T. gondii were found in 6 (27.3%) of 22 cheetahs (Acynonyx jubatus jubatus), 2 of 4 African lynx (Caracal caracal), 1 of 7 clouded leopards (Neofelis nebulosa), 1 of 5 Pallas cats (Otocolobus manul), 12 (54.5%) of 22 African lions (Panthera leo), 1 of 1 jaguar (Panthera onca), 1 of 1 Amur leopard (Panthera pardus orientalis), 1 of 1 Persian leopard (Panthera pardus saxicolor), 5 (27.8%) of 18 Amur tigers (Panthera tigris altaica), 1 of 4 fishing cats (Prionailurus viverrinus), 3 of 6 pumas (Puma concolor), 2 of 2 Texas pumas (Puma concolor stanleyana), and 5 (35.7%) of 14 snow leopards (Uncia uncia). Antibodies were found in 10 of 34 feral domestic cats (Felis domesticus) trapped in 3 zoos. Toxoplasma gondii oocysts were not found in any of the 78 fecal samples from wild and domestic cats. Among the macropods, antibodies were detected in 1 of 3 Dama wallabies (Macropus eugenii), 1 of 1 western grey kangaroo (Macropus fuliginosus), 1 of 2 wallaroos (Macropus robustus), 6 of 8 Bennett's wallabies (Macropus rufogriseus), 21 (61.8%) of 34 red kangaroos (Macropus rufus), and 1 of 1 dusky pademelon (Thylogale brunii). Among prosimians, antibodies were detected in 1 of 3 blue-eyed black lemurs (Eulemur macaco flavifrons), 1 of 21 ring-tailed lemurs (Lemur catta), 2 of 9 red-ruffed lemurs (Varecia variegata rubra), and 2 of 4 black- and white-ruffed lemurs (Varecia variegata variegata). Among the avian species tested, 2 of 3 bald eagles (Haliaeetus leucocephalus) were seropositive. Among 7 possible risk factors, sex, freezing meat temperature (above -13 C vs. below -13 C), washing vegetables thoroughly, frequency of feral cat sightings on zoo grounds (occasionally vs. frequently), frequency of feral cat control programs, capability of feral cats to enter hay/grain barn, and type of animal exhibit, exhibiting animals in open enclosures was the only factor identified as a significant risk (OR 3.22, P = 0.00).     

Environmental Effects on the Behavior of Zoo-housed Lions and Tigers,with a Case Study o the Effects of a Visual Barrier on Pacing

Tigers and lions in the wild are nocturnal nonhuman animals who may hunt and mate opportunistically during daylight hours. In captivity, they spend most time on exhibit sleeping or pacing. To better understand their activity budget, this study examined the daily behavior patterns of 2 Sumatran tigers and 3 African lions in different housings. The proportion of scans the large felids spent engaged in stereotypic pacing varied by time of day and environment. The tigers spent different amounts of time pacing when housed in different exhibits; the lions paced more in off-exhibit housing than when on exhibit. These differences suggest changes to the cats' immediate housing environment may decrease pacing but provide little insight into altering specifics. Carnivores' pacing relates to their inability to control sensory access to social partners. Both environments with increased pacing contained chain-link fencing. allowing uncontrolled sensory contact. Where the tigers paced, the study placed a visual barrier between one female and keepers' or conspecifics' cues. This did not significantly decrease pacing. However, the study suggests considering sensory access and environmental variables when designing environments for captive carnivores.     

Visitors' Effects on the Welfare of Animals in the Zoo: A Review

Since the 1970s, research about zoo visitors' effects on the welfare of nonhuman animals in captivity has intensified. Numerous studies have shown that characteristics such as visitor presence, density, activity, size, and position are associated with animal behavioral and—to alesser extent physiological—changes. Studies usually interpret these changes as negative (undesirable) or positive (enriching), but it remains unclear whether they significantly impinge on animal welfare. To make confident conclusions about visitors' effects necessitates more studies using (a) a wider range of animal groupings, (b) measures of stress, (c) visitor-animal variables, and (d) other methodological improvements In the meantime, in addition to further research, individual zoos need to emphasize (a) monitoring the stress indicators of their captive animals, (b) observing visitor behavior, and (c) ensuring that staffs are aware of the “visitor effect” concept.     

Captive breeding and infant mortality in Asian elephants: A comparison between twenty western zoos and three eastern elephant centers

Poor reproductive success compromises the long-term viability of captive Asian elephant populations. A questionnaire was designed to assess the importance of reproductive behavior and husbandry factors on breeding success. This was circulated to a number of institutions, zoos, and circuses in Asia, Europe, and North America, all of which kept Asian elephants. The aims were to compare Asian elephant breeding success in different institutions, establish possible causes for any differences, and make recommendations for improving the welfare and breeding success of the animals. The results showed that breeding success in most of the zoos was notably lower and the percentages of stillbirths and infant mortality were relatively higher when compared with those of the institutions in Asia. Female elephants in zoos appeared to reach sexual maturity and reproduce earlier than those in the Asian establishments. However, zoo elephants produced fewer young per female. The different facilities and husbandry methods used are described. Recommendations are made for both short- and long-term changes that could be used to modify existing practices to improve the welfare and breeding success of captive Asian elephants. Zoo Biol 17:311–332, 1998. © 1998 Wiley-Liss, Inc.     

Non-invasive monitoring of ovarian function in several felid species by measurement of fecal estradiol-17β and progestins

An extraction and assay procedure to measure fecal estradiol-17β and progestin concentrations in several cat species was developed and validated for use for noninvasive monitoring of ovarian function. Fecal samples were collected over a range of 3–20 months from female tigers (three), lions (three), snow leopards (three), cheetahs (two), caracals (two), and domestic cats (five). Samples were extracted with 90% methanol, lipids removed with petroleum ether, and the estradiol and progestins in the methanol measured by radioimmunoassay (RIA). High Performance Liquid Chromatography (HPLC) fractionation and subsequent RIA of the fractions indicated that the estradiol-17β antiserum cross-reacted primarily with estradiol-17β in the feces of lions and tigers and was assumed to be specific for estradiol-17β in the feces of other species as well. However, there were several immunoreactive compounds, presumably progesterone metabolites, excreted in the feces which varied both quantitatively and qualitatively among species. The behavior of tigers, lions, cheetahs, and caracals was visually monitored during the collection period and frequency of sexual behaviors was positively correlated with increases in fecal estradiol in all species observed. The mean fecal estradiol-17β peaks were as follows: tigers, 128.0 ± 13.1; lions, 186.0 ± 14.8; snow leopards, 136.7 ± 15.9; cheetahs, 140.9 ± 9.0; caracals, 24.5 ± 4.0; and domestic cats 158.9 ± 19.3 ng/gm. Fecal progestin concentrations rose significantly (P < 0.001) only after breeding or during pregnancy and were as follows: tigers, 5.6 ± 0.6; lions, 1.9 ± 0.1; cheetahs, 8.4 ± 1.1; and caracals, 2.4 ± 0.4 μg/gm. Fecal progestins were elevated for one-half to two-thirds of the gestation length during presumed pseudopregnancy but remained elevated throughout successful pregnancies. These results suggest that ovarian function can be monitored noninvasively in the family Felidae by the measurement of fecal estradiol-17β and progestin concentrations. © 1995 Wiley-Liss, Inc.     

Behavioral abnormalities in captive nonhuman primates

In this study, we dealt with 11 species of nonhuman primates across 10 zoos in India. We recorded behavior as instantaneous scans between 9 a.m. and 5 p.m. In the study, we segregated behaviors for analyses into abnormal, undesirable, active, and resting. The 4 types of abnormal behavior exhibited included floating limb, self-biting, self-clasping, and stereotypic pacing. In the study, we recorded 2 types of undesirable behavior: autoerotic stimulation and begging. Langurs and group-housed macaques did not exhibit undesirable behaviors. A male lion-tailed macaque and a male gibbon exhibited begging behavior. autoerotic stimulation and self-biting occurred rarely. Males exhibited higher levels of undesirable behavior than did females. Animals confiscated from touring zoos, circuses, and animal traders exhibited higher levels of abnormal behaviors than did animals reared in larger, recognized zoos. The stump-tailed macaque was the only species to exhibit floating limb, autoerotic stimulation, self-biting, and self-clasping. Our results show that rearing experience and group composition influence the proportions of abnormal behavior exhibited by nonhuman primates in captivity. The history of early social and environmental deprivation in these species of captive nonhuman primates probably is critical in the development of behavioral pathologies. Establishing this will require further research.     

Diagnosis and seroprevalence of leptospirosis in California sea lions from coastal California

The sensitivity and specificity of the microscopic agglutination test (MAT) as a method for detection of exposure to Leptospira spp. in California sea lions (Zalophus californianus) were determined. Sera came from individuals that demonstrated clinical signs of renal disease, had lesions suggestive of leptospirosis at necropsy, and had visible leptospires in silver stained kidney sections as positive controls. Sera from unexposed captive individuals were used as negative controls. The test was 100% sensitive at 1:3,200 for confirming renal infection and 100% specific at negative < 1:100 for detection of Leptospira interrogans scrovar pomona antibodies by MAT in California sea lions. Leptospira interrogans serovar pomona was used as a screening serovar because it has been isolated previously from the kidneys and placentas of California sea lions, and there appears to be cross-reactivity between serovar pomona and other serovars. Sera from 225 free-ranging California sea lions presented to one of three participating California (USA) coastal marine mammal rehabilitation centers in 1996 were then evaluated for antibodies to serovar pomona using the MAT. The overall seroprevalence was 38.2% (86/225), although the prevalence varied among locations from 100% (38/38) in animals at the Marine Mammal Care Center (Fort MacArthur, California, USA) to 0% (0/14) at SeaWorld California (San Diego, California). At The Marine Mammal Center (Sausalito, California) [prevalence 27.8% (48/173)], the majority of seropositive animals were subadults and adults, and males were 4.7 times more likely to be seropositive to serovar pomona than females. When combining results from all three centers, subadult and adult animals were more likely to be seropositive than pups and juvenile sea lions, and the highest proportion of seropositive animals presented during the autumn months. Serum elevations of blood urea nitrogen, creatinine, phosphorus, and/or calcium were associated with seropositivity to serovar pomona. We found no association between potassium or sodium levels and seropositivity.     

Validation of gum-line recession as a reliable technique to age tigers

Like other members of the Panthera genus, tigers are threatened throughout their range. Given their conservation status research focused on their population dynamics in the wild is needed, including population growth, lifespan, and breeding success, which requires reliable estimates of age. Current techniques to estimate age in tigers are either not reliable and/or difficult to apply in the field. Gum-line recession accurately estimates age for mountain lions, but has never been tested for tigers. The goal of this study was to determine whether gum-line recession of the upper canine teeth is a reliable indicator of age in tigers and if so, to define the equation that enables age estimation. We measured gum-line recession in 12 individuals of known ages and performed linear regression analysis to investigate the validity of this technique for tigers. We found a strong relationship between gum-line recession and age, where the model provided reliable age estimates for animals within 1-year age classes in 10 out of 12 tigers measured, providing increased accuracy over current methods.