Environmental influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in Southern India

To eliminate abnormal behaviors in leopards (Panthera pardus), such as stereotypic pacing, by utilizing environmental enrichment techniques, a proper understanding of their behavior in captive environments is required. Hence there is a need for animal welfare studies in Indian zoos. The activity budgets of 16 leopards were recorded across four southern Indian zoos: Thiruvananthapuram Zoo, Arignar Anna Zoological Park, Shri Chamarajendra Zoological Gardens, and the Guindy Children's Park. Of the 16 study animals, 14 were studied on‐exhibit on zoo holidays as well as on days with visitors present, and all 16 individuals were studied off‐exhibit on other days with visitors present. The 11 behaviors recorded were categorized into active, resting, and stereotypic behaviors. Leopards exhibited higher levels of activity in the on‐exhibit enclosures on days with no visitors. Feeding time influenced the behavioral repertoire of all 14 leopards studied on‐exhibit. Lower proportions of resting were exhibited during the hours before feeding. The proportion of active behaviors differed significantly across zoos. Stereotypic pacing levels were not influenced by the presence of visitors or by feeding time, but was significantly influenced by enclosure features. Higher levels of stereotypic pacing were exhibited in off‐exhibit than on‐exhibit enclosures. Our study shows that the behavior of captive leopards is influenced by enclosure type, feeding regime, and the presence of visitors. Zoo Biol 21:585–595, 2002. © 2002 Wiley‐Liss, Inc.     

The effect of competing carnivores on the feeding behaviour of leopards (Panthera pardus) in an African savanna

Knowledge of competition dynamics among Africa’s large carnivores is important for conservation. However, investigating carnivore behaviour in the field can be challenging especially for species that are difficult to access. Methods that enable remote collection of data provide a means of recording natural behaviour and are therefore useful for studying elusive species such as leopards (Panthera pardus). Camera traps and Global Positioning System (GPS) collars are powerful tools often used independently to study animal behaviour but where their data are combined, the interpretation of a species’ behaviours is improved. In this study we used data from baited camera trap stations to investigate the feeding habits of leopards at Malilangwe Wildlife Reserve, Zimbabwe. We investigated the influence of spotted hyenas, lions and other competing leopards on the feeding duration of leopards using Generalized Linear Mixed Effects Modelling. To test the influence of competing predators on resting distances from bait sites, eight leopards were fitted with GPS collars. Results showed that leopards spent the shortest time feeding on the baits in the presence of competing male leopards compared to other predators while lion presence caused animals to rest farthest from bait sites. Interaction analysis indicated that small‐bodied leopards spent significantly shorter durations feeding when spotted hyenas were present. Our findings demonstrate that competition from guild carnivores has negative impacts on the food intake of leopards, which may have implications for fitness and survival. This study provides a snapshot of the competition dynamics at bait sites which may give insight to ecosystem level interactions among large carnivores in savanna ecosystems.     

A survey assessment of variables related to stereotypy in captive giraffe and okapi

Stereotypic behavior has been investigated in a wide variety of animals, but little published information is available on this problem in captive exotic ungulates. A survey was used to gather information on the prevalence of stereotypic behavior in giraffe and okapi and to identify variables associated with these behaviors. Of the 71 institutions that received a survey, 69.0% responded. Data were reported for 257 individuals, including 214 giraffe (representing five subspecies) and 29 okapi. Of the animals included in the survey, 79.7% performed at least one type of stereotypic behavior. Licking of non-food objects (72.4%) and pacing (29.2%) were the most prevalent stereotypic behaviors, though other stereotypies were reported in 3.2% of the animals. The results of a logistic regression performed on the data indicated that sub species, number of hours the individuals spent indoors, access at night to conspecifics, feeding frequency, method of feeding, and type of food provided were predictors of stereotypic licking. Sub species, birth history, size of the indoor enclosure, environmental change, and type of food provided were found to be significant predictors of stereotypic pacing. In general, feeding motivation appears to be related to an oral stereotypy, whereas other environmental factors appear to be associated with a locomotor stereotypy. The results of this study suggest changes in management strategies that may be empirically studied and applied to improve the well-being of captive populations of giraffe and okapi.     

Quantification of abnormal repetitive behaviour in captive European starlings (Sturnus vulgaris)

Stereotypies are repetitive, unvarying and goalless behaviour patterns that are often considered indicative of poor welfare in captive animals. Quantifying stereotypies can be difficult, particularly during the early stages of their development when behaviour is still flexible. We compared two methods for objectively quantifying the development of route-tracing stereotypies in caged starlings. We used Markov chains and T-pattern analysis (implemented by the software package, Theme) to identify patterns in the sequence of locations a bird occupied within its cage. Pattern metrics produced by both methods correlated with the frequency of established measures of stereotypic behaviour and abnormal behaviour patterns counted from video recordings, suggesting that both methods could be useful for identifying stereotypic individuals and quantifying stereotypic behaviour. We discuss the relative benefits and disadvantages of the two approaches.     

Stereotypic behavior in Asiatic black and Malayan sun bears

The stereotypies of individually caged Asiatic black bears (Ursus thibetanus) and Malayan sun bears (Helarctos malayanus) were studied in detail. Stereotypies were performed by 27 of the 29 subjects, were primarily locomotory in form (e.g., pacing), and occupied on average 18% (standard error of the mean (SEM)=2.5) of daylight hours. Stereotypy levels during the night were almost negligible and were highly correlated with daytime levels. Total stereotypies peaked prior to food arrival, although oral stereotypies were most frequent after feeding. In general, stereotypies were performed in locations from which food arrival could be viewed, although Asiatic black bears were equally likely to exhibit stereotypy near a neighboring bear. Across individuals, stereotypy frequency was inversely correlated with inactivity and increased with age. Older bears also showed less normal activity and a reduced diversity of normal behavior. Stereotypy levels were unrelated to levels of “compulsive” behavior (e.g., hair plucking) or repetitive self‐sucking–a potential deprivation stereotypy. More frequent stereotypies were performed more invariantly (i.e., were more predictable from one repetition to the next) and in more diverse contexts, namely 1) outside the pre‐feeding period, and 2) during the night. Contrary to observations reported elsewhere, higher frequencies of stereotypy were not associated with reduced behavioral diversity, or with a more elaborate repertoire of stereotypy forms and sequences. Although the two species did not differ in overall frequency, the stereotypies of sun bears appeared to be more food‐motivated than those of Asiatic black bears: the sun bears displayed a higher frequency and diversity of oral stereotypies, and higher levels of pre‐feeding stereotypy, and performed significantly more of their total stereotypies in locations from which they could view food arrival. This study demonstrates how analyzing stereotypies in detail can help identify the motivations that underlie these behaviors, and potentially reveal their degree of establishment–both of which are important factors in stereotypy treatment. Zoo Biol 23:409–430, 2004. © 2004 Wiley‐Liss, Inc.     

Do tigers displace leopards? If so, why?

We investigated predictions concerning the competitive relationships between tigers Panthera tigris and leopards Panthera pardus in Bardia National Park, Nepal, based on spatial distributions of scats and territorial markings (sign), analyses of scat content and census of wild ungulate prey. Medium-sized ungulates, in particular chital Axis axis, was the main food of both predators, but leopards consumed significantly larger proportions of domestic animals, small mammals, and birds than tigers. Tiger sign were never found outside the park, while leopard sign occurred both inside and outside, and were significantly closer to the park border than tiger sign. Significantly higher prey densities at locations of tiger sign than that of leopards were mainly due to a preference of the latter species for the park border areas. Our results imply that interference competition––and not competition for food––was a limiting factor for the leopard population, whose distribution was restricted to the margins of the tiger territories. We suggest that the composition of the prey base is a key factor in understanding the different results and interpretations reported in studies on tiger/leopard coexistence. There are two potential mechanisms that link interference competition and prey: (1) low abundance of large ungulate prey decreases foraging efficiency of tigers, leading to increased energetic stress and aggression towards leopards; and (2) increased diet overlap due to scarcity of large prey leads to increased encounter rates and increased levels of interference competition.     

Effects of temporary closure of a national park on leopard movement and behaviour in tropical Asia

Across Asia protected areas serve as refuges for carnivores inside human-dominated landscapes. However, the creation of hard edges around reserve boundaries where conflicts with humans arise and disturbance from human activities inside the reserves may affect carnivore behaviour and ecology. Thailand’s largest protected area, Kaeng Krachan National Park (2915 km²) receives >100,000 visitors annually while maintaining an intact assemblage of prey species for large carnivores, making it a potentially important site for population recovery of leopards (Panthera pardus), tigers (Panthera tigris) and dholes (Cuon alpinus). We assessed the abundance of leopards and their prey base, and their response to changes in levels of human activity after an unexpected flooding event that resulted in the park being closed to visitors for >6 months. Using camera-traps, we identified 6 individual leopards and used spatially explicit capture-recapture (SECR) methods, incorporating humans and prey as covariates, to test for factors affecting the detection probability of leopards before and after the park closure. Leopard density was unchanged between the two periods, however the movement and activity patterns were clearly different. In the absence of tourist activity, leopards tended to move more frequently, leopard detection rates increased by 70% and activity shifted towards being more diurnal. The consequences of these changes in behaviour may include improved health, reproduction and survival. A management strategy involving seasonal closure of parks may serve to alleviate pressure on leopards and other carnivores. We recommend using information on abundance of large carnivores and their prey species, and human disturbance as the key indicators for long-term monitoring and management of protected areas in Southeast Asia.     

Frustrated appetitive foraging behavior, stereotypic pacing, and fecal glucocorticoid levels in snow leopards (Uncia uncia) in the Zurich Zoo

This study hypothesized that permanently frustrated, appetitive-foraging behavior caused the stereotypic pacing regularly observed in captive carnivores. Using 2 adult female snow leopards (Uncia uncia), solitarily housed in the Zurich Zoo, the study tested this hypothesis experimentally with a novel feeding method: electronically controlled, time-regulated feeding boxes. The expected result of employing this active foraging device as a successful coping strategy was reduced behavioral and physiological measures of stress, compared with a control-feeding regime without feeding boxes. The study assessed this through behavioral observations and by evaluating glucocorticoid levels noninvasively from feces. Results indicated that the 2 snow leopards did not perform successful coping behavior through exercising active foraging behavior or through displaying the stereotypic pacing. The data support a possible explanation: The box-feeding method did not provide the 2 snow leopards with the external stimuli to satisfy their appetitive behavioral needs. Moreover, numerous other factors not necessarily or exclusively related to appetitive behavior could have caused and influenced the stereotypic pacing.     

Environmentally Enriched Male Mink Gain More Copulations than Stereotypic,Barren-Reared Competitors

Wild carnivores in zoos, conservation breeding centres, and farms commonly live in relatively small, unstimulating enclosures. Under these captive conditions, in a range of species including giant pandas, black-footed ferrets, and European mink, male reproductive abilities are often poor. Such problems have long been hypothesized to be caused by these animals'' housing conditions. We show for the first time that rearing under welfare-improving (i.e., highly valued and stress-reducing) environmental enrichments enhances male carnivores'' copulatory performance: in mate choice competitions, enriched male American mink (Neovison vison) mated more often than non-enriched males. We screened for several potential mediators of this effect. First was physiological stress and its impact on reproductive physiology; second, stress-mediated changes in morphology and variables related to immunocompetence that could influence male attractiveness; and third, behavioural changes likely to affect social competence, particularly autistic-like excessive routine and repetition (‘perseveration’) as is reflected in the stereotypies common in captive animals. Consistent with physiological stress, excreted steroid metabolites revealed that non-enriched males had higher cortisol levels and lower androgen levels than enriched conspecifics. Their os penises (bacula) also tended to be less developed. Consistent with reduced attractiveness, non-enriched males were lighter, with comparatively small spleens and a trend to greater fluctuating asymmetry. Consistent with impaired social competence, non-enriched males performed more stereotypic behaviour (e.g., pacing) in their home cages. Of all these effects, the only significant predictor of copulation number was stereotypy (a trend suggesting that low bodyweights may also be influential): highly stereotypic males gained the fewest copulations. The neurophysiological changes underlying stereotypy thus handicap males sexually. We hypothesise that such males are abnormally perseverative when interacting with females. Investigating similar problems in other taxa would be worthwhile, since many vertebrates, wild and domestic, live in conditions that cause stereotypic behaviour and/or impair neurological development.     

Unterartenfrage Persischer Leoparden geklärt

The Studbook for the Persian Leopard, Panthera pardus saxicolor, was analyzed. The whole population derives from a few founder animals, imported in the midth fifties from Iran and in the late sixties from Afghanistan. To avoid inbreeding later on the Iranian and the Afghan lines were mixed. A female imported in 1968 from Kabul to Cologne is represented in each of the more than 100 animals living today.This study deals with the question of subspecies of leopards in Afghanistan. Out of the 27 subspecies described four are believed to exist in Afghanistan. However, according to a molecular-biological revision of the species there is only one subspecies in Afghanistan, Panthera pardus saxicolor. To clarify the subspecies question various measures of furs have been taken in the bazars. The results revealed that the leopards in Afghanistan are the biggest of its species. However a further differentiation according to the area of origin within the country was not possible. Also the traditional differentiation on the basis of colours and patterns on the furs was not possible.In contrast to the molecular-biological investigations published, not only samples of zoo animals were available in this study but also samples from the wild. The results confirm that almost all leopards from Afghanistan and Iran belong to one and the same subspecies. Only in the most eastern part of Afghanistan, the Indian leopard, Panthera pardus fusca, can be found.Mixing the two lines subsequently is justified by the results of this study. Recently acquired animals from the Caucasus, however, should be tested genetically before integrating them into the zoo population.     

The effects of physical characteristics of the environment and feeding regime on the behavior of captive felids

The behavior of captive felids is influenced by enclosure design and management regime. The behavior of nine felid species housed in 11 enclosures was recorded using instantaneous scan sampling. Stereotypic pacing was observed in 15 out of 19 individuals. Size of enclosure did not affect pacing behavior, but edges of enclosures were found to be used specifically for pacing behavior. Cats in relatively larger enclosures had a higher level of apparent movement, but only about 50% of enclosure space was used. Raised areas such as tree branches were found to be preferred sites in enclosures, particularly for observation of surroundings. The feeding regime was found to affect stereotypic pacing levels. Cats fed on a 3 day cycle paced more on fast days than on days they were fed. Although not statistically significant, 6 out of 7 of these cats paced more in the hour after feeding, whereas the cats fed daily paced more in the hour before feeding. Further research is required to understand the relationship between feeding and stereotypic behavior. Zoo Biol 16:71–83, 1997. © 1997 Wiley-Liss, Inc.     

Environmental enrichment reduces behavioural alterations induced by chronic stress in Japanese quail

Animals perceiving repeated aversive events can become chronically stressed. Chronic activation of the hypothalamic–pituitary–adrenal (HPA) axis can have deleterious consequences on physiological parameters (e.g. BW, blood chemistry) and behaviour (e.g. emotional reactivity, stereotypies, cognition). Environmental enrichment (EE) can be a mean to reduce animal stress and to improve welfare. The aim of this study was first, to assess the effects of EE in battery cages on the behaviour of young Japanese quail and second, to evaluate the impact of EE on quail exposed to chronic stress. The experiment involved quail housed in EE cages and submitted or not to a chronic stress procedure (CSP) (EE cages, control quail: n=16, CSP quail: n=14) and quail housed in standard cages and exposed or not to the CSP (standard non-EE cages, control quail: n=12, CSP quail: n=16). Our procedure consisted of repeated aversive events (e.g. ventilators, delaying access to food, physical restraint, noise) presented two to five times per 24 h, randomly, for 15 days. During CSP, EE improved quail’s welfare as their stereotypic pacing decreased and they rested more. CSP decreased exploration in all quail. After the end of CSP, quail presented increased emotional reactivity in emergence test. However, the effect of EE varied with test. Finally, chronic stress effects on comfort behaviours in the emergence test were alleviated by EE. These results indicate that EE can alleviate some aspects of behavioural alterations induced by CSP.     

Tongue twisters: feeding enrichment to reduce oral stereotypy in giraffe

Stereotypic behavior has been well‐studied and documented in a variety of animals including primates, carnivores, and domesticated ungulates. However, very little information is known about stereotypic behavior of captive exotic ungulates. Giraffe have been found to perform a wide range of stereotypic behaviors. According to a survey of zoological institutions, oral stereotypies, specifically the licking of nonfood objects are the most prevalent stereotypic behaviors observed in giraffe. Their performance appears to be related to feeding and rumination and may be a result of the inability of a highly motivated feeding behavior pattern, tongue manipulation, to be successfully completed. To test this hypothesis, the indoor and outdoor feeders for three giraffe housed at Zoo Atlanta were modified to require the giraffe to perform more naturalistic and complex foraging behaviors. Data were collected using instantaneous scan sampling in both exhibit and holding areas. Our results showed that, for the giraffe that engaged in the highest rates of oral stereotypic behavior in the baseline, more complex feeders that required tongue use to access grain or alfalfa had the greatest effect on behavior. For the giraffe that performed low baseline rates of oral stereotypic behavior, adding slatted tops to the alfalfa feeders indoors virtually eliminated the behavior. Although some changes in ruminating and feeding behavior were observed, the decreases in stereotypic behavior were not associated with the changes in ruminating or feeding behavior. These results provide evidence for the hypothesis that oral stereotypy in herbivores can be reduced by encouraging giraffe to engage in more naturalistic foraging behavior. Zoo Biol 27:200–212, 2008. © 2008 Wiley‐Liss, Inc.     

A quantitative study of copulatory behaviour of large Felidae

A total of 109 copulations was observed in six male-female pairs from four species of large Felidae. The mean intromission durations were 3.0 sec for Asian leopards (Panthera pardus), 3.3 sec for African leopards (Panthera pardus), 12.9 sec for snow leopards (Uncia uncia), 2.3 sec for spotted jaguars (Panthera onca), 3.3 sec for black jaguars (Panthera onca), and 12.4 sec for Siberian tigers (Panthera tigris). Behavioural patterns were qualitatively similar across species; all displayed a copulatory pattern with no lock, no intra-vaginal thrusting, ejaculation on a single insertion, and multiple ejaculations. Whereas domestic cats are reported to assume a neck grip and to tread prior to insertion, these larger Felidae generally did so after intromission had been achieved. After copulation, females of some pairs swiped at the male and displayed a rolling after-reaction.     

A Survey of Abnormal Repetitive Behaviors in North American River Otters Housed in Zoos

Stereotypic behaviors, indicating poor welfare and studied in a variety of species (especially carnivores), appear related to characteristics of current and past environments. Although North American river otters (Lontra canadensis) often develop abnormal, repetitive, possibly stereotypic behaviors, no published reports describe otter housing and management or characterize how these variables relate to abnormal repetitive behavior (ARB) occurrence. The first author developed surveys to gather data on housing, individual history, management, and the prevalence of ARBs in otters housed in facilities accredited by the Association of Zoos and Aquariums. Consistent with anecdotal evidence that otters are prone to ARBs, 46% of river otters in the study exhibit them. ARBs were mostly locomotor and often preceded feeding. Exhibits where otters were fed and trained housed a greater percentage of nonhuman animals with ARBs. This study supports the Tarou, Bloomsmith, and Maple (2005) report that more hands-on management is associated with higher levels of ARBs because management efforts are only for animals with ARBs. Escape motivation, breeding season, feeding cues, and ability to forage may affect ARBs in river otters and should be investigated.     

Plasma cortisol and faecal cortisol metabolites concentrations in stereotypic and non-stereotypic horses: do stereotypic horses cope better with poor environmental conditions?

Background

Stereotypic behaviours, i.e. repetitive behaviours induced by frustration, repeated attempts to cope and/or brain dysfunction, are intriguing as they occur in a variety of domestic and captive species without any clear adaptive function. Among the different hypotheses, the coping hypothesis predicts that stereotypic behaviours provide a way for animals in unfavourable environmental conditions to adjust. As such, they are expected to have a lower physiological stress level (glucocorticoids) than non-stereotypic animals. Attempts to link stereotypic behaviours with glucocorticoids however have yielded contradictory results. Here we investigated correlates of oral and motor stereotypic behaviours and glucocorticoid levels in two large samples of domestic horses (N _Study1 = 55, N _Study2 = 58), kept in sub-optimal conditions (e.g. confinement, social isolation), and already known to experience poor welfare states. Each horse was observed in its box using focal sampling (study 1) and instantaneous scan sampling (study 2). Plasma samples (collected in study 1) but also non-invasive faecal samples (collected in both studies) were retrieved in order to assess cortisol levels.

Results

Results showed that 1) plasma cortisol and faecal cortisol metabolites concentrations did not differ between horses displaying stereotypic behaviours and non-stereotypic horses and 2) both oral and motor stereotypic behaviour levels did not predict plasma cortisol or faecal cortisol metabolites concentrations.

Conclusions

Cortisol measures, collected in two large samples of horses using both plasma sampling as well as faecal sampling (the latter method minimizing bias due to a non-invasive sampling procedure), therefore do not indicate that stereotypic horses cope better, at least in terms of adrenocortical activity.     

Hunting behaviour in West African forest leopards

The leopard (Panthera pardus) is a major predator of mammals within the rainforest ecosystem of West Africa. Most of the available information on leopard hunting behaviour comes from studies conducted in open savannah habitats, while little is known about forest leopards. Our radio‐tracking data and scat analysis show that forest leopards differ in various ways from the savannah populations. Forest leopards are diurnal and crepuscular hunters who follow the activity pattern of their prey species. They exhibit seasonal differences in activity patterns, and they develop highly individualized prey preferences. These findings challenge the widespread notion of leopards as opportunistic nocturnal predators.     

THE OLFACTORY-GUSTATORY BASIS OF FOOD PREFERENCE IN THE HERBIVOROUS PROSOBRANCH, LITTORINA LITTOREA (LINNAEUS)

Studies of food preference often measure the rate of consumptionof prey items by a predator; this confounds the factors determiningattractiveness and edibility, ignoring the fact that preferencesare probably resolved at the pre-ingestive stage of a consumer'sfeeding behaviour. In this paper, a novel technique has beendeveloped to measure the importance of chemical stimuli to feed,perceived by olfactory and gustatory means, as determinantsof the subsequent feeding behaviour of the generalist intertidalherbivore,Littorina littorea (L.). Cell-free extracts of a rangeof algae were presented simultaneously, impregnated in artificialcellulose-based substrates. Subsequent ranking of feeding preferencesreveals hierarchies which correspond with those establishedby other workers, using intact algae to feed L. littorea. Extractsof ephemeral early successional species (e.g. Ulva lactuca,Porphyra umbilicalis) generally provoke a more positive feedingresponse than perennial late successional species (e.g. Fucusvesiculosus, Asco-phyllum nodosum). Animals fed a preferredalga (Ulva lactuca) prior to preference trials displayed a reductionin the strength of preference relative to starved animals. Therewas no evidence of ‘switching’ of preference rankingsdue to satiation, however. These findings confirm the importanceof olfactory-and gustatory-mediated feeding behaviour as theprimary determinant of food preference in L. littorea. Theyare consistent with the hypothesis that the factors which determinethe attractiveness of a food type, such as chemical cues, arethe criteria by which consumers predict the value of that food.     

Stereotypic behavior of a female Asiatic elephant (Elephas maximus) in a zoo

This study recorded daytime behavior of a female Asiatic elephant at the Municipal Zoo, Wroclaw, Poland, in both an indoor pen and an outdoor paddock as continuous scan sampling for 140 hr, over 35 days in 1 year. Stereotypic sequences involved bouts of highly repetitive stereotypic movements and much more variable interbout behavior. The study found both stereotypic movements, nodding and body (corpus) swaying, were asymmetric, accompanied by protraction of the right hind leg and to-and-fro swinging of the trunk. The elephant spent 52% of the daytime in stereotypic movements, 3.5 times the level reported for females in other zoos' groups. The share of time devoted to stereotypic behavior was lowest in the summer when the elephant was regularly released to the paddock and highest in the late fall after she had stayed in the pen after months of days outside. This suggests that changes in the management routine enhance stereotypies. Comparing the summer and winter stable management periods, stereotypies were much more frequent in the indoor pen than the outdoor paddock, suggesting that the confinement to a barren pen contributed to the observed levels of stereotypies.     

Individual identification of Amur leopards (Panthera pardus orientalis) using molecular-genetic methods and the population size estimation

For the first time, the genetic structure of a population of Amur leopards (Panthera pardus orientalis) in southwest Primorie was analyzed in detail. In 2010–2012, 23 individuals were identified individually. It was shown that the studied microsatellite markers are suitable for individual identification of leopards, monitoring the population numbers, and creating a unified database of genetic profiles of this species to solve research and nature-conservation tasks.