Variation in dental wear and tooth loss among known‐aged,older ring‐tailed lemurs (Lemur catta): a comparison between wild and captive individuals

Tooth wear is generally an age‐related phenomenon, often assumed to occur at similar rates within populations of primates and other mammals, and has been suggested as a correlate of reduced offspring survival among wild lemurs. Few long‐term wild studies have combined detailed study of primate behavior and ecology with dental analyses. Here, we present data on dental wear and tooth loss in older (>10 years old) wild and captive ring‐tailed lemurs (Lemur catta). Among older ring‐tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar (n=6), the percentage of severe dental wear and tooth loss ranges from 6 to 50%. Among these six individuals, the oldest (19 years old) exhibits the second lowest frequency of tooth loss (14%). The majority of captive lemurs at the Indianapolis Zoo (n=7) are older than the oldest BMSR lemur, yet display significantly less overall tooth wear for 19 of 36 tooth positions, with only two individuals exhibiting antemortem tooth loss. Among the captive lemurs, only one lemur (a nearly 29 year old male) has lost more than one tooth. This individual is only missing anterior teeth, in contrast to lemurs at BMSR, where the majority of lost teeth are postcanine teeth associated with processing specific fallback foods. Postcanine teeth also show significantly more overall wear at BMSR than in the captive sample. At BMSR, degree of severe wear and tooth loss varies in same aged, older individuals, likely reflecting differences in microhabitat, and thus the availability and use of different foods. This pattern becomes apparent before “old age,” as seen in individuals as young as 7 years. Among the four “older” female lemurs at BMSR, severe wear and/or tooth loss do not predict offspring survival. Am. J. Primatol. 72:1026–1037, 2010. © 2010 Wiley‐Liss, Inc.     

Tailored Enrichment Strategies and Stereotypic Behavior in Captive Individually Housed Macaques (Macaca spp.)

The welfare of nonhuman animals in captivity is widely dependent on the natural psychological, physical, and behavioral needs of the animals and how adequately these needs are met. Inability to engage in natural behaviors can lead to chronic stress and expression of stereotypic behavior. The majority of research on decreasing stereotypic behavior in captivity addresses problems at the group level and does not account for individual variability in each animal's needs, history, and preferences. This study combined physiological and behavioral measures of well being to comprehensively assess the unique needs of individually housed captive macaques (Macaca spp.) with the aim of developing tailored welfare strategies. Behavioral and hormonal data were collected under 2 conditions: baseline and individualized enrichment. The results showed a significant decrease in stereotypic behavior under the enrichment condition. Additionally, 7 out of 9 individuals showed a decrease in fecal glucocorticoid (stress hormone) levels, indicating a reduction in hypothalamic-pituitary-adrenal activity. Addressing welfare on an individual, rather than group, level allows for a better overall characterization of well being and maximizes the probability of improving the welfare of each animal.     

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.     

Assessing the Welfare of Dairy Cattle

This article attempts to determine the effects of environment (captive or wild) and a simple form of environmental enrichment on the behavior and physiology of a nonhuman animal. Specifically, analyses first compared behavioral budgets and stereotypic behavior of captive coyotes (Canis latrans) in kennels and pens to their counterparts in the wild. Second, experiments examined the effect of a simple form of environmental enrichment for captive coyotes (food-filled bones) on behavioral budgets, stereotypies, and corticosteroid levels. Overall, behavioral budgets of captive coyotes in both kennels and pens were similar to those observed in the wild, but coyotes in captivity exhibited significantly more stereotypic behavior. Intermittently providing a bone generally lowered resting and increased foraging behaviors but did not significantly reduce stereotypic behavior or alter corticosteroid levels. Thus, coyote behavior in captivity can be similar to that exhibited in the wild; in addition, although enrichment can affect proportions of elicited behaviors, abnormal behaviors and corticosteroid levels may require more than a simple form of environmental enrichment for their reduction.     

Neurobiology of secure infant attachment and attachment despite adversity: a mouse model

Attachment to an abusive caregiver has wide phylogenetic representation, suggesting that animal models are useful in understanding the neural basis underlying this phenomenon and subsequent behavioral outcomes. We previously developed a rat model, in which we use classical conditioning to parallel learning processes evoked during secure attachment (odor‐stroke, with stroke mimicking tactile stimulation from the caregiver) or attachment despite adversity (odor‐shock, with shock mimicking maltreatment). Here we extend this model to mice. We conditioned infant mice (postnatal day (PN) 7–9 or 13–14) with presentations of peppermint odor and either stroking or shock. We used ¹⁴C 2‐deoxyglucose (2‐DG) to assess olfactory bulb and amygdala metabolic changes following learning. PN7‐9 mice learned to prefer an odor following either odor‐stroke or shock conditioning, whereas odor‐shock conditioning at PN13‐14 resulted in aversion/fear learning. 2‐DG data indicated enhanced bulbar activity in PN7‐9 preference learning, whereas significant amygdala activity was present following aversion learning at PN13‐14. Overall, the mouse results parallel behavioral and neural results in the rat model of attachment, and provide the foundation for the use of transgenic and knockout models to assess the impact of both genetic (biological vulnerabilities) and environmental factors (abusive) on attachment‐related behaviors and behavioral development .     

Effects of odors on behaviors of captive Amur leopards Panthera pardus orientalis

Captive environments often fail to resemble the wild environment in respects of limited space,unchanging habitat,lack of stimulus and contingency. Common animal welfare problems which occur in captive animals include low behavioral diversity,abnormal behavior and excessive inactivity. Environmental enrichment,as an effective strategy to tackle these problems and promote mental health of captive animals,has been recognized as an important principal for captive animal management. Among all the enrichment techniques,olfactory enrichment is a simple and effective method for improving the well-being of the olfactory sensitive felids. Behavioral problems were observed in six Amur leopards Panthera pardus orientalis at Beijing Zoological Garden.These were held in the older type exhibits which have now been rebuilt. These behaviors include stereotypic behavior and excessive inactivity caused by the spatially limited enclosures with low levels of stimuli. To determine the effects of predator,prey,and herb odors as potential enrichment materials for captive leopards,we conducted olfactory enrichment experiments for the leopards and tested the effects of nutmeg Myristica fragrans,feces of roe deer Capreolus capreolus and urine of Amur tiger Panthera tigrisaltaica to test for an increase in behavioral repertoire and activity. Odors provided in this study were also believed to improve the psychological and physiological health of individuals. To standardize the method of presentation the odors were introduced to the enclosures by rubbing or spraying onto a clean towel. Our results show that the selected three odors effectively increased the behavioral diversity. Ten new behavior types were observed in the nutmeg experiment,eight in the feces of roe deer experiment and six in the tiger urine experiment. Among the three odors,cats responded to nutmeg for the longest duration,followed by tiger urine and feces of roe deer. Leopards showed more play behavior in presence of nutmeg while more investigatory behavior in presences of feces of roe deer and tiger urine. Providing novel odors increased the spatial use of the exhibit and the animal' s increased use of the logs,sleeping platforms and bars in the cages. Novel odors also significantly increased the overall activity of the leopards,but the effects were diminished in about three hours.     

Characterization of new microsatellite loci for the ring‐tailed lemur (Lemur catta)

In this report we describe the development and characterization of six dinucleotide microsatellite loci for the ring‐tailed lemur (Lemur catta). The new markers were isolated from the genomic DNA of L. catta and all loci were found to be polymorphic when evaluated by genotyping a minimum of 34 individuals. Mendelian inheritance of each locus was verified using four families of captive ring‐tailed lemurs. The loci presented will facilitate the genetic survey of free‐ranging L. catta, enabling study of their social organization and mating patterns.     

The effects of cage volume and cage shape on the condition and behaviour of captive European starlings (Sturnus vulgaris)

Cage size is widely recognised as an important determinant of captive animal welfare, but in contrast, cage shape has received far less attention. Husbandry recommendations for flying birds state that cages should be long in shape because this allows greater potential for flight. However, so far no studies have investigated the impact of cage shape on the behaviour or welfare of captive flying birds. We measured the effects of cage size and shape on the condition and behaviour of captive wild-caught European starlings (Sturnus vulgaris) using a 2 × 3 factorial design in which birds were individually housed for 1 week in cages of one of two volumes (either medium at 0.3 m³ or large at 1 m³), and one of three shapes (long with an aspect ratio (i.e. length/height) of 3.43), standard with an aspect ratio of 1.72 or tall with an aspect ratio of 0.86). We found effects of cage size and the interaction of cage size and shape on the behaviour and condition of birds. In interpreting the welfare implications of our results we focused on stereotypic behaviour as measured by incidence of somersaulting and a novel statistic that quantifies sequential dependencies in the birds’ locations within the cage. The lowest measures of stereotypic behaviour were recorded in the large cages and the medium long cage. Cage shape was more important in determining the quantity of stereotypic behaviour in the medium cages than the large cages. Our findings support the recommendation that starlings be housed in long-shaped cages.     

Improving the Welfare of a Zoo-Housed Male Drill (Mandrillus leucophaeus poensis) Aggressive Toward Visitors

Improving the welfare of nonhuman animals in captivity and maintaining behavioral competence for future conservation purposes is of the highest priority for zoos. The behavior of an aggressive male drill (Mandrillus leucophaeus poensis) was assessed in Barcelona Zoo. The 2-year study presented in this article examined the effects of introducing changes in the exhibit of the drill to improve his welfare by analyzing scan behaviors. First, a partial visual barrier was applied and proved to be insufficient to decrease the long-term stress indicators assessed. Next, a feeding enrichment program was implemented. The results supported the hypothesis that feeding and explorative activities would increase, whereas apathetic and stereotypic behaviors would decrease. However, visitor-directed aggression did not vary, indicating that more profound structural modifications were needed to reduce the negative impact of the agonistic interactions between the drill and the public. The study emphasized the usefulness of environmental enrichment evaluations in assessing captive animal welfare.     

Comparison of several types of enrichment for captive felids

Enrichment can increase the complexity of the captive environment and possibly enhance captive animals' well‐being by stimulating active behaviors and reducing stereotypical behaviors commonly seen in zoo felids. In this study, three different enrichment items were added to outdoor enclosures of felids at the Montgomery Zoo to test their effects on activity levels and stereotypic pacing. Bones, frozen fish, and spices (cinnamon, chili powder, and cumin) were presented over a 3‐month period to six species of felids: cheetah, cougar, jaguar, lion, ocelot, and tiger. Proportion of time spent engaging in active behaviors and stereotypic pacing were compared before, during, and after treatments. All treatments resulted in a significant increase in activity level from baseline (bones: +15.59%; frozen fish: +35.7%; spices: +12.38%). Effects of enrichment items on activity levels were not sustained 7 days after removal. Proportion of time spent pacing significantly decreased during presentation of spices (?21.25%) and frozen fish (?26.58%), but not with the addition of bones. However, only the effect of frozen fish on stereotypic behavior was sustained 7 days after removal of the enrichment item. In conclusion, bones, spices, and frozen fish are inexpensive and easy‐to‐administer enrichment items that may be used to increase active behaviors of captive felids. Zoo Biol 26:371–381, 2007. © 2007 Wiley‐Liss, Inc.     

Weak olfaction increases seed scatter‐hoarding by Siberian chipmunks: implication in shaping plant–animal interactions

Scatter‐hoarding of seeds by animals plays an essential role in seed dispersal of plants and in shaping plant–animal interactions in forest ecosystems, but the function of scatter‐hoarding behavior is still unclear. We hypothesize that weak olfactory cues between seeds and scatter‐hoarding animals would increase scatter‐hoarding. Using a rodent–plant system of Siberian chipmunks Tamias sibiricus and Korean pines Pinus koraiensis, we tested the effects on seed scatter‐hoarding intensity by measuring and modifying the seed odor intensities and the abilities of the animals to detect seed odor. Siberian chipmunks seemed to scatter‐hoard more seeds with weaker odor signals, and Siberian chipmunks with reduced olfactory ability scatter‐hoarded more seeds, supporting our hypothesis. Our studies suggest that olfaction may have played an important role in the evolution of the strength of seed odor and scatter‐hoarding behavior of animals, and in shaping plant–animal interactions.     

Genetic population structure of endangered ring‐tailed lemurs (Lemur catta) from nine sites in southern Madagascar

Madagascar's ring‐tailed lemurs (Lemur catta) are experiencing rapid population declines due to ongoing habitat loss and fragmentation, as well as increasing exploitation for bushmeat and the illegal pet trade. Despite being the focus of extensive and ongoing behavioral studies, there is comparatively little known about the genetic population structuring of the species. Here, we present the most comprehensive population genetic analysis of ring‐tailed lemurs to date from across their likely remaining geographic range. We assessed levels of genetic diversity and population genetic structure using multilocus genotypes for 106 adult individuals from nine geographically representative localities. Population structure and F_ST analyses revealed moderate genetic differentiation with localities being geographically partitioned into northern, southern, western and also potentially central clusters. Overall genetic diversity, in terms of allelic richness and observed heterozygosity, was high in the species (AR = 4.74, H_O = 0.811). In fact, it is the highest among all published lemur estimates to date. While these results are encouraging, ring‐tailed lemurs are currently affected by ongoing habitat fragmentation and occur at lower densities in poorer quality habitats. The effects of continued isolation and fragmentation, coupled with climate‐driven environmental instability, will therefore likely impede the long‐term viability of the species.     

Gait‐specific metabolic costs and preferred speeds in ring‐tailed lemurs (Lemur catta), with implications for the scaling of locomotor costs

Metabolic costs of resting and locomotion have been used to gain novel insights into the behavioral ecology and evolution of a wide range of primates; however, most previous studies have not considered gait‐specific effects. Here, metabolic costs of ring‐tailed lemurs (Lemur catta) walking, cantering and galloping are used to test for gait‐specific effects and a potential correspondence between costs and preferred speeds. Metabolic costs, including the net cost of locomotion (COL) and net cost of transport (COT), change as a curvilinear function of walking speed and (at least provisionally) as a linear function of cantering and galloping speeds. The baseline quantity used to calculate net costs had a significant effect on the magnitude of speed‐specific estimates of COL and COT, especially for walking. This is because non‐locomotor metabolism constitutes a substantial fraction (41–61%, on average) of gross metabolic rate at slow speeds. The slope‐based estimate of the COT was 5.26 J kg^?1 m^?1 for all gaits and speeds, while the gait‐specific estimates differed between walking (0.5 m s^?1: 6.69 J kg^?1 m^?1) and cantering/galloping (2.0 m s^?1: 5.61 J kg^?1 m^?1). During laboratory‐based overground locomotion, ring‐tailed lemurs preferred to walk at ～0.5 m s^?1 and canter/gallop at ～2.0 m s^?1, with the preferred walking speed corresponding well to the COT minima. Compared with birds and other mammals, ring‐tailed lemurs are relatively economical in walking, cantering, and galloping. These results support the view that energetic optima are an important movement criterion for locomotion in ring‐tailed lemurs, and other terrestrial animals. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

Visitor effects on the behavior of captive Western lowland gorillas: the importance of individual differences in examining welfare

Given the conflicting and somewhat limited findings available on the effect of zoo visitors on primate behavior, the primary purpose of this study was to provide additional data on gorillas' response to variations in crowd size and to look at what other factors—both intrinsic (e.g. personality, sex, and rearing history) and extrinsic (e.g. group)—might influence such responses. Subjects included four groups (three mixed‐sex and one bachelor) of captive western lowland gorillas living at Zoo Atlanta. Overall activity budgets and rates of social behaviors in high and low crowd conditions were compared. Behaviors suggestive of general welfare did not vary as a function of crowd size alone, although we did observe one significant interaction and several trends. Specifically, two groups spent more time engaged in undesirable behaviors in the high crowd condition, whereas the other two groups showed the opposite response pattern. Additionally, males, but not females, showed a trend toward greater rates of contact aggression in the high crowd condition, although wounding rates did not vary with crowd size. We also found trends towards variation in response to crowd size as a function of individual personality ratings. These results suggest that although the visitor effect may constitute an impediment to optimal animal welfare, this may only apply to some individuals or groups. We emphasize the importance of continuing to explore individual differences and the limitations of a one‐size‐fits‐all approach when describing influences on animal welfare. Zoo Biol 31:586‐599, 2012. © 2011 Wiley Periodicals, Inc.     

狒狒圈舍废弃栖杠的嗅觉丰容对圈养食肉动物行为的影响

单调的饲养环境是导致圈养食肉动物表现刻板行为的主要原因之一。为减少圈养动物刻板行为的发生,探索便于操作、经济且有效的丰容方式是动物饲养管理者面临的一个挑战。本研究以狒狒圈舍废弃栖杠作为嗅觉丰容材料,对北京动物园小型(9种)、中型(4种)和大型(7种)食肉动物进行嗅觉丰容实验。在非投喂时段,采用扫描动物取样和瞬时记录法,分别对28只动物在丰容前后的5种行为进行观察和比较分析。结果显示,小型和中型食肉动物在丰容后对旧设施的使用频次显著下降(小型：P=0.026;中型：P=0.038),而大型食肉动物无显著变化(P> 0.05)。仅小型食肉动物的刻板性走动、休息和观望行为频次显著下降(走动：P=0.023;休息：P=0.023;观望：P=0.017),其他类群的各类行为均无显著变化(P> 0.05)。同时,丰容后小型食肉动物的行为多样性指数显著降低(P=0.008),主要表现为动物花费较多的时间探究新的丰容设施;中型和大型食肉动物的行为多样性指数变化不显著。结果表明,使用带有狒狒身体气味的栖杠进行嗅觉丰容,仅对小型食肉动物有效,对中型和大型食肉动物无效。研究认为,以其他动物圈舍的...     

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.     

Measuring social tolerance: An experimental approach in two lemurid primates

Social tolerance crucially affects the life of group‐living animals as it can influence, among other things, their competitive regimes, access to food, learning behavior, and recruitment. However, social tolerance tests were mainly conducted in semi‐free or captive populations, and we know little about the behavioral mechanisms and consequences of social tolerance under natural conditions. We therefore developed a co‐feeding experiment to measure social tolerance in groups of wild and captive animals across two primate species. Specifically, we recorded the social tolerance level of redfronted lemurs (Eulemur rufifrons, four wild, one captive group) and ringtailed lemurs (Lemur catta, three wild, three captive groups) by presenting a clumped food resource in an experimental arena, and recorded patterns of resource use during the experiment. Because redfronted lemurs exhibit lower levels of decided conflicts than ringtailed lemurs, we predicted that they would be socially more tolerant. The probability for an individual to feed in the arena was higher in redfronted lemurs than in ringtailed lemurs. In addition, in both species, the probability for an individual to feed in the arena was higher in the captive populations than in their wild counterparts, suggesting that proximate factors, such as a relaxation of feeding competition in captivity, may adapt species‐specific levels of social tolerance to local levels of food availability. Hence, the number of individuals co‐feeding on a valuable food resource appears to be a useful proxy of social tolerance that could be measured with this experimental setup in other wild and captive species as well.     

Captive ring‐tailed lemur breeding in semi‐free ranging conditions and genetic parentage analysis

The ring‐tailed lemur (Lemur catta), one of the most iconic and widely recognized primates in the world, is threatened in its native range and classified as endangered by the International Union for Conservation of Nature. The global conservation strategy for the species includes ex situ conservation efforts led by zoological institutions in the framework of regional captive breeding programs. To maximize the conservation of genetic diversity and optimize breeding programs, an accurate pedigree must be established in captive populations. Our study documents the formation and subsequent monitoring of a large ring‐tailed lemur group in a French zoological institution. Based on staff's behavioral observations and DNA analyses using 11 microsatellite markers, we were able to document the survival and reproduction rates of the lemurs in this situation and reconstruct the pedigree of infants born in the institution. In total, 22 of the 28 imported animals as well as 4 locally born individuals gave birth to 58 infants of which 28 survived. The consistent genotypes obtained from the 53 sampled animals allowed us to identify 25 of the sires and 27 of the dams for the 28 surviving infants. A total of 12 different females and 14 different males produced the 28 surviving infants, suggesting that no individual dominates reproduction. This pioneering study has practical applications for the captive management of the species, which can be raised to the individual level instead of the group level.     

促进人工饲养实验猕猴心理康乐

目的促进实验猕猴心理康乐,既能减少动物异常行为的发生、获得可靠的科学数据,同时也是实现这一珍贵非人灵长类实验动物福利的重要内容。实验猕猴社会化集群、环境优化、婴猴饲养方式是影响动物心理康乐几个较大的因素,本文对其研究进展进行了综述,对推进我国灵长类实验动物福利具有积极作用。