Cage Use and Feeding Height Preferences of Captive Common Marmosets (Callithrix j. jacchus) in Two-Tier Cages

Determining appropriate feeding regimes has important welfare implications for captive primates. This study examined the preference of food bowl heights in 6 pairs of common marmosets (Callithrix jacchus) housed in a 2-tier cage system. Given that marmosets are arboreal and spend most of their time in the upper half of their cages, we predicted that the marmosets would prefer a food bowl positioned at the top of the cage over one positioned at the bottom. We further predicted that this would be more apparent for the marmosets housed in lower tier than upper tier cages. Given a choice regarding where to feed, marmosets did prefer the top bowl to the bottom bowl; however, when only 1 food bowl was presented, its position had no significant effect on the marmosets' feeding behavior. In addition, contrary to the prediction, there were few differences in the marmosets' feeding behavior in the upper and lower tier cages. Feeding the marmosets in a bowl at the bottom of their cage did not result in greater cage use. On the basis of this study, we recommend positioning captive marmosets' food bowls high in the cage.     

The puzzle-feeder as feeding enrichment for common marmosets (Callithrix jacchus): a pilot study

The use of a puzzle-feeder, as feeding enrichment, was investigated in three families of captive common marmosets (Callithrix jacchus). The study was carried out as a simultaneous choice test between two cages: one contained the puzzle-feeder, the other contained the usual food dishes, but otherwise both were arranged similarly. The monkeys were allowed to choose whether to feed from the usual dishes, or from the puzzle-feeder which required more effort. They were observed for two sessions in which they were differently motivated to feed. The enriched cage was always visited first, the marmosets managed to extract food from the puzzle-feeder, and spent more time eating from the puzzle-feeder when less hungry. These data contribute to a wider understanding on the use, and the effects, of feeding enrichments with different captive non-human primates.     

Exploratory behavior and learning in laboratory marmosets (Callithrix jacchus jacchus): Comparisons between experimental-cage and home-cage activity

In this paper I examine exploratory behavior and learning in two groups of common marmosets (Callithrix jacchus jacchus), both living under laboratory conditions. The main aim of my studies was to compare behavior occurring in an experimental testing situation with home-cage behavior, and to assess conditions under which exploration is enhanced. One group of marmosets was tested individually in an experimental room away from a larger animal holding room, and a second group was observed in their own home cages, surrounded by other marmosets. Marmosets in both groups were given the opportunity to learn simple tasks, such as pressing a lever for food or jumping on to a wire grid to open a door and see a neighbouring marmoset, and were provided with sets of novel or familiar objects to encourage play and exploration. In the isolated experimental cage, marmosets which learnt a lever-pressing task showed higher general activity levels than controls; in the home cages the mere addition of novel objects resulted in enhancements in exploratory behavior (measured in terms of contacts with the objects). Although the activities associated with learning tended to decline over time, the novel objects remained a constant interest throughout the experiment. The results have implications for maintaining marmosets in captivity, especially in situations when they are housed separately.     

Primate Location Preference in a Double-Tier Cage: The Effects of Illumination and Cage Height

Nonhuman primates are frequently housed in double-tier arrangements with significant differences between the environments of the upper and lower-row cages. Although several studies have investigated whether this arrangement alters monkeys' behavior, no studies have addressed the two most notable differences, light and height, individually to determine their relative importance. This experiment examined how rhesus and long-tailed macaques allocated their time between the upper and lower-row cages of a 1-over-1 apartment module under different lighting conditions. In Condition A, monkeys' baseline degree of preference for the upper- and lower-row was tested. In Condition B, the lighting environment was reversed by limiting illumination in the upper-row cage and increasing illumination in the lower-row cage. In both conditions, monkeys spent more time in the upper-row cage, thus indicating a strong preference for elevation regardless of illumination. The amount of time that monkeys spent in the lower-row cage increased by 7% under reversed lighting, but this trend was not significant. These results corroborate the importance of providing captive primates with access to elevated areas.     

Fear responses of individually-caged laying hens as a function of cage level and aisle

Chickens kept under intensive conditions are often housed in multi-deck battery cage systems. The effects on egg production of housing birds at different cage levels have been extensively studied, but little is known of the behavioural consequences of this. The present study examined the responses of individually-caged adult laying hens from each tier of a 3-tier battery system in a number of situations intended to elicit fear. Birds housed in the top tier showed (a) longer durations of tonic immobility, (b) greater avoidance of a novel rod placed at the front of the cage, and (c) lower levels of approach and greater inhibition when placed in a pen containing either a human being or one of two novel, inanimate objects, than did those from middle and bottom tiers. The latter birds behaved remarkably similarly. The consistently higher fear scores recorded by hens from the top tier are considered likely to reflect differences in general fearfulness as a function of cage level, and may be a consequence of long-term exposure to different degrees of environmental stimulation.     

Development of a system for individual feeding of baboons maintained in an outdoor group social environment

We developed a system that allows individual feeding of adult baboons, 8-15 years of age, maintained in an outdoor group social environment. The purpose of the system is to allow careful monitoring and control of individual diet. Baboons were housed in two group cages, 16 females and a single male in one and 12 females and a single male in the other. Baboons exited the group cage once daily and passed along a chute and over a scale into individual cages where they received their individual diets. Food intake was monitored during their 2-hour stay in the individual cages. Baboons rapidly learned to use this system. Food intake and weight were stable within 20 days. Food consumed decreased during the period of sexual receptivity. The maintenance of the group social environment allowed observations on the group's dominance structure and the relationship of dominance to food consumption. Speed of food access in the group cage was related to dominance. Dominance was not related to food consumed in individual cages. The system permits study of many variables related to behavior and food intake while still retaining critical social interactions.     

Common variations in the pretest environment influence genotypic comparisons in models of anxiety

The behavioral characterization of rodent strains in different studies and laboratories can provide unreplicable results even when genotypes are kept constant and environmental control is maximized. In the present study, the influence of common laboratory environmental variables and their interaction with genotype on the results of behavioral tests of anxiety/emotionality were investigated. To this end, the inbred rat strains Lewis (LEW) and spontaneously hypertensive rats (SHR), which are known to differ for numerous emotionality-related behaviors, were tested in the open field (OF), elevated plus maze (EPM) and black/white box (BWB), while three environmental factors were systematically controlled and analyzed: (1) the experimenter handling the animal (familiar or unfamiliar); (2) the position of the home cage (top or bottom shelf of the rack) and (3) the behavioral state of the animal immediately before the test (arousal or rest). Experimenter familiarity did not alter the behavior of rats in the OF. Cage position, on the other hand, influenced the behavior in the OF and BWB, with rats housed in top cages appearing less anxious than those housed in the bottom. In the BWB (but not in the OF), these effects were genotype dependent. Finally, the behavioral state of the animals prior to testing altered the results of the EPM in a strain-dependent manner, with some anxiety-related genotypic differences being found only among rats that were aroused in their home cages. This study showed that common variations in the laboratory environment interact with genotype in behavioral tests of anxiety/emotionality. Recognizing and understanding such variations can help in the design of more effective experiments.     

Behavioral effects of enrichment on singly-housed,yearling rhesus monkeys: An analysis including three enrichment conditions and a control group

Three cohorts of yearling rhesus monkeys (Macaca mulatta) were maintained in single cages for one year as part of a derivation program to produce a breeding colony of specific pathogen-free (SPF) monkeys. During this year of social restriction, subjects were provided with three different types of environmental enrichment (physical, feeding, and sensory) to counteract the known effects of social restriction and to quantify the effects of these different conditions of enhancement on their behavior. Focal animal observations were conducted on enriched and control subjects for all cohorts. Enrichment conditions were presented in a different order to each cohort. Monkeys provided with enrichment spent significantly more time playing and less time self-grooming than did control monkeys in unenriched cages, suggesting that the overall enrichment program was of some benefit to the monkeys, because these changes in behavior were in species-typical directions. Among enriched subjects only, there were significant differences in the amount of time spent drinking, grooming, feeding, playing, exploring, and using enrichment across the three enrichment conditions. Both the physical and feeding enrichment conditions led to species-appropriate changes in behavior, therefore enhancing psychological well-being as some define it. Sensory enrichment was of little benefit. The first cohort was housed indoors, received less stimulation from the environment outside of the single cage, and used enrichment more than did the other two cohorts housed outdoors. This suggests that the external environment influences behavior in the single cage and that enrichment may be most effective for animals housed indoors. © 1995 Wiley-Liss, Inc.     

Moving callitrichid monkeys from cages to outside areas

To assess the important aspects of a large area for environmental enrichment, the behavior of families of common marmosets Callithrix jacchus and cotton-top tamarins Saguinus oedipus when in laboratory cages and when in much larger outside areas was compared. All animals avoided areas with little cover. The two tamarin families preferred an indoor cage to a large open area with little cover and consequently only showed a limited range of behavior when outside. When dense cover was provided to the marmoset family, they used this area extensively, showing a wider range of behavior than when in cages and shifting to less active behavior patterns. By feeding marmosets in a central area, it was possible to allow unlimited access to the outside while effectively containing them.     

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.     

The effect of housing and environmental enrichment on stereotyped behavior of adult vervet monkeys (Chlorocebus aethiops)

Little information is available on the response of vervet monkeys to different housing conditions or on the suitability of enrichment devices or methods for vervet monkeys. In this study, the authors evaluated the occurrence of stereotyped behavior in adult vervet monkeys under various conditions of housing and enrichment. The variables included cage size, cage level (upper or lower), enrichment with a foraging log, enrichment with an exercise cage and presence of a mate. The authors first determined the incidence of stereotyped behavior in captive-bred, singly housed adult female and male vervet monkeys. They then exposed monkeys to different housing and enrichment situations and compared the incidence of stereotyped behavior among the monkeys. The authors found that more females than males engaged in stereotyped behavior and that females, on average, engaged in such behavior for longer periods of time than males. Stereotyped behavior was most often associated with a small, single cage. The average amount of observed stereotyped activity in monkeys housed in a small cage was significantly lower when the monkeys had access to either a foraging log or an exercise cage. Stereotyped behavior was also lower in female monkeys that were housed (either with a male or without a male) in a larger cage. The least amount of abnormal behavior was associated with the largest, most complex and enriched housing situation. Males and females housed in cages on the lower level of two-level housing engaged in more stereotyped behavior than did monkeys housed in the upper level, regardless of the presence or type of enrichment provided.     

Physical Environmental Effects on Infant Care and Development in Captive Callithrix jacchus

Environmental enrichment may affect infant care and development in captive primates. We investigated the effects of this factor in laboratory common marmosets (Callithrix jacchus). An enriched physical environment enhanced the social activities of the marmosets and elicited a greater repertoire of behaviors, without negatively affecting the provision of infant care. In addition, infants in enriched cages displayed certain behaviors sooner than infants in non-enriched cages did, which suggests an increased developmental rate. Infants in enriched cages also ate more solid food and engaged in solitary play and exploration more than ones in non-enriched cages did. Play and exploration probably improve spatial cognition and motor skills, which, together with a higher degree of independence, may allow infants to cope better with laboratory routines and general social interactions later in life than their counterparts reared in less complex enclosures. We conclude that laboratories can significantly increase the welfare of marmosets by providing a more complex physical environment.     

Encouraging natural feeding behavior in captive-bred black and white ruffed lemurs (Varecia variegata variegata)

Captive breeding of endangered species is commonly proposed as a means of conserving biodiversity. The suggestion is that captive populations can be built up to provide individuals to reinforce or re-establish wild populations. However, there is evidence to suggest that captive-bred animals lack the skills necessary for survival in their natural habitat. This research was designed to assess whether a group of captive-bred Varecia variegata variegata exhibit such behavioral deficiencies in relation to feeding behavior compared to two wild groups. A further aim was to determine which of four methods of food presentation and two captive environments were most effective in encouraging the exhibition of natural feeding behavior. An identical focal animal, instantaneous time-sampling technique was used to collect data from the wild groups in the Betampona Reserve, Madagascar, and the captive group at Chester, UK. Results from Betampona confirm the highly frugivorous and arboreal nature of V. v. variegata. Under all captive conditions, except the rooftop feed in the cage environment, the captive V. v. variegata spent significantly less time feeding than their wild conspecifics. Suspensory feeding postures are an important adaptation enabling wild V. v. variegata to harvest fruit in the small-branch setting. Similar frequencies of use of such postures to those observed at Betampona were most effectively encouraged among captive V. v. variegata in the cage environment by the rooftop food presentation method and on a naturalistic island exhibit by the suspended method of food presentation. Differences in feeding behavior between the wild and captive V. v.variegata can be explained in terms of structural differences between their environments. As naturalistic captive environments allow lemurs to experience the challenges associated with feeding in the wild, it is strongly recommended that zoos endeavor to provide them with such conditions. Zoo Biol 17:379–392, 1998. © 1998 Wiley-Liss, Inc.     

The effects of different types of individually ventilated caging systems on growing male mice

Ventilation rate and turnover rate of dry air vary among different types of ventilation systems used with individually ventilated cages (IVCs) and can affect the well-being of rodents housed in these cages. The authors compared the effects of two types of IVC systems, forced-air IVCs and motor-free IVCs, on 4-week-old C57Bl/6J male mice. The mice were acclimatized to the cages for 8 d and then monitored for 87 d. Their body weights, food and water consumption and preferred resting areas were recorded. Mice that were housed in motor-free IVCs had a significantly greater increase in body weight than those housed in forced-air IVCs, despite having similar food consumption. Mice in forced-air IVCs had greater water consumption than mice in motor-free IVCs. In addition, mice in forced-air IVCs were more frequently located in the front halves of their cages, whereas mice in motor-free IVCs were located with similar frequency in the front and back halves of their cages, perhaps because of the higher ventilation rate or the location of the air inlets and outlets in the rear of the cage. These results suggest that body weight, food and water consumption and intracage location of growing male mice are influenced by the type of ventilation system used in the cages in which the mice are housed.     

The effect of cage size and enrichment on core temperature and febrile response of the golden hamster

The aim of this study is to determine the effect of cage size and cage enrichment. Golden hamsters were individually housed in standard cages of four different sizes and in enriched cages of three different sizes since 3 weeks of age. Each of the seven housing groups consisted of 12 hamsters. After 14 weeks of housing in their respective environments the measurements started. The mean baseline rectal temperature was significantly higher in hamsters housed in small cages than in hamsters housed in large cages. After the injection of fever-inducing lipopolysaccharide rectal temperature increased by 1 to 2 degrees C. The increase of rectal temperature and the fever index were the highest in animals housed in large cages and the smallest in animals housed in small cages. Through cage enrichment and increasing cage size the mean febrile response increased while the mean baseline rectal temperature decreased. Cage size and cage enrichment had no effect on the dispersion of the measured values. The differences in microclimate between large and small cages were too small to have an effect on thermoregulation. The results indicate that housing in small cages induce chronic stress which obviously affects thermoregulation. The findings demonstrate that the results of some physiological experiments are significantly influenced by the pre-experimental housing conditions.     

Establishing Meal Patterns by Lickometry in the Marmoset Monkey (Callithrix jacchus): Translational Applications From the Bench to the Field and the Clinic

The ability to measure and interpret variables associated with feeding behavior and food intake is essential to a variety of nonhuman primate study modalities. The development of a technique to accurately and efficiently measure food intake and meal patterning in captivity will enhance both the interpretation of foraging behavior in the wild as well as our ability to model clinically relevant human feeding pathologies. In this study, we successfully developed the use of a rodent lickometer system to monitor meal patterning in captive common marmosets. We describe the modifications necessary for this type of instrumentation to be used successfully with marmosets. We define variables of interest that relate to both previous rodent literature and human clinical measures. Finally, we relate our findings to potential translational value for both primate field research and biomedical applications. Am. J. Primatol. 74:901‐914, 2012. © 2012 Wiley Periodicals, Inc.     

Relationship between production factors and dominance in White Leghorn hens in a study on social rank and cage design

The effects of social rank and cage shape on feeding frequency, weight gain, production rate, egg size, shell strength and overt aggressive activity were determined for White Leghorn layers housed six per cage in deep and shallow cages. Social rank significantly affected feeding frequency, production rate, egg size, and aggressive activity for birds in both cage designs. Birds ranking high in the social order fed more frequently, had higher production rates, larger eggs and delivered more aggressive head pecks than birds low in the peck order. The effect for production rate was manifested only at the sixth bird level. Significant social rank effects on weight gain, final body weight and shell strength were not observed. Birds in shallow cages fed more frequently, gained more weight and were involved in more aggressive acts with cage mates than those in deep cages.     

Age class differences in the feeding behavior of captive Japanese macaques (Macaca fuscataia) in the forested and nonvegetated enclosure groups

Age class differences in feeding behavior of primates are affected by many factors, including feeding competition, foraging skills, habitat type, food abundance and distribution, body mass, and food types. Two captive groups of Japanese macaques (Macaca fuscata), one housed in a forested enclosure and the other in a nonvegetated enclosure, were studied to examine the effect of environmental enrichment on age class differences in feeding behavior. Although there was no significant age class difference in time spent feeding on provisioned foods in either enclosure, the feeding rate (intake of unit food/minute) of adults consuming provisioned monkey chow was significantly higher than that of immatures in both enclosures, and was faster for both age groups in the nonvegetated than in the forested enclosure. Overall, feeding time was greatly extended for individuals of both age classes in the forested enclosure compared with their counterparts in the nonvegetated enclosure. Immatures in the forested enclosure utilized a significantly greater number of plant species and food items, exploiting many food items available among the terminal branches, and spent significantly more time feeding than adults. Perhaps constrained by larger body size, adults fed more often on the ground or middle height of the trees, likely reducing competition over plant food resources between adults and immatures. The natural vegetation played an important role in extending feeding time and segregating substrate use during feeding by adults and immatures. This study revealed the benefits concerning environmental enrichment of a naturally forested enclosure, which provides captive primates the opportunity to exhibit age class and species-typical feeding behaviors of importance for their dietary maintenance and general health.     

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.     

Comparison of behaviour,performance and mortality in restricted and ad libitum-fed growing rabbits

The objective of this study was to determine whether rabbits fed in a restricted regimen (75%) showed increased competition for feeding, drinking and use of specific areas of the cages as compared with those provided feed ad libitum. This evaluation was carried out by measuring their space utilisation in the cage, the incidence of agonistic behaviour and rates of mortality. In total, 504 rabbits between 31 and 66 days of age were used in this study. A total of 200 heavy-weight rabbits and 56 light-weight rabbits were randomly housed in 32 cages, each cage containing eight rabbits: 25 cages housing heavy rabbits and seven cages housing the light-weight ones. They were all fed ad libitum (AD). In addition, a total of 208 heavy-weight rabbits and 40 light-weight rabbits were randomly housed in 31 cages, each of them containing eight rabbits: 26 cages housing heavy weight rabbits and five cages housing light-weight ones. They were all fed a restricted diet (R) regimen. The restriction was calculated to be 75% of the feed consumed by the AD group. The total space available in the cage was 3252 cm², with a stocking density of 24.6 animals/m². Animals between 32 and 60 days of age from 20 different cages were observed nine times per week (morning or afternoon) by means of scan and focal sampling by one observer. During each period, cages were assessed for 5 min, registering every minute the position of all the animals in relation to Area A (feeder), Area B (central part) or Area C (back and drinker area). The incidence of agonistic behaviour such as displacement, biting and jumping on each other was also assessed. Performance variables such as daily gain and feed conversion ratio, in addition to general health status and mortality rates, were recorded for all rabbits. When the rabbits were under restricted feeding, the competition for feed and drink increased with clear signs of agonistic behaviour such as biting, displacement and animals jumping on top of each other. Although this competition was maintained during the entire growing period, the BW homogeneity between animals in the same cage was similar in both cases, suggesting that all animals could consume similar quantities of feed. The possible advantages of a restricted diet, such as better feed conversion ratio, were observed in this study only in the last few weeks of the growing period.