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 behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates: Lemuridae)

A stable social group of 7 semifree-ranging black-and-white ruffed lemurs (Varecia variegata variegata) was studied for 4 months to catalog the behavioral repertoire of this species. Observations focussed on particular aspects of behavior were conducted before and after this 4-month period to supplement information gathered. Behavior in 11 major categories is detailed: postures, terrestrial locomotion, arboreal locomotion, feeding behavior, vocalizations, scent-marking, affinitive social behavior, agonistic social behavior, play behavior, sexual behavior, and parental behavior. Ruffed lemurs frequently used body positions and locomotor patterns unusual among lemurids, including bipedal hanging and long-descent leaps. These behaviors reinforce dental evidence that Varecia are among the most frugivorous of the Malagasy lemurs. Low intragroup cohesion, infrequent social interaction, and antiphonal use of several long-distance vocalizations suggest that ruffed lemurs naturally exhibit fission-fusion sociality. Social structure based on interindividual familiarity probably extends across foraging parties for several of the diurnally active lemurs; however, thus far only Varecia seems likely to exhibit fission-fusion sociality analogous to that seen in spider monkeys and chimpanzees.     

Diet and feeding behaviour of Indri indri in a low-altitude rain forest

The diet and feeding behaviour of Indri indri were investigated in the Betampona Reserve, eastern Madagascar, over 12 months from February 2000 to February 2001. The highly folivorous diet of this species was confirmed--feeding on foliage (leaves and petioles) accounting for 82% of feeding records. Immature leaves were the preferred dietary item, but at times of relative scarcity mature leaves, fruit, seeds, flowers and bark were substituted. The indri were observed to feed on parts from 22 plant families, 37 genera and at least 42 species. The most important plant families in the diet of Indri were Lauraceae, Clusiaceae and Myristicaceae. Most feeding at Betampona was observed at 5-20 m above the forest floor amongst small (2.1-5.0 cm), oblique/horizontal supports (0-45 degrees). The indri spent 41.4% of their active period feeding most commonly in above-branch postures. Studies such as this are important for the development of conservation management plans for this endangered species.     

The re-stocking of captive-bred ruffed lemurs (Varecia variegata variegata) into the Betampona Reserve, Madagascar: methodology and recommendations

Since November 1997 the Madagascar Fauna Group has released 13 captive-bred black and white ruffed lemurs (Varecia variegata variegata) into the Betampona Reserve in eastern Madagascar. The release programme has three major aims: (1) to assess the ability of captive-bred V. v. variegata to adapt to life in their natural habitat; (2) to investigate the contribution that such a release programme can make to reinforcing the existing small wild population of V. v. variegata in Betampona; and (3) to contribute to the long-term protection and conservation of the reserve. Criteria for the selection of release candidates, veterinary screening and pre-release experience in naturalistic environments are described and discussed. Methods for post-release monitoring of health and behaviour are covered in detail. The importance of considering the social dynamics of the species involved is emphasised. The survival of five of the releasees, plus successful reproduction and integration with the wild population have led to the conclusion that the release was a success.     

Environmental enrichment to address behavioral differences between wild and captive black-and-white ruffed lemurs (Varecia variegata)

I compared the behaviors of wild Varecia variegata living in a Malagasy rain forest with those of caged groups living in zoos in the United Kingdom in order to design environmental enrichment to encourage more natural behaviors. Comparisons were made between wild and captive animals in terms of activity budgets (instantaneously sampled at 1-min intervals) and social and solitary behaviors, which were continuously recorded for focal individuals. I followed the same sampling protocol during behavioral enrichment experiments, with additional monitoring of the amount and type of food consumed, and with more detailed observations of feeding behavior. No significant differences were found in resting or moving between wild and captive V. variegata. However, captive V. variegata spent more time on self-grooming and social behaviors, and less time feeding than wild V. variegata. There was also a lack of manual manipulation of food items. Behavioral enrichment experiments were carried out in which whole rather than chopped fruit was provided and presented in a more naturalistic manner. With this method of dietary presentation, manual manipulation of dietary items increased. Time spent feeding also increased significantly. Captive conservation breeding programs should not be wholly concerned with maintaining a diverse gene pool-they should also be concerned with conserving species-typical behaviors, especially if they are to produce behaviorally intact captive animals that can be reintroduced to the wild with minimal training, financial resources, and loss of individuals.     

Body weights of ruffed lemurs (Varecia variegata) in European zoos with reference to the problem of obesity

Qualitative observations in several European zoos revealed a high proportion of obese individuals in different species of lemurs. This phenomenon was examined in both subspecies of the ruffed lemur (Varecia variegata variegata and Varecia variegata rubra). Data on body weight were obtained from 43 animals in 13 European zoos and were compared with body weights of wild ruffed lemurs. The captive individuals’ mean weight was significantly higher than either of two different samples of wild V. variegata variegata. Using a weight‐based definition of obesity, 46.5% of the individuals in our sample were obese. Neither significant differences in body weight between the two subspecies nor between sexes could be found. Body weight did not correlate with age. The findings are discussed with reference to the feeding ecology of ruffed lemurs and their nutrition in captivity and to implications for captive breeding programs for this species. Zoo Biol 20:261–269, 2001. © 2001 Wiley‐Liss, Inc.     

Reproductive activity of ruffed lemurs (Varecia variegata variegata) in a Madagascar rain forest

Mating activity was observed during four breeding seasons in two groups of black and white ruffed lemurs (Varecia variegata variegata) living in lowland rain forest on Nosy Mangabe island, Madagascar. The onset of the May-July breeding season was signalled by behavioral changes in adult males. Males made forays outside their usual home ranges, were more aggressive to other males, and performed appetitive and other sex-specific behaviors more frequently. Females showed receptive and proceptive behaviors during a 1-2 day behavioral estrus. Ruffed lemurs mated monogamously, polyandrously, and polygynously. These observations do not support previous assertions that they live only in monogamous families. Limited evidence suggests females exercised mate choice and may have preferred familiar males. © 1993 Wiley-Liss, Inc.     

Hematology and serum chemistry values of juvenile and adult ruffed lemurs (Varecia variegata)

Hematologic and serum chemistry values are presented for adult and juvenile red ruffed lemurs (Varecia variegata rubra) and black and white ruffed lemurs (Varecia variegata variegata) maintained in a zoological collection. Hematologic and serum chemical values are compared between age groups and subspecies and with other primate species. Elevated hematocrit, total protein, and serum albumin values were noted. Significant differences in cholesterol, total protein, and serum albumin values between the two age groups are discussed.     

Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: I. Interspecific patterns

Niche separation was documented in a year-long study of Varecia variegata rubra and Eulemur fulvus albifrons on the Masoala Peninsula, Madagascar. Feeding trees were measured, and diet, forest height, and forest site were recorded at 5-min time points on focal animals. For time point data, multivariate and bivariate analysis of frequencies was employed to examine how niche dimensions vary between species according to sex, season, and reproductive stage. V. v. rubra feeds in larger trees than E. f. albifrons. V. v. rubra has a diet consisting mainly of fruit, whereas E. f. lbifrons has a more varied diet. V. v. ubra ranges mainly above 15 m in tree crowns, whereas E. f. albifrons ranges mainly below 15 m in a wide array of forest sites. Both species are largely frugivorous, but they harvest fruit in different-sized trees, in different quantities, and in different forest strata. Niche partitioning varies in tandem with seasonal shifts in climate and food availability and with reproductive stages. Seasonal shifts in forest site and forest height use are largely attributed to species-specific tactics for behavioral thermoregulation and predator avoidance. The diet of E. f. albifrons is diverse whether examined by season or reproductive stage. However, females of both species diversify their diets with more low-fiber protein than males during gestation, lactation, and the hot seasons. This pattern is most pronounced for V. v. rubra females and may be directly attributed to high energetic investment in reproduction. These results suggest that niche partitioning may be driven more by the energetic requirements of reproductive females than males.     

Some observations of two kinds of lemuridae (Varecia variegata variegata andLemur fulvus albifrons) in the reserve of Nosy Mangabe

A total of nine groups of ruffed lemurs (Varecia variegata variegata), as well as one solitary individual, were observed on Nosy Mangabe, an island located off the eastern coast of Madagascar, for a total 536 min between November 30 and December 8, 1983. The average group size was 2.8 animals (N=5), and the population density was 175 animals/km², as estimated from direct observation and location of vocalization. During the same period, nine groups of brown lemurs (Lemur fulvus albifrons) and one solitary individual were observed for a total 320 min. One group of brown lemurs was composed of eight animals (two adult males and females, one male juvenile, two infants, and one individual of undetermined age and sex). Feeding competition occurred between the two species, with whichVarecia variegata variegata dominating.     

Description of the gastrointestinal tract of five lemur species: Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus, and Lemur catta

The objective of this project was to better define the similarities and differences in gastrointestinal morphology present in lemur species. Measurements of the gastrointestinal tract of lemurs were obtained at necropsy from the captive population at Duke University Primate Center. Measurements of body length and weight, as well as gastrointestinal length, were recorded from five prosimian species: Propithecus tattersalli, Propithecus verreauxi, Varecia variegata, Hapalemur griseus, and Lemur catta. Photographs and measurements were used to obtain illustrations. Preliminary results suggest differences in gastrointestinal morphology among lemur species that coincide with differences in diet. Distinct sacculations in either the cecum or the colon were present for H. griseus, L. catta, P. verreauxi, and P. tattersalli, but not for V. variegata. The Propithecus specimens possessed a much greater ratio of gastrointestinal length to body length than the other three species. A short, blunt cecum and a shortened and sacculated colon were unique characteristics of the H. griseus specimens. These differences correlate well with a dietary shift from consumption of large amounts of structural plant cell wall (Propithecus sp.) to consumption of variable or moderate amounts (H. griseus, L. catta, and V. variegata). They also suggest that captive groups would benefit from further diet refinement in captivity.     

Can Captive-Bred Varecia variegata variegata Adapt to a Natural Diet on Release to the Wild?

We compared the diets of 3 groups of released captive-bred Varecia variegata variegata (RG1, RG2, RG3) in the Betampona Reserve to that recorded for a resident wild group, between 1998 and 2001. We investigated whether the released captive-bred Varecia, from differing captive backgrounds, could cope with seasonal changes in climate and consequently food availability, finding sufficient food to meet their nutritional requirements, and dietary choices and selection. We collected data on diet, including plant part, family, genus and, if known, species. In addition, we collected data on seasonal variation in dietary composition. Dietary overlap is significant at the familial level between RG1/RG3 and the wild group. There is some dietary overlap between RG2 and the wild group, but it is not significant. In general, RG1 and RG3 more closely followed the dietary choices and seasonal changes in diet exhibited by the wild group. We conclude that Varecia raised in free-ranging environments are better adapted to meet their nutritional requirements in the wild than those raised in cages are. However, even they struggle to deal with seasonal climatic changes and consequent changes in food availability. We suggest that future re-introduction efforts for primates include attempts to integrate released individuals rapidly into wild groups so that they can learn to cope with a seasonal environment through direct observation of wild conspecifics.     

Tactics of care for young infants by forest-living ruffed lemurs (Varecia variegata variegata): Ground nests,parking, and biparental guarding

Over a 4 month period, systematic and ad libitum observations were conducted on two adult female black-and-white ruffed lemurs (Varecia variegata variegata) and their infants in a 3.5 ha forest enclosure. The females were mother and daughter, members of a family group that had been semifree-ranging for 2 years and 3 months at the time of the births. One to two weeks before parturition, the females independently constructed nests, in which they kept their infants during the first few weeks following parturition. The older mother, cage-reared herself, prepared at least one nest. Her daughter, who has lived in the forest since late juvenescence, prepared at least four. Two to three weeks after parturition, the mothers moved their infants high into trees. During periods of maternal absence, the infants were often alone, and they rarely or never moved, vocalized, or groomed themselves. The mothers often kept their infants together after nests were no longer used. Each infant nursed freely from both lactating females. The infants were carried orally only by their mothers and were never transported by clinging to the pelage of any group members. Previously, researchers suggested that ruffed lemurs build nests for care of infants high up in trees. The present observations, however, suggest that two major modes of neonate care in Varecia exist: serial use of multiple ground nests and “parking” of infants high in trees. Advance preparation of several nest sites, relative lack of large predators, alternate maternal and paternal guarding of infants, infant immobility during absence of mother, and rapid infant development make this tactic of care for neonates plausible.     

Laterality in semi‐free‐ranging black and white ruffed lemurs (Varecia variegata variegata): head‐tilt correlates with hand use during feeding

Previous studies in human and chimpanzee infants have identified a predictive relationship between early rightward head orientation and later right hand use. Data from lemurs suggest a leftward bias in hand preference, but there are no data on head positioning. The purpose of this study was to examine the relationship between head and hand preferences in the black and white ruffed lemur (Varecia variegata variegata). Ruffed lemurs rotate the head vertically during chewing in a behavior called head‐tilting. Frequency of head‐tilting and bouts of unimanual hand use were measured during normal feeding in a semi‐free‐ranging population of lemurs. Subjects were provisioned at feeding platforms twice daily with fresh fruits, vegetables, and other food items. Sampling was spontaneous and all observations were videotaped. No group‐level bias was found for head‐tilting, but a left hand bias emerged for hand use. A positive relationship was found between direction of head‐tilting preference and direction of hand use preference such that left head‐tilts increased as left hand use increased. Furthermore, left head‐tilts increased as the degree of hand preference lateralization increased. When the hand used to bring food to the mouth just before head‐tilting was examined, there was a strong bias for the left hand to precede left head‐tilts. For right head‐tilts, however, lemurs were equally likely to use either hand before head‐tilting. Overall a strong relationship was found between the left hand and left head‐tilting in black and white ruffed lemurs, suggesting a common link between these behaviors. However, the direction of bias was different from that seen in human and chimpanzee studies. Additional studies on patterns of laterality would be informative for understanding how laterality has changed across the primate order and the adaptive significance of laterality in primates. Am. J. Primatol. 71:1032–1040, 2009. © 2009 Wiley‐Liss, Inc.     

The zoophilic fruitfly Phortica variegata: morphology, ecology and biological niche

Abstract.  Flies belonging to the subfamily Steganinae (Drosophilidae) display unusual zoophilic feeding habits at the adult and/or larval stage. Phortica variegata (Fallén) feeds on tears or eye liquid around the eyes of humans and carnivores. When feeding it is a potential vector of Thelazia callipaeda (Railliet and Henry) eyeworms. Adult and larval stages of this fly may be easily confused with other species belonging to the same genus, and little is known on the biology and ecology of P. variegata . In April–November 2005, a total of 969 P. variegata were collected in an area with a high prevalence of canine thelaziosis. The number of flies collected weekly was then related to climatic and environmental parameters (e.g. temperature, relative humidity and total rainfall) recorded daily at the collection site. The highest number of Phortica were collected during July–August. The sex ratio (number of males : females) rose from ∼ 0.5 during May–July, to ∼ 3.0 in August and 181 during September–October. Distributional data, representing 242 sites at which P. variegata has been collected in Europe, were analysed using a desktop implementation of the genetic algorithm for rule-set prediction (GARP) to model ecological requirements across Europe, as well as in Italy. P. variegata is shown to be mainly active at 20–25 °C and 50–75% RH. The ecological niche model suggests with a high degree of confidence that large areas of Europe are likely to represent suitable habitat for this species, mostly concentrated in central Europe. The results reported here contribute basic knowledge on the ecology and geographical distribution of P. variegata flies, which will be fundamental to gaining a better understanding of their role as vectors of human and animal pathogens.     

Sex ratio affects sex-specific innovation and learning in captive ruffed lemurs (Varecia variegata and Varecia rubra)

Recent years have witnessed extensive research into problem solving and innovation in primates, yet lemurs have not been subjected to the same level of attention as apes and monkeys, and the social context in which novel behavior appears has rarely been considered. We gave novel foraging puzzlebox devices to seven groups of ruffed lemurs (Varecia variegata and Varecia rubra) to examine the factors affecting rates of innovation and social learning. We found, across a range of group sex ratios, that animals of the less-represented sex were more likely to contact and solve the puzzlebox sooner than those of the more-represented sex. We established that while some individuals were able to solve the puzzleboxes there was no evidence of social learning. Our findings are consistent with previously reported male deference as a sexual strategy, but we conclude that the need for male deference diminishes when, within a group, males are rare.     

Induction of a fertile mating in a red ruffed lemur (Varecia variegata rubra) using pregnant mare serum gonadotropin

Pregnant mare serum gonadotropin (PMSG) was administered to an adult female red ruffed lemur (Varecia variegata rubra) as part of a medical evaluation to determine the cause of reproductive failure. Successful fertilization, pregnancy, and parturition occurred following PMSG treatment. This report documents an approach to evaluating reproductive failure in an endangered primate species and illustrates the value of collecting objective data on all individuals in a colony for retrospective and comparative analysis. Data from basic and applied research on a variety of species were synthesized to establish a logical protocol for fertility evaluation of an individual. The use of PMSG to induce estrus, ovulation, or fertilization has not been documented for an endangered primate species.     

Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. Intraspecific patterns

Based on a year-long field study in northeastern Madagascar, I summarize annual patterns of niche use (food patch size, diet, forest height, and forest site) in two sympatric lemurs, Varecia variegata rubra and Eulemur fulvus albifrons. Furthermore, I examine intraspecific patterns of niche use according to sex, season, and reproductive stage in these two lemurs that differ in terms of energetic investment in reproduction. Lemurs as a group provide a special opportunity to test hypotheses concerning sex differences in niche use. Due to their body size monomorphism and seasonal, synchronous pattern of breeding, it is possible to directly evaluate whether sex differences in diet reflect high energetic investment in reproduction by females. Results confirm the hypothesis that intraspecific variation in niche use (e.g., sex differences, seasonal differences) would be more pronounced in V. v. rubra than in E. f. albifrons, due in large measure to the former's relatively high energetic investment in reproduction: 1a) Dietary sex differences in V. v. rubra are most pronounced during costly reproductive stages and involve acquisition of low-fiber, high-protein plant foods. Females of both species consume more seasonally available low-fiber protein (young leaves, flowers) relative to conspecific males during the hot dry season, but only in V. v. rubra females is this pattern also evident during gestation and lactation. 1b) The diets of female V. v. rubra and female E. f. albifrons are more similar to each other than are the diets of conspecific males and females in the case of V. v. rubra. This is not uniformly the case for female E. f. albifrons. This finding confirms a hypothesis put forward in Vasey ([2000] Am J Phys Anthropol 112:411-431) that energetic requirements of reproductive females drive niche separation more than do the energetic requirements of males. 1c) Both species synchronize most or all of lactation with seasonal food abundance and diversity. E. f. albifrons shows a more protracted period of synchrony, and this may contribute to its wide biogeographic distribution in Madagascar. 2) Sex differences and seasonal differences in microhabitat use reflect intraspecific patterns of thermoregulation, predator avoidance, and in the case of V. v. rubra, reproduction. One important factor selecting for body size monomorphism in lemurs appears to be the tight synchrony between lactation and periods of food abundance afforded by annual, seasonal breeding.     

Use of desferoxamine and S-adenosylmethionine to treat hemochromatosis in a red ruffed lemur (Varecia variegata ruber)

Hemochromatosis was diagnosed in a 14-year-old, male, red ruffed lemur (Varecia variegata ruber) on the basis of abnormal results of serum biochemical analysis, including high serum ferritin and transferrin saturation values, and of liver biopsy. Therapy included chelation, using desferoxamine to remove excess iron and S-adenosylmethionine to improve liver function, and monthly peripheral blood removal by phlebotomy to reduce total body iron content. Response to treatment was assessed by changes in the lemur's attitude and appetite, as well as variations in serum biochemical and iron panel values. Initial improvement was associated with the onset of therapy. After 56 days of treatment, results of serum biochemical analysis indicated a decrease in iron panel values. Treatment was temporarily discontinued from days 56 to 65, and the lemur's condition worsened, so therapy was re-instituted. However, the lemur died of hepatocellular carcinoma on day 110 of treatment.     

Diet of the brown howler monkeyAlouatta fusca in a semi-deciduous forest fragment of southeastern Brazil

The diet of a group of six brown howlers was studied weekly during 12 months in a reserve of 250 ha of secondary, mesophytic, semi-deciduous forest. The phenology of 186 trees of 72 species and 29 families was monitored simultaneously. Scan sampling was used to record the diet from dawn until dusk on a total of 60 days of observation, yielding 718 hr of animal-observer contact and 2,943 feeding scans. The diet was composed of leaves (73%), flowers (12%), and fruits (5%), from 68 identified plant species.Celtis iguanae, Cassia ferruginea, andInga spp. were the main food sources, accounting for approximately 50% of the diet. Young leaves (59%) were preferred to mature leaves (31%), trees contributing 56% and lianas 41% of the leaf diet. The ingestion of young leaves was correlated to the availability of these items, however, the correlations were not significant for flowers and fruits. The diet was poorer in fruits and richer in young leaves of lianas in comparison to other howler monkey species studies, probably as a consequence of the liana abundance in this forest fragment.