Population, Diet and Conservation of Malayan Flying Lemurs in Altered and Fragmented Habitats in Singapore

The Malayan flying lemur (Cynocephalus variegatus) is a nocturnal mammalian arboreal folivore that inhabits the forests of Southeast Asia. Surveys were conducted from August to November 2003 to estimate the population density of Malayan flying lemurs for the first time in the Singapore Zoological Gardens. The study area consisting of Singapore Zoo and Night Safari was located in the Central Catchment Nature Reserve, where most of Singapore’s remaining natural forest is found. The Zoo consisted of 28 ha of landscaped habitat and the adjacent Night Safari consisted of 40 ha of secondary rainforest. The density estimates of flying lemurs in the Zoo and Night Safari were 15 and 24 individuals respectively. Seven plant species that were the preferred food items and an additional 10 plants that were common in the sites but not eaten by the flying lemurs were analysed to compare the mineral and phytochemical contents. Flying lemurs consumed leaves containing significantly less potassium and nitrogen but higher tannin (p < 0.05). The study shows that flying lemurs are able to survive in altered and fragmented landscapes. Conservation and management strategies are essential to protect the shrinking habitats in Singapore.     

Digestive strategy of the asian colobine genusTrachypithecus

The Asian colobines,Trachypithecus obscurus andT. cirstantus, eat plant-based diets containing 55–80% leaves. The structural polysaccharides in leaves and other plant parts require microbial fermentation before they can be used as an energy source by the monkeys. The major compartments of the gastro-intestinal tract ofTrachypithecus are a voluminous haustrated stomach, a long small itnestine and capacious haustrated hindgut, all of which contribute to the digestive strategy of these two species. Results of digesta marker passage studies indicate there is prolonged retention of digesta for fermentation in both the stomach and haustrated colon. The digestive strategy of these colobines is defined as gastro-colic fermentation, unlike that of other forestomach fermenters in which the hindgut fermentation is of secondary importance.     

The head and neck muscles of the Philippine colugo (Dermoptera: Cynocephalus volans), with a comparison to tree‐shrews,primates, and other mammals

The colugos, or flying lemurs (Dermoptera), are arboreal gliding mammals that are commonly grouped with tree‐shrews (Scandentia) and Primates in the superorder Euarchonta. However, little is known about the head and neck muscles of these gliding mammals. This raises difficulties for the discussion of not only the functional morphology and evolution of colugos, but also the origin, evolution, functional morphology, and phylogenetic relationships of the Euarchonta as a whole, and thus also of our own clade, the Primates. In this work, I describe the head and neck muscles of the colugo Cynocephalus volans, and compare these muscles with those of other mammals, either dissected by me or described in the literature. My observations and comparisons indicate that, with respect to the number of muscles, the plesiomorphic condition for euarchontans as well as for primates is more similar to that found in extant tree‐shrews than in extant colugos. This is because various muscles that were probably plesiomorphically present in the euarchontan and primate clades, as, e.g., the stylohyoideus, mandibulo‐auricularis, cleido‐occipitalis, omohyoideus, and sternohyoideus, are not present as independent elements in extant colugos. These observations and comparisons also indicate that various laryngeal and facial muscles that are present in modern humans were absent in the last common ancestor of extant primates. J. Morphol., 2009. © 2008 Wiley‐Liss, Inc.     

Digesta passage rates in the Florida manatee (Trichechus manatus latirostris)

The Florida manatee, Trichechus manatus latirostris (Sirenia: Trichechidae), is an herbivorous marine mammal found within coastal areas throughout the state of Florida, which feeds on both fresh and salt water sea grasses. Manatees, like other Sirenians, are a tropical species with little tolerance for water temperatures below 20°C, rely on a relatively poor nutritional food source, and have a low metabolic rate. Although manatees are hindgut fermenting herbivores, they are very efficient at extracting nutrients from the plants on which they feed. Slow passage rates of digesta have been suggested to be a factor in this increased efficiency. Two studies monitored the digesta passage times and mixing of particulate digesta within the manatee digestive tract using MicroGrits colored corncob grit as a fecal marker. Fecal samples were collected subsequently from four manatees in Study 1 and 3 manatees in Study 2, grit pieces removed, counted, and measured. The digesta passage times ranged from 6 and 10 days in Study 1, and 4.3 and 8.3 days in Study 2, supporting data presented in previous studies. When two different colored markers were administered on sequential days, minimal to no mixing was seen in recovered feces, suggesting that the digesta from a given day traveled through the tract as a bolus. Less than 1% of the marker fed was recovered and we hypothesize that perpendicular folds of the large intestine may be the major contributing factor, with pieces being retained and eventually digested. Zoo Biol 26:503–515, 2007. © 2007 Wiley‐Liss, Inc.     

Spatial ecology and conservation of two sloth species in a cacao landscape in limón,Costa Rica

The spatial ecology of sloths was studied in an agricultural landscape in Limón Province, Costa Rica. Two sloth species, the three-toed sloth (Bradypus variegatus) and the two-toed sloth (Choloepus hoffmanni), actively used and traveled through a cacao agroforest and its contiguous living fence rows and riparian forests. This agroecosystem was embedded in an agricultural landscape dominated by banana and pineapple plantations and pastures with dispersed trees. The two-toed sloth (C. hoffmanni) was found in 101 tree species and used 34 for food; the three-toed sloth (B. variegatus) was found in 71 tree species and used 15 for food. Choice of preferred species differed between the two sloth species. Trees commonly used by sloths for food and/or refuge in the cacao agroforest included Erythrina poeppigiana, Cecropia obtusifolia, Leucaena leucocephala; in the living fence rows, Cordia alliodora, Erythrina poeppigiana, Ocotea sinuata and Trophis racemosa; in the riparian forests, Coussapoa villosa, Cecropia obtusifolia, Hura crepitans, Pterocarpus officinalis and Spondias mombin; and in the pastures with dispersed trees, Cordia alliodora, Coussapoa villosa, Erythrina poeppigiana, Ocotea sinuata and Hura crepitans. This study demonstrates the importance of the cacao agroforest as well as arboreal elements in other land uses in providing resources for sloth conservation in a larger agricultural landscape.     

Comparative Phylogeography of the Atlantic Forest Endemic Sloth (Bradypus torquatus) and the Widespread Three-toed Sloth (Bradypus variegatus) (Bradypodidae, Xenarthra)

The comparative phylogeographic study of the maned sloth (Bradypus torquatus) and the three-toed sloth (Bradypus variegatus) was performed using a segment of mitochondrial DNA (mtDNA) control region. We examined 19 B. torquatus from two regions and 47 B. variegatus from three distant regions of Atlantic forest. This first characterization of molecular diversity indicates a great diversity (B. torquatus: h = 0.901 ± 0.039 and π = 0.012 ± 0.007; B. variegatus: h = 0.699 ± 0.039 and π = 0.010 ± 0.006) and very divergent mitochondrial lineages within each sloth species. The different sampled regions carry distinct and non-overlapping sets of mtDNA haplotypes and are genetically divergent. This phylogeographic pattern may be characteristic of sloth species. In addition, we infer that two main phylogeographic groups exist in the Atlantic forest representing a north and south distinct divergence.     

Species ofBertiella (Cestoda: Anoplocephalidae) in dermopterans and squirrels from South-East Asia

Bertiella elongata (Bourquin, 1905) andB. plastica (Sluiter, 1896) both fromCynocephalus volans (Linnaeus, 1758) andC. variegatus (Audebert, 1799) are redescribed and illustrated. A neotype forB. plastica is designated.B. boholensis Spasskii, 1951 is reduced to synonymy withB. elongata andB. cynocephali Spasskii, 1951 is synonymised withB. plastica. A new species,B. rauschi, is described fromC. volans in the Philippines. It differs from its congeners in having an accessory seminal receptacle and testes which do not extend to the aporal extremity of the medulla.Bertiella musasabi Yamaguti, 1942 is redescribed from a specimen fromPetaurista petaurista (Pallas, 1766) from Taiwan.Indotaenia indica Singh, 1962 andAprostatandrya petauristae Sawada & Kugi, 1979 become synonyms ofB. musasabi. The biogeography of the genus is briefly discussed.     

Hemosiderosis in lemurs

In the late 1960s, pathologists at the San Diego Zoo began to notice iron storage in the internal organs of captive lemurs. Hemosiderin was found in liver, spleen, lymph nodes, duodenum, and occasionally other organs. This was most pronounced in Lemur macaco, least pronounced in Lemur catta, with the severity in Lemur variegatus variegatus and Lemur variegatus ruber falling somewhere in between. Since 1968, 20 of 29 necropsied lemurs had hemosiderosis, three with hepatomas, three with cholangiomas, and one with a metastatic pheochromocytoma. In a preliminary attempt to compare their iron absorption, five black-and-white ruffed lemur (Lemur variegatus variegatus) weanlings and five rhesus monkey weanlings were each given ～500 nmol/kg FeCI₃ (27.9 μg iron/kg) containing 5 μCi of ⁵⁹Fe in 0.1 M HCl via a nasogastric tube. Retained ⁵⁹Fe was measured by whole body gamma counting and found to be roughly the same in the two groups, possibly because insufficient quantities of iron were administered and/or excessive iron absorption becomes apparent only in older animals. Our conclusions were the following: (1) Hemosiderosis in lemurs is associated with tissue damage similar to that seen in humans with idiopathic hemochromatosis. (2) Because iron deposits occur both in parenchymal cells and reticuloendothelial cells, hemosiderosis in lemurs is probably not a model for idiopathic hemochromatosis in a pure sense.     

Digesta passage and functional anatomy of the digestive tract in the desert tortoise (Xerobates agassizii)

The herbivorous tortoise Xerobates agassizii contents with large fluctuations in the quality and abundance of desert pastures. Responses to grass (Schismus barbatus), herbage (Sphaeralcea ambigua) and pelleted diets were studied in captive animals. Digestive anatomy was investigated in wild tortoises. Cornified esophageal epithelia and numerous mucus glands along the digestive tract indicated a resistance to abrasive diets. Gastric contents were acidic whereas hindgut digesta were near neutral pH. The colon was the primary site of fermentation with short-chain fatty acids mainly comprised of acetate (69–84%), propionate (10–15%) and n-butyrate (1–12%). Fibre digestion was extensive and equivalent to 22–64% of digestible energy intakes. Large particles of grass (25 mm Crmordants) were excreted as a pulse but retained longer than either fluids (Co-EDTA) or fine particles (2 mm; Yb). Patterns of marker excretion suggested irregular mixing of only the fluid and fine particulate digesta in the stomach and the colon. Mean retention times of Crmordants were 14.2–14.8 days on the grass and highfibre pellets. Intakes of grass were low and accompanied by smaller estimates of digesta fill than for the high-fibre pellets. Digestive capacity was large and estimated at 11–21% of body mass on these diets. The capacious but simple digestive anatomy of the tortoise may provide the greatest flexibility in utilizing a variety of forages in its unreliable habitat.Abbreviations bm body mass - DM drymatter - EDTA ethylene-diamine tetra-acetic acid - MRT mean retention time - NDF neutral detergent fibre - SCFA short-chain fatty acid(s) - T _max time to maximum marker concentration     

Digestive physiology of wild capybara

The capybara (Hydrochaeris hydrochaeris) is a hindgut fermenter whose digestive efficiency is comparable to that of ruminants on similar diets. It is an interesting case for study because it is the largest caecum fermenter and uses coprophagy as part of its digestive strategy. It practices coprophagy in the early morning and forages and defaecates in the evening. Its anatomy is well known but the limited information available about its digestive physiology has been obtained from captive animals. In this work we studied the capybara's digestive physiology, using microbial and chemical information from samples taken from wild capybaras in the early wet season in the morning (0600–0700 hours), noon (1200–1300 hours) and evening (1800–1900 hours), key points in the digestive cycle. Bacteria (cellulolytic and non-cellulolytic) and protozoa were present in high concentrations in the caecum and colon. There were no significant differences in nitrogen concentrations between digestive tract compartments in the coprophagy period (0600 hours), but in the other two periods nitrogen concentrations were significantly higher in the caecum than in the stomach and colon. This is suggestive of selective retention of microbial cells with fluid digesta in the caecum and of cecotrophy (the production of two distinctly different kinds of faeces — one kind called cecotrophes formed from caecal contents and ingested). The capybara hindgut (caecum and colon) with its content, was heavier during the dry season (period of poor diet quality) than in the wet season, but there were no significant seasonal differences between the stomach or small intestine and their contents. This suggests changes in the capacity of the hindgut, the site of microbial fermentation, related to seasonal variation in resource quality.Abbreviations NDF neutral-detergent fibre - SCFA Short-chain fatty acid(s)     

Digesta retention in the gastro-intestinal tract of the orang utan (Pongo pygmaeus)

The diet of the orang utanPongo pygmaeus consists of fruit, leaves, communal insects, and bark, and contains appreciable amounts of non-starch polysaccharides. These complex carbohydrates require microbial fermentation before they can be used as an energy source by the orang utans. The gastrointestinal tract ofP. pygmaeus consists of a simple or unipartite stomach, a relatively long small intestine, and a complex haustrated caecum and colon. This morphology suggests that the capacious proximal colon is the principal site of digesta retention and fermentation of non-starch polysaccharides. We measured several parameters of digesta retention by giving three captive adultP. pygmaeus a pulse dose of inert markers specific for the solute and particulate phases of the digesta and collected their faeces at regular intervals over 192–338 hours. Transit times (times of first appearance of the markers in the faeces) and mean retention times (MRT) were long, consistent with a large complex gastro-intestinal tract. MRTs for the particulate marker were longer (p=0.032) than for the solute marker, indicative of selective retention of large particulate digesta. These results are consistent with the patterns of marker excretion in other mammals that use the digestive strategy of colon fermentation.     

Leaf chemistry and the biomass of folivorous primates in tropical forests

Summary Recent results have suggested that the biomass of folivorous arboreal primates per unit area in Africa and Asia is positively correlated with the average quality of leaves, expressed as the ratio of protein to fiber concentrations in a given forest. This hypothesis has been tested in different forests of Madagascar. Leaf selection of all folivorous femus species was studied in relation to leaf chemistry. Except for two populations ofLepilemur subspecies all other folivorous lemur species (including two other subspecies ofLepilemur) select leaves with high concentrations of easily extractable protein or low concentrations of fiber, or both. This confirms the prominent role of these two components in leaf selection by folivorous lemurs. The average quality of mature leaves in a given forest, expressed as the ratio of protein to fiber concentrations, is positively correlated with the biomass of folivorous lemurs. This confirms the hypothesis tested and suggests rather uniform selection processes for arboreal folivorous primates across the world.     

Microsatellite loci for the Siberian flying squirrel,Pteromys volans

We report the isolation and characterization of polymorphic microsatellite loci for the Siberian flying squirrel Pteromys volans. The seven most useful loci had between six and 11 alleles and expected heterozygosities ranging from 0.477 to 0.866. We also tested the utility of these loci in other squirrel species, northern flying squirrels (Glaucomys sabrinus and G. volans) and the common red squirrel (Sciurus vulgaris). Three of the Siberian flying squirrel loci were polymorphic in other squirrel species, suggesting a limited potential for cross‐species use.     

Pitch control and speed limitation during overground deceleration in lemurid primates

An animal's fitness is influenced by the ability to move safely through its environment. Recent models have shown that aspects of body geometry, for example, limb length and center of mass (COM) position, appear to set limits for pitch control in cursorial quadrupeds. Models of pitch control predict that the body shape of these and certain other primates, with short forelimbs and posteriorly positioned COM, should allow them to decelerate rapidly while minimizing the risk of pitching forward. We chose to test these models in two non-cursorial lemurs: Lemur catta, the highly terrestrial ring-tailed lemur, and Eulemur fulvus, the highly arboreal brown lemur. We modeled the effects of changes in limb length and COM position on maximum decelerative potential for both species, as well as collecting data on maximal decelerations across whole strides. In both species, maximum measured decelerations fell below the range of pitch-limited deceleration values predicted by the geometric model, with the ring-tailed lemur approaching its pitch limit more closely. Both lemurs showed decelerative potential equivalent to or higher than horses, the only comparative model currently available. These data reinforce the hypothesis that a relatively simple model of body geometry can predict aspects of maximum performance in animals. In this case, it appears that the body geometry of primates is skewed toward avoiding forward pitch in maximal decelerations.     

Feeding enrichment by self‐operated food boxes for white‐fronted lemurs (Eulemur fulvus albifrons) in the Masoala exhibit of the Zurich Zoo

In the new Masoala exhibit of the Zurich Zoo four self‐operated food boxes were installed to encourage arboreal behavior and higher activity levels, and to increase the attractiveness to visitors of a group of three white‐fronted lemurs (Eulemur fulvus albifrons) and one Alaotran gentle lemur (Hapalemur griseus alaotrensis). Data obtained by direct observations with and without food boxes present were compared. In addition, visitors were surveyed to investigate attractiveness of the lemurs. Overall activity and locomotor behavior increased due to food box presentation. Furthermore, the visitor survey documented that the lemurs were spotted more often in trees when the food boxes were present. Because behavior patterns of the subjects approached natural levels with food boxes, the presentation of self‐operated food boxes seems a valuable tool to improve the captive environment of lemurs. Zoo Biol 0:1–10, 2005. © 2005 Wiley‐Liss, Inc.     

Ecological correlates to social structure in two lemur species in Madagascar

In this study, I tested two hypotheses regarding the relationship of ecological variables (size, density, and distribution of patches) and infant developmental patterns to lemur social structure using two prosimian primates in Ranomafana, Madagascar: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). Three predictions regarding the general effects of patch size and subgroup size on lemur feeding rates were supported: (1) Rufous lemurs used large patches; red-bellied lemurs used smaller patches; (2) larger subgroups of rufous lemurs used larger patches; and (3) rufous lemur feeding rates decreased significantly with increases in subgroup size and patch size, whereas size and patch size had no significant effect on red-bellied lemur feeding rates. However, food item size (fruit) had a more significant effect on rufous and red-bellied lemur feeding rates than either patch size or subgroup size. When similar-sized fruits were compared, rufous lemur feeding rates on small fruit were most affected by patch size, yet feeding rates on medium-sized fruit were most affected by subgroup size. Neither lemur species used patches in consistent ways seasonally. During periods of food abundance, rufous lemurs used many small, common, and clumped patches. In food scarcity periods, they used fewer, larger, rarer, and less clumped patches; groups migrated when food became most scarce. Red-bellied lemurs also used patches in variable ways, but these patterns were not linked with food availability. Finally, infant development patterns differed between lemur species; red-bellied lemur males cared for offspring and infants reached developmental landmarks faster than rufous lemur infants. Therefore, red-bellied lemur group size may be constrained by the need for additional infant care by other group members. In contrast, rufous lemur group size may be constrained by patch availability during the most critical period of food scarcity. © 1996 Wiley-Liss, Inc.     

The passage of digesta, particle size, and in vitro fermentation rate in the three-toed sloth Bradypus tridactylus (Edentata: Bradypodidae)

The digestive physiology of six three-toed sloths ( Bradypus tridactylus ) fed exclusively on Cecropia palmata foliage was studied. The mass of digesta in the gut was between 17 and 37% of body mass. This was between 133 and 282% of that expected in an animal of this size, based on published allometric equations. The concentration of total short chain fatty acids in the stomach was similar to that in the fermentative regions of other foregut fermenting herbivores but the rate of fermentation measured in vitro was very slow (6–12 mmol.l^-1.h^-1) and substantially lower than that observed using similar techniques in other small foregut fermenters.
The overall (dose to excretion) mean retention time of particulate and solute digesta markers was about 150 h. Most of this (73%) occurred in the stomach but a substantial proportion (17%) could be attributed to the storage of faeces in the rectum.
The slow rate of passage of digesta through the gut together with the slow rate of fermentation in the stomach is not typical of small foregut fermenting herbivores. However, such a pattern is feasible in Bradypus tridactylus because of the large volume of digesta retained in the gut and the very low metabolic rate of these mammals.     

Effect of habitat structure on positional behavior and support use in three species of lemur

This study compares locomotor and postural behavior and substrate use of three species of lemur, the diademed sifaka (Propithecus diadema edwardsi), the brown lemur (Eulemur fulvus rufus), and the red-bellied lemur (Eulemur rubriventer) at two different localities within Ranomafana National Park. The object of the study is to see if there are quantitative differences in the behavior of the lemurs or their choice of substrates in forests that have different structural attributes. Analysis of the physical characteristics of the habitat demonstrates that compared to the Talatakely area, the forest at Vatoharanana has a higher proportion of larger, taller trees. The behavior of the lemurs also differs in the two areas: all species leap less and climb and move quadrupedally more at Vatoharanana. All species use small size supports less frequently at Vatoharanana, choosing insted medium size supports (all three species) or tiny supports (Propithecus andE. fulvus) found in tree crowns and terminal branches. The lemurs prefer (i.e. use more often than would be expected based on abundance) large trees at both sites. At Vatoharanana however, they are more frequently observed higher in trees and in taller trees with greater trunk breadth. The differences in locomotor behavior are in part due to the fact that at Vatoharanana, more bouts are collected during feeding and foraging than during travel. The relationship between this difference in activity pattern and the structural differerences in the two forests, however, is not clear. This study points out the need for longer term field studies of positional behavior and substrate use that incorporate the variety of forest types the subject species inhabit.     

Brief communication: Blue eyes in lemurs and humans: Same phenotype,different genetic mechanism

Almost all mammals have brown or darkly‐pigmented eyes (irises), but among primates, there are some prominent blue‐eyed exceptions. The blue eyes of some humans and lemurs are a striking example of convergent evolution of a rare phenotype on distant branches of the primate tree. Recent work on humans indicates that blue eye color is associated with, and likely caused by, a single nucleotide polymorphism (rs12913832) in an intron of the gene HERC2, which likely regulates expression of the neighboring pigmentation gene OCA2. This raises the immediate question of whether blue eyes in lemurs might have a similar genetic basis. We addressed this by sequencing the homologous genetic region in the blue‐eyed black lemur (Eulemur macaco flavifrons; N = 4) and the closely‐related black lemur (Eulemur macaco macaco; N = 4), which has brown eyes. We then compared a 166‐bp segment corresponding to and flanking the human eye‐color‐associated region in these lemurs, as well as other primates (human, chimpanzee, orangutan, macaque, ring‐tailed lemur, mouse lemur). Aligned sequences indicated that this region is strongly conserved in both Eulemur macaco subspecies as well as the other primates (except blue‐eyed humans). Therefore, it is unlikely that this regulatory segment plays a major role in eye color differences among lemurs as it does in humans. Although convergent phenotypes can sometimes come about via the same or similar genetic changes occurring independently, this does not seem to be the case here, as we have shown that the genetic basis of blue eyes in lemurs differs from that of humans. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Isolation of new microsatellite markers and application in four species of mouse lemurs (Microcebus sp.)

We report the development of 13 new microsatellite markers for mouse lemurs (Microcebus sp.). Two markers were isolated from the fat tailed dwarf lemur (Cheirogaleus medius) and 11 from the grey mouse lemur (Microcebus murinus). A total of 561 individuals from four different species of mouse lemurs was genotyped with the newly developed markers. All markers showed Mendelian inheritance in 21 families of mouse lemurs. All markers show polymorphism in several species of mouse lemurs and seven amplified in C. medius. Among these new markers are the first 10 published for M. berthae and the first 11 for M. griseorufus.