Locomotor ecology of Lepilemur edwardsi and Avahi occidentalis

A well-known principle holds that where food supply is limited, two sympatric species with the same diet, morphology, and behavior will compete, leading to exclusion of one species or differentiation of their ecological niches. Avahi occidentalis and Lepilemur edwardsi are two saltatory, nocturnal folivorous lemurs of similar body size which live sympatrically over much of their range and may often be seen feeding in the same trees. We report a study of their locomotor behavior, carried out in order to determine to what extent locomotion might contribute to niche separation. Avahi lives at a higher level in the forest and is the more committed leaper, with a much larger home range and nightly travel distance, while Lepilemur climbs more and has a very small nightly travel distance. Avahi uses small, low-angled supports more often, while Lepilemur makes more use of large, high-angled supports (however, neither species uses vertical supports at a frequency greater than the availability of such supports in the forest stratum in which they live). Both species tend to land on larger-diameter supports on longer leaps, but Avahi also takes off from larger-diameter supports in longer leaps, reducing loss of energy to the substrate during takeoff. We suggest that the differences in locomotion and ranging behavior between them are consistent with niche differentiation on the basis of food quality, Avahi investing more energy in harvesting better quality but more patchy food, Lepilemur minimizing expenditure in harvesting a less selective, quantitatively poorer diet. Am J Phys Anthropol 104:471–486, 1997. © 1997 Wiley-Liss, Inc.     

Genetic Differentiation among Natural Populations of Lepilemur ruficaudatus

We studied the genetic differentiation of five populations of red-tailed sportive lemur Lepilemur ruficaudatus by means of allozyme variability and RAPD polymorphisms in order to test whether the Tsiribihina River separates the distribution areas of Lepilemur ruficaudatus and and L. edwardsi. Genetic data as well as the karyotype of a male individual clearly indicate that the Andramasay Forest in the north of Tsiribihina River is inhabited by Lepilemur ruficaudatus and not by L. edwardsi. We propose that the distribution of the two species are separated by the Manambolo River. However, the northernmost population of Lepilemur ruficaudatus inhabiting the Andramasay Forest is gentically differentiated from those that inhabit the dry forest in the south of Tsiribihina River.     

Resting metabolic rates of Lepilemur ruficaudatus

Seventeen sportive lemurs (Lepilemur ruficaudatus) were captured in a dry, deciduous forest in western Madagascar, and the resting metabolic rates were measured. According to the data, resting metabolic rates of Lepilemur ruficaudatus are among the lowest of mammalian folivores recorded so far. © 1996 Wiley-Liss, Inc.     

Does nonnutritive tree gouging in a rainforest‐dwelling lemur convey resource ownership as does loud calling in a dry forest‐dwelling lemur?

Nonhuman primates may defend crucial resources using acoustic or chemical signals. When essential resources are limited, ownership display for a resource may be enhanced. Defending resources may depend on population density and habitat characteristics. Using the Milne Edwards' sportive lemurs (Lepilemur edwardsi) and weasel sportive lemurs (L. mustelinus) as models, we tested whether two cryptic nocturnal lemur species differing in population density and habitat show differences in their vocal and chemical communication for signaling ownership of resources. L. edwardsi inhabits a western dry deciduous forest in a high‐density population, whereas L. mustelinus is found in an eastern rainforest in low density. We followed ten L. edwardsi (six males and four females) and nine L. mustelinus (four males and five females) for 215 hr during the early evening (06:00–10:00 p.m.) and the early morning (02:00–05:00 a.m.) and recorded their behavior using focal animal sampling. We found that both species differed in their vocal and chemical communication. L. edwardsi was highly vocal and displayed loud calling in the mornings and evenings while feeding or in the vicinity of resting places. In contrast, L. mustelinus never vocalized during observations, but displayed tree‐gouging behavior that was never observed in L. edwardsi. Tree gouging occurred more often during early evening sessions than early morning sessions. Subjects gouged trees after leaving their sleeping hole and before moving around. We suggest that, in weasel sportive lemurs, non‐nutritive tree gouging is used as a scent‐marking behavior in order to display ownership of sleeping sites. Altogether, our findings provide first empirical evidence on the evolution of different communication systems in two cryptic nocturnal primate species contrasting in habitat quality and population density. Further investigations are needed to provide more insight into the underlying mechanisms. Am. J. Primatol. 72:1062–1072, 2010. © 2010 Wiley‐Liss, Inc.     

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.     

Determinants of Pair‐Living in Red‐Tailed Sportive Lemurs (Lepilemur ruficaudatus)

Pair‐living and a monogamous mating strategy are rare and theoretically unexpected among mammals. Nevertheless, about 10% of primate species exhibit such a social system, which is difficult to explain in the absence of paternal care. In this study, we investigated the two major hypotheses proposed to explain the evolution of monogamy in mammals, the female defence hypothesis (FDH) and the resource defence hypothesis (RDH), in red‐tailed sportive lemurs (Lepilemur ruficaudatus), a nocturnal primate from Madagascar. We analysed behavioural data from eight male–female pairs collected during a 24‐mo field study to illuminate the determinants of pair‐living in this species. Male and female L. ruficaudatus were found to live in dispersed pairs, which are characterised by low cohesion and low encounter rates within a common home range. Social interactions between pair partners were mainly agonistic and characterised by a complete absence of affiliative interactions – body contact was only observed during mating. During the short annual mating season, males exhibited elevated levels of aggression towards mates, as well as extensive mate guarding and increased locomotor activity. In addition, males were exclusively responsible for the maintenance of proximity between pair partners during this period, and they defended their territories against neighbouring males but not against females. Together, these results point towards the importance of female defence in explaining pair‐living in L. ruficaudatus. We discuss the spatial and temporal distribution of receptive females in relation to the female defence strategies of males and suggest possible costs that prevent male red‐tailed sportive lemurs from defending more than one female.     

Infanticide by a Male Milne-Edwards' Sportive Lemur (Lepilemur edwardsi) in Ampijoroa,NW-Madagascar

During a long-term field study on the behavioral ecology and communication of a population of the monogamous Milne-Edwards' sportive lemur (Lepilemur edwardsi) in NW-Madagascar, we recorded for the first time an infanticide in a nocturnal lemur. A male newcomer killed the infant of a female whose male partner had left her recently. Both the social-pathology and the sexual-selection hypotheses may explain infanticidal behavior in Lepilemur edwardsi.     

Locomotion and habitat utilization in free-rangingTarsius bancanus: A preliminary report

Four adultTarsius bancanus were followed for a total of over 120 hrs in Sepilok Forest Reserve, Sabah, using radiotracking techniques. Seven hundred and twenty-two records of locomotor and postural behaviour were gathered.Tarsius bancanus travels a mean of 1,800 m per night, over large (4.5 to 11.25 ha) ranges. They move at a mean height of 0.89 m, utilizing primarily vertical sapling trunks of diametre 2 to 4 cm. Lateral movement is carried out largely by leaping.Tarsius were found on the ground in 5.3% of cases, but movement on the ground is very largely restricted to short investigative movements by walking. Climbing is mostly related to foraging behaviour and characteristically occurs on relatively small supports.Tarsius bancanus' locomotion is similar to, but more specialized than that ofT. spectrum, Galago alleni, andGalago senegalensis, all of which have rather similar patterns of habitat utilization. We suggest that the energetic constraints of small body size together with the need to patrol large home ranges may have lead both toTarsius bancanus extreme degree of locomotor specialization and to its exclusive animalivory.     

Positional behavior of Siberian chipmunks (Tamias sibiricus) in captivity

Arboreal and semi-arboreal mammals have remarkably diverse positional behavior and associated morpho-functional adaptations related to the three-dimensional nature of their arboreal habitat. In this context, we investigated the positional behavior of captive Siberian chipmunks (Tamias sibiricus), small bodied semi-arboreal sciurids, in an aviary-type wire-mesh cage containing both terrestrial and arboreal supports. We sampled four adult individuals during a five-month period using focal animal sampling every 30 s. Results showed that animals preferred 8–10 cm horizontal supports and always avoided vertical supports. Locomotion occurred on both terrestrial and 8–10 cm arboreal supports whereas postural behavior occurred primarily on 8–10 cm arboreal supports. Quadrupedal walk dominated during locomotion, and occurred primarily on terrestrial horizontal supports, as is observed for other squirrels. The predominance of quadrupedal locomotion is consistent with the postcranial morphology of chipmunks. In contrast, clawed locomotion occurred on wire mesh and on >13 cm arboreal vertical supports. Finally, pronograde and orthograde sitting, both on 8–10 cm arboreal supports and on terrestrial supports, were the predominant postures, implying general predisposition to selection of stable postures on stable supports for food item manipulation and ingestion.     

SmTRC1, a novel Schistosoma mansoni DNA transposon, discloses new families of animal and fungi transposons belonging to the CACTA superfamily

Background

The number of species within the Malagasy genus Lepilemur and their phylogenetic relationships is disputed and controversial. In order to establish their evolutionary relationships, a comparative cytogenetic and molecular study was performed. We sequenced the complete mitochondrial cytochrome b gene (1140 bp) from 68 individuals representing all eight sportive lemur species and most major populations, and compared the results with those obtained from cytogenetic studies derived from 99 specimens.

Results

Interspecific genetic variation, diagnostic characters and significantly supported phylogenetic relationships were obtained from the mitochondrial sequence data and are in agreement with cytogenetic information. The results confirm the distinctiveness of Lepilemur ankaranensis, L. dorsalis, L. edwardsi, L. leucopus, L. microdon, L. mustelinus, L. ruficaudatus and L. septentrionalis on species level. Additionally, within L. ruficaudatus large genetic differences were observed among different geographic populations. L. dorsalis from Sahamalaza Peninsula and from the Ambanja/Nosy Be region are paraphyletic, with the latter forming a sister group to L. ankaranensis.

Conclusion

Our results support the classification of the eight major sportive lemur taxa as independent species. Moreover, our data indicate further cryptic speciation events within L. ruficaudatus and L. dorsalis. Based on molecular data we propose to recognize the sportive lemur populations from north of the Tsiribihina River, south of the Betsiboka River, and from the Sahamalaza Peninsula, as distinct species.     

Forest Structure and Support Availability Influence Orangutan Locomotion in Sumatra and Borneo

The influence of habitat structure and support availability on support use is an important aspect of understanding locomotor behavior in arboreal primates. We compared habitat structure and support availability in three orangutan study sites—two on Sumatra (Pongo abelii) in the dry‐lowland forest of Ketambe and peat swamp forest of Suaq Balimbing, and one on Borneo (Pongo pygmaeus wurmbii) in the disturbed peat swamp forest of Sabangau—to better understand orangutan habitat use. Our analysis revealed vast differences in tree and liana density between the three sites. Sabangau had a much higher overall tree density, although both Sumatran sites had a higher density of larger trees. The two peat swamp forests were more similar to each other than to Ketambe, particularly with regard to support availability. Ketambe had a wider variety of supports of different sizes and types, and a higher density of larger lianas than the two peat swamps. Orangutans in all three sites did not differ substantially in terms of their preferred supports, although Sumatran orangutans had a strong tendency to use lianas, not observed in Sabangau. Differences in observed frequencies of locomotor behavior suggest the homogeneous structure of Sabangau limits the locomotor repertoire of orangutans, with high frequencies of fewer behaviors, whereas the wider range of supports in Ketambe appears to have facilitated a more varied locomotor repertoire. There were no differences among age‐sex classes in the use of arboreal pathways in Suaq Balimbing, where orangutans selected larger trees than were typically available. This was less apparent in Sabangau, where orangutans generally used trees in relation to their environmental abundance, reflecting the homogeneous nature of disturbed peat swamp forest. These results demonstrate that forest architecture has an important influence on orangutan locomotion, which may become increasingly important as the structure of orangutan habitat continues to be altered through human disturbance. Am. J. Primatol. 74:1128‐1142, 2012. © 2012 Wiley Periodicals, Inc.     

Locomotion of free-ranging golden lion tamarins (Leontopithecus rosalia) at the National Zoological Park

Locomotor behavior and substrate use of cage-reared golden lion tamarins (Leontopithecus rosalia), newly released and free-ranging on the grounds of the National Zoological Park, were studied to determine if locomotion changed following exposure to naturalistic conditions. The animals employed a predominantly quadrupedal locomotor profile, incorporating leaping and vertical climbing to a lesser degree. There was no clear evidence of a change in locomotion due to the high degree of variability in these behaviors. The locomotor repertoire of the free-ranging group differed from that of groups occupying unenriched but relatively large conventional enclosures, indicating that whereas locomotion is plastic with respect to environment, substrate characteristics influence locomotor behavior and may promote stereotypical behavior. However, due to anatomical constraints, the locomotor repertoire tended to be less variable than substrate use. Similar behaviors were used in moving through a variety of habitat features in spite of strong associations between specific locomotor styles and substrate classes. © 1994 Wiley-Liss, Inc.     

Positional behavior and social organization of the philippine tarsier (Tarsius syrichta)

This study provides preliminary data on the positional behavior and habitat use of the Philippine tarsier,Tarsius syrichta, which was studied in its natural habitat on the island of Leyte. The locomotor behavior ofT. syrichta is quite comparable to the other species of tarsiers but frequency of use of different postures and support types does seem to distinguish this species from the others.Tarsius bancanus appears to be the most specialized, using vertical clinging postures the most frequently and sitting the least;Tarsius dianae uses vertical clinging the least frequently and sitting the most, andT. syrichta is intermediate. The Philippine tarsier has a small home range similar to that ofT. spectrum. On the other hand, this species likely does not have the small family groups typical of Sulawesi tarsiers but instead uses a noyau system likeT. bancanus. This data supports some apsects ofNiemitz’s (1977) model of anatomical and behavioral specialization among tarsier species.     

Vertical Clinging and Leaping Revisited: Locomotion and Habitat Use in the Western Tarsier, <Emphasis Type="Italic">Tarsius bancanus</Emphasis> Explored Via Loglinear Modeling

Napier and Walker’s (1967) locomotor category of vertical clinging and leaping (VC&L) is one of the most familiar in primatology, and tarsiers are probably the most morphologically specialized of its membership. However, the link between vertical clinging and leaping remains unelucidated. We attempt to do so by reanalysis of Crompton’s 1985 and 1986 field observations of locomotion and habitat use in Tarsius bancanus, using loglinear modeling. Loglinear modeling is better suited to the categorical variables used in many field studies than more traditional statistics, such as ANOVA, developed for continuous variables. We show that climbing, as well as leaping, is one of the predominant forms of locomotion, and that all other things being equal, tarsiers tend to take off from, and land on, similar sized supports, which suggests that the following findings are not likely to be a result of substrate availability alone. Small body size lead to a prediction that tarsiers should leap down but climb up: this was not sustained: rather leaps tend to be level, and climbing accounts for more height loss than randomly expected. However, a prediction that to avoid energy loss to the substrate, the tarsiers should show a preference for large diameter supports for takeoff when leaping longer distances was supported, although tarsiers do not avoid moderately compliant supports. The prediction from ballistic principles that the longest leaps should start from high-angled supports was only weakly sustained, but low-angled supports tend to be strongly associated with short leaps, suggesting that such supports do not facilitate 45° takeoff trajectories. However, tarsiers displayed a preference for landing on medium-sized supports when leaping long distances, suggesting a preference for balancing the need for stability with minimizing musculoskeletal shock.     

Locomotor and postural behavior in Alouatta palliata and Cebus capucinus

Positional behavior of two platyrrhine monkeys, Alouatta palliata and Cebus capucinus, was observed at La Pacifica and Santa Rosa National Park, Costa Rica. Frequency data for locomotion, postures, support diameters, orientation of supports, and use of canopy were recorded on focal males and females. Alouatta palliata is a frequent user of arboreal quadrupedalism (47%) and climbing (37%), with bridging (10%) representing the next most frequent type of locomotion. Intraspecific comparisons show the smaller-sized females of Alouatta to prefer very small diameter supports, the lower canopy, and to climb more frequently than the larger males—a pattern opposite to that which has been documented to occur with increasing body size across species. A more limited study on Cebus capucinus shows this species to be highly quadrupedal (54%) with moderately high locomotor frequencies for climbing (26%) and leaping (15%).     

Substrate alters forelimb to hindlimb peak force ratios in primates

It is often claimed that the walking gaits of primates are unusual because, unlike most other mammals, primates appear to have higher vertical peak ground reaction forces on their hindlimbs than on their forelimbs. Many researchers have argued that this pattern of ground reaction force distribution is part of a general adaptation to arboreal locomotion. This argument is frequently used to support models of primate locomotor evolution. Unfortunately, little is known about the force distribution patterns of primates walking on arboreal supports, nor do we completely understand the mechanisms that regulate weight distribution in primates. We collected vertical peak force data for seven species of primates walking quadrupedally on instrumented terrestrial and arboreal supports. Our results show that, when walking on arboreal vs. terrestrial substrates, primates generally have lower vertical peak forces on both limbs but the difference is most extreme for the forelimb. We found that force reduction occurs primarily by decreasing forelimb and, to a lesser extent, hindlimb stiffness. As a result, on arboreal supports, primates experience significantly greater functional differentiation of the forelimb and hindlimb than on the ground. These data support long-standing theories that arboreal locomotion was a critical factor in the differentiation of the forelimbs and hindlimbs in primates. This change in functional role of the forelimb may have played a critical role in the origin of primates and facilitated the evolution of more specialized locomotor behaviors.     

How to climb a tree: lizards accelerate faster,but pause more,when escaping on vertical surfaces

Many species of lizards effectively traverse both two and three‐dimensional habitats. However, few studies have examined maximum locomotor performance on different inclines. Do maximum acceleration and velocity differ on a level and inclined surface? Do lizards pause more on an inclined surface? To address these questions, Sceloporus woodi lizards (N = 12) were run in the laboratory on a level trackway and a vertical tree trunk. This species is known to frequently utilize both vertical and horizontal aspects of its habitat. Average maximum acceleration on the vertical surface exceeded that on the level surface, although average maximum velocity exhibited the opposite pattern. The average number of pauses during level locomotion was lower compared to vertical locomotion. In addition, the average location of the first pause on the level surface was 0.51 m, which is farther than the average for vertical locomotion where the first pause was at 0.35 m. The combination of performance and pause data suggests that the relative lack of pausing during level locomotion allows individuals to reach higher maximum velocities on level surfaces because they accelerate over greater distances. The increased pausing when moving vertically could be a result of high energetic demands of vertical locomotion, or greater microhabitat complexity as a result of branching and/or refuges. The faster acceleration exhibited during vertical locomotion by S. woodi likely offsets the frequent pauses. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 83–90.     

Locomotor behavior,body size,and comparative ecology of seven Surinam monkeys

The locomotor behavior, of seven sympatric species of New World monkeys—Saguinus midas midas, Saimiri sciureus, Pithecia pithecia, Chiropotes satanas chiropotes, Cebus apella apella, Alouatta seniculus, and Ateles paniscus panisus—was studied at the Raleighvallen-Voltzberg Nature Reserve in Central Surinam. This paper examines the way in which locomotor behavior is related to body size and to ecological parameters such as forest stratification, forest type, and diet. Locomotor behavior is clearly related to the size of the species; with increasing size, the amount of climbing increases and the amount of leaping decreases. In general, larger monkeys use larger arboreal supports; however, Saguinus midas midas uses relatively larger, and Ateles paniscus paniscus relatively smaller supports than expected from body size alone. Leaping is associated with use of the forest understory and with use of liane forest. Other types of locomotion are associated with main canopy use in a variety of forest types. There are no consistent associations between diet and either locomotor behavior or forest utilization; rather, monkeys with similar diets show locomotor and habitat differentiation.     

Positional behavior of the white uakari (Cacajao calvus calvus)

The positional behavior and habitat use of a group of white uakaries (Cacajao calvus calvus) was observed for 6 weeks in the dry season at Lake Teiú, Brazil. Data are presented for feeding, traveling, and resting activities. The most common feeding posture is sit, followed by stand. Cacajao frequently exhibits locomotor behaviors while in feeding trees, using pronograde clamber and quadrupedal walk. The most frequently used locomotor behaviors in travel are quadrupedal walk, leap, and pronograde clamber. Quadrupedal run and drop also figure importantly in the behavioral repertoire. The most frequent resting posture was sit, followed by ventral lie. Compared to representative members of the other pitheciin genera, Pithecia and Chiropotes, Cacajao engages in more locomotion while feeding, and uses more pedal suspension. While traveling, pronograde clamber and drop are more frequently used by Cacajao. Multiple, deformable supports are used more by Cacajao than by the other pitheciins throughout all activities. Overall, the positional behavior of Cacajao is more similar to that of Chiropotes than of Pithecia. Cacajao's behavioral solutions to the problems of balance imposed by its greatly reduced tail are discussed. © 1996 Wiley-Liss, Inc.     

Functional divergence between morphs of a dwarf chameleon: differential locomotor kinematics in relation to habitat structure

Arboreal lizards are extremely effective at moving in structurally complex habitats, including surfaces of varying diameter and incline. Chameleons exemplify this by exhibiting a number of morphological specializations for moving in these habitats, including the use of prehensile feet and tail to grasp branches. Despite their unique morphology and behaviour, little is known about how locomotor movements vary between species. In addition, some species, such as the Cape Dwarf Chameleon, Bradypodion pumilum, consist of two morphs that differ in ecology, morphology, and behaviour. The two morphs can be found in either closed canopy woodland habitat or relatively open fynbos habitat. The morph that occupies the woodland habitat tends to be larger and utilizes larger diameter perches. Although their ecological and morphological divergence is established, whether this translates into differences in three‐dimensional kinematics of locomotion is not known. Given the potentially strong selective pressures from structurally different habitats, kinematic differences might reveal the functional basis of incipient speciation. We determined that the two morphs diverge significantly in multidimensional kinematic space, and that this occurs for the forelimb and hindlimb independently. These differences outweigh the effects of substrate within each morph, although the differences between morphs were more pronounced on the vertical treatments.