Overview of Sensory Systems of <Emphasis Type="Italic">Tarsius</Emphasis>

Tarsiers form the sister taxon to anthropoid primates, and their brains possess a mix of primitive and specialized features. We describe architectonically distinct subdivisions of the somatosensory, auditory, and visual systems for tarsiers, as well as nocturnal New World owl monkeys (Aotus) and strepsirhine galagos (Otolemur) for comparison. In general, the dorsal column nuclei, the ventroposterior nucleus, and primary somatosensory cortex are somewhat less distinctly differentiated in tarsiers, suggesting that the somatosensory system is less specialized for somatosensory processing. Although the inferior colliculus and the medial geniculate complex of the auditory system are architectonically similar across the 3 primates, the primary auditory cortex of tarsiers is more distinct, suggesting a greater role in auditory cortical processing. In the visual system, the differentiation of the superior colliculus is similar in all 3 primates, whereas the laminar pattern in the lateral geniculate nucleus and the subdivisions of the inferior pulvinar in tarsiers resemble those of anthropoid primates rather than strepsirhines, in agreement with the evidence that tarsiers form the sister clade for anthropoids. In addition, primary visual cortex has more distinct sublayers in tarsiers than other primates, attesting to its importance in this visual predator. Overall, tarsiers have well developed visual and auditory systems, and a less well developed somatosensory system, suggesting an enhanced reliance on the visual and auditory senses, rather than somatosensory sense.     

Tarsier brain component composition and its implications for systematics

The taxonomic position ofTarsius has been a topic of some debate. Recent molecular and anatomical studies have shoen that tarsiers share a number of derived traits with Anthropoids. These include aspects of their reporductive biology and aspects of their olfactory and visual systems. It has, therefore, been suggested that, despite a number of convergences with strepsirhine primates, tarsiers should be classified with the Anthropoid primates. We use comparative analyses of relative primate brain part volumes to determine whetherTarsius should be classified as a Haplorhine. We show that, for each of seven brain components whose relative size discriminates unequivocally between Strepsirhines and Haplorhines, the tarsiers fall in the Haplorhine distribution. These results confirm their classification with the Haplorhines.     

The Genera and Species of Tarsiidae

We revise the taxonomy of the primate family Tarsiidae. We classify extant tarsiers in 3 genera—Tarsius, Cephalopachus, and Carlito—each of which originated in the Miocene, or earlier, and each of which is allopatrically distributed within a distinct biogeographic region: Sulawesi, Sundaland, and Greater Mindanao, respectively. Within the genus Tarsius, formerly regarded as a single species, Tarsius spectrum, we recognize 8 allopatric and parapatric species, 9 if the inclusion of pumilus is warranted, and note that more are likely to be described in the near future. We restrict Tarsius tarsier, the senior taxon of the genus, to the island of Selayar, off the tip of the southwestern peninsula of Sulawesi. In doing so, it is required that we resurrect Tarsius fuscus Fischer 1804, for the population of tarsiers from the southwestern peninsula near the city of Makassar. We note that neither Cephalopachus nor Carlito has been the subject of anywhere near as much field research as has Tarsius; thus we question if the currently accepted α taxonomy for these genera is based on knowledge or ignorance.     

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.     

The extraordinary athletic performance of leaping gibbons

The distance that animals leap depends on their take-off angle and velocity. The velocity is generated solely by mechanical work during the push-off phase of standing-start leaps. Gibbons are capable of exceptional leaping performance, crossing gaps in the forest canopy exceeding 10 m, yet possess none of the adaptations possessed by specialist leapers synonymous with maximizing mechanical work. To understand this impressive performance, we recorded leaps of the gibbons exceeding 3.7 m. Gibbons perform more mass-specific work (35.4 J kg(-1)) than reported for any other species to date, accelerating to 8.3 ms(-1) in a single movement and redefining our estimates of work performance by animals. This energy (enough for a 3.5 m vertical leap) is 60 per cent higher than that achieved by galagos, which are renowned for their remarkable leaping performance. The gibbons' unusual morphology facilitates a division of labour among the hind limbs, forelimbs and trunk, resulting in modest power requirements compared with more specialized leapers.     

Checkerboard Patterns,Interspecific Competition,and Extinction: Lessons from Distribution Patterns of Tarsiers (<Emphasis Type="Italic">Tarsius</Emphasis>) and Slow Lorises (<Emphasis Type="Italic">Nycticebus</Emphasis>) in Insular Southeast Asia

Tarsiers (Tarsius) and slow lorises (Nycticebus) are the only extant nocturnal primates occurring in Southeast Asia. Harcourt (1999) hypothesized that in insular Southeast Asia, slow lorises and tarsiers showed a checkerboard distribution on 12 small (<12,000 km²) islands, i.e., only one or the other occurs, and attributed this to extreme levels of competition between these 2 largely faunivorous primates. Further, he predicted slow lorises were able to persist on smaller islands than tarsiers. We re-evaluated these findings using an expanded dataset including 49 islands where tarsiers or slow lorises occur. Tarsiers and slow lorises live on islands of similar size (median size of ca. 300–900 km²), and both taxa inhabit an equal proportion of small, medium, and large islands. On small islands within their area of sympatry tarsiers occur on 1 island, slow lorises on 8, both genera on 3, and we can assume they have become extinct from 11 small islands since the Last Glacial Maximum. Sizes of islands where tarsiers or slow lorises have become extinct do not differ from islands where they are still extant. We show that slow lorises occur on more islands in insular Southeast Asia than perhaps previously assumed, but these islands are not smaller on average than islands where tarsiers occur. A checkerboard distribution between these taxa is not evident. More studies are needed at the macroecological level to assess the importance of biogeographic history in explaining their present-day distribution patterns.     

The behavior of wild spectral tarsiers

Field data are presented from a 15-month study of spectral tarsiers in North Sulawesi, Indonesia, based on over 300 sightings of animals in the wild and supplemented by observations from other parts of the island. Animals in study area were caught in mist nets and marked with colored plastic bird rings so that tarsiers followed at night could be individually recognized. Ecological data presented cover the locomotion, use of forest strata, and diet of tarsiers. Although clearly specialized for vertical clinging and leaping, the spectral tarsier is less specialized than the western tarsier, occupying a wider range of habitats and using a wider range of vegetation strata and locomotor patterns. Diet is mostly insects collected both on the ground and in trees. Spectral tarsiers were found to be monogamous and territorial. Families regularly slept at the same sites each day and gave loud duet songs as they congregated at sleeping sites each dawn. Sometimes similar songs were given in the night during territorial conflicts. Family home ranges were plotted and average about 1 ha. Observations are included on mating, the development of young tarsiers, and the dispersion of juveniles. Tarsier young are very precocious and may travel independently as little as 23 days after birth. Tarsiers regularly scent marked their ranges by rubbing branches with urine and special epigastric glands. In addition, they have a varied repertoire of calls and the main vocalizations are described.     

The Skull of <Emphasis Type="Italic">Tarsius</Emphasis>: Functional Morphology,Eyeballs, and the Nonpursuit Predatory Lifestyle

Little is known about the impact of enormous eyeballs on the tarsier's head, apart from facial morphology. I used a biomechanical analysis to compare the cranium of Tarsius with the Eocene fossil Necrolemur, a moderately large-eyed surrogate for ancestral tarsiid cranial morphology. Eyeball hypertrophy has radically influenced the neurocranium and basicranium, driving the evolution of such derived features as recession of orbital fossae, ectopically located eyeballs, uptilted brain and rounded braincase, anteroventrally shifted foramen magnum, enlarged and horizontally leveled nuchal plane, laterally displaced and narrowed tympanic cavities, and shortened external auditory tubes. The gestalt is an adaptation to efficient orthograde head carriage, balanced head-turning movements, and spatial packaging of cranial components, responses to an extreme loading regimen in which the eyes, with a mass approximating twice the bulk of the brain, profoundly eccentrically load the skull. Specializations of the retina and cortex suggest tarsiers have an acutely developed spatial sense, especially adept at detecting and mapping motion. Spanning several anatomical systems, this configuration represents an extreme form of vertical clinging and leaping (XVCL) geared for noiseless, nonpursuit predation, an energy-minimizing procurement strategy that may be a trade-off for relying on metabolically expensive, outsized eyeballs, maintained by a highly nutritious, super-specialized, animalivorous food source. A more varied galago-like locomotor profile and foraging habit was common among fossil tarsiiforms and preadaptive to this lifestyle, partly by canalizing the forward orientation of the tarsier's predatory gaze in VCL mode. Tarsier ecomorphology evolved to minimize the costs of being extraordinarily “top heavy,” carrying a heavy load that is roughly equivalent to 3 brains.     

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.     

Evolutionary aspects of primate locomotion

Both neontological and phylogenetic studies are necessary to interpret primate locomotion. Reference to palaeoprimatology and palaeocology, for instance, will lead to a fuller understanding of the roots of such gaits as the vertical clinging and leaping of Tarsius, Indri and Propithecus. Evolutionary trends in posture and locomotion are discussed. The postural trend has been towards maintenance of trunk verticality and the locomotor trend towards an increasing dependence on the forelimbs among arboreal primates. Three stages are recognized in the phylogenetic course of arboreal locomotor adaptation: Stage A. Vertical clinging and leaping; Stage B. Quadrupedalism; Stage C. Brachiation. The role of prehensility of the hand in the evolution of locomotor types is discussed in relation to forest morphology and, in particular, to stratification. Finally a scheme of evolution, set in the framework of ecology, for Old World Monkey groups is presented.     

Vertical clinging and leaping revisited: vertical support use as the ancestral condition of strepsirrhine primates

A re-examination of primate foot and knee anatomy suggests that strepsirrhine primates (adapiforms and lemuriforms) possess a unique and derived hindlimb related to their use of vertical supports. In contrast, leaping adaptations are older and shared by both major euprimate clades, Strepsirrhini and Haplorhini. Combining this derived hindlimb anatomy with leaping suggests that ancestral strepsirrhines were at least frequent vertical support users and leapers, and perhaps vertical clingers and leapers. These initial strepsirrhine adaptations were preadaptive for later lemuriform vertical clingers and leapers. In contrast, haplorhine vertical clingers and leapers require additional foot and leg modifications to accommodate a vertical clinging and leaping lifestyle. The movement pattern called vertical clinging and leaping evolved independently among different primate lineages throughout primate evolutionary history for several different ecological reasons.     

Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates

Tarsiers are small nocturnal primates with a long history of fuelling debate on the origin and evolution of anthropoid primates. Recently, the discovery of M and L opsin genes in two sister species, Tarsius bancanus (Bornean tarsier) and Tarsius syrichta (Philippine tarsier), respectively, was interpreted as evidence of an ancestral long-to-middle (L/M) opsin polymorphism, which, in turn, suggested a diurnal or cathemeral (arrhythmic) activity pattern. This view is compatible with the hypothesis that stem tarsiers were diurnal; however, a reversion to nocturnality during the Middle Eocene, as evidenced by hyper-enlarged orbits, predates the divergence of T. bancanus and T. syrichta in the Late Miocene. Taken together, these findings suggest that some nocturnal tarsiers possessed high-acuity trichromatic vision, a concept that challenges prevailing views on the adaptive origins of the anthropoid visual system. It is, therefore, important to explore the plausibility and antiquity of trichromatic vision in the genus Tarsius. Here, we show that Sulawesi tarsiers (Tarsius tarsier), a phylogenetic out-group of Philippine and Bornean tarsiers, have an L opsin gene that is more similar to the L opsin gene of T. syrichta than to the M opsin gene of T. bancanus in non-synonymous nucleotide sequence. This result suggests that an L/M opsin polymorphism is the ancestral character state of crown tarsiers and raises the possibility that many hallmarks of the anthropoid visual system evolved under dim (mesopic) light conditions. This interpretation challenges the persistent nocturnal–diurnal dichotomy that has long informed debate on the origin of anthropoid primates.     

Genomic data reject the hypothesis of a prosimian primate clade

The phylogenetic position of tarsiers within the primates has been a controversial subject for over a century. Despite numerous morphological and molecular studies, there has been weak support for grouping tarsiers with either strepsirrhine primates in a prosimian clade or with anthropoids in a haplorrhine clade. Here, we take advantage of the recently released whole genome assembly of the Philippine tarsier, Tarsius syrichta, in order to infer the phylogenetic relationship of Tarsius within the order Primates. We also present estimates of divergence times within the primates. Using a 1.26 million base pair multiple sequence alignment derived from 1078 orthologous genes, we provide overwhelming statistical support for the presence of a haplorrhine clade. We also present divergence date estimates using local relaxed molecular clock methods. The estimated time of the most recent common ancestor of extant Primates ranged from 64.9 Ma to 72.6 Ma, and haplorrhines were estimated to have a most recent common ancestor between 58.9 Ma and 68.6 Ma. Examination of rates of nucleotide substitution in the three major extant primate clades show that anthropoids have a slower substitution rate than either strepsirrhines or tarsiers. Our results provide the framework on which primate morphological, reproductive, and genomic features can be reconstructed in the broader context of mammalian phylogeny.     

The functional morphometrics of the hip and thigh in leaping prosimians

Examination of the form of the hip and thigh through discriminant function analysis of a series of 15 osteometric indices taken upon 289 specimens of 20 sets of leaping prosimians distinguishes four groups. Around a centrally located group of the various species of Lemur are three separate rays: one containing the three indriid genera (Propithecus, Indri, and Avahi), a second including the galagines and Tarsius, and a third comprising the two species of Cheirogaleus and the genus Microcebus. The lemurine genus Lepilemur lies intermediately between the central group of lemurs and the indriids. The lemurine genus Hapalemur lies intermediately between, on the one hand, the centrally located group of lemurs, and on the other, each of the two groups, cheirogaleines and galagines-plus-tarsiers. The arrangements of the particular species within each of these last two groups separately is from those that leap least to those that leap most. Given that the structure of the hip and thigh is related to the biomechanical demands of leaping, the existence of these separate morphological groups implies the existence of different biomechanical modes of leaping. Such meager taxonomic and behavioral information as is available seems to support this idea, although it is not impossible that other aspects of the behaviors of the animals may also be associated. This information sets up a series of new behavioral hypotheses that might be tested by better field and laboratory studies aimed more precisely at locomotion. And this information may be useful in helping to make assessments of particular fossils and in helping determine how various prosimian locomotor modes may have evolved.     

Postcranial adaptation and evolution in lorisidae

With the exception of leaping, lorises and galagos move in many similar ways although frequencies and styles differ. This peculiar locomotor distinction in two closely related subfamilies has profoundly altered their respective postcranial anatomies from their common ancestor. A comparison of postcranial adaptation in extant forms shows that lorises and galagos differ somewhat in forelimb mobility, but are more fundamentally disparate in hindlimb adaptation. Inferences concerning locomotor adaptation in the lorisid fossil record indicate a more generalized locomotor pattern which is more like that of extant cheirogaleids than either living galagos or lorises. Thus, vertical clinging and leaping in galagines and the slow-climbing and suspensory movements of lorisines appear to be evolutionarily recent innovations from a more generalized locomotor past.     

<Emphasis Type="Italic">Tarsius wallacei</Emphasis>: A New Tarsier Species from Central Sulawesi Occupies a Discontinuous Range

On the basis of distinguishing characteristics of various genetic markers, pelage color, tail tuft, and vocalizations, we describe a new species of the genus Tarsius Storr 1780. The new taxon Tarsius wallacei sp. nov. occupies a disjunct range in Central Sulawesi, Indonesia. The two isolated populations differ significantly in body size, but are alike in color, tail tuft dimensions, vocalizations, and genetic composition. Morphologically, the new species is similar to other Sulawesi lowland tarsiers. In the field, it can be distinguished from its congeners via a characteristic duet song and its yellow-brown pelage coloration and a copper-colored throat. Genetic analyses prove Y-chromosomal and mitochondrial DNA sequences and also microsatellite allele frequencies to be absolutely diagnostic.     

Influence of Orbit Size on Aspects of the Tarsier Postorbital Septum

Explanations invoking the complex mechanical effects of orbital enlargement in Tarsius have been extended to several areas of the skull, including the conformation of the postorbital septum. The strong cline in the degree of relative orbital enlargement across tarsier species groups presents an unexploited opportunity to test such scenarios. Our goal is to evaluate hypotheses concerning the impact of orbital hypertrophy on the size of specific components of the postorbital region including the frontal, zygomatic, alisphenoid, and maxillary bones. The frontal process is almost always viewed as a functional projection whose bracing role requires a positive morphometric association with orbital hypertrophy. Conversely, the periorbital expansion of the zygomatic is often perceived as functionally unrelated to orbital enlargement and therefore is not expected to track increases in relative orbit size. Interpretations of the alisphenoid and maxillary periorbital processes range from vestigial remnants of once larger structures reduced because of ocular enlargement to structures large in tarsiers because of their functionally relevant role in supporting the enlarged ocular apparatus. We measured these attributes in an extensive sample of 4 tarsier species groups including Tarsius bancanus, T. syrichta, T. spectrum, and T. pumilus. In contrast to proposed functional interpretations, our results indicate that variation in most linear parameters might be better explained by differences in body size than intrageneric differences in orbit size. As expected, width of the zygomatic postorbital contribution does not parallel intrageneric variation in orbit size. However, morphometric relationships between relative orbit size and other parts of the septum are complex but not clearly associated with orbit size differences within Tarsius.     

New postcranial elements for the earliest Eocene fossil primate Teilhardina belgica

Teilhardina belgica is one of the most primitive fossil primates known to date and the earliest haplorhine with associated postcranials, making it relevant to a reconstruction of the ancestral primate morphotype. Here we describe newly discovered postcranial elements of T. belgica. It is a small primate with an estimated body mass between 30 and 60 g, similar to the size of a mouse lemur. Its hindlimb anatomy suggests frequent and forceful leaping with excellent foot mobility and grasping capabilities. It can now be established that this taxon exhibits critical primate postcranial synapomorphies such as a grasping hallux, a tall knee, and nailed digits. This anatomical pattern and behavioral profile is similar to what has been inferred before for other omomyids and adapiforms. The most unusual feature of T. belgica is its elongated middle phalanges (most likely manual phalanges), suggesting that this early primate had very long fingers similar to those of living tarsiers.     

Habitat use,foraging behavior,and activity patterns in reproducing western tarsiers,Tarsius bancanus,in captivity: A managment synthesis

As the only obligatorily predatory primates, tarsiers are notoriously difficult to keep successfully in captivity. Here we report empirical and experimental results from a 5-year study of behavior and life history in captive Tarsius bancanus. Four reproducing adult tarsiers used space nonrandomly, preferring small-diameter vertical or near-vertical locomotor substrates at midlevel enclosure heights (1.2–2.1 m) for sleeping, scanning, and prey capture. The tarsiers were completely nocturnal, and spent 78% of the scotophase scanning, 13% sleeping, and 9% in prey capture and other activities. Only live crickets were eaten; prey capture rates were highest in the first hour after waking, but overall activity rates were highest later in the scotophase. Adult males and nonpregnant or lactating females ingested approximately 44.7–49.7 kJ/day. Growing and lactating individuals ingested approximately 84.4–94.1 KJ/day. An energetically conservative, sit-and-wait predatory strategy was employed, in which 88% of capture attempts were successful. Most successful prey captures involved reaching for, or leaping from, 90° or 60° supports in a horizontal or downward direction onto prey less than 0.6 m away. Virtually all prey captures were in arboreal locations, despite much higher densities of crickets on enclosure floors. Prey capture rates during the first hour of the nocturnal activity period were positively correlated with arboreal cricket densities. At constant arboreal cricket densities, capture rates were negatively correlated with ambient light intensity, with optimum levels for prey capture ranging from 0.1 to 2.0 Lux. In terms of social behavior, these T. bancanus were nongregarious. Females enforced interindividual spacing by chasing and displacing males. Chase/displacement rates increased significantly during late pregnancy and lactation, apparently in an attempt to keep males from harassing infants. There was no direct male parental care. Infants were precocial at birth, and grew at a rate of 0.35–0.5 g/day, until nutritional weaning at approximately 60 days of age. The implications of specialized predatory morphology and behavior for management are discussed. © 1993 Wiley-Liss, Inc.