Geographical Variation in Duet Songs of Sulawesi Tarsiers: Evidence for New Cryptic Species in South and Southeast Sulawesi

Geographic populations of Sulawesi tarsiers differ conspicuously in the acoustic structure of the loud duet calls produced by mated pairs. There is evidence that the differences in call features relate to species differentiation. Duet calls can thus be used as a tool to identify cryptic species and for their monitoring in the field. We recorded duets from various geographically isolated populations of Tarsius tarsier in south and southeast Sulawesi to survey the species identity of the tarsiers in these regions. We compared their calls with the duet calls of the Manado tarsier (= Tarsius spectrum), Tarsius dianae, and the Togian Island tarsier. In addition, we recorded and analyzed the duet call of the tarsier from Peleng Island, Tarsius pelengensis. Qualitative characteristics of duet songs of both sexes, analysis of frequency and temporal parameters, and multivariate statistics show 4 distinct vocal forms that predict the existence of 4 new species. These are found on Selayar Island, on the south mainland (Bantimurung), on the southeast mainland (Puwato), and on the Islands of Kabaena and Buton. Our analysis of the call of the Peleng tarsier revealed striking similarities with the call of Tarsius dianae. Further morphological analyses are needed to support the proposed new species in south and southeast Sulawesi and to clarify the taxonomic affinity between the central Sulawesi tarsier species Tarsius pelengensis and T. dianae.     

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.     

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.     

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.     

Preliminary Data on the Behavior,Ecology, and Morphology of Pygmy Tarsiers (<Emphasis Type="Italic">Tarsius pumilus</Emphasis>)

We here present the first behavioral, morphological, and ecological data on a living group of highland pygmy tarsiers, Tarsius pumilus, and compare them with the lowland tarsier species of Sulawesi. Pygmy tarsiers were previously known only from 3 museum specimens and had not been seen alive since the first specimens were collected in 1917 and 1930. As part of a 2-mo exploratory study, we recently located a group consisting of ≥4 pygmy tarsiers in the mossy cloud forest of Lore Lindu National Park, Central Sulawesi, Indonesia. We captured 1 adult female and 2 adult male group members. The tarsiers weighed a mean of 50 g, less than half the weight of adult lowland tarsiers. Our behavioral observations indicate that these tarsiers live in small groups that return to the same sleeping tree each morning. Though our data are preliminary, pygmy tarsier body proportions appear to differ from the lowland Sulawesian tarsier species, with relatively long hind limbs compared to total body length. We also observed differences in grouping and communication behaviors. Unlike lowland tarsiers, pygmy tarsiers possess multiple adult males per group and rarely vocalize or scentmark. These differences may correlate with variables unique to their high altitude habitat, especially a reduction in food and tree resources, given that tree density declined sharply along an altitudinal gradient. Our preliminary study identifies the importance of altitudinal ecological gradients to tarsier behavioral ecology in Central Sulawesi, providing questions and predictions for future research directions.     

Small,odd and old: The mysterious Tarsius pumilus is the most basal Sulawesi tarsier

In this study, we present the first genetic evidence of the phylogenetic position of Tarsius pumilus, the mountain tarsier of Sulawesi, Indonesia. This mysterious primate is the only Eastern tarsier species that occurs exclusively in cloud forests above 1800 m.a.s.l. It exhibits striking morphological peculiarities—most prominently its extremely reduced body size, which led to the common name of ‘pygmy tarsier’. However, our results indicate that T. pumilus is not an aberrant form of a lowland tarsier, but in fact, the most basal of all Sulawesi tarsiers. Applying a Bayesian multi-locus coalescent approach, we dated the divergence between the T. pumilus lineage and the ancestor of all other extant Sulawesi tarsiers to 9.88 Mya. This is as deep as the split between the two other tarsier genera Carlito (Philippine tarsiers) and Cephalopachus (Western tarsiers), and predates further tarsier diversification on Sulawesi by around 7 Myr. The date coincides with the deepening of the marine environment between eastern and western Sulawesi, which likely led to allopatric speciation between T. pumilus or its predecessor in the west and the ancestor of all other Sulawesi tarsiers in the east. As the split preceded the emergence of permanent mountains in western Sulawesi, it is unlikely that the shift to montane habitat has driven the formation of the T. pumilus lineage.     

Isolation and characterization of 12 microsatellite loci for population studies of Sulawesi tarsiers (Tarsius spp.)

This study reports the development and characterization of the first 12 microsatellite markers for tarsiers. Nine loci were isolated from Dian's tarsier, Tarsius dianae and three from the Philippine tarsier, Tarsius syrichta. The 12 markers were used to screen 40 individuals of Dian's tarsier and 40 individuals of the Lariang tarsier, Tarsius lariang for allelic diversity. This suite of highly polymorphic microsatellites provides the first chance to genetically study parentage patterns in tarsiers.     

The westernmost tarsier: A new genus and species from the Miocene of Pakistan

As the closest living sister group of anthropoids, tarsiers (Family Tarsiidae) are an important group in primate evolution. However, their fossil record is poor: only four species have been described, two from the Eocene of China and two from the Miocene of Thailand. All are from outside the range of the living species, which occur only on islands off Southeast Asia. Here, we describe a new fossil tarsier from Pakistan, a significant range extension. This record consists of two lower molars, an upper molar, and a lower premolar found in the Miocene Manchar Formation (∼18–16 Ma [millions of years ago]) of Sindh Province, southern Pakistan. The Pakistani tarsier is morphologically distinct from all living and fossil tarsiers, but most similar to the middle Miocene Thai species Tarsius thailandicus. Though living tarsiers have traditionally been classified in a single genus, a recent revision proposed a division into three genera, which is strongly supported by molecular data. The Pakistani species is not referable to any of these genera, and we create for it and T. thailandicus a new tarsiid genus. This discovery broadens our understanding of the geographic range and morphological diversity of Miocene tarsiers and helps to put the living tarsiers into their evolutionary context.     

The Social System of Lariang Tarsiers <Emphasis Type="Italic">(Tarsius lariang)</Emphasis> as Revealed by Genetic Analyses

Previous sociobiological studies of tarsiers were invariably based on field observations. Sulawesi tarsiers are known for monogamous or facultative polygynous social mating systems, but, to date, no data exist to describe the genetic mating system. We here bring together behavioral studies and molecular tools for the first time to elucidate mating behavior and kinship within a tarsier population. We investigated the social system of the recently described Tarsius lariang, which researchers have never studied before. Between September and November 2005, we conducted field observations and sampling in central Sulawesi, Indonesia, where this species is endemic. Ten of 11 social groups of the focal population were composed of 1 adult male, 1 adult female, and putative offspring. To enlighten genetic relationships, we used 12 microsatellite loci and mitochondrial DNA sequences of 26 captured and sampled Lariang tarsiers for parentage and relatedness analyses. A significant number of young were the offspring of the sampled group adults, suggesting a predominantly monogamous social and genetic mating system. There is evidence for extrapair young in groups in which adult pairs exhibit close relationships, leading to the assumption that extrapair mating is solicited to avoid inbreeding. Ten of 11 social groups lived in monogamous social systems, indicating monogamy to be the rule in Tarsius lariang.     

Duet Vocalizations among Different Populations of Sulawesi Tarsiers

A most conspicuous vocal behavior of Sulawesi tarsiers is the loud calls that males and females coordinate into duets. Differences in the acoustic structure of this display relate to specific differentiation in Tarsius spectrum and T. dianae. More recent studies on dueting behavior indicated the existence of a new species of tarsiers on the Togian Islands in Tomini Bay. I analyzed the duet calls of the Togian tarsier to assess the differences in acoustic structure of duet calls between this putative new species and T. spectrum or T. dianae. Discriminant function analysis revealed that Togian tarsiers, T. spectrum and T. dianae, are clearly separated by acoustic characteristics in songs. The degree of separation of the Togian tarsiers from the mainland species support them being a distinct species.     

Strengths and Weaknesses of a Population Viability Analysis for Philippine Tarsiers (<Emphasis Type="Italic">Tarsius syrichta</Emphasis>)

Population viability analysis (PVA) has been increasingly used to guide conservation planning for many primate species. I present an assessment of a PVA for Philippine tarsiers (Tarsius syrichta) in Corella, Bohol. The objectives were to determine 1) area requirements and 2) spatial configurations of habitat patches necessary for viable populations in Corella. I used available life history parameters and ecological data for the Philippine tarsier derived from a radiotelemetry study on 4 male and 6 female Tarsius syrichta in Corella from early March to October 1999. I used analysis of the likelihood of extinction (ALEX), a Monte Carlo simulation model that uses pseudorandom numbers to simulate a scenario involving different stochastic processes. Sensitivity analysis showed that the model output, i.e. extinction risk, was influenced by the values used for newborn, juvenile, and adult mortality but the effect of variation on adult mortality was more pronounced; a slight increase in adult mortality renders the population very unstable. Simulation of movements between habitat patches showed that addition of diffusion corridors and variation in diffusion parameters did not significantly alter the probability of extinction of the species. Models are only as useful as the data that are input, and a major weakness of this model is the lack of detailed life history and mortality data for Philippine tarsiers. Future studies should concentrate on obtaining more life history data and ecological data from additional localities. I discuss key priorities for future research that include use of alternative PVA software, a simpler modeling approach, and extensive genetic studies of different Philippine tarsier island populations.     

Successful breeding attempt of a pair of Philippine tarsier (Tarsius syrichta) in a conservation center in Bilar,Bohol, Philippines and recommendations for tarsier husbandry

The Philippine tarsier (Tarsius syrichta) belongs to the least known nocturnal primates. Tarsiers and remaining biodiversity of the Philippines are under tremendous threats from increasing human expansion, with habitat loss and illegal pet trade being the main reasons for tarsier population decline. In addition, even though the attempts were made by western and local facilities, tarsiers have not survived well in captivity. In this paper, I present an example of successful breeding of the Philippine tarsier in captive conditions but in natural climate. As the most important elements of success, I see a large amount of space provided to tarsiers, the climate similar to their natural habitat and the food resembling their natural diet. Our pair of tarsiers were joined during the mating period and held separately outside the mating period, which corresponds with their behavior in the wild and may have played a crucial role in breeding success. Eliminating stress to animals is also important. The study can provide valuable guidelines for other facilities keeping tarsiers in the Philippines and help to improve tarsiers’ welfare and in the future help to establish a viable captive population of the Philippine tarsier that will serve as a backup population and also will decrease demand on tarsiers captured from the wild.     

Stop and Go – Waves of Tarsier Dispersal Mirror the Genesis of Sulawesi Island

The Indonesian island of Sulawesi harbors a highly endemic and diverse fauna sparking fascination since long before Wallace’s contemplation of biogeographical patterns in the region. Allopatric diversification driven by geological or climatic processes has been identified as the main mechanism shaping present faunal distribution on the island. There is both consensus and conflict among range patterns of terrestrial species pointing to the different effects of vicariant events on once co-distributed taxa. Tarsiers, small nocturnal primates with possible evidence of an Eocene fossil record on the Asian mainland, are at present exclusively found in insular Southeast Asia. Sulawesi is hotspot of tarsier diversity, whereby island colonization and subsequent radiation of this old endemic primate lineage remained largely enigmatic. To resolve the phylogeographic history of Sulawesi tarsiers we analyzed an island-wide sample for a set of five approved autosomal phylogenetic markers (ABCA1, ADORA3, AXIN1, RAG1, and TTR) and the paternally inherited SRY gene. We constructed ML and Bayesian phylogenetic trees and estimated divergence times between tarsier populations. We found that their arrival at the Proto-Sulawesi archipelago coincided with initial Miocene tectonic uplift and hypothesize that tarsiers dispersed over the region in distinct waves. Intra-island diversification was spurred by land emergence and a rapid succession of glacial cycles during the Plio-Pleistocene. Some tarsier range boundaries concur with spatial limits in other taxa backing the notion of centers of faunal endemism on Sulawesi. This congruence, however, has partially been superimposed by taxon-specific dispersal patterns.     

Infanticide by a male spectral tarsier (<Emphasis Type="Italic">Tarsius spectrum</Emphasis>)

As part of a long-term field study on the behavioral ecology and conservation of a population of spectral tarsiers (Tarsius spectrum) in Tangkoko Nature Reserve, Sulawesi, Indonesia, I observed the first known instance of infanticide in this species. A young infant was killed by a neighboring male. Neither the epiphenomenal aggression hypothesis, social pathology hypothesis, nutritive benefits of cannibalism hypothesis, nor sexual selection hypothesis are supported by this observation. The only hypothesis that could not be rejected outright, on the basis of this single observation, was the competition for limited resources hypothesis.     

Habitat-specific ranging patterns of Dian's tarsiers (Tarsius dianae) as revealed by radiotracking

Dian's tarsier Tarsius dianae, one of the smallest primates on earth, is endemic to the central regions of Sulawesi, Indonesia. To evaluate the effects of increasing land use by humans on the ranging patterns of this nocturnal insect hunter, four study plots along a gradient of anthropogenic disturbance were selected for this study. In these plots, 71 tarsiers were captured with mist nets, and 30 of these were fitted with 3.9 g radiotransmitters and subsequently tracked over the course of 2 weeks per animal. The average home ranges were 1.1-1.8 ha in size, with the smallest ranges in slightly disturbed habitat and the largest ranges in a heavily disturbed plantation. These findings coincide with different estimates of insect abundance in the study plots. Nightly travel distances were smallest in undisturbed old-growth forest and slightly increased along a gradient of human disturbance. The tarsiers were most active shortly after dusk and just before dawn. The results of this comprehensive radiotracking study on tarsiers show that T. dianae adapts its ranging behavior to the degree and type of human land use. Integrated data on home range size and travel distance indicate that slightly disturbed forest is as favorable to these animals as undisturbed habitat. However, with increasing anthropogenic effects, the living conditions of the tarsiers appear to deteriorate, resulting in the necessity for larger home and night ranges. The results of this study provide an important tool for directing conservation efforts targeted at the survival of this primate in central Sulawesi.     

<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.     

Introducing an innovative semi‐captive environment for the Philippine tarsier (Tarsius syrichta)

In response to demands for research, captive breeding, and tourism, a semi‐captive environment was created for the Philippine tarsiers (Tarsius syrichta) in Corella, Bohol, Philippines. The 7600‐m² enclosure was continuous with the surrounding habitat, and utilized a unique predator control fence design and a lighting system to attract nocturnal insects. During 2 years of observation, the locations of over 500 tarsier sleeping sites were recorded. Tarsiers were found to prefer dense, low‐level vegetation in secondary forests, with perching sites averaging 2 m above the ground. Up to 10 tarsiers were observed within the enclosure at one time, which is a high density compared to densities based on home‐range estimates for wild tarsiers in the vicinity of the study site. In addition, the tarsiers were observed to be more social than previously reported. Zoo Biol 24:101–109, 2005. © 2005 Wiley‐Liss, Inc.     

Intraspecific Variation in the Mating System of Spectral Tarsiers

Historically, a species’ social system was perceived to be a fixed attribute and deviations were usually treated as aberrant or maladaptive. Over the last few decades, socioecologists have started to recognize that variation in social systems is normal and adaptive. Here I explore how ecological variation affects the mating system of a nocturnal primate, the spectral tarsier, Tarsius spectrum. Several studies of the spectral tarsier have illustrated variation in this species’ mating system. Although most groups exhibit a monogamous mating system, a small proportion of the population consistently exhibits a polygynous mating system. I conducted this study at Tangkoko Nature Reserve in Sulawesi, Indonesia during 2007. I found that group size was highly variable, ranging from 2 individuals to as many as 8 individuals per sleeping site. Although most groups (21 of 26) were composed of a single adult male and a single adult female, ca. 19% of the groups contained 2 adult females. Three of the 5 groups with 2 adult females contained 2 young infants. As might be expected, polygynous groups were larger than were monogamous groups. The mean group size of monogamous groups was 2.9, whereas the mean group size of polygynous groups was 6.0. Polygynous groups were also more likely to use Ficus caulocarpa trees than were the monogamous groups. Polygynous groups consistently used more sleeping sites as well as larger diameter sleeping trees, than did monogamous groups. The large-diameter fig trees are ideal homes for the spectral tarsiers in that they offer multiple entrances and exits as well as protection from the elements. Polygynous and monogamous groups exhibited no differences in insect biomass available, home range size, or height of sleeping tree. These results support the hypothesis that ecological variation is an important determinant of mating system within spectral tarsiers.     

Control Region Length Dynamics Potentially Drives Amino Acid Evolution in Tarsier Mitochondrial Genomes

Patterns and processes of molecular evolution critically influence inferences in phylogeny and phylogeography. Within primates, a shift in evolutionary rates has been identified as the rationale for contrasting findings from mitochondrial and nuclear DNA studies as to the position of Tarsius. While the latter now seems settled, we sequenced complete mitochondrial genomes of three Sulawesi tarsiers (Tarsius dentatus, T. lariang, and T. wallacei) and analyzed substitution rates among tarsiers and other primates to infer driving processes of molecular evolution. We found substantial length polymorphism of the D-loop within tarsier individuals, but little variation of predominant lengths among them, regardless of species. Length variation was due to repetitive elements in the CSB domain—minisatellite motifs of 35 bp length and microsatellite motifs of 6 bp length. Amino acid evolutionary rates were second highest among major primate taxa relative to nucleotide substitution rates. We observed many radical possibly function-altering amino acid changes that were rarely driven by positive selection and thus potentially slightly deleterious or neutral. We hypothesize that the observed pattern of an increased amino acid evolutionary rate in tarsier mitochondrial genomes may be caused by hitchhiking of slightly deleterious mutations with favored D-loop length variants selected for maximizing replication success within the cell or the mitochondrion.     

Effect of Seasonality on the Behavior of an Insectivorous Primate, Tarsius spectrum

The distribution and quality of food resources is generally recognized as the preeminent factor explaining much interspecific and intraspecific variation in the behavior of nonhuman primates. Primates that live in seasonal environments often show predictable responses to fluctuating resources. In order to compensate for the reduction in resource availability, primates variously switch to alternative, poorer quality food sources, increase the amount of time they spend foraging, or increase their daily path length. Some primate species reduce their group size or maximize the group dispersion. I address whether spectral tarsiers (Tarsius spectrum), which are insectivores, modify their behavior in the same ways as frugivores and folivores in response to seasonal or scarce resources. My results indicate that wild spectral tarsiers modify their activity budget in response to seasonal resources. Specifically, during periods of low resource availability, spectral tarsier males and females spent more time traveling and foraging compared to their activity budget during the wet season. Males and females not only increased the amount of time they spent foraging during times of low resource abundance but also modified their foraging behavior. During the wet season, when resource abundance was high, they consumed Orthoptera and Lepidoptera with greater frequency than during the dry season. During the dry season, when resource abundance was low, spectral tarsiers still ate numerous Orthoptera and Lepidoptera, but they also increased consumption of Coleoptera and Hymenoptera. Spectral tarsiers were also more likely to be involved in territorial disputes during the dry season than during the wet season. Intragroup encounters decreased in frequency in the dry season versus the frequency of encounters during the wet season.