Living in small spaces: Forest fragment characterization and its use by Philippine tarsiers (Tarsius syrichta Linnaeus, 1758) in Mindanao Island, Philippines.

The Philippine tarsier (Tarsius syrichta) is a charismatic species that is threatened by illegal hunting and deforestation. Although they occur in forest and disturbed habitats, ecological information about them is still considerably lacking, which consequently hampers our ability to effectively protect tarsiers from further endangerment. Here, we characterized a 36-ha forest fragment in Mindanao Island where a population of tarsiers persist, and assessed the factors that could have influenced their distribution within the area. We sampled trees (> 1 cm DBH) within 10 × 10-m sampling plots (N = 54), which were established within 1-ha grids (N = 32) and locations where tarsiers were captured (N = 22). The habitat was characterized as a regenerating forest over limestone, with a generally homogeneous structure in terms of tree species richness, abundance, mean DBH, and height. In both sampling plots, we found an abundance of trees below 5 cm in DBH (> 50%) and between 2.6 and 5 m in height (> 40%), which, accordingly, the tarsiers appeared to prefer to use when foraging or sleeping. Lianas were among the most important features of the forest, possibly being a keystone structure in such habitats. Community assemblage, species richness, and mean height of trees, as well as distance to the forest edge, were found to be significant factors that influenced tarsier distribution in the fragment. Our study provides basic yet critical information on the habitat and ecology of Philippine tarsiers in Mindanao, and highlights the importance of forest fragments with rich flora diversity to the survival of the species.

Social Behavior of a Reproducing Pair of the Philippine Tarsier (Tarsius syrichta) in Captivity.

Social interactions of the nocturnal primates are not well studied. One of the species for which social behavior is scarcely known is the Philippine tarsier (Tarsius [= Carlito] syrichta). We observed a reproducing pair of captive individuals over two mating seasons for two consecutive years. The tarsiers spent approximately 4% of their activity budget on social interactions; ca. 20% of time in 0-1 m proximity to each other; and shared sleeping sites for half of the study time. The majority of the animals' social interactions were peaceful: affiliative and sexual (83%), and the smallest component of the behavior was agonistic (17%). We witnessed two copulation events (one per estrus day), each lasting ca. 5 min, and both occurring just after waking. We revealed temporal - nightly and hourly - fluctuations in the frequency of social interactions, in the distances the individuals spent from each other and in the number of vocalizations. The results present the first assessment of the social behavior of the Philippine tarsier, much needed to improve the captive breeding management for this highly sensitive species threatened with extinction.

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.

Cryptic Communication in a Montane Nocturnal Haplorhine, Tarsius pumilus.

Crypsis, including visual and auditory concealment, usually manifests in primates as an antipredator strategy. Other factors may also influence cryptic communication style, including habitat structure and phylogenetic history. Compared to less cryptic lowland Sulawesian tarsiers, montane pygmy tarsiers (Tarsius pumilus) exhibit a communication style that lacks scent marks and lower-frequency vocalisations. This study examines why auditory crypsis occurs in montane tarsiers more so than in larger tarsier species and presents the only known spectrograms of T. pumilus in the field. T. pumilus regularly exhibited calls with a dominant frequency of 60-80 kHz (n = 4) in both social situations (duet calls) and stressed contexts. These results indicate that highland, smaller-bodied tarsiers habitually communicate at high frequencies in contexts where Sulawesian and Philippine tarsiers use lower frequencies. While predation threats and habitat acoustics may influence the use of high-frequency vocalisations, this study found that T. pumilus shows an expected relationship between vocal frequency and body mass. These traits may represent a retention of primitive haplorhine traits rather than derived adaptations to a montane environment.

Echolocation in a Nocturnal Primate?

Recently it has been noted that Gursky's spectral tarsier emits ultrasonic calls. Because high-frequency sounds are capable of travelling only short distances, their function is limited by the distance the sound can be discerned. One possible function for these short-distance, high-frequency sounds is that they might be used by the tarsiers to navigate throughout their environment. I conducted this study at Tangkoko Nature Reserve in Sulawesi, Indonesia, from May to August 2017. Using the focal follows, I recorded the start of each locomotor activity to the nearest second. I also simultaneously recorded all ultrasonic vocalisations that the focal individual emitted using a Wildlife Acoustics Ultrasonic Song Meter BAT3. Approximately 42% of the ultrasonic calls that I recorded during this study were given within 1 s prior to engaging in locomotor activity. The tarsiers gave statistically more ultrasonic calls during locomotion than during other behaviours (rest, forage and social). Four types of ultrasonic calls were given while locomoting: whistles, doubles, trills and frequency-modulated calls. Of these, the trill and the frequency-modulated call were only given during locomotion, and trills were only given prior to leaping. These results preliminarily suggest that the tarsiers do use ultrasonic calls for navigation. Studying echolocation in organisms closely related to bats is critical for understanding the evolution of echolocation.

Activity Patterns of Captive Philippine Tarsiers (Tarsius syrichta): Differences Related to Sex and Social Context.

Among tarsiers, nocturnal, obligatory faunivorous primates inhabiting islands of South-East Asia, the Philippine tarsier (Tarsius [= Carlito] syrichta) is one of the least studied. To date, activity patterns of this threatened species have not been the subject of any investigation. In the present study, we provide the first quantitative data on how captive male and female T. syrichta apportion their time for various activities in two social contexts: solitary and paired. We found that the sexes do not differ in activity budgets during the non-mating season, both spending most of their time scanning, resting, foraging and travelling. Comparison of activity budgets of the sexes between the mating and non-mating seasons revealed that although both tarsiers noticeably increased travelling time at the expense of time spent resting, the male changed his behaviour to a much greater extent than the female. We also report on fluctuations in the tarsiers' activities throughout a night and compare time budgets of T. syrichta with available data on the western and eastern species of tarsiers. The results extend the current knowledge of tarsier behaviour and may also assist in practical considerations for keeping this highly sensitive, difficult-to-breed species in captivity.

Assessing female reproductive status of spectral tarsier (Tarsius tarsier) using fecal steroid hormone metabolite analysis.

The wild population of spectral tarsier is declining and attempts to breed the species in captivity have been of limited success. One possible reason for this is that information on the reproductive biology of Tarsius tarsier is extremely limited and data on the species reproductive physiology are completely lacking. We validated fecal estrogen (E-total) and progesterone metabolite (5-P-3OH) measurements for monitoring female ovarian activity and pregnancy. We used this approach to provide the first data on cycle and pregnancy length based on endocrine information in this species. We collected regular fecal samples in combination with observations on socio-sexual behaviors for a maximum of 15 months from three females maintained at Primate Research Center of Bogor Agricultural University, Indonesia. Hormonal profiles indicated that behavioral estrus was associated with marked elevations in fecal E-total concentrations followed by increases in 5-P-3OH levels indicating luteal function. Pregnancy was characterized by low levels of E-total and 5-P-3OH during the first month and markedly rising concentrations thereafter. An ovarian cycle length of 21.7 ± 5.7 days was found. Gestation length was 128d (live infant), 131d (stillbirth), and 164d (death of mother and infant due to dystocia). Despite the small sample size, the study demonstrates the overall validity of fecal sex hormone metabolite measurements for reproductive monitoring in female T. tarsier, as such, the methods described here may ultimately help to improve the breeding management of the species in captivity. They may also offer new opportunities for investigating basic questions of tarsier reproductive biology in the wild by using fecal hormone metabolite analysis to diagnose pregnant animals and determine reproductive rates in relation to ecological and other factors influencing tarsier reproduction. Thus, non-invasive assessment of female reproductive condition as described here may ultimately contribute to facilitate in and ex situ conservation efforts of this endangered primate species.

Sexual Behaviour of the Spectral Tarsier (Tarsius spectrum) in Captivity.

Tarsius spectrum is a primate species endemic to Sulawesi. Populations of the species have decreased due to habitat destruction and hunting. The sexual behaviour of T. bancanus and T. syrichta are known, but that of T. spectrum has not been reported until recently. The aim of this research was to study the sexual behaviour of T. spectrum in captivity. We observed 3 pairs of T. spectrum at the captive breeding facility of the IPB Primate Research Centre for 9 months using focal animal sampling. We showed that principal courtship behaviours were scent marking (36.7%) and genital marking for females (16.2%) and genital inspection for males (16.0%). Copulations lasted between 3 and 4 min, starting with the male mounting the female and thrusting quickly as many as 168-236 times followed by slow thrusting 9-20 times. When slow thrusting occurred, females vocalized up to 6 times. At the end of the copulation sequence, males remained motionless with their penis inserted within the female's genitalia for about 31 s. Copulation occurred only once for each pair during the observation period. Our results should be useful to support breeding programmes and conservation actions for tarsiers.

Impact of Typhoon Haiyan on a Philippine Tarsier Population.

Over the last 2 decades the Philippine tarsier (Carlito syrichta aka Tarsius syrichta) has had its conservation status revised from Endangered to Data Deficient to Near Threatened. The last status change was based on a study of the species' population density, which suggested that a single natural catastrophe could potentially wipe out the Philippine tarsier. In 2013 typhoon Haiyan hit Bohol, one of the island strongholds for this species. In this study we compare the density of the Bohol tarsier population within the Philippine Tarsier and Wildlife Sanctuary before and after the typhoon. We demonstrate that the typhoon significantly affected the density of the Philippine tarsier in the sanctuary. Before the typhoon, tarsier density was approximately 157 individuals/km2 whereas after the typhoon the density was a mere 36 individuals/km2. Prior to the typhoon, more Philippine tarsiers were found in older secondary forest than in younger secondary forest, whereas after the typhoon all observed individuals were found in relatively younger secondary forest. Vegetation plots where we observed Philippine tarsiers prior to the typhoon contained a mean of 33 trees/m2, with a mean diameter at breast height (DBH) of 24 cm, and a mean height of 4 m. After the typhoon vegetation plots contained an average of 156 trees, had a mean DBH of 6 cm, and a mean height of 2 m. Based on the IUCN Red List criteria, the reduction and fluctuation in the density of this species suggests that the conservation status of the Philippine tarsier should be changed to Vulnerable. This study indicates natural disasters can have a significant effect on the extinction risk of primates, with implications for future effects of anthropogenic climate change.

Jumping in the Night: An Investigation of the Leaping Activity of the Western Tarsier (Cephalopachus bancanus borneanus) Using Accelerometers.

Accelerometers enable scientists to quantify the activity of free-living animals whose direct observation is difficult or demanding due to their elusive nature or nocturnal habits. However, the deployment of accelerometers on small-bodied animals and, in particular, on primates has been little explored. Here we show the first application of accelerometers on the western tarsier (Cephalopachus bancanus borneanus), a nocturnal, small-bodied primate endemic to the forests of Borneo. The fieldwork was carried out in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysian Borneo. We provide guidelines for the deployment of accelerometers on tarsiers that might also be applied to other primate species. Our collected data on 2 females show levels of leaping activity comparable to those previously described using direct observation of wild or captive individuals. The 2 females showed different patterns of leaping activity, which calls for work to explore individual differences further. Our work demonstrates that accelerometers can be deployed on small primates to acquire body motion data that would otherwise be demanding to collect using classic field observations. Future work will be focused on using accelerometer data to discriminate in more detail the different behaviours tarsiers can display and to address the causes and consequences of individual variations in activity.

Functional preservation and variation in the cone opsin genes of nocturnal tarsiers.

The short-wavelength sensitive (S-) opsin gene OPN1SW is pseudogenized in some nocturnal primates and retained in others, enabling dichromatic colour vision. Debate on the functional significance of this variation has focused on dark conditions, yet many nocturnal species initiate activity under dim (mesopic) light levels that can support colour vision. Tarsiers are nocturnal, twilight-active primates and exemplary visual predators; they also express different colour vision phenotypes, raising the possibility of discrete adaptations to mesopic conditions. To explore this premise, we conducted a field study in two stages. First, to estimate the level of functional constraint on colour vision, we sequenced OPN1SW in 12 wild-caught Philippine tarsiers (Tarsius syrichta). Second, to explore whether the dichromatic visual systems of Philippine and Bornean (Tarsius bancanus) tarsiers-which express alternate versions of the medium/long-wavelength sensitive (M/L-) opsin gene OPN1MW/OPN1LW-confer differential advantages specific to their respective habitats, we used twilight and moonlight conditions to model the visual contrasts of invertebrate prey. We detected a signature of purifying selection for OPN1SW, indicating that colour vision confers an adaptive advantage to tarsiers. However, this advantage extends to a relatively small proportion of prey-background contrasts, and mostly brown arthropod prey amid leaf litter. We also found that the colour vision of T. bancanus is advantageous for discriminating prey under twilight that is enriched in shorter (bluer) wavelengths, a plausible idiosyncrasy of understorey habitats in Borneo.This article is part of the themed issue 'Vision in dim light'.

Ultrasonic Vocalizations by the Spectral Tarsier, Tarsius spectrum.

Although the vocalizations of spectral tarsiers have been studied for over 3 decades by numerous primatologists, the data in this paper represent the first evidence that this species communicates in the ultrasonic range. In addition, this paper characterizes the types of ultrasonic vocalizations by spectral tarsiers, Tarsius spectrum. Data were collected at Tangkoko Nature Reserve in Sulawesi, Indonesia, from January through April 2013. Recordings were made on a Wildlife Acoustics Ultrasonic Song Meter BAT2 from 10 groups of varying sizes and compositions. The ultrasonic recorder was placed at the base of the group's sleeping tree and recorded from 5.00 to 7.00 h using an omnidirectional microphone. The ultrasonic vocalizations fell into 5 main categories: chirps, twitters, choruses, doubles and whistles. Chirps were the most frequent ultrasonic vocalizations, followed by twitters, choruses, doubles and then whistles. While chirps, twitters and choruses extended from the audible to the ultrasonic range, the doubles and whistles were pure ultrasound. Currently, the function of these ultrasonic vocalizations is not yet clear and requires additional research.

Are tropical small mammals physiologically vulnerable to Arrhenius effects and climate change?

There is some urgency in the necessity to incorporate physiological data into mechanistic, trait-based, demographic climate change models. Physiological responses at the individual level provide the mechanistic link between environmental changes and individual performances and hence population dynamics. Here we consider the causal relationship between ambient temperature (Ta) and metabolic rate (MR), namely, the Arrhenius effect, which is directly affected by global warming through increases in average global air temperatures and the increase in the frequency and intensity of extreme climate events. We measured and collated data for several small, free-ranging tropical arboreal mammals and evaluated their vulnerability to Arrhenius effects and putative heat stress associated with climate change. Skin temperatures (Tskin) were obtained from free-ranging tarsiers (Tarsius syrichta) on Bohol Island, Philippines. Core body temperature (Tb) was obtained from the greater hedgehog tenrec (Setifer setosus) and the gray brown mouse lemur (Microcebus ravelobensis) from Ankarafantsika, Madagascar. Tskin for another mouse lemur, Microcebus griseorufus, was obtained from the literature. All four species showed evidence of hyperthermia during the daytime rest phase in the form of either Tskin or Tb that was higher than the normothermic Tb during the nighttime active phase. Potentially, tropical arboreal mammals with the lowest MRs and Tb, such as tarsiers, are the most vulnerable to sustained heat stress because their Tb is already close to Ta. Climate change may involve increases in MRs due to Arrhenius effects, especially during the rest phase or during torpor and hibernation. The most likely outcome of increased Arrhenius effects with climate change will be an increase in energy expenditure at the expense of other critical functions such as reproduction or growth and will thus affect fitness. However, we propose that these hypothetical Arrhenius costs can be, and in some species probably are, offset by the use of hyperthermic daily torpor, that is, hypometabolism at high Ta.

Acoustic characterization of ultrasonic vocalizations by a nocturnal primate Tarsius syrichta.

This preliminary study characterizes the ultrasonic vocalizations produced by Philippine tarsiers, Tarsius syrichta. Data were collected at the Philippine Tarsier Foundation Sanctuary in Corella, Bohol, Philippines, from July through October 2010. Recordings were made on a Wildlife Acoustics Ultrasonic Song Meter 2 BAT from 29 wild, free-living adult resident T. syrichta (23 females and six males). A total of 10,309 USVs were recorded. These vocalizations fell into three main categories: chirps, twitters, and whistles. Chirps were the most frequent, followed by twitters and whistles. Whereas chirps and twitters were emitted by both male and female Philippine tarsiers, whistles were only emitted by adult males. Given that vocalizations reported in this study were exclusively recorded during capture and handling, it is very likely that these vocalizations function as distress calls. However, as the long whistle was only given by adult males who were captured at the same time as the female or the group's infant, the function of the long whistle might be slightly different than the function of the other relatively lower-frequency USVs.

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.

Altitude and forest edges influence the density and distribution of pygmy tarsiers (Tarsius pumilus).

In this study, we examine how high-altitude ecology and anthropogenic edges relate to the density and distribution of pygmy tarsiers. Pygmy tarsiers (Tarsius pumilus) are extremely small-bodied primates (55 g) that are endemic to high-altitude forest and exhibit several differences from lowland Sulawesian tarsier species. From June to September 2010 and January to March 2012, we conducted a population census of pygmy tarsiers across multiple altitudes. Sampling took place within a 1.2 km(2) area encompassing altitudes of 2,000-2,300 m a.s.l. on Mt. Rore Katimbu in Lore Lindu National Park, central Sulawesi, Indonesia. We observed 22 individuals, with an estimated population density of 92 individuals per 100 ha. These results indicate that pygmy tarsiers live at a lower density than lowland Sulawesian tarsier species. Lower density was associated with decreased resources at higher altitudes, including decreased tree size, tree density, and insect biomass. Within the sample area, we found pygmy tarsiers in only 8 of 24 (33%) quadrats, suggesting a nonrandom distribution that probably overinflated this population density estimate. Pygmy tarsiers exhibited a clumped distribution near anthropogenic edges that were associated with increased insect abundance and biomass. Airborne insects were more abundant along forest edges than within the forest interior, and pygmy tarsiers were observed to forage along edges where there was a higher abundance of Lepidoptera and Orthoptera. Tarsiers may mitigate the decreased availability of insects at high altitudes by adjusting their ranging patterns to remain near forest edges.

Primate communication in the pure ultrasound.

Few mammals-cetaceans, domestic cats and select bats and rodents-can send and receive vocal signals contained within the ultrasonic domain, or pure ultrasound (greater than 20 kHz). Here, we use the auditory brainstem response (ABR) method to demonstrate that a species of nocturnal primate, the Philippine tarsier (Tarsius syrichta), has a high-frequency limit of auditory sensitivity of ca 91 kHz. We also recorded a vocalization with a dominant frequency of 70 kHz. Such values are among the highest recorded for any terrestrial mammal, and a relatively extreme example of ultrasonic communication. For Philippine tarsiers, ultrasonic vocalizations might represent a private channel of communication that subverts detection by predators, prey and competitors, enhances energetic efficiency, or improves detection against low-frequency background noise.

Population survey of the Philippine tarsier (Tarsius syrichta) in Corella, Bohol.

In 1986, in response to the rapid habitat destruction throughout the archipelago, the Philippine tarsier was classified as endangered. Since that time, this tarsier has been reclassified as data deficient and more recently as near threatened despite a significant lack of information on the population density of the species. Data were collected at the Philippine Tarsier Foundation Sanctuary from June to October 2010. Population density was estimated using a modified form of the quadrat census method. A total of 55 individuals were located within the sampled area. This is equivalent to approximately 1.55 tarsiers per hectare. Ecologically, there were significantly more tarsiers found in the young secondary forest than in areas characterized as old secondary forest. Extrapolating to the entire protected area, as many as 258 tarsiers may reside in the sanctuary. The vegetation plots where tarsiers were found had substantially more trees per plot, contained trees with larger diameters, and contained slightly taller trees than did the plots where no tarsiers were observed.

Infanticide by a male spectral tarsier (Tarsius spectrum).

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.

Pattern and pace of dental eruption in Tarsius.

This article uses data on the dental eruption pattern and life history of Tarsius to test the utility of Schultz's rule. Schultz's rule claims a relationship between the relative pattern of eruption and the absolute pace of dental development and life history and may be useful in reconstructing life histories in extinct primates. Here, we document an unusual eruption pattern in Tarsius combining early eruption (relative to molars) of anterior replacement teeth (P2 and incisors) and relatively late eruption of the posterior replacement teeth (C, P3, and P4). This eruption pattern does not accurately predict the "slow" pace of life documented for Tarsius [Roberts: Int J Primatol 15 (1994) 1-28], nor aspects of life history directly associated with dental development as would be expected using Schultz's rule. In Tarsius, the anterior teeth and M1 erupt at an early age and therefore are not only fast in a relative sense but also fast in an absolute sense. This seems to be related to a developmental anomaly in the deciduous precursor teeth, which are essentially skipped. This decoupling among dental eruption pattern, dental eruption pace, and life history pace in Tarsius undermines the assumptions that life histories can accurately be described as "fast" or "slow" and that dental eruption pattern alone can be used to infer overall life history pace. The relatively and absolutely early eruption of the anterior dentition may be due to the utility of these front teeth in early food acquisition rather than with the pace of life history.