Predator Mobbing in <Emphasis Type="Italic">Tarsius spectrum</Emphasis>

Whereas most animals make considerable effort to avoid their predators, numerous species tend to approach and to confront predators as a group: mobbing. Among the types of predators that elicit mobbing, snakes seem to be one of the more consistent recipients of it. I describe the mobbing behavior of spectral tarsiers toward live and model snakes. In particular, I explore individual differences—sex, age and reproductive status—in mobbing behavior at Tangkoko Nature Reserve, Sulawesi, Indonesia. In 1994–1995, I observed 11 groups for 18 mo, and in 1999, I observed 9 groups for 6 mo. Over all I recorded, 11 natural mobbing events and 9 artificially induced mobbing events. The mean number of individuals at a natural mobbing is 5.1 with an average duration of 33 min. The duration of a mobbing event is strongly correlated with the number of mobbers. Adults were more likely than other age classes to participate in mobbings. Males were more likely than females to participate in mobbings. Mobbing groups often contained > 1 adult male despite the fact that no spectral tarsier group contains > 1 adult male. Vis-à-vis Curios (1978) 9 hypotheses for the function of mobbing suggests that its primary function in spectral tarsiers may be perception advertisement or teaching snakes to move on.     

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.     

Hand‐raising a spectral tarsier (Tarsius tarsier) at the Ueno Zoological Gardens

On February 10, 2008, a newborn male spectral tarsier (Tarsius tarsier) was found on the floor of the indoor exhibit room in the Small Mammal House of the Ueno Zoological Gardens. The dam showed no signs of providing maternal care and therefore we decided to hand‐raise the infant. Its birth weight was 18.7 g. We placed the dam and infant in an incubator and gave 12.5–25% formula (for kittens), until the 145th day after birth. We limited the volume of formula intake to avoid excessive intake and to prevent diarrhea. For nutrition enrichment, we added a chicken liver homogenate to the formula 1–3 times per day. The infant was given a sunbath for 10 min on the 28th day. He showed no serious decline in health, except for diarrhea that occurred during the first few days after birth. He ate a small cricket for the first time on the 50th day and easily caught mealworms on his own on the 105th day. Gradual changes in feeding times, formula concentration, and the nutritionally enriched formula were essential for successfully hand‐raising the tarsier. Zoo Biol 30:218–224, 2011. © 2010 Wiley‐Liss, Inc.     

Gestation length in Tarsius bancanus

A gestation length of 178 days was determined for Tarsius bancanus based on a vaginal smear containing whole sperm. This value replaces the only previously reported information on gestation length in tarsiers, a rough estimate of approximately 6 months for T. syrichta.     

Molecular evolution of the primate developmental genes MSX1 and PAX9

In primates, the craniofacial skeleton and the dentition are marked by high levels of interspecific variation. Despite this, there are few comparative species studies conducted at the molecular level to investigate this functional diversity. We have determined nucleotide sequences of MSX1 and PAX9, two developmental genes, in a sample of 27 diverse primate species in order to identify coding or regulatory variation that may be associated with phenotypic diversity. Our analyses have identified four highly conserved noncoding sequences, including one that is conserved across primates and with dogs but not with mice. Although we find that substitution rates vary significantly across MSX1 exons, comparisons of nonsynonymous and synonymous substitution rates (dN/dS) suggest that, as a whole, MSX1 and PAX9 amino acid sequences have been under functional constraint throughout primate evolution. Compared to all other primates in our sample, our analysis of exon 1 in MSX1 finds an unusual pattern of amino acid substitution for Tarsius syrichta, a member of a lineage (tarsiers) that has many unique features among primates. For example, tarsiers are the only extant primates without deciduous incisors, and MSX1 is expressed exclusively in the incisor regions during the earliest stages of dental development. Our overall results provide insight into the utility of comparative species analyses of highly conserved developmental genes and their roles in the evolution of complex phenotypes.     

Function of snake mobbing in spectral tarsiers

Numerous species are known for their tendency to approach and confront their predators as a group. This behavior is known as mobbing. Snakes seem to be one of the more consistent recipients of this type of predator-directed behavior. This paper explores individual differences (sex and age) in the mobbing behavior of the spectral tarsier toward live and model snakes. This study was conducted at Tangkoko Nature Reserve (Sulawesi, Indonesia) during 2003-2004. During this research, 11 natural mobbing events and 31 artificially induced mobbing events were observed. The mean number of individuals at a mobbing was 5.7. The duration of mobbing events was strongly correlated with the number of assembled mobbers. Adults were more likely than other age classes to participate in mobbings. Males were more likely than females to participate in mobbings. Mobbing groups often contained more than one adult male, despite the fact that no spectral tarsier group contains more than one adult male. No difference in body size between extragroup males and resident males was observed, refuting the "attract the mightier" hypothesis. The number of mobbers did not affect whether the tarsier or the snake retreated first, countering the "move-on" hypothesis. The "perception advertisement" hypothesis was tentatively supported, in that live snakes were rarely seen in the area following mobbing calls, in comparison to when tarsiers either ignored the snake or alarm call.     

Feeding behavior,mastication, and tooth wear in the western tarsier (Tarsius bancanus)

We assessed feeding and masticatory function in western tarsiers, Tarsius bancanus,from field study, from videotaped recordings of the feeding and chewing behavior of wild-caught animals in temporary captivity, from dissections of the muscles of mastication, and from scanning electron microscopic (SEM) examination of wear features of the teeth. Ingestion of large items of animal prey is made possible by the animal’s extremely wide gape. Anterior translation of the knob-like mandibular condyle in the anteroposteriorly elongated mandibular fossa makes possible a gape angle of 60–70‡. We observed two means of ingestion of grasshopper prey: ingestion by mastication, in which the postcanine teeth sever and reduce bites of the food as it is thrust into the mouth cavity, and repeated gape-shove sequences, during which the tarsier pushed grasshoppers of large diameter into the anterior part of its mouth and attempted to sever a bite with its anterior teeth. Morsels were successfully severed after three to five such sequences, and reduced quickly,with relatively few powerful, crushing chews. The insect cuticle was not evenly comminuted during mastication. We observed a marked side-to-side grinding component in the normal chewing cycle of T. bancanuson videotape and confirmed it by SEM. The main jaw adductors are bulky, long-fibered muscles that can accommodate wide grapes and still generate, at wide degrees of gape,the high occlusal pressures necessary to fracture thick chitinous exoskeletons of the scarabid beetles that form a substantial element of the western tarsier’s diet.     

Reproductive cycles in Tarsius bancanus

The reproductive condition of three pairs of Bornean tarsiers (Tarsius bancanus) was documented for 16 months. Each pair was housed separately under a constant photoperiod (L:D = 11.5:12.5) similar to that in their native habitat. Reproductive cycles of females were monitored visually for 6 months and were then monitored with vaginal smears and measurements of external genitalia for an additional 10 months. Progressive proliferation and cornification of vaginal epithelial cells during proestrus and estrus was accompanied by an enlargement of the external genitalia. Cycle lengths averaged 24.0 ± 3.2 days. The external genitalia were swollen each cycle for a period of 6–9 days. Copulations occurred on the 1st day of estrus, which lasted 1–3 days. No menstruation was observed. There was no evidence of seasonality of estrous cycles with this photoperiod. Testicular measurements of males showed no overt seasonal changes. There was variation in testicular size, and one male copulated at a range of testicular sizes. The data indicate that T. bancanus has estrous cycles similar to those of prosimian primates and some New World monkeys and that these cycles occur throughout the year under constant photoperiodic conditions.