Friday, December 18, 2015

The Singular Uniqueness of Tarsiers

South-East Asia draws the attention of many tourists and travelers because of its rich cultural heritage, globally famous cuisine, and picturesque views. But there are a growing number of people who are starting to shift their attention to the native wildlife of the region, both terrestrial and marine. Among others, nature lovers are attracted to small, forest-dwelling animals with huge eyes, jumping enormously long distances: tarsiers. Those tiny creatures are becoming a mandatory part of the travel itinerary of many visitors. Some of the people find them cute, some of them describe them as aliens from another world. But the question remains, what actually are they?

Image by Paige Carter.

Tarsiers are the distinct group among primates. This is an unquestionable fact all scientists agree on. Still, what kind of primate is a much more difficult question to answer. There are a few reasons behind this difficulty in classifying them. Their nocturnal nature and morphology would, at first glance, suggest their close relationship to lemurs, lorises and bushbabies, often referred to as prosimians or strepsirrhine. On the other hand, another set of traits, mainly anatomical and reproductive characteristics, would tempt us to place them together with monkeys, apes and humans, which together are called haplorhine. Despite uniform attempts to clarify their relationship to other primates, scientists remain divided on this issue. Why is this issue so difficult to decide?

First of all, along with characteristics common for strepsirrhine on one hand and for haplorhine on the other, tarsiers possess their own distinctive traits. Those creatures are the most carnivorous primates currently known, preying upon various animals, ranging from arachnids and insects to amphibians, reptiles and even birds.[1] Even though they are considered one of the smallest primates, their eyes are disproportionately big, with just one eyeball being bigger than their brain. This is their adaptation for better vision at night, making them better predators, as they do not have tapetum lucidum, the reflective layer behind the retina, which facilitates night vision in lemurs, lorises and bushbabies. Tarsiers are also the only mammals that can rotate their head by 180 degrees, which significantly increases their vision angle and improves their hunting ability. Furthermore, two of their leg bones, the fibula and tibia, are fused, which is an adaptation for their interesting, long-distance leaping.[1]

In 1918 Pocock proposed tarsiers be classified with haplorhines based on his revision of their anatomy, looking especially into the upper lip and nose, placenta, and postorbital partition. However, many of the traits making tarsiers closer to haplorhines have been discussed as convergence or loss as a result of specialization on visual, rather than olfactory, predation (dry rhinarium to give an example).[1] Because of this and other traits, like postorbital partition, placing tarsiers with haplorhines is still a controversy. Thus, since the findings of Pocock in 1918, some primatologists use “Prosimii” and “Anthropoidea,” classifying tarsiers with prosimians, and the others use “Strepsirrhini” and “Haplorhini,” with the latter including tarsiers, monkeys, apes and humans.

Fossil records also fail to resolve this discussion. The fossils of tarsiers are very rare, and the only certain information derived from them is the fact that they come from the Eocene epoch.[1] Therefore, it is not sure whether early tarsiers should be linked with Omomyidae or Anthropoids.[1] It seems that the tarsiers’ affiliation and origins will not be easily solved.
However, some fossil evidence of past forms of tarsiers is available. This includes mainly teeth, lower jaws, and one postcranial skeleton. Four species of fossil tarsiers were recognized: Afrotarsius chatrathi found in Egypt, Tarsius thailandicus collected in Thailand, and Xanthrorhysis tabrumi and Tarsius eocaenus, both excavated in China, with the latter dating back 45 million years.[2] A comparative study of the teeth and tibiofibula from African specimen with modern species reveal many matches. Although smaller than extant specimen, the fossils do not exhibit any major differences in morphology, indicating that currently living tarsiers have not changed in any aspects which could be evaluated based on the excavated material. The animals are essentially “living fossils.”[2]

We also know at least some about the animal’s evolutionary history. All of the present day tarsiers live in rainforests of South-East Asia, and it is known that the physical structure of the forests and insects guilds living there have not changed substantially from Tertiary period, providing a stable of the environment for tarsiers.[2] Put simply, the rainforest of this region is basically the same as it was at the time of the earliest tarsiers. Thus, we can trace back the evolutionary history to some degree.

In the Eocene epoch the forest composition started forming closer understory vegetation in forms of buttressed trunks, lianas and epiphytes.[2] This created a habitat for many animals, including arthropods. However, only a small part of forest-dwelling animals focused on utilizing invertebrate niches, mostly bats and birds.[2] This is explicable when one considers conditions at the understory where most of the arthropods live and their biology itself. Habitat in lower parts of the forest is harder for travelling, resulting in animal predator adaptations of moving up and down vertical tree trunks, crossing gaps and balancing on thin branches and lianas.[2] Additionally, a large part of arthropods are and most likely were, since the beginning of their evolution, nocturnal, which makes foraging challenging. All of the adaptations the tarsiers developed made them successful in exploiting this kind of niche. Foraging in the dense understory became possible due to leaping as a primary locomotion mode, which is enabled by elongated hindlimbs.[2] They also have low metabolic rates and lower body temperatures to save energy expenditure.[2] This made them very efficient in exploiting niche of nocturnal insectivores and carnivores foraging in rainforest dense understory, which apparently has not changed since its origin.[2]

Putting aside the past, currently there are 10 species of tarsiers inhabiting rainforests of BIMP countries: Brunei, Indonesia, Malaysia and the Philippines.[3] Their habitats stretch from primary and secondary lowland evergreen to mossy upper montane rainforests.[2] Except for different distribution, they also differ from each other by some aspects of their biology, ecology and behaviour.  For example, in some species the sexual dimorphism exist with larger males, while in others it is not existent, without differences between sexes.[4] Few species live in family groups, sharing their sleeping sites, while others are solitary, sleeping separately.[4] In terms of their future survival, the tarsiers situation does not seem that bright as one might expect. All of 10 tarsiers species exhibit decreasing population trend; however, the conservation status assessment differs and they were assigned with different categories: one species is Critically Endangered (CR), two are Endangered (EN), two are Vulnerable (VU) and one is Near Threatened (NT).[3] Three remaining species are Data Deficient (DD), showing an immediate need for studies on them.[3]

One of the most famous but most poorly known of these animals is the Philippine tarsier (Tarsius syrichta). Despite some obvious facts, incorrect myths have accumulated along the years to draw the attention of visitors to this tiny primate. First, completely wrong information about Philippine tarsiers can be found in almost every tourist guidebook and is repeated by local guides immediately upon arrival. Even worse, this information is passed to young Filipinos in textbooks for elementary schools. For example, visitors coming to the Philippines, especially to Bohol, will be bombarded with the offer to see the “smallest monkey on the world.” As already mentioned above, it is not a monkey; moreover it is not the smallest primate (this title is held by Madame Berthe’s Mouse Lemur (Microcebus bertahe)),[5] or even the smallest tarsier (the smallest among tarsier is pygmy tarsier (Tarsier pumilus)).[4]

What, then, do we know about the Philippine tarsier? This species, of weight range 83-183g, occupies few Philippine islands.[6] In addition to Bohol (recognized as subspecies T. syrichta fraterculus), other places where it can be found include Leyte and Samar (T. syrichta syrichta), Mindanao (T. s. carbonarius) as well as Surigao, Basilan and Dinagat.[6] The latter includes tarsiers that, according to the latest genetic findings, may soon be considered as a separate lineage.[7] On the other hand, the natural history of the Philippine tarsiers looks vague. The evidence, especially geological, is scarce, but it is believed that the species immigrated to the Philippines from Borneo between late Miocene to mid-Pleistocene via Sulu archipelago.[6]

The behaviour of tarsiers is very difficult to uncover. However, thanks to radio, telemetry and other technical advancements, some important data on the Philippine tarsier, although limited, was collected in the past several years.[8-12] Studies revealed that this species on average occupies home ranges of 2.45 ha for females and 6.45 ha for males, travels nightly from 260 m to 2284 m and its primary locomotor behaviour is leaping on vertical supports.[8,9] The Philippine tarsiers inhabit mainly secondary lowland rainforest in early to mid-successional stage.[9] Based on recordings from 25 individuals, 8 types of audible calls were distinguished for the species, which are emitted mainly around sunset and a less frequently at sunrise.[10] What is more, it was found that in addition to vocalizations heard by human hearing, the Philippine tarsiers produce ultrasonic vocalizations (USVs).[11] It was also reported that Philippine tarsiers can be predated by cats and monitor lizards, and probably many more.[8,12] Finally, though no one is sure of its exact social system, available evidence suggests that the Philippine tarsiers are rather solitary.[8,9]

The Philippine tarsier was assessed as Near Threatened (NT).[13] This is because while there are still tarsiers in the forest, we do not know the exact or even approximate population estimates. What is more, the particular subspecies are not studied and assessed properly. Finally, the main threats the species faces, which are disappearing forest cover and hunting, still occur.[13] Deforestation in the Philippines is a major problem. Still, the second threat, hunting, due to its faster pace, is the main for the species. Expanding human population encourages development that is closer and closer to the tarsiers’ habitat. It not only increases predation by domesticated cats, more frequent in the area, but increases temptation of relatively easy income in the form of selling captured tarsiers. Based on my observation, it can take place directly, with the primates as the main target to catch, or they can be obtained from the wild as “by-catch,” which occurs when the hunter goes to the forest to collect other animals, for example, birds, but when tarsiers are spotted, they are captured as additional benefit. Later on, they are sold to private owners as pets. Tourism encourages this. Tarsiers are rarely kept in suitable conditions. For example, instead of resting during the day like their biology demands, tarsiers are exposed to crowds of people during the day. In some places visitors can touch them. Under those circumstances, along with inappropriate feeding, they ultimately die, and breeding does not occur, due to challenges in keeping this sensitive species in captivity. However, because of intervention from foreign organizations, the situation has become slightly better.[14]

As mentioned above, keeping this sensitive species in captivity is extremely difficult. Efforts to breed the Philippine tarsier were made across Western countries in past decades, without any success. The same is happening in the Philippines. The biggest problem is the very low survival of offspring. The backup captive population for any conservation action is therefore not existent. Recently, an attempt to change the situation has been made by Tarsius Project, which is working on the development of the Tarsier Conservation Center. The core activity of this complex initiative is to establish a viable breeding colony in the country of origin in a purely scientific way. All of the possible causes of failure in Western countries were minimalized by reducing stress due to transportation of animals, providing natural climate and conditions (enclosures are big and planted with natural vegetation providing a miniature habitat for tarsiers live in) as well as providing tarsiers with a variety of natural nutritionally rich food, including crickets, prey mantids, spiders, katydids, grasshoppers, dragonflies, cicadas and moths. Results look promising.

However, it is not enough to secure the survival of tarsiers. To make that happen local people should be knowledgeable about tarsiers and other wildlife, as well as their relationships and dependence on forest. The current situation in this regard is not satisfactory. Thus, staff of the Project created a few educational programs for different school levels, from elementary schools to universities with several institutions already involved in those activities. What is more, to improve environmental awareness among pupils, the traineeship curriculum for teachers has been designed and conducted. Trained teachers are aware about environmental issues and are encouraged to incorporate their gained knowledge in early teaching. Further, the Project tries to involve as many local residents as possible in small livelihood projects, reducing dependence of villagers on natural resources. Those activities provide solutions and ideas which can be easily adopted by other projects or conservation centers in the Philippines. Only this kind of complex initiatives, touching all of the issues related to wildlife conservation are successful to improve the situation and reduce the risk of extinction of any of endemic and interesting species, including tarsiers.

Filip Wojciechowski is a primate lover and holds a Master’s degree in environmental biology, majoring in zoology, obtained from Adam Mickiewicz University in Poland. For a few years, he had assisted in primate husbandry in the Poznań Zoological Garden and conducted fieldwork in Vietnam, contributing to the conservation status assessment of the critically endangered Delacour’s langur. Since July 2014, he is tied up with the Tarsius Project, currently as a Field Manager in charge of research, environmental and conservation education and tarsiers husbandry in developing Tarsier Conservation Center in Bilar, Bohol, Philippines focused on the Philippine tarsier.

 












Notes

  1. Simons, E. L. The Fossil Record of Tarsiers Evolution. 2003. In: Wright, P.C., E.L. Simons & S.L. Gursky (Eds.). 2003. Tarsiers: Past, Present, and Future (Rutgers Series in Human evolution). Rutgers University Press, New Jersey, London: 9-34.
  2. Jablonski, N. G. The Evolution of the Tarsiid Niche. 2003. In: Wright, P.C., E.L. Simons & S.L. Gursky (Eds.). 2003. Tarsiers: Past, Present, and Future (Rutgers Series in Human evolution). Rutgers University Press, New Jersey, London: 35-49.
  3. The IUCN Red List of Threatened species. http://www.iucnredlist.org/.
  4. Grow, N. & Gursky, S.L. 2010. Preliminary Data on the Behavior, Ecology, and Morphology of Pygmy Tarsiers (Tarsius pumilus). International Journal of Primatology 31, 1174–1191.
  5. Madame Berthe’s Mouse Lemur. http://www.arkive.org/madame-berthes-mouse-lemur/microcebus-berthae/.
  6. Dagosto, M., Gebo, D. L. and Dolino, C. N. The Natural History of the Philippine Tarsier (Tarsius syrichta). 2003. In: Wright, P.C., E.L. Simons & S.L. Gursky (Eds.). 2003. Tarsiers: Past, Present, and Future (Rutgers Series in Human evolution). Rutgers University Press, New Jersey, London: 237-259.
  7. Brown, R. M., Weghorst, J.A., Olson, K.V., Duya, M.R.M., Barley, A.J., Duya, M.V., et al. (2014). Conservation Genetics of the Philippine Tarsier: Cryptic Genetic Variation Restructures Conservation Priorities for an Island Archipelago Primate. PLoS ONE 9(8): e104340. doi:10.1371/journal.pone.0104340
  8. Dagosto, M., Gebo, D.L. & Dolino, C. 2001. Positional Behavior and Social Organization of the Philippine Tarsier (Tarsius syrichta). Primates 42, 233-243.
  9. Neri-Arboleda, I., Stott, P. & Arboleda, N.P. 2002. Home Ranges, Spatial Movements and Habitat Associations of the Philippine Tarsier (Tarsius Syrichta) in Corella, Bohol. Journal of Zoology 257, 387-402.
  10.  Gursky-Doyen, S.L. 2013. Acoustic characterization of ultrasonic vocalizations by a nocturnal primate Tarsius syrichta. Primates, DOI 10.1007/s10329-013-0349-3
  11. Řeháková-Petrů M., Peške L., Daněk T. 2012. Predation on a wild Philippine tarsier (Tarsius syrichta). Acta Ethologica, 15, 2, 217-220, DOI: 10.1007/s10211-011-0096-7
  12. Řeháková-Petrů, M., Policht, R., Peške L. (2012) Acoustic repertoire of the Philippine tarsier (Tarsius syrichta) and individual variation of long distance calls, International Journal of Zoology, Volume 2012 (2012), Article ID 602401, doi:10.1155/2012/602401
  13. Shekelle, M. & Arboleda, I. 2008. Tarsius syrichta. The IUCN Red List of Threatened Species 2008: e.T21492A9289252. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T21492A9289252.en. Downloaded on 28 October 2015.
  14. Tarsius Project: Research and Conservation on the Philippine Tarsier (Tarsius syrichta). www.tarsiusproject.org.
  15. Padua, M. A. 1994. Conservation Awareness through an Environmental Education Programme in the Atlantic Forest of Brazil. Environmental Conservation, 21 (2), DOI: 10.1017/S0376892900024577.
  16. Patel, E. R., Marshall, J. J., and Parathian, H. 2005. Silky Sifaka (Propithecus candidus) Conservation Education in Northeastern Madagascar. Laboratory Primate Newsletter, 44 (3): 8-11.

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