Primates of the Oriental Night

CONTENTS Foreward v Preface vii Acknowledgments ix Taxonomic History of the Tarsiers, Evidence for the Origins of...

Author: Myron Shekelle ... et al. . Indonesian Institute of Sciences(LIPI)

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CONTENTS Foreward

v

Preface

vii

Acknowledgments

ix

Taxonomic History of the Tarsiers, Evidence for the Origins of Buffon’s Tarsier, and the Fate of Tarsius spectrum Pallas, 1778

01

Distribution and Biogeography of Tarsiers

13

A Tarsier Capture in Upper Montane Forest on Borneo

29

Distribution of Tarsier Acoustic Forms, North and Central Sulawesi: With Notes on the Primary Taxonomy of Sulawesi’s Tarsiers

35

Distribution of Tarsier Haplotypes for Some Parts of Northern and Central Sulawesi

51

A Method for Multivariate Analysis and Classification of Tarsier Tail Tufts

71

Tarsier Longevity: Data from a Recapture in the Wild and from Captive Animals

85

Eastern Tarsiers in Captivity, Part I: Enclosure and Enrichment

91

Eastern Tarsiers in Captivity, Part II: A Preliminary Assessment of Diet

97

The Conservation Status of Indonesia’s Tarsiers

105

Craniometry of Slow Lorises (Genus Nycticebus) of Insular Southeast Asia

115

Enclosure Design for Captive Slow and Pygmy Lorises

123

Confiscation, Rehabilitation and Placement of Slow Lorises: Recommendations to Improve the Handling of Confiscated Slow Lorises Nycticebus coucang Dedication

137 146

Foreword PROF. DR. ROCHADI ABDULHADI PRESIDENT OF THE INDONESIAN BIOLOGICAL SOCIETY EXECUTIVE SECRETARY INDONESIAN INSTITUTE OF SCIENCES (LIPI) I am extremely pleased to see that “Primates of the Oriental Night” has, at last, been completed. This book is a fabulous example of the benefits of true collaboration between researchers of many nations. The list of authors includes people from Austalia, England, Germany, Indonesia, Mexico, the Philippines, and the United States of America. It is wonderful what we can accomplish when we all work together. We live in a globalized world, and it is increasingly necessary that we do so. I am particularly pleased to see several Indonesian authors are involved, and that the book is being published in Indonesia, by the Indonesian Institute of Sciences. We can point to this book as proof that many Indonesians are mentally prepared for the globalized world. Indonesia is a country of vast biodiversity resources, but also vast conservation challenges. When looking for conservation solutions, too often we focus only on the large charismatic animals like orangutan, tiger, and elephant. In Indonesia we are blessed with a wealth of animals like this, to the extent that we forget that there are small charismatic animals. Tarsiers and lorises, the primates of the oriental night, also have tremendous charisma. We need only point to examples from popular movies, such as the Yoda character and the Ewoks, from the “Star Wars” movie series, to see the powerful influence of these charismatic animals on the global society. Unfortunately, we can also point to the prevalence of tarsiers and lorises for sale in the markets of Indonesia and other southeast Asian countries to offer proof that the general public is fascinated with these creatures. The publication of this book marks a sea change in the knowledge about tarsiers and lorises that is available to readers in southeast Asia. I am delighted to learn that one hundred copies of this book will be distributed free of charge to scientists and schools throughout Indonesia. I hope that this effort motivates other Indonesians to follow in the footsteps of the Indonesian authors who contributed to “Primates of the Oriental Night” and become serious biodiversity scientists, committed to the pursuit of knowledge about, and the preservation of, Indonesia’s vast and valuable biodiversity.

v

PREFACE

Some of the manuscripts contained in this volume have existed in various forms for several years now and, in order to avoid some confusion, it may help to offer an explanation as to why they have finally appeared in their current form. Plans for this volume began with the International Primatological Society Congress in Adelaide, Australia, in January 2001. Colin Groves and myself organized a symposium “Advances in Tarsier Biology”. Our intentions were to present a series of seminars that would complement the book “Tarsiers: Past, Present, and Future” edited by Patricia C. Wright, Elwyn L. Simons, and Sharon Gursky, which had been scheduled for release prior to the congress. With the delayed release of that book, and the poor attendance at Adelaide, our plans for an edited volume from that symposium were delayed. By the summer of 2002, Colin Groves, Alexandra Nietsch, and myself had been exchanging emails on the issue of tarsier taxonomy and unrecognized species within the T. tarsier species complex—what we were calling Eastern tarsiers—for several years, and were ready to meet to discuss the issue face-to-face. We located a sponsor, Dr, Willie Smits, of The Gibbon Foundation, and planned a meeting for early November 2002, in Jakarta. As the world is well aware, terrorists exploded several bombs in tourist areas of Bali on October 12, 2002, resulting in the deaths of over 200 people. Particularly affected was Australia, from where about half of the victims originated. If for no reason better than to appease our worried family members, the Tarsier Taxonomy Workshop in Jakarta was postponed. It is hard to imagine a silver lining in that tragedy, and yet the “Indonesian Prosimian Workshop”, upon which this book is ultimately based, owes it genesis to that event. Concurrent to our planning for this event, Dr. Smits opened the Schmutzer Primate Center, a world class, semi-autonomous primate facility within Ragunan Zoo in Jakarta. Within Indonesia large numbers of lorises, as well as some tarsiers, are for sale on the black market. Large numbers of these primates would need to be confiscated to stem the trade, and the Schmutzer Primate Center would require expertise in the management of nocturnal primates. Therefore, during the weeks after the bombing I asked Dr. Smits if he would like for me to contact my colleagues with loris expertise, and expand the focus of our workshop to include captive care and conservation of tarsiers and lorises. He readily agreed to an expanded budget that would allow to us invite experts who were active and specialized in those areas. To help organize the workshop, I contacted Helena Fitch-Snyder, whom I had met through our work together in the North American Prosimian Taxon Advisory Group, and Helga Schulze, whom I had met at the “Creatures of the Dark” conference in Durham, North Carolina in 1993. In the end, the foreign invitees at the workshop included three researchers active in tarsier field biology, three who were active in loris husbandry and conservation, one who had conducted field work on both tarsiers and lorises, and one taxonomist. In addition to Dr. Alexandra Nietsch and myself, tarsier field biology was represented by Irene Neri-Arboleda, who had recently completed the most thorough field study of Philippine tarsiers to date. This workshop was particularly blessed by the participation of Dr. Sharon Gursky, Assistant Professor of Anthropology at Texas A & M University who not only has amassed more hours of field data than anybody else on tarsiers, but is quite possibly the one-and-only person who has conducted systematic field studies on both tarsiers and lorises. Dr. Helena Fitch-Snyder and Helga Schulze, who edited the book “A Manuaul of Loris Husbandry”, and who between them have possibly more experience than anyone else in maintaining loris colonies outside of their native countries, represented lorises. Dr. Ulriche Streicher, D.V.M. came to the attention of the organizers from her presentation at the Beijing, IPS meetings, wherein she offered evidence that showed how coat markings in lorises change seasonally. Her participation was quite fortunate, because as a D.V.M. working at a primate rescue center in Vietnam that specializes in lorises, her experience proved to be invaluable to her Indonesian counterparts on the frontline of combating the illegal trade in lorises.

vii

The workshop benefited greatly from the participation of Dr. Colin Groves, Professor of Anthropology and Archeology at Australian National University, author of the book “Primate Taxonomy” and an expert in seemingly everything. The workshop itself led to a new collaboration with Indonesian scientists, including mammalian taxonomist, Ibnu Maryanto, who co-authored a manuscript with Dr. Groves and graciously agreed to assist in the editing of this book. Two other long time colleagues and friends, loris biologist Anna Nekaris and tarsier biologist Stefan Merker, were invited to attend but were unable to because of other obligations. Thus, the objective of this book is to pull together several manuscripts that are related to each other as least as much by history as by subject matter. As such, this book does not present as cohesive a narrative as “Tarsiers: Past, Present, and Future”, and in some respects, it is more a complement to that book. In other respects, however, this book publishes the results of the “Indonesian Prosimian Workshop”. As such, it includes information on animal rescue and captive care. This book, therefore, is written by specialists in tarsier and loris biology, and is written for the larger community of specialists—scientists, conservationists, animal keepers, monitors, and others—who require current information about our subject matter, the nocturnal primates of Asia. It is worth commenting on our choice of publishers. Given this book’s earliest origin as a symposium for the IPS Congress at Adelaide, there were discussions with academic publishing houses. In the end, by choosing the Indonesian Institute of Sciences, we wound up with great freedom in terms of manuscript length and color illustrations. Additionally, given the cost savings, we will be able to distribute 100 copies, free of charge, to schools, libraries, and other institutions throughout Indonesia. Myron Shekelle et al. Jakarta, 5 July 2008

Some participants at the Indonesian Prosimian Workshop, Schmutzer Primate Center, 21 February 2003.

viii

ACKNOWLEDGMENTS The editors are deeply indebted to Dr. Willie Smits and the Gibbon Foundation, who funded the workshop and this volume. The Schmutzer Primate Center Staff hosted many of the workshop activities, and several staff members assisted with the workshop, including Femka Den Haas, and Made Wedana. Dr. Siti Nuramaliati Prijono, director of the Indonesian Institute of Sciences’s Museum Zoologicum Bogoriense sponsored a seminar that featured the workshop’s participants and hosted other workshop activities.

Dr. Willie Smits

Dr. Siti Nuramaliati Prijono

Dr. Ibnu Maryanto

ix

Primates of The O riental Night

TAXONOMIC HISTORY OF THE TARSIERS, EVIDENCE FOR THE ORIGINS OF BUFFON’S TARSIER, AND THE FATE OF Tarsius spectrum Pallas, 1778 Colin Groves 1), Myron Shekelle 2), & Douglas Brandon-Jones 3) School of Archaeology and Anthropology, Australian National University Canberra, ACT 0200, Australia. Email: [email protected] 2) Center for Biodiversity and Conservation Studies, Faculty of Mathematics and Natural Sciences University of Indonesia, Depok 16421, Indonesia, Email: [email protected] 3) 22 Karenia Street, Bray Park, QLD 4500, Australia 1)

ABSTRACT A survey of the history of tarsier taxonomy indicates that Tarsius tarsier Erxleben, 1777 is a senior subjective synonym of T. spectrum Pallas, 1778. Buffon’s tarsier, long thought lost or possibly destroyed, has been recently rediscovered and is identified as being eastern in origin (i.e. from within what has previously been classified as T. spectrum or the T. spectrum complex). The identification of Buffon’s tarsier as an Eastern tarsier alters Hill’s taxonomy by making T. spectrum a junior subjective synonym of T. tarsier. Eastern tarsiers become the type species of the genus. Our work, conducted, before the rediscovery of Buffon’s specimen, is based on illustrations of the skin and cranium by Daubenton. Investigations of Buffon’s specimen are ongoing, but do not alter our fundamental conclusions. Daubenton’s illustration of the cranium shows a nasal profile that is not consistent with published illustrations of Philippine and Western tarsiers. Several other characteristics are argued to be consistent with Buffon’s tarsier being eastern in origin. Keywords: T. tarsier, T. bancanus, T. syrichta, Taxonomy

A BRIEF HISTORY OF TARSIER TAXONOMY - Linnaeus’s tarsier Standing last in the list of Linnaeus’s (1758) 21 species of the genus Simia is Simia syrichta, reading as follows: S. caudata imberbis, ore ciliisque vibrissatis. Syst.nat.3. Cercopithecus luzonicus minimus. Pet.gaz. 21.t.13.t.11. Habitat in Luzonum insulis. Cabrera (1923) showed that Petiver (“Pet.”) took his 1705 description in turn from the papers of a Jesuit missionary, G..J. Camel, who was clearly referring to a tarsier, and that the locality, Luzon is probably to be explained as being a place to which tarsiers were traded from nearby Samar. Cabrera (1923) used the form Tarsius syrichtus, but, as Linnaeus (1758) spelt the name Syrichta with a capital initial letter, it is probable that he was using it as a noun in apposition (he began adjectives with a small letter), so it does not change gender: see Musser & Dagosto, 1987.

Consequently, the earliest available name for a Philippine tarsier is syrichta Linnaeus, 1758. Cabrera’s (1923) mention of Samar may be taken as a restriction of the type locality. Cabrera’s (1923) opinion that Simia syrichta is a Philippine tarsier has been supported by numerous authors since that date. Hill (1953a,b), in his influential revision, accepted Cabrera’s (1923) assessment of Linnaeus’s Simia syrichta as the Philippine tarsier; so did Musser & Dagosto (1987). Remarking on its essential accuracy, Niemitz (1984) translated Camel’s description, including the comment, “it is said to live on charcoal, but this is wrong”! Meyer (1895), not knowing all this, described the Philippine tarsier as Tarsius philippinensis, with type locality Samar, while Heude (1898:164) clearly thought that he was the first to name a Philippine tarsier when he described T. carbonarius from two specimens from Mindanao: from the Gulf of Davao and the valley of the River Poulangui. He distinguished this from the only other species he knew, “Tarsius spectrum de Java” (sic), by dental characters and by the narrowness and greater length

1

Groves, Shekelle & Brandon-Jones- Taxonomic History of The Tarsiers

of the skull, adding, in a curious but quite independent echo of Camel, “On m’a dit qu’il mangeait du charbon!” Buffon’s tarsier Buffon (1749:87, and pl. 219) gave the vernacular name Tarsier or Woolly Jerboa to an animal he received from an unknown locality. Remarking on its long hind legs and other characters, he described

“the inferior part of the hind legs” as being hairless and its tail as being, like that of the jerboa, garnished with long hairs towards the tip. It is not clear exactly what is meant by “the inferior part of the hind legs” – evidently, not necessarily the whole of the tarsus, because in the plate the proximal part of the tarsus is haired (Figure 1). This, and the conspicuously tufted tail, eliminates

Figure 1: Buffon’s tarsier. This illustration has the gestalt of an Eastern tarsier in having a tail that is more hirsute than is common in Western and Philippine tarsiers, relatively small eyes, long and pointed ears, woolly appearance of the fur, and similarities of the relative leg length (from Buffon 1765).

2


the almost naked-tailed Philippine tarsier (Figure 2). The head is not excessively broad, and the very long, dark, conspicuous tail tuft suggests it is not a Western tarsier. Buffon’s colleague Daubenton published, as an addendum (p.114 [N°MCCXXXV]), a description of the skull and skeleton of the tarsier (always assumed, perhaps not correctly, to be of the same specimen). A plate of the skull and skeleton was published by Fischer (1804), who called it “Daubenton’s tarsier”. Poor as they are, the figures show the relatively small orbits and long braincase of the Sulawesi tarsier (Figure 3). Other than a few specimens mounted for public display, I. Geoffroy St. Hilaire (1851:ii, fn.2) found Buffon’s collection neglected, and “ne tardait pas à être attaqué par les insects”. Nonetheless, the mounted tarsier specimen does still exist; it is the subject of a paper in preparation by CPG, in collaboration with C. Callou and J. Cuisin. Suffice it to say that it is indeed a Sulawesi tarsier, and we cannot understand why Elliot (1910) baldly claimed that its “bare tarsi and nearly naked tail” (sic!) shows it came from the Philippines. Elliot refused to fix a type locality and considered it indeterminable, adding that as Pallas’s spectrum was based upon it, “Tarsius spectrum must be dropped from the list of recognized species”. Buffon was the main source for Erxleben’s (1777:72) name Lemur tarsier, which consequently is not a Philippine tarsier as listed by Hill (1953a), but is the earliest available name for a Sulawesi tarsier. Schreber (1778:554) cited Buffon and Erxleben for the description of his Didelphys? macrotarsos, which he inclined to think was actually a marsupial. Gmelin (1788) cited Buffon first, and Pennant second, for his Didelphis macrotarsus. Link (1795) likewise based the name Macrotarsus buffonii on Buffon’s tarsier, as did Audebert (1797) for Tarsius daubentonii.

probably Ambon”, and is called podje by the Macassans. Pallas described its teeth and its general external appearance, ending with “Cauda nudiuscula”, meaning “Tail virtually naked”. According to Smit et al. (1986), Schlosser ’s cabinet may have been purchased by Boddaert, but thereafter nothing is known about it. Hill (1953a) argued that the description was that of a Sulawesi tarsier, and fixed the type locality as Macassar (=Makassar, until recently known as Ujung Pandang, but the name recently reverted to its original, Makassar), because of Pallas’s mention of its Macassan name, podje. Possibly influenced by Sody (1949), Niemitz (1984:13) influentially gave the type locality as Minahasa (far northern Sulawesi). In the absence of any evidence to the contrary, Hill’s fixation is better substantiated. As Cabrera (1923) recognized, Lemur tarsier Erxleben, 1777, based on Buffon’s description (see above), predates Lemur spectrum Pallas, 1778 and Didelphys? macrotarsos Schreber, 1778. Unfortunately, therefore, the well-known name Tarsius spectrum, commonly used for Sulawesi lowland tarsiers, must be superseded by Tarsius tarsier (Erxleben, 1777). Geoffroy (1796) later redescribed Pallas’ specimen as Tarsius pallassii.

Pallas’s tarsier Pallas (1778) also based Lemur spectrum in Buffon’s tarsier, but referred to it a specimen in the museum of his late friend Schlosser, which in effect formed the bulk of his description. He stated that it came from “the furthest islands of the Indian Ocean,

Citing Pallas (1778), Pennant (1781) gave Amboina (=Ambon) as the locality, and podje as the Macassan name. Later Kerr (1792) paraphrased Pennant’s (1781) description, naming it Lemur podje. “Doctor Hunter” is almost certainly the famous surgeon John Hunter (1728-1793), whose

-Pennant’s tarsier Pennant (1771) redescribed Buffon’s tarsier, and ten years later (Pennant, 1781) he described “two fine specimens from the cabinet of Doctor Hunter” as having A pointed visage… hairs on the legs and feet short, white, and thin; tail almost naked: the greater part round and scaly, like that of a rat; but grows hairy towards the end, which is tufted.

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4

Philippine tarsier

T. tarsier (unknown prov.)

T. tarsier Togian Islands

Eastern tarsiers

T. dentatus

Figure 2: Diagnostic value of tarsier tails. The Philippine tarsier in this figure has a very slight, almost invisible tuft of fur on the distal few centimeters of the tail. The tuft fur is sparse, very short, and light in coloration. Western tarsiers have a clearly apparent tuft of fur on the distal end of the tail, in appearance like that of a feathered arrow shaft. The fur on the tail of Eastern tarsiers is altogether different than the other two and gives the tail of an Eastern tarsier an appearance similar to that of a bottle brush. The tail fur of Eastern tarsiers is generally longer, darker, and the tuft typically covers as much as 1/3 to 1/2 of the length of the tail, but it develops gradually along the length of the tail such that its actual length is difficult to measure accurately. In T. sangirensis, the tail tuft is in the same position as it is in other Eastern tarsiers, but the fur is shorter, sparser, and lighter in color. (adapted from Shekelle 2003)

T. b. bancanus T. s. fraterculus T. sangirensis Tarsier photos © Myron Shekelle, 2002, except T. syrichta, Sheena Hynd

Western tarsier



Buffon’s tarsier

Eastern tarsiers

Philippine tarsier

Western tarsier

Figure 3a: Buffon’s tarsier is most similar to Eastern tarsiers in the shape of the nasal profile (adapted from Musser and Dagosto 1987, Fischer 1804, and Shekelle 2003).

Buffon’s tarsier

Eastern tarsiers

Philippine tarsier

Western tarsier

Figure 3b: Buffon’s tarsier is most similar to Eastern tarsiers in that the shape of the cranium is oblong and has a slight postorbital constriction (adapted from Musser and Dagosto 1987 and Fischer 1804). Note: Tarsius dianae is a junior synonym of T. dentatus

Buffon’s tarsier

Eastern tarsiers

Philippine tarsier

Western tarsier

Figure 3c: Buffon’s tarsier is most similar to Eastern Tarsiers in the relative height of the orbits and the braincase (adapted from Musser and Dagosto 1987 and Fischer 1804).

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anatomical preparations and manuscripts were bequeathed to the nation under the trusteeship of the Royal College of Surgeons collection upon his death, forming the basis for what became the Hunterian Museum. The Royal College of Surgeons took a direct hit during the Second World War, and many valuable specimens were destroyed, presumably including the tarsiers. Although the description is not absolutely clear-cut, the “pointed visage” and the description of the tail strongly suggest a Sulawesi tarsier, so Lemur podje Kerr, 1792 is best regarded as a junior synonym of Lemur tarsier although it is of course available to anyone who might consider Hunter’s specimens as distinct. Fischer’s revision of tarsiers Fischer (1804) considered that he had evidence for not one but three species of tarsier: Tarsius pallassii (adopting Geoffroy’s renaming of Lemur spectrum Pallas, 1778), T. daubentonii (an explicit renaming of Lemur tarsier Erxleben, 1777 and Didelphis macrotarsus [sic] Gmelin, 1788, apparently unaware of Audebert’s similar action), and a new species T. fuscus or fuscomanus. This new species was said to have come from Madagascar, probably (as he remarked) an error for Macassar. His description of the tail could only be that of a Sulawesi tarsier. Differences between his three species, which in effect, therefore, are all Sulawesi tarsiers, are based on stages of wear on the incisors and other features. Hill (1953a) presumed that the type of Fischer’s T. fuscus was lost, and there seems no contrary evidence. Tarsius pallassii and T. daubentonii are objective junior synonyms of Lemur spectrum and Lemur tarsier, respectively. Given the type locality, Macassar, for all three of Fischer’s taxa, T. fuscus (which he also called T. fuscomanus) must rank as a subjective junior synonym of Lemur tarsier, despite the fact that Miller and Hollister (1921), obscurely, referred to “Tarsius fuscus fuscus from northeastern Celebes”. Desmarest (1804) combined Fischer’s first two species into one, which he called “Tarsier aux mains rousses, Tarsius spectrum Geoffroy” [sic],

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including Buffon’s, Pallas’s and Pennant’s tarsiers; and renamed the third “Tarsier aux mains brunes, Tarsius fischerii = T. fuscomanus Fischer”. Other 19th century revisions of tarsiers Horsfield (1824) described the first welllocalised tarsier, Tarsius bancanus from Jeboos (=Jebus), Bangka. It was described as being dark, lacking upper central incisors (but the type was evidently an infant, and having rounded, horizontal ears, shorter than the head, and a flatter facial profile (Figure 4). Horsfield (1824) compared it to Fischer’s (1804) three species, citing T. fuscus as T. fischeri. Fitzinger’s (1870) revision differed little from Horsfield’s (1824) arrangement, recognising four species: Tarsius spectrum (based on Pallas’s tarsier, and from Ambon), T. fuscomanus (Fischer’s tarsier, but said to be from Mindanao and Bohol), T. daubentonii (including Buffon’s, Pennant’s, Schreber’s and Erxleben’s tarsiers, from Celebes, Selayer and Borneo), and Tarsius bancanus (from Sumatra and Bangka). His nomenclature aside, his revision is noteworthy for being the first to compare Philippine and Sulawesi tarsiers, and to widen the known distribution by the inclusion of some new localities. Meyer (1897) had a different view of the nomenclature. He used Tarsius fuscus Fischer for the Sulawesi tarsier, T. philippensis Meyer (1895) for the Philippine species, and T.spectrum (Pallas) for the one from Borneo (which he also knew from the Karimata and Natuna Is., Belitung and Sumatra). He described a new species, T. sangirensis from the Sangihe Is. This represents a further step towards a modern understanding of the species of tarsiers. 20th century revisions Elliot (1910) described two new species, Tarsius saltator from Belitung and Tarsius borneanus from the Landak River, West Kalimantan. Chasen (1940) regarded these as subspecies of the only species he recognized, Tarsius tarsier Erxleben, and described a further subspecies, T. t. natunensis from Sirhassen, in the South Natuna Is.


Figure 4: Buffon’s and Horsfield’s tarsiers. The illustration of Buffon’s tarsier (upper left) does not have the gestalt of an infant, as seen in the illustration Horsfield’s tarsier (upper right), and the mother / infant photo (right) (from Buffon 1765 and Horsfield 1824). Tarsier photo (c) Myron Shekelle 2008.

Miller (1910:404) described a new species, Tarsius fraterculus, from Bohol in the Philippines, said to resemble T. philippensis but smaller in size. Miller & Hollister (1921) described two new tarsiers from Sulawesi: Tarsius fuscus dentatus, from Labuan Sore in the lowlands near Parigi, and Tarsius pumilus, from Rano Rano, in the central highlands.

To T. pumilus they referred two specimens from Gimpu, in the nearby lowlands, in addition to the type. Tarsius pumilus is a valid species, but the Gimpu specimens do not belong to it (Musser & Dagosto, 1987); more recently, Merker & Groves (2006) have included them in their new species, Tarsius lariang.

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Sody (1949:138-143) adamantly assigned Sulawesi and Western tarsiers to separate species, but could not decide whether those from the Philippines were identical to either or neither of them. He used T. fuscus for the Sulawesi tarsier, and T. bancanus for the Western. In T. bancanus he recognised T. b. bancanus (synonym saltator) and T. b. borneanus, without mentioning Chasen’s natunensis. In T. fuscus he recognized T. f. fuscus from Minahassa, T. f. dentatus from central Sulawesi (“very weak”), a new subspecies T. f. pelengensis from Peleng (“we must acknowledge that we are describing a very poor race”), and T. f. sangirensis from Great Sangir (“a very good race”). It was Hill (1953a,b) who first definitively split Tarsius into three species, revising their nomenclature (Hill, 1953a) and describing in detail the striking differences in their tails (1953b) His revision was followed for over 30 years, and has been the basis for all subsequent treatments. Niemitz (1984a) reviewed the differences between the three species, commenting on the synonymy and refusing to recognize any subspecies except for T. s. spectrum and T. s. pumilus, and T. b. bancanus and T. b. borneanus. Contrary to Hill (1953a), however, Niemitz indicated Minahassa as the type locality of T. spectrum (1984:13). Musser & Dagosto (1987) further reviewed some of the nomenclatorial history of tarsiers. They accepted that Linnaeus’s Simia syrichta was a Philippine tarsier, but were skeptical of the association of Pallas’s Lemur spectrum with Sulawesi tarsiers although provisionally prepared to accept Hill’s (1953a) opinion. They revised the differences between T. bancanus, T. syrichta and T. spectrum, indicating that the first two are somewhat more closely related than either is to the third. Most importantly, Musser & Dagosto (1987) pointed out that the type specimen of Tarsius pumilus represents a valid species, and that Miller & Hollister (1921) had muddied the waters by inexplicably assigning to it the two Gimpu specimens (which are juveniles of what Musser and Dagosto regarded as the one and only lowland species, T. spectrum). Their demonstration that T.

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pumilus is a valid species raised the number recognized since Hill (1953a) from three to four. Feiler (1990) proposed raising T. sangirensis Meyer, 1897 to specific rank. Niemitz et al. (1991) described a new species, Tarsius dianae, from central Sulawesi without, however, comparing their new taxon to T. fuscus dentatus, even though the type localities of these two taxa are separated by only about 80 km. Groves (1998) produced a preliminary revision of tarsiers, corroborating the provisional findings of Musser & Dagosto (1987) that the Philippine species, T. syrichta, is closer to T. bancanus, but nonetheless very distinct, while T. pumilus is closer to T. spectrum. Discriminant analysis of admittedly small samples confirms that, within T. spectrum (understood broadly), samples from the mainland, Selayar (a single specimen), Peleng and Sangihe are all distinct, and the latter at least is probably a distinct species. On the mainland, northern and central Sulawesi samples separate, if less clearly. Finally Merker and Groves (2006) described another new species from Sulawesi: Tarsius lariang from Gimpu, Central Sulawesi. This finally resolved the true identity of the two juveniles from Gimpu which had been spuriously associated by Miller and Hollister with Tarsius pumilus, and unceremoniously expelled from that species by Musser and Dagosto. Generic names for tarsiers The earliest generic name for tarsiers is Tarsius Storr, 1780, based on Lemur tarsier Erxleben, 1777, hence on Buffon’s tarsier, a Sulawesi tarsier (see above). The next name, Macrotarsus Link, 1795, was likewise based on Buffon’s tarsier. E. Geoffroy St. Hilaire (1812) also listed Tarsius, in his Strepsirrhini, citing no sources for the generic name but listing two species, T. spectrum (referring to Buffon and to Pallas) and T. fuscomanus (referring to Fischer). Gray (1821) included tarsiers in his order Heteronychae of the class Quadrumana; other members of the order were the lemurs and lorises. His tarsiers belonged to the family Loridae, and were placed in two genera:


Tarsier, Tarsius. Geoff. Lemur tarsium Pallas. Rabienus. Gray. Lemur spectrum Pallas. The first of these two genera is incorrectly ascribed to E. Geoffroy and awarded, as type species, a non-existent name of Pallas’s. Rabienus, based on Pallas’s genuine name, is a junior subjective synonym of Tarsius. Swainson (1835) described a genus Cephalopachus, and Lesson (1840) described Hypsicebus, both erected for T. bancanus Horsfield, 1824. These names are available if the Western tarsier is regarded as generically distinct from Sulawesi tarsiers. Presuming Lemur tarsier Erxleben, 1777 was correctly identified as a Philippine tarsier, Groves (1998) concluded Tarsius Storr is available for a genus containing Philippine tarsiers, leaving Rabienus Gray for Sulawesi tarsiers; but as L. tarsier Erxleben actually refers to a Sulawesi tarsier (see above), Groves’s (1998) conclusion is error. No generic name is available for Philippine tarsiers. DISCUSSION Given this history, Tarsius spectrum is a junior objective synonym of T. tarsier. At first glance, the loss of this name, that has been used for tarsiers for over two centuries, seems regrettable. There is a silver lining, however, since the name T. spectrum is also associated with more taxonomic ambiguity than any other tarsier nomen. At one time or another, virtually all species of tarsier were referred to as Tarsius spectrum, though not always at the same time. Consequently, Clark’s (1924) “Notes on the living tarsier (Tarsius spectrum)” is an account of T. bancanus borneanus. Likewise, Woollard’s (1925) monograph “Anatomy of Tarsius spectrum” is not an Eastern tarsier, but a Western tarsier. Adding further to the confusion, Eastern Tarsiers were not generally referred to as T. spectrum until Hill (1955). Prior to that time, Eastern tarsiers were referred to by a plethora of names, but most often as T. fuscus. Thus, it is no overstatement to say that, prior to Hill, the majority of references to T. spectrum referred to something other

than an Eastern tarsier, while nearly all references to Eastern tarsiers used a name other than T. spectrum. A further consolation is that it turns out that not one, but a number of different species inhabit Sulawesi, each restricted to a particular part of the island. It will possibly cause less confusion if the name Tarsius spectrum applies to none of them than if it is applied to different species, by different authors. ACKNOWLEDGEMENTS The authors were introduced by way of the workshop Primate Taxonomy for the New Millenium and thanks are due to the organizers, Russell Mittermeier, Don Melnick, and John Oates, for bringing the three of us together to discuss tarsier taxonomy. Marian Dagosto reviewed a draft of this manuscript. C.G. offers grateful thanks to Boeadi, Paula Jenkins, Chris Smeenk, Dick Thorington and Guy Musser for access to material under their care; to Guy Musser for useful discussions; and to Marian Dagosto for sending me measurements of additional specimens. M.S. acknowledges the following: This material is based on work supported by the National Science Foundation under Grant No. INT 0107277. Much of the work for this was completed while receiving funding from the Margot Marsh Biodiversity Foundation. Additional collaboration between between M.S. and C.G. was facilitated by the Gibbon Foundation, which sponsored the “Indonesian Prosimian Workshop” in Jakarta, Indonesia. Portions of this appeared in the dissertation of M.S. and I thank Washington University in St. Louis and my thesis committee. REFERENCES Audebert, JB. 1797. Histoire Naturelle des Singes et des Makis. Paris: Desray. Bearder, SK, PE. Honess & L. Ambrose. 1994. Species diversity among galagos with special reference to mate recognition. Pp 1-22 in Alterman, L, Doyle, GA & Izard, MK (eds.),

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Creatures of the Dark: the Nocturnal Prosimians. New York: Plenum Press. Buffon, GLL. Comte de. 1765. Histoire Naturelle, Générale et Particulière. Vol. 13. Paris: Imprimerie du Roi. Cabrera, A. 1910. On the specific names of certain Primates. Annals & Magazine of Natural History (8) 6:617-618. Cabrera, A. 1923. On the identification of Simia syrichta Linnaeus. Journal of Mammalogy, 4:89-91. Chasen, FN. 1940. A handlist of Malaysian mammals. Bulletin of the Raffles Museum, Singapore, 15:I-xx, 1-209. Clark, W. & E. LeGros 1924. Notes on the living tarsier (Tarsius spectrum). Proceedings of the Zoological Society of London, 217-223. Desmarest, A. 1804. Tarsier. Nouveau Dictionnaire d’Histoire Naturelle, Appliquée aux Arts, à l’Agriculture, à l’Economie rurale et domestique, à la Médecine, etc. par une Société de Naturalistes et d’Agriculteurs. Paris: Deterville. Elliot, DG. 1910. On the genus Presbytis Esch., and ‘le Tarsier’ Buffon, with descriptions of two new species of Tarsius. Bulletin of the Mamerican Museum of Natural History, 28:151-154. Erxleben, JCP. 1777. Systema Regni Animalis per Classes, Ordines, Genera, Species, Varietates, cum Synonymia et Historia Animalium. Classis I. Mammalia. Leipzig: Weygand. Feiler, A. 1990. Ueber die Säugetiere der Sangiheund Talaud-Inseln der Beitrag A.B.Meyers für ihre Erforschung (Mammalia). Zoologische Abhandlungen der Staatlisches Museum für Tierkunde in Dresden, 46:75-94. Fischer, G. 1804. Anatomie der Maki. Frankfurt a.M.: Andrea. Fitzinger, LJ. 1870. Revision der Ordnung der Halbaffen oder Aeffer (Hemipitheci). II. Abtheilung. Familie der Schlafmaki’s (Stenopes), Galago’s (Otolicni) und Flattermaki’s (Galeopitheci). Sitzungsberi-

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chte der Mathematisch Naturwissenschaftlichen Classe der Kaiserlichen Akademie der Wissenschaften, Wien, 62, 1:685-783. Geoffroy St.Hilaire, E. 1796. Mémoire sur les rapports naturels des makis Lemur, L. et description d’une espèce nouvelle de mammifère. Magasin encyclopèdique (2) 1:20-50. Geoffroy St.Hilaire, E. 1812. Suite au tableau des Quadrumanes. Seconde Famille. Lémuriens. Strepsirrhini. Annales du Muséum d’Histoire Naturelle, Paris, 19:156-170. Geoffroy St.Hilaire, I. 1851. Muséum d’Histoire Naturelle: Catalogue méthodique de la Collection des Mammifères, de la Collection des Oiseaux et des Collections annexes. Paris: Gide & Baudry. Gmelin, JF. 1788. Caroli a Linné, Systema Naturae, 13th edition. Leipzig: G.E.Beer. Gray, JE. 1821. On the natural arrangement of vertebrose animals. London Medical Repository, 15:296-310. Groves, CP. 1998. Systematics of tarsiers and lorises. Primates, 39:13-27. Heude, PM. 1898. Etudes odontologiques: Quatrièeme Partie. Quadrumanes. Chap.I, Lémuriens, Tarsiens, Galéopitheciens et Cébiens. Mémoires concernant l’Histoire Naturelle de l’Empire Chinois, 4:155-208. Hill, WCO. 1953a. Note on the taxonomy of the genus Tarsius. Proceedings of the Zoolo-gical Society of London, 123:13-16. Hill, WCO. 1953b. Caudal cutaneous specializations in Tarsius. Proceedings of the Zoological Society of London, 123:17-26. Hill, WCO. 1955. Primates: Comparative Anatomy and Taxonomy. II. Haplorhini: Tarsioidea. Edinburgh: Edinburgh University Press. Horsfield, T. 1824. Zoological Researches in Java, and the Neighbouring Islands. London: Kingsbury, Parbury & Allen. International Commission on Zoological Nomenclature. 1999. International Code of Zoological Nomenclature, Fourth Edition.


London: International Trust for Zoological Nomenclature. Kerr, R. 1792. The Animal Kingdom, or Zoological System, of the Celebrated Sir Charles Linnaeus. Class I. Mammalia. London: J.Murray and R.Faulder. Lesson, RP. 1840. Species des Mammifères bimanes et quadrumanes. Paris. Link, HF. 1795. Beyträge zur Naturgeschichte, Rostock & Leipzig, 1974-1801, Bd. I. Stck. 2, pp. 65-66. Linnaeus, C. 1758. Systema Naturae per Regna Tria Naturae, secundum Classes, Ordines, Genera, Species, cum Synonymis, Locis. I. 10th ed. Stockholm: Laurent Salvi. MacKinnon, J. & K. MacKinnon. 1980. The behavior of wild Spectral Tarsiers. International Journal of Primatology, 1:361-379. Merker, S. & CP. Groves. 2006. Tarsius lariang: a new Primate species from Western Central Sulawesi. International Journal of Primatology, 27: 465-485. Meyer, AB. 1897. Säugethiere vom Celebes- und Philippinen-Archipel, I. Abhandlungen und Berichte der Kaiserlich Zoologische und Anthropologische-Ethnologische Museum zu Dresden, 6:I-VIII, 1-36. Miller, GS. 1910. Descriptions of two new genera and sixteen new species of mammals from the Philippine Islands. Proceedings of the United States National Museum, 38:391404. Miller, GS. & N. Hollister. 1921. Twenty new mammals collected by H.C.Raven in Celebes. Proceedings of the Biological Society of Washington, 34:93-104. Musser, GG. & M. Dagosto. 1987. The identity of Tarsius pumilus, a pygmy species endemic to the montane mossy forests of Central Sulawesi. American Museum Novitates, 2867:1-53. Musser, GG. & M. Dagosto. 1987. The identity of Tarsius pumilus, a pygmy species endemic to the montane mossy forests of Central

Sulawesi. American Museum Novitates, 2867:1-53. Niemitz, C. 1979. Relationships among anatomy, ecology, and behavior: a model developed in the Genus Tarsius, with thoughts about phylogenetic mechanisms and adaptive interactions. In M. E. Morbeck, H. Preuschoft, & N. Gomberg (Eds.), Environment, Behavior, and Morphology: Dynamic Interactions in Primates (pp. 119-137). New York: Gustav Fischer. Niemitz, C. 1984a. Taxonomy and distribution of the genus Tarsius Storr, 1780. Pp 1-16 in C. Niemitz, ed., Biology of Tarsiers. Stuttgart: Gustav Fischer Verlag. Niemitz, C. 1984b. Vocal communication of two tarsier species (Tarsius bancanus and Tarsius spectrum). In C.Niemitz (ed.), Biology of Tarsiers, 129-141. Gustav Fischer Verlag, Stuttgart & New York. Niemitz, C, A. Nietsch, S. Warter & Y. Rumpler 1991. Tarsius dianae: a new primate species from Central Sulawesi (Indonesia). Folia primatologica, 56:105-116. Nietsch, A. & ML.Kopp. 1998. Role of vocalization in species differentiation of Sulawesi Tarsiers. Folia primatologica, 68(suppl.1): 371-378. Nietsch, A. & C. Niemitz 1993. Diversity of Sulawesi Tarsiers. Deutsche Gesellschaft für Säugetierkunde, 67. Hauptversammlung, 4546. Pallas, PS. 1778. Novae Species Quadrupedum e Glirium Ordine cum Illustrationibus Variis Complurium ex Hoc Ordine Animalium. Erlangen: Wolfang Walther. Pennant, J. 1771. Synopsis of Quadrupeds. Chester: J.Monk. Pennant, J. 1781. History of Quadrupeds. London: B.White. Schreber, JCD.von. 1778. Die Säugethiere in Abbildungen nach der Natur. Leipzig: T.D.Weigel. Shekelle, M., SM. Leksono, LLS. Ichwan, & Y. Masala. 1997. The natural history of the tarsiers of

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North and Central Sulawesi. Sulawesi Primate Newsletter, 4(2):4-11. Smit, P., APM. Sanders & JPF. van der Veer. 1986. Hendrik Engel’s Alphabetical List of Dutch Zoological Cabinets and Menageries. 2nd ed. Amsterdam: Rodopi B.V. Sody, HJV. 1949. Notes on some Primates, Carnivora, and the Babirusa from the Indo-Malayan and

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Indo-Australian regions. Treubia, 20:121190. Storr, GLC. 1780. Prodromus Methodi Mammalium. Tubingen. Swainson, W. 1835. On the Natural History and Classification of Quadrupeds. London. Woollard, HH. 1925. The anatomy of Tarsius spectrum. Proceedings of the Zoological Society of London, 70, 1071-1184.


DISTRIBUTION AND BIOGEOGRAPHY OF TARSIERS Myron Shekelle Center for Biodiversity and Conservation Studies, Faculty of Mathematics and Natural Science University of Indonesia, Depok 16421, Indonesia. Email: [email protected] ABSTRACT Three clearly distinct taxa of tarsiers each inhabit a distinct biogeographic region: Western tarsiers, from island areas of Sundaland; Philippine tarsiers from Greater Mindanao; and Eastern tarsiers from Sulawesi and nearby islands. Multiple species and / or subspecies have been described from each region, and continued investigations into the alpha taxonomy of each group are warranted. Within each region tarsiers currently have discontinuous distributions, at least partly the result of anthropogenic habitat alterations. Their presence in a variety of primary and secondary habitats indicates that the historical distribution of tarsiers may have once been much more continuous, perhaps limited more by elevation and ocean barriers than by variation among lowland habitats. The distributions of Philippine and Eastern tarsiers conform well to Ice Age landmasses. The distribution of Western tarsiers does not, and is hypothesized to indicate a Holocene range expansion. A model of historical biogeography is here presented, wherein events in the Miocene led to the isolation of the three species groups. Tarsiers’ last appearance in the fossil record of mainland Asia also occurs during the Miocene.

Keywords: Tarsius, Taxonomy

INTRODUCTION All known tarsier taxa are distributed either allopatrically or parapatrically; there is not a single known case of sympatric tarsiers. Understanding their geographic distributions, therefore, is crucial for understanding tarsier taxonomy. Extant tarsiers have a curious distribution on a scattering of southeast Asian islands. They are found on both sides of Wallace’s Line, which approximates the separation between the Asian and Australian biotic communities, and although fossil tarsiers are found on mainland Asia, none exist there today (Hill 1955, Niemitz 1984, Musser & Dagosto 1987). Hill (1953, 1955) classified tarsiers into three species, all in the genus Tarsius and each endemic to a distinct biogeographic region: Tarsius syrichta Linnaeus, 1758, from islands of the southern Philippines; Tarsius spectrum Pallas, 1778 from Sulawesi and surrounding islands; and Tarsius bancanus Horsfield, 1824, from various islands of the Sunda Shelf including Borneo, southern Sumatra, Bangka, Belitung, the Karimata Islands, the South Natuna Islands, and several smaller islands. BrandonJones et al. (2004) provided an argument, which was greatly elaborated on by Groves et al. (this volume), that T. tarsier Erxleben, 1777 is a senior subjective synonym of T. spectrum (Fig. 1).

There are several conspicuous anatomical features that are diagnostic of each species group. Relative eye size is largest in Western tarsiers, smallest in Eastern tarsiers, and intermediate in Philippine Tarsiers, while relative ear length is largest in Eastern tarsiers, smallest in Western tarsiers, and intermediate in Philippine tarsiers (Niemitz 1984). The mid-tarsal segment appears naked or nearly naked in Philippine tarsiers, but is well-furred in both Eastern and Western tarsiers. The tails of all tarsiers are long and superficially rat-like, but the amount of fur varies among the species groups. Eastern tarsiers have the most fur on the tail, its appearance being almost like a bottlebrush. Philippine tarsiers have the least fur on the tail, with very short, sparse hairs that are almost invisible unless viewed at close range (although the tail tufts in a large collection of T. syrichta carbonarius from Mindanao, in Chicago’s Field Museum, approach the condition seen in T. bancanus, unpublished data). Western tarsiers are intermediate, having a noticeable tuft of fur on the tail, but not nearly so much as do Eastern tarsiers (Fig. 2). Hill (1955) accepted subspecies within each of the three species he recognized, but remarked that some of these were of dubious distinctiveness. Niemitz (1984) also used the three species taxonomy, but he synonymized the bulk of Hill’s subspecies,

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Myron Shekelle - Distribution and Biogeography of Tarsiers

Figure 1: Distribution of Extant Tarsiers. The northwestern boundary of tarsiers in Sumatra is figured here as the Musi River, but this is speculative. The actual distribution is less continuous than figured here, tarsiers being rare or nonexistent in high elevations and tarsiers having gone locally extinct in many areas of intense human usage.

accepting only two subspecies of T. bancanus and two subspecies of T. tarsier (=T. spectrum). Several authors have noted that, based upon acoustic and biogeographic evidence, numerous other unrecognized taxa of tarsiers are likely to exist within T. tarsier (MacKinnon & MacKinnon 1980; Niemitz et al. 1991; Nietsch & Niemitz 1993; Nietsch & Kopp 1998; Nietsch 1999; Shekelle 2003). The trend after Niemitz has been to recognize each of Hill’s subspecies of T. tarsier as a distinct species, including: T. pumilus Miller & Hollister, 1921, (Niemitz 1985; Musser & Dagosto 1987; Groves 1998, 2001), T. sangirensis (Feiler 1990; Shekelle et al. 1997; Groves 1998, 2001), and T. pelengensis (Groves 2001). Additionally,

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Niemitz et al. (1991) described a new taxon, T. dianae, from central Sulawesi. However, Shekelle et al. (1997) surveyed tarsiers at the type localities of both T. dianae and T. dentatus, Miller & Hollister, 1921 and found the same acoustic form at both locations, indicating that T. dianae is quite likely a junior subjective synonym of T. dentatus. Other forms, not included in Hill’s list of T. tarsier subspecies have since been described, including T. lariang (Merker and Groves 2006) from central Sulawesi and T. sp. (Shekelle et al. in press), an insular population from Siau Island, North Sulawesi (Table 1). Tarsiers from Sulawesi are now recognized as a species complex with at least seven species and


Western tarsier

Philippine tarsier

Eastern tarsier

Figure 2: Anatomical variation among tarsier species groups. Western tarsiers have the largest eyes, shortest ears, and longest legs and hands. Eastern tarsiers have the smallest eyes, longest ears, and shortest legs and hands. Philippine tarsiers are intermediate in all of these. Eastern tarsiers have the furriest tail, Philippine the least furry, and Western tarsiers are intermediate. The mid-tarsal segment of the hind foot is nearly naked in Philippine tarsiers, but is wellfurred in both Western and Eastern tarsiers (adapted from Shekelle 2003). Photos Myron Shekelle (c) 2008, except where noted.

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Table 1: Review of Tarsier Taxonomy. Hill 1955 T. syrichta syrichta T. s. carbonarius T. s. fraterculus T. bancanus bancanus T. b. borneanus T. b. saltator

T. syrichta

Musser & Dagoso 1987 T. syrichta

*

**

*

**

T. b. bancanus

T. bancanus

T. b. bancanus

T. b. borneanus *

**

T. b. borneanus T. b. saltator

T. b. natunensis T. spectrum T. s. sangirnesis T. s. pumilus

*

**

T. spectrum *

T. spectrum **

T. b. borneanus T. b. saltator T. b. natunensis T. spectrum T. sangirnesis

T. b. natunensis T. spectrum T. sangirnesis

T. b. borneanus T. b. saltator T. b. natunensis T. spectrum T. sangirnesis

T. s. pumilus * *

T. pumilus

T. pumilus

T. pumilus

T. pumilus

** **

*** T. pelengensis

T. dentatus T. pelengensis

T. dentatus T. pelengensis

T. s. dentatus T. s. pelengensis

Niemitz 1984

**

Groves 2001 T. syrichta

Brandon-Jones 2004 T. syrichta

T. syrichta

T. s. carbonarius T. s. fraterculus T. b. bancanus

T. s. carbonarius T. s. fraterculus T. b. bancanus

T. dianae***

This Paper

T. lariang T. sp. (Siau)

* **

Niemitz found museum specimen variation to be insignificant among several taxa accepted by Hill Musser and Dagosto found museum specimen variation to be an insufficient basis for determining the validity of several taxa accepted by Hill *** cited Shekelle et al. 1997 for noting a likely conflict between T. dianae and T. dentatus. **** according to Brandon-Jones et al., a taxon “whose recognition is doubtful and requires further investigation”

probably more, and it now seems plausible that each of Hill’s three tarsier species may be a cluster of closely related taxa. To sidestep the current debates on the numbers of taxa and their formal names, I refer to Hill’s three species—T. syrichta, T. tarsier (i.e. T. spectrum), and T. bancanus—by the common names, Philippine, Eastern, and Western tarsiers, respectively, with the assumption that each of these is monophyletic and that each might be a constellation of related taxa, that is, species groups. The assumption of monophyly within species groups has not been exhaustively examined, but is consistent with the results of Musser & Dagosto (1987) and Groves (1998). Musser & Dagosto (1987) indicated that their morphologic analysis of museum specimens supported two distinct clades of tarsiers, a T. bancanus / T. syrichta clade, and a T. tarsier / T. pumilus clade. Groves (1998) went further and

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suggested generic separation of the Eastern tarsiers from a Philippine-Western tarsier clade based upon his own analyses of morphological variation. Genetic data (Shekelle et al. 2001; Meireles et al. 2003) indicate that generic separation of Philippine and Western tarsiers might also be warranted if one were to accept a time-based classification scheme, such as proposed by Goodman et al. (1998) and Groves (2001). The value of designating new tarsier genera is that each species group could be addressed by a formal name (as opposed to the common names, Eastern, Western, and Philippine tarsiers, for example); and, if taxonomy is to be an information retrieval system, it might symbolically emphasize the underappreciated variation among tarsier species groups in taxonomy, behavior, and ecology (see Shekelle 2003). Nevertheless, for the time being I prefer to retain a single genus for extant tarsiers for the reasons that:


(1) Tarsius as used by Hill is a clearly defined monophyletic clade with only three species; (2) taxonomic variation in addition to that accepted by Hill, and the question of whether or not Hill’s subspecies should be elevated to full species level is the focus of much ongoing research and debate; and (3) the monophyly of each of Hill’s three species groups, although seemingly sensible, has not been rigorously tested. Thus, the dangers of classifying tarsiers in one or two new genera at this point are that ongoing research might show either or both of them to be either monotypic or not monophyletic. Previous Estimates Before estimating the historical distribution of tarsiers, I review previous work to examine how current knowledge helps resolve discrepancies, errors, and omissions. Regarding erroneous reports there are claims of tarsiers having originated from outside the range listed by Hill (1955), Niemitz (1984), and Musser & Dagosto (1987), including the islands of Luzon, Ambon, Savu, Java, and even Madagascar. Cabrera (1923) questioned the accuracy of Camel’s (1705) report of tarsiers from Luzon, and there are no longer serious discussions of Luzon being within the historical range of tarsiers. Fischer (1804) reported that tarsiers in his study were allegedly from Madagascar, but he went on to infer that Madagascar had been confused with Makassar, a port city on Sulawesi. Hill (1955) discounted Pallas’s (1778) report of tarsiers from Ambon. Reports of tarsiers from Java and nearby Savu are still sometimes treated seriously by researchers (e.g., Niemitz 1984). Savu (= Sabu) is south of Flores in the Lesser Sunda Island chain. The nearest known tarsier populations are those in South and Southeast Sulawesi, from which Savu is separated not only by hundreds of kilometers of open ocean in the Flores Sea, but also by the island of Flores itself. It is separated from Sumatran tarsiers and hypothetical Javan tarsiers by the islands of Bali, Lombok, Sumbawa, and Sumba. Thus any dispersal for tarsiers to Savu would not only have to cross expanses of open ocean, but would also have to skip over one or

more intervening islands along the route. It would give tarsiers a strikingly discontinuous distribution – much more so than they already have. Given the lack of any additional reports of tarsiers from Savu, it seems prudent to assume that Savu is outside the range of tarsiers. Jentink (1892) provides two Javan locales for tarsiers, Surabaya and Preanger (near Bandung). The possibility of tarsiers on Java is more plausible than Savu and warrants careful consideration. Tarsiers are present on Sumatra. Sumatra and Java were a single landmass as recently as the last ice age. So, it is conceivable that tarsiers had a historical distribution on Java. Contrary to this, however, there is no evidence of tarsiers on Java today. This leaves three possibilities: 1.Tarsiers are present on Java today but their presence has gone unnoticed. 2.Tarsiers are locally extinct on Java today, but were present in Jentink’s time. 3.The historical distribution of tarsiers does not include Java and Jentink’s records are erroneous, possibly owing to specimens transported from elsewhere and purchased at the localities provided by Jentink. I argue that the weight of the evidence argues for the third possibility. Regarding the first possibility listed above, tarsiers are small, nocturnal, and cryptic by nature, such that the possibility that their presence has gone unnoticed in one or more areas should not be discounted— at least until an experienced tarsier field biologist has conducted surveys. Tarsiers are recorded in the wet lowlands of Way Kambas National Park, just across the Sunda Straits from Java in the province of Lampung on the island of Sumatra (Yanuar and Sugardjito 1993). The most extensive pristine lowland habitat on Java today is Ujung Kulon National Park, at the extreme western end of Java, surrounded on three sides by the Sunda Straits and less than 200 km from Way Kambas. If the historical distribution of tarsiers were to include Java, it is highly probable that their distribution would include the Ujung Kulon area. Ujung Kulon National Park has been the subject of several field surveys, including some that have used

17


nocturnal camera trapping, without any evidence of tarsiers (Whitten et al. 2002). Indeed, one experienced tarsier field biologist has been surveying Ujung Kulon National Park for more than 20 years with no evidence whatsoever of tarsiers, while he was able to easily locate them in Bukit Barisan Selatan National Park, less than 200 km from Ujung Kulon on the southern end of Sumatra; his opinion is that the evidence is overwhelming that tarsiers are not present in Ujung Kulon (Haerudin R. Sadjudin of Yayasan Cipta Citra Lestari, personal communication). The possibility that tarsiers have gone locally extinct on Java might seem plausible, even likely, if one adopted a misconception that tarsiers are relictual taxa clinging to survival in their isolated island homes. Several lines of evidence counter this assumption, however. First, nearly 40 years of field research contradict the misconception that tarsiers, being a relictual taxon, are therefore teetering on the precipice of extinction. On the contrary, tarsiers have been found to be a weedy animal that exists in high densities in a remarkable array of habitats and varying human use (Niemitz 1984, Merker 2003, Shekelle 2003). Indeed, Island Biogeography Theory predicts that it is unlikely for tarsiers to have gone locally extinct on an island as large as Java, while they persist on tiny islands such as Sangihe, Siau, Serasan, and Subi. Nevertheless, the human population density of Java is among the highest in the world, and several Holocene extinctions are known to have occurred there, such as the Javan tiger. The wet lowland habitat of Ujung Kulon is suitably pristine to support the only remaining population of the Javan rhinoceros on Java. It seems unlikely that tarsiers, with a home range of a few hectares at most, could have gone locally extinct from Ujung Kulon, and indeed all of Java, while rhinoceroses remain. Thus, strong evidence exists that tarsiers are currently absent from Ujung Kulon National Park. By comparison with a much more vulnerable taxon, the Javan rhino, we can extrapolate that it is unlikely that tarsiers exist on Java today, or did so in the past. The most reasonable assumption is that the historical distribution in Sundaland stops at the Sunda Straits, and the two records of tarsiers on Java in Jentink—

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the only evidence of tarsiers on Java— are erroneous, and direct examination of the specimens might shed further light. Hill’s (1955) distribution map of the genus Tarsius (upon which most subsequent research has been based) includes a few discrepancies from what is known today. For instance, he shows T. bancanus natunensis as being from the North Natuna Islands, and absent from the South Natuna Islands, when in fact, the actual distribution is the reverse (Chasen 1940). Hill omits Basilan, off the southwestern tip of Mindanao, from the range of the Philippine Tarsier, but Musser & Dagosto (1987) list specimen 35256 from the Museum of Comparative Zoology, Harvard University (MCZ) as being from Basilan. Likewise, Biliran Island, off the northern tip of Leyte is excluded from the range of Philippine Tarsiers, but NeriArboleda et al. (2002) list Biliran as having tarsiers. Hill’s map shows a spotty, discontinuous distribution of Eastern tarsiers that entirely omits the southwestern peninsula of Sulawesi, even though Hill himself identified the type locality of T. spectrum as Makassar (= Ujung Pandang). Indeed, evidence from museum specimens indicates that the distribution of Eastern tarsiers is far more continuous than appears in Hill’s map (Musser & Dagosto 1987), and subsequent field surveys have found tarsiers almost everywhere they have been looked for (e.g. MacKinnon & MacKinnon 1980; Nietsch 1999; Nietsch & Kopp 1998; Nietsch & Babo 2001, Nietsch & Burton 2002; Shekelle 2003, Shekelle & Leksono 2004). Likewise, Tarsius bancanus borneanus is marked by Hill (1955) as present in coastal regions of Borneo, but not the central regions (generally of higher elevation), perhaps because this species was thought to be present only in extreme lowlands (e.g. Clark 1924). Gorog and Sinaga’s (this volume) capture of a tarsier from the montane interior of Borneo contradicts both Clark and Hill. Distribution maps in Hill (1955), Niemitz (1984), and Musser and Dagosto (1987) all show the distribution of tarsiers on the west coast of Sumatra as extending northward about to the city of Bengkulu. On the east coast, however, Niemitz (1984) and Musser and Dagosto (1987) show the distribution stopping at what appears to be the Musi River, while Hill’s map


shows it extending further to what is possibly the Hari River. All three depict a predominantly coastal distribution. Hard evidence to resolve this discrepancy is lacking, but anecdotal reports from locals indicate that tarsiers are not present in the vicinity of the Hari River. Musser & Dagosto (1987) omit the Buton Island chain from the distribution of Eastern Tarsiers, but subsequent field surveys by Nietsch & Burton (2002) reported tarsiers from Kabaena and Buton. They are presumably on Muna, as well, but owing to deforestation, Burton was unable to locate any (Nietsch, personal communication). Musser & Dagosto (1987) omit Subi Island, although it is biogeographically linked to Serasan (see Banks 1949). Suroso Leksono reported that during surveys in 2003, inhabitants of Subi claimed tarsiers existed there, although he did not see them himself (personal communication). An Hypothesis of The Historical Extent of Occurence In the following sections, I hypothesize the historical extent of occurrence for tarsiers. These hypotheses are meant to be refutable statements that can be corrected by future field surveys and more careful examination of available museum specimens. The hypotheses are based on the assumption that historical distributions on landmasses known to contain tarsiers are limited more by elevation than by habitat type, but regions of high elevation are not specifically excluded from the distribution maps for reasons of practicality. Tarsier densities vary by habitat type (see Merker 2003) and the hypothesis that the presence of tarsiers in various sub-optimal habitats, such as agroforestry and alang-alang, could represent sink populations has not been examined (Wright 2003). In many cases, evidence is lacking (e.g. the precise limit of the distributions of Western and Philippine tarsiers in the Jolo archipelago, the precise eastward limit of Eastern tarsiers in the Banggai Islands, etc.). In other cases, the data (or distribution maps, rather) are conflicting (e.g. the northwestern boundary of Western tarsiers on Sumatra being the Musi River or the Hari River, etc.).

Eastern Tarsiers To the east of Wallace’s Line, I hypothesize a historical distribution of Eastern tarsiers that is nearly continuous on Sulawesi and surrounding islands, including all land areas that were exposed during the Ice Ages (Fig. 3). Tarsius pumilus, a montane endemic, is known from three specimens collected between 1800-2200 m in elevation (Miller & Hollister 1921, Musser & Dagosto 1987, Maryanto & Yani 2004). Records of other Eastern tarsiers, of the T. tarsiercomplex, exist from sea level to 1500 m (MacKinnon & MacKinnon 1980; Musser & Dagosto 1987; Shekelle 2003). Eastern tarsiers have been recorded in almost all habitats except areas with dense human populations, areas of intensive agriculture where all potential sleeping sites have been cleared, and areas where pesticides and / or herbicides are used intensively (MacKinnon & MacKinnon 1980; Shekelle et al. 1997; Leksono et al. 1997). Any current gaps in the distribution of Eastern tarsiers are hypothesized to be recent events owing to human activity, such as habitat destruction. The range of these tarsiers extends to the offshore island groups of Togian (Nietsch & Niemitz 1993; Shekelle et al. 1997), Banggai (Sody 1949), Selayar (Musser & Dagosto 1987; Nietsch & Babo 2001), and Buton (Nietsch & Burton 2002). A chain of volcanic islands leads north from the northernmost tip of Sulawesi, and of these, at least Siau and Greater Sangihe are known to have tarsiers (Meyer 1897). The neighboring limestone islands of the Talaud chain do not, however (Yunus Masala, Forest Ranger, North Sulawesi, personal communication). Nor does it seem that tarsiers have crossed the narrow Salue Timpaus Strait to the Sula Islands—Taliabu, Mangole, and Sanana—as there are no records of tarsiers from there, although Whitten et al. (2002) indicate that these are geologically part of Sulawesi. Similarly, there is a chain of islands, the Bonerate Islands, which run southeast from Selayar into the Flores Sea toward the Lesser Sunda Islands, from which there are no reports of tarsiers. The same is true for the Tukang Besi Archipelago, southeast of Buton Island. Several species of Eastern tarsiers have been described. Reviews are found in Hill (1955), Niemitz

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(1984), Musser & Dagosto (1987), Groves (1998, 2001), Shekelle (2003) and Brandon-Jones et al. (2004). Excluding known synonyms, these include Tarsius tarsier Erxleben, 1777 (type locality most probably Makassar, South Sulawesi); T. sangirensis Meyer, 1897 (type locality, Greater Sangihe Island*, North Sulawesi); T. pumilus Miller & Hollister, 1921 (type locality, Rano Rano, Central Sulawesi); T. dentatus Miller & Hollister, 1921 (type locality, Labua Sore, Central Sulawesi); T. pelengensis Sody, 1949 (type locality, Peleng Island, Central Sulawesi), T. lariang Merker and Groves, 2006 (type locality, Gimpu, Central Sulawesi), and T. sp. (Shekelle et al. in press) (type locality, Siau Island, North Sulawesi) (Fig. 4). Several other populations probably warrant taxonomic separation (MacKinnon & MacKinnon 1980; Nietsch & Niemitz 1993; Shekelle et al. 1997; Nietsch & Kopp

1998; Groves 1998; Shekelle 2003; Brandon-Jones et al. 2004). Notably, Sulawesi is the only place with parapatrically distributed tarsiers (e.g. T. dentatus and T. lariang). *Sangi and Sangir are alternate spellings of Sangihe. **Laboea Sore, Labuan Sore, and Laboean Sore are all alternate spellings of Labua Sore. Philippine tarsiers The current distribution of Philippine tarsiers is thought to be spotty, but I hypothesize a historical distribution that was nearly continuous on islands that made up the ice age landmass of Greater Mindanao (Heaney 1985) (see also Neri-Arboleda 2002) (Fig. 5). This includes Mindanao, Samar, Leyte, and Bohol, as well as the smaller islands of Siargo, Dinagat, Basilan,

Figure 3: Distribution of Eastern Tarsiers—schematic (left) and satellite (right) views. The hypothesized historical range of these tarsiers extends as far west and north as Wallace’s Line (1), and includes the island of Sulawesi and the offshore island groups of Togian (2), Banggai (3), Selayar (4), Buton (5), and Sangihe (6). The northwestern limit of the range of Eastern Tarsiers lies between Sangihe Island and the Talaud Island chain to the northeast (7). Eastwards, it appears that the range is bounded by the Salue Timpaus Strait (8). From the southwestern peninsula, the distribution stops between Selayar Island and the Bonerate Islands (9), and from the southeastern peninsula, the boundary lies between the Buton Islands and the Tukang Besi Islands (10).

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Figure 4: Map of Eastern Tarsier type localities, with the names as they appeared in the original descriptions. The type localities of both T. dentatus and T. dianae are illustrated for reference, although they are now treated as synonyms.

Biliran, and many others. Although commonly thought of as an exclusively lowland taxon (e.g. Fulton 1939; Wharton 1950; Dagosto & Gebo 1997; Neri-Arboleda et al. 2002), Gorog & Sinaga (this volume) review evidence for Philippine tarsiers above 800 m. They have been recorded from a variety of primary and secondary habitats (Rickart et al. 1993; Dagosto & Gebo 1997; Neri-Arboleda et al. 2002). I find no records of tarsiers from Palawan, or other islands that extend from the northwest corner of Borneo, and neither Hill (1955), nor Niemitz (1984), nor Musser & Dagosto (1987) indicate that these regions have (or have ever had) tarsiers. Tarsiers have not crossed the narrow straits that separate Samar from Luzon, Leyte from Masbate, nor Bohol from Cebu. The Jolo Archipelago makes a logical dispersal corridor between Borneo and Mindanao, but I can find no records of tarsiers there, other than from Basilan near the southwestern tip of Mindanao (Musser & Dagosto 1987). Dagosto et al. (2003) state that tarsiers are absent from this archipelago, except for Basilan. Three subspecies of Philippine tarsiers have been described, but their taxonomic distinctiveness has been questioned (Hill 1955; Niemitz 1984; Musser

& Dagosto 1987; Groves 2001; Brandon-Jones et al. 2004). These include: Tarsius syrichta syrichta Linnaeus, 1758, (type locality, Samar); Tarsius syrichta fraterculus Miller, 1910, (type locality, Bohol), and T. s. carbonarius Heude, 1899 (type locality, Mindanao). Tarsiers from other islands are classified as T. s. syrichta, but this gives that taxon an illogically disjunct distribution, and other classifications are more probable. For instance, should T. s. carbonarius warrant taxonomic separation, then tarsiers from Basilan Island are more likely referable to T. s. carbonarius. Western tarsiers The Western tarsier has, perhaps, the most curious distribution of all in that it has an incomplete distribution on the ice age landmass, Sundaland (Fig. 6). Western tarsiers are recorded from several parts of Borneo, where I hypothesize a historical distribution that is nearly continuous. They have also been found in southern areas of Sumatra and a few smaller islands including Bangka, Belitung, the Karimata Islands, and the South Natuna Islands (Chasen 1940, Hill 1955, Musser and Dagosto 1987). Like other tarsiers,

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Figure 5: Distribution of Philippine Tarsiers—schematic (left) and satellite (right) views. Philippine Tarsiers have been found on islands that composed the ice age landmass, Greater Mindanao. These include Mindanao (1), Samar (2), Leyte (3), Bohol (4), and many smaller islands. Tarsiers have not been reported from Palawan (5) nor other islands that extend from the northwestern tip of Borneo. The northern extent of the range of these tarsiers is the narrow strait that separates Samar from Luzon (6). Philippine Tarsiers have not crossed the narrow expanse of ocean that separates Leyte from Masbate (7) to the north and Cebu (8) to the west. Similarly, tarsiers from Bohol have not crossed the narrow straits that separate Bohol from Cebu (9). Tarsiers are recorded from Basilan, off the southwestern tip of Mindanao, but their presence in the Jolo archipelago (between 10 and 11) is uncertain, although this is a logical dispersal corridor between Borneo and Mindanao. Wallace’s Line (12) demarcates the southern and eastern limits of the Philippine Tarsiers.

Western tarsiers have been recorded from a variety of primary and secondary habitats (Clark 1924, Fogden 1974, Niemitz 1979, Crompton and Andau 1986). As with Philippine tarsiers, Western tarsiers are most often recorded as a lowland species from sea level to 100200 m (e.g. Clark 1924), but Gorog and Sinaga (this volume) report a tarsier capture from 1200 m on Borneo. The entire extent of occurrence of Western tarsiers is on the Ice Age landmass Sundaland, but not all of Sundaland has tarsiers. For instance, tarsiers are absent from the Asian mainland, all areas of Sumatra except the southernmost tip, and the North Natuna Islands. Also, there are no credible accounts of tarsiers on Java or Bali. I hypothesize the northwestern boundary of tarsiers in Sumatra to be the Musi River, as did Musser and Dagosto (1987), but this has not been confirmed with surveys and other possibilities exist, such as the Hari River (Hill 1955). Four subspecies of Western tarsiers have been described, but again, their taxonomic

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distinctiveness has been questioned (Hill 1953, 1955, Niemitz 1984, Musser and Dagosto 1987, Groves 1998, 2001, Brandon Jones et al. 2004). These include: Tarsius bancanus bancanus Horsfield, 1821, (type locality, Jebus (=Jeboos), on the northwest tip of the island of Bangka); Tarsius bancanus borneanus Elliot, 1910, (type locality, Borneo), T. b. saltator Elliot, 1910, (type locality, Belitung (=Beliton), and T. b. natunensis Chasen, 1940, (type locality, Serasan Island). Biogeographic Inferences Several authors have inferred that extant tarsiers are closely related taxa (e.g. MacKinnon and MacKinnon 1980, Musser and Dagosto 1987, Simons 2003), but that otherwise reasonable inference appears to be contradicted by genetic data that indicates that the origin of all three clades dates to the Miocene. Meireles et al. (2003) used nDNA for a molecular clock estimate of 5.6 mya for the split between Western and Philippine tarsiers. Preliminary results of mtDNA sequence data reported by Shekelle et al. (2001) that


Figure 6: Distribution of Western Tarsiers—schematic (left) and satellite (right) views. Western Tarsiers presumably have a nearly ubiquitous historical distribution on Borneo (1). They have also been found on southern parts of Sumatra (2), Bangka (3), Belitung (4), and the South Natuna Islands (5). They have not been recorded from the Asian mainland (6), most of Sumatra (7), the North Natuna Islands (8), nor are there reliable reports from Java (9). The eastern extent of their distribution is Wallace’s Line (10). To the north, their distribution is limited somewhere in the Jolo Archipelago (11, 12), and somewhere before the Philippine island of Palawan (13). Their westward distribution corresponds with the drowned riverbed of the ice age Sunda River (14), and one of its modern day tributaries, shown here as the Musi River (15). Western Tarsiers did not cross the Sunda Straits (16), nor did they disperse south of Borneo (17).

found Philippine, Eastern, and Western tarsiers to be an unresolved trichotomy that most likely dates to the middle Miocene. In the preliminary analysis, genetic distances among Philippine, Eastern, and Western tarsiers were nearly as great as the average genetic distances among hominoids. The average genetic distance among the three tarsier species groups was 0.1157, while the average genetic distance for Hylobates vs. Homo and Pan was 0.1272. Even allowing for unequal rates of evolution, it is most likely that Philippine, Eastern, and Western tarsiers are not particularly closely related taxa. Morley (1998) found evidence of biotic exchange across the Makassar Straits in palynological data at 17 mya, 14 mya, 9.5 mya, 3.5 mya, and 1 mya. The genetic data reported by Shekelle et al. (2001) are most consistent with tarsiers crossing the Makassar Straits at any of the three older dates identified by Morley, and least consistent with the two younger dates. Hall (2001) identified the most likely time for faunal exchange across the Makassar Straits as being about 10 mya, based upon reconstructions of tectonic activity. Mercer and Roth (2003) used a molecular

clock date to estimate the arrival of squirrels to Sulawesi as approximately 11.5 mya, indicating that at least some of the small terrestrial mammals from Sulawesia are as ancient as I hypothesize for tarsiers. The last known record of tarsiers from mainland Asia is a Miocene fossil from Thailand (Ginsburg and Mein 1986). There is an intriguing synchronicity, therefore, between the fossil record, the estimated divergence of extant tarsiers based on mtDNA, the molecular clock date for squirrels, and two independent predictions for biotic exchange across the Makassar Straits, all during the middle Miocene. It is worth noting that both Musser and Dagosto (1987) and Groves (1998) argued that Philippine and Western tarsiers form a clade relative to Eastern tarsiers based on morphological data. Such a tree topology is consistent with this hypothesis. Results of the preliminary mtDNA analysis found an unresolved trichotomy, but this does not imply a trifurcation. Some inferences about tarsier biogeography within species groups can be drawn from the estimated historical distributions. Notably, the incomplete distribution of Western tarsiers on Sundaland

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contrasts sharply with the distributions of Philippine and Eastern tarsiers that cover all of Greater Mindanao and Sulawesi, respectively. At first glance, one might invoke the paradigm that tarsiers are a relictual taxon and are experiencing a gradual range reduction in Sundaland. An alternative hypothesis, however, is that Western tarsiers experienced a marked range expansion at the end of the last ice age. Banks (1949) hypothesized that the ice age Sunda River, which flowed northward from Sumatra and between the North and South Natuna Islands, formed an east-west faunal boundary in Sundaland. Brandon-Jones (1996) further hypothesized that large tracts of Sundaland were too dry to support habitat suitable for tropical primates in much of the Pleistocene. His hypothesis includes the prediction that many tropical primates experienced marked Holocene range expansions throughout Sundaland as Holocene climatic patterns permitted the spread of wetter, more suitable habitats (see also Meijaard 2003). The Western tarsiers appear to fit the predictions of both Banks and BrandonJones. The historical distribution of Philippine tarsiers is, essentially, a perfect fit with the ice age landmass, Greater Mindanao. They are typically regarded as a lowland species, but have been recorded above 800 m. Other than elevation, there are no known ecological constraints that would restrict their historical distribution throughout much of Greater Mindanao. It is not known when tarsiers dispersed to the Philippines, nor from where, but it is probable that they have been genetically isolated from other tarsiers since the Miocene, as mentioned previously. The subspecies of Philippine tarsiers recognized by Hill (1955) are allopatric populations on islands that separated after the end of the last ice age, implying a relatively short time frame for differentiation of Philippine tarsier populations. Thus, the current best guess for diversification within Philippine tarsiers is that a panmictic population on Greater Mindanao became fragmented as ocean levels rose at the end of the last ice age. Other possibilities should not be overlooked, however, given the several million years that Phillipine tarsiers were isolated from Western and Eastern tarsiers, including the possibility of deeper

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biogeographic patterns on Greater Mindanao, such as are present on Sulawesi. Dagosto et al. (2003) cited evidence that the Zamboanga peninsula is geologically part of Sundaland, and accreted onto the main body of Mindanao about 5 mya, with the first evidence of emergent land in the late Miocene. These events seem to be conspicuously coincidental to the 5.6 mya molecular estimate for the origins of the Philippine tarsier clade. Additionally, they point out that changing ocean levels have subsequently rearranged the configuration of emergent land in Greater Mindanao several times, creating possibilities for vicariance events that could promote taxonomic diversity, such as is seen in Sulawesi. Unfortunately, the museum specimens of Philippine tarsiers are heavily concentrated from the Davao region of Mindanao (51 out 60 specimens examined by Dagosto et al. 2003), and field studies are hampered the Philippine tarsiers’ lack of a duet call with which to survey them and provide an initial estimate of population subdivision. The historical distribution of Eastern tarsiers includes all areas of Sulawesi that were exposed during the ice ages, as well as several landmasses that probably were not contiguous with Sulawesi during those times, including the Sangihe Islands, Banggai Islands, Togian Islands, and Selayar. There is a montane form recorded from three localities between 1800-2200 m. Lowland forms are common up 1100 m (Merker 2003), and have been recorded up to 1500 m (MacKinnon and MacKinnon 1980). It is not known when tarsiers migrated to Sulawesi, nor from where, but it is probable that they have been genetically isolated from other tarsiers since the Miocene, and almost certainly predate the coalescence of Sulawesi into a single landmass from a diverse archipelago (Hall 2001). The parapatric tarsiers on Sulawesi are hypothesized to be evidence of this ancient archipelago (Shekelle and Leksono 2004). Eastern tarsiers, therefore, are like the reverse of Philippine tarsiers; several allopatric populations were isolated on different islands, and then brought together by tectonic activity in the last 1-2 million years to form parapatric populations.


Several generalizations can be drawn from the historical distributions of tarsiers hypothesized above. First, tarsiers are found in almost all lowland habitats that have not been severely degraded. Second, tarsier distributions are limited by elevation, the maximum reported elevation for Eastern tarsiers is 2200 m, for Western tarsiers is 1200 m, and for Philippine tarsiers is in excess of 800 m. Some of these differences could be sampling error, but an endemic montane species is recorded from Sulawesi, as opposed to Sundaland and the Philippines for which there is no known endemic montane tarsier. Mountain ranges limit dispersal to higher elevations, but are not known to form barriers to dispersal around the flanks. Third, other landforms, such as rivers are not effective barriers to tarsier dispersal over geologic time. In only a single instance is a river hypothesized to be a species boundary, i.e. the northern boundary of T. bancanus on Sumatra. Fourth, the chief barrier to dispersal in almost all instances is open ocean. Only on Sulawesi are parapatric tarsier populations known, and many of the contact zones are interpreted as evidence of an ancient archipelago, one that is predicted by geologic data. Finally, the presence of tarsiers on both sides of Wallace’s Line might suggest a certain aptitude for rafting across open ocean over geologic time intervals. The fact that tarsiers have not crossed numerous narrow ocean straits in the Philippines and Sulawesi, however, conflicts with this assessment, and successful dispersal by rafting is probably very rare for tarsiers. ACKNOWLEDGEMENTS This material is based on work supported by the National Science Foundation under Grant No. INT 0107277, and by a grant from the Margot Marsh Biodiversity Foundation. Portions of this appeared in the dissertation of M.S. and I thank Washington University in St. Louis and my thesis committee. Erik Meijaard, Vincent Nijman, Antonio Gorog, Colin Groves, and Matt Richardson reviewed this manuscript and offered helpful criticism.

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MacKinnon, J, K. MacKinnon. 1980. The behavior of wild spectral tarsiers. International Journal of Primatology 1(4):361-379. Maryanto, I & M. Yani. 2004. The third record of pygmy tarsier (Tarsius pumilus) from Lore Lindu National Park, Central Sulawesi, Indonesia. Tropical Biodiver-sity. 8(2):79-85. Meijaard, E. 2003. Mammals of south-east Asian islands and their Late Pleistocene environments. Journal of Biogeography 30(8):1245-1257. Meireles, CM, J. Czelusniak, SL. Page, DE. Wildman, & M. Goodman. 2003. Phylogenetic position of tarsiers within the order Primates: evidence from γ–globin DNA sequences. In Tarsiers: Past, Present, and Future. Wright PC, Simons EL, Gursky S. (eds) pp:145-160. New Brunswick: Rutgers UP. Mercer, JM, & VL. Roth (2003). The effects of Cenozoic global change on squirrel phylogeny. Science 299:1568-1572. Merker, S. 2003. Vom Aussterben bedroht oder anpassungsfaehig? - Der Koboldmaki Tarsius dianae in den Regenwaeldern Sulawesis. PhD-Dissertation, University of Goettingen, Germany. Merker, S. & CP. Groves. 2006. Tarsius lariang: A new primate species from western central Sulawesi. Int. J. Primatol. 27: 465–485. Meyer, AB. 1897. Säugethiere vom Celebes- und Philippinen-Archipel, I. Abhandlungen und Berichte des Kaiserlich Zoologis-che und A n t h r o po l o g i s c h e - E t hn o l o gi s - c h e n Museums zu Dresden, 6: I–VIII, 1–36. Miller, Jr. GS, & N. Hollister. 1921. Twenty new mammals collected by H. C. Raven in Celebes. Proceedings of the Biological Society of Washington 34:93-104. Morley, RJ. 1998. Palynological evidence for tertiary plant dispersals in the SE Asian region in relation to plate tectonics and climate. In Biogeography and Geologi-cal Evolution of SE Asia. Hall R, Holloway JD (eds) pp:211234. Leiden: Backhuys.


Musser, GG & M. Dagosto. 1987 The identity of Tarsius pumilus, a pygmy species endemic to the montane mossy forests of Central Sulawesi. American Museum Novitates 2867:1-53. Neri-Arboleda I, P. Stott & NP. Arboleda. 2002. Home ranges, spatial movements, and habitat associations of the Philippine tarsier (Tarsius syrichta) in Corella, Bohol. J. Zool. Lond. 257:387-402. Niemitz, C. 1979. Results of a field study on the Western tarsier (Tarsius bancanus borneanus Horsfeld, 1821) in Sarawak.” Sarawak Museum Journal 27 (1979a): 171228. Niemitz, C. 1984. Taxonomy and distribution of the genus Tarsius Storr, 1780. In Biology of Tarsiers. Niemitz C. (ed) pp:1-16. New York: Gustav Fischer Verlag. Niemitz, C. 1985. Der Koboldmaki - Evolutionsforschung an einem Primaten. Naturwiss Runsch 38:43-49. Niemitz, C, A. Nietsch, S. Warter, & Y. Rumpler. 1991 Tarsius dianae: A new primate species from Central Sulawesi(Indonesia). Fol ia Primatologica 56:105-116. Nietsch, A. 1999. Duet vocalizations among different populations of Sulawesi tarsiers. Int. J. Primatol. 20(4):567-583. Nietsch, A & C. Niemitz. 1993. Diversity of Sulawesi tarsiers. Deutsche Gesellschaft fur Saugetierkunde 67:45-46. Nietsch, A & ML. Kopp. 1998. Role of vocalization in species differentiation of Sulawesi Tarsiers. Folia primatologica 68(suppl.1):371-378. Nietsch, A & N. Babo. 2001. The tarsiers of South Sulawesi. In Konservasi Satwa Primata. pp:114-119. Yogyakarta: Fakultas Kedokteran Hewan dan Fakultas Kehutanan Universitas Gajah Mada University - Yogyakarta. Nietsch, A & J. Burton. 2002. Tarsier Species in Southwest and Southeast Sulawesi. Abstracts, The XIXth Congress of the International Primatological Society (IPS), 49 Aug. 2002, Beijing, China: 20-21.

Pallas, PS. 1778. Novae species quad e glirium ordine cum illustrationibus variis complurium ex hoc ordine animalium. Erlangen: W. Walther. Rickart, EA, LR. Heaney, PD. Heideman, & RCB. Utzurrum. 1993. The distribution and ecology of mammals on Leyte, Biliran and Maripipi Islands, Philippines. Fieldiana Zoology 72:162. Shekelle, M. 2003. Taxonomy and biogeography of Eastern Tarsiers. Doctoral thesis. Washington University, St. Louis. Shekelle, M, SM. Leksono, Ichwan LLS, & Y. Masala. 1997. The natural history of the tarsiers of North and Central Sulawesi. Sulawesi Primate Newsletter, 4 (92):4-11. Shekelle, M, JC. Morales & DM. Melnick. 2001. Genetic and acoustic evolution among Eastern Tarsiers of northern and central Sulawesi. Presented at the International Society of Primatologists, 14th Congress, Adelaide, Australia. January 7-12, 2001. Shekelle, M, & SM. Leksono (2004) “Rencana Konservasi i Pulau Sulawesi: Dengan Menggunakan Tarsius Sebagai ‘Flagship Taxon’”. Biota 9 (1):1-10. Shekelle, M, C. Groves, S. Merker & J. Supriatna. In Press. Tarsius tumpara: A New Tarsier Species from Siau Island, North Sulawesi. Primate Conservation 2008 (23). Simons, EL. 2003. The fossil record of tarsier evolution. In Tarsiers: Past, Present, and Future. Wright PC, Simons EL, Gursky S (eds) pp:934. New Brunswick, New Jersey: Rutgers University Press. Sody, HJV. 1949. Notes on some Primates, Carnivora, and the babirusa from the Indo-Malayan and indo-Australian regions. Treubia 20:121-185. Wharton, CH. 1950. The tarsier in captivity. Journal of Mammalogy 31(3):260-268. Whitten, A, M. Mustafa, & G. Henderson. 2002. The Ecology of Sulawesi. 2 nd ed. Singapore: Periplus. Yanuar, A & J. Sugardjito. 1993. Population survey of primates in Way Kambas National Park, Sumatra, Indonesia. Tiger Paper. 30-36

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A TARSIER CAPTURE IN UPPER MONTANE FOREST ON BORNEO

1

Antonia J. Gorog1 & Martua H. Sinaga2 Museum of Zoology and Department of Ecology and Evolutionary Biology, 1109 Geddes Ave. University of Michigan 2 Indonesian Institute of Sciences (LIPI) & Museum Bogoriense, Cibinong, West Java 16911, Indonesia ABSTRACT

In November of 1998, we captured a tarsier above 1200 m elevation in West Kalimantan, Indonesia. This capture is the highest recorded elevation for a Western tarsier and is furthermore unusual in that the Bornean tarsier (Tarsius bancanus) is generally described as a lowland species. In this paper, we briefly summarize the geographic distributions and habitat associations of the seven recognized species of tarsiers, report on our high elevation capture, and discuss the implications of our finding. Keywords: Tarsius bancanus, T. syrichta, T. tarsier, T. spectrum, biogeography, habitat, elevational distribution.

INTRODUCTION The recognized species of Tarsius are restricted to Southeast Asia. T. tarsier group (or Eastern tarsiers), comprising T. tarsier (=T. spectrum, see Groves et al. this volume), T. pumilus, T. dentatus, T. pelengensis, T. sangirensis, T. lariang, and T.sp is endemic to Sulawesi and nearby small islands (Groves 2001; Shekelle this volume). Tarsius tarsier shows great geographic variation in cranial morphology (Groves 1998) and vocalization (MacKinnon & MacKinnon 1980; Shekelle et al. 1997), and is likely a complex of several species. Brandon-Jones et al. (2004) identified T. tarsier as a senior subjective synonym of T. spectrum, and accepted Makassar (Ujung Pandang) in the southwestern peninsula as the type locality. It can be inferred from Groves (1998) that the tarsier in the northern peninsula of Sulawesi, which has been the focus of most behavioral and ecological research on Eastern tarsiers (e.g., Gursky 1998; MacKinnon & MacKinnon 1980), is an unnamed species. Tarsius bancanus, the Western tarsier, is found on Borneo, Sumatra and some of the interlying islands (e.g, Banka, Belitung and Serasan). Tarsius syrichta is restricted to the Philippine islands of Mindanao, Bohol, Samar, and Leyte (Groves 2001). The Philippine and Western tarsiers, T. syrichta and T. bancanus, are generally described as lowland species (e.g., Musser & Dagosto 1997; Sussman 1999) but range into lower montane forest as well. Shekelle (personal communication) noted that

two Philippine specimens in the Field Museum of Natural History (FMNH56159 and FMNH67744) from the island of Mindanao (Davao City, Mt. McKinley, east slope, and Zamboanga, Sigayan, Katipunan, respectively) include provenence data stating that they were collected at 2500 ft (758 m). Tarsius bancanus is found in a variety of forest types including secondary growth (Le Gros Clark 1924; Niemitz 1979). Payne and Francis (1998) describe the range of this species as extending “above 900 m in the Kelabit Uplands of northern Sarawak”, in addition to lowlands of other regions of Borneo. Their upland reference probably corresponds to a single specimen in the Sarawak Museum that is identified as T. bancanus and whose associated information (Kool & Nawi 1995) includes only a collection date and a locality (12 August 1949, Bario Kelabit). The elevation at Bario is approximately 1100 m; thus, this record may represent the highest and the only previous montane record for this species. Tarsius syrichta is found in many habitats including early-mid successional forest, late successional secondary forest, agroforestry systems, primary lowland forest, and montane forest from 50 to 800 m (Dagosto & Gebo 1997; Neri-Arbodela et al. 2002; Rickart et al. 1993). Eastern, or Sulawesian, tarsiers fall into two broad ecological groups—one that occupies a diversity of habitats from lowland forests and agroecosystems to lower montane forest, and another restricted to mountain tops. The members of the T. tarsier complex have been reported from all major

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Gorog & Sinaga - A Tarsier Capture in Upper Montane Forest on Borneo

forest formations and some types of cultivated vegetation from sea level to 1500 m (MacKinnon & MacKinnon 1980) and are represented by museum specimens from this range of elevations (Musser & Dagosto 1987). Tarsius dentatus has been captured at sea level (Shekelle et al. 1997) and from 650 to 1100 m, and detected audibly from 500 to 1200 m (S. Merker, pers com), indicating an elevational distribution similar to that of the T. tarsier complex (although studies focusing on montane areas may show that it occurs higher as well). The pygmy tarsier, T. pumilus, alone is restricted to high elevation mossy forest; the species is known from only three specimens, one from 1800 m and two from 2200 m, taken in the central region of Sulawesi (Musser & Dagosto 1987; Maryanto & Yani 2004). No overlap has been reported in the altitudinal distribution of T. pumilus and other Eastern tarsiers. Findings During a survey of small mammal diversity in 1998, we captured a tarsier above 1200 m elevation in Bukit Baka-Bukit Raya National Park (BBNP) in West Kalimantan, Indonesia. To our knowledge, this represents the highest capture of a tarsier on the island of Borneo reported to date. BBNP lies in the Schwaner Range, part of the axial chain of mountains that bisects Borneo. The park spans the border between West and Central Kalimantan, lying approximately between 112°15’113°E and 0°1’-0°29’S (Jarvie et al. 1998). Bukit Baka (1600 m) and Bukit Raya (2278 m) are the two tallest mountains in Kalimantan, the Indonesian part of Borneo, and occur within the boundaries of BBNP. Our survey of small terrestrial mammals and bats was conducted on the northern slopes of Bukit Baka in an area known locally as Gunung Lubang Tedung. We accessed the region by foot from the village of Nanga Juoi, which lies within the park and to the north of Lubang Tedung. Terrestrial mammals were trapped and bats were mist-netted in each major forest formation from lowland forest at 350 m to mossy forest at 1550 m, the peak of Lubang Tedung. The KKP logging concession borders BBNP to the north and west of Bukit Baka. Thus, lowland

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forest surrounding the park is heavily disturbed or has been converted to agriculture. Lowland forest at the foot of Gunung Lubang Tedung is utilized by local Dayak people, who occasionally harvest fruits, firewood, pig, and deer in the area. However, the lower slopes of Bukit Baka in the region of Lubang Tedung have not been deforested, and support a large zone (from approximately 350 to 700 m) of healthy, intact lowland and hill dipterocarp forest dominated by canopy trees in the genus Shorea. At about 700 m, the forest undergoes a transition from lowland dipterocarp forest to montane forest dominated by Fagaceae and patchy stands of Agathis. The mossy forests of the highest elevations (occurring above ~1500 m on Lubang Tedung) are dominated by Ericaceae and support high elevation specialists such as Nepenthes and podocarps in the genera Dacrydium and Phyllocladus (Jarvie et al. 1998). On 23 November 1998, during the portion of our survey conducted in upper montane forest (Figure. 1), we captured a tarsier in a mist net (Figure 2). The elevation of the capture site was between 1200 and 1250 m, a short walk (300 m) downslope of our camp at 1300 m. The net was set on a mossy ridge in low canopy forest 15-20 m in height. The bottom of the net hung approximately 1.5 m from the ground, and the animal was removed from the net at a height of 2.5-3.0 m. We photographed it at our camp and released it at the capture site. Other small mammals captured in the upper montane habitat of Lubang Tedung include the murid rats Leopoldamys sabanus, Maxomys whiteheadi, and M. surifer, the shrew Crocidura monticola, and the montane squirrel Dremomys everetti and bat Aethelops alecto. As on several other mountains in West Kalimantan, fewer montane endemics are present than on mountains of northern Borneo. In addition, the ecological ranges of several species that in the north are generally considered to be lowland species extend well into the uplands in southwestern Borneo, demonstrating a regional lack of altitudinal zonation in most species (Gorog 2003).


Figure 1. Montane forest in BBNP near the capture site of a montane tarsier.

Figure 2: Western Tarsiers. (clockwise from upper left) montane tarsier from BBNP, montane tarsier from BBNP, T. bancanus borneanus from Sebangau (Central Kalimantan), captive T. b. bancanus from Taman Safari, captive T. b. bancanus from Taman Safari, montane tarsier from BBNP. Although the photos of the montane tarsier are slightly blurry, the tail tuft from the montane tarsier in this report appears to have fur that is shorter, sparser, and extends further along the tail than is seen in other Western Tarsiers. Appearance of the tail tuft is a key identifying feature in tarsier taxonomy, and is functionally related to leaping performance among other things. (Note: the color of the fur of captive tarsiers fades to shades that are not seen in wild animals).

Antonia Gorog © 2004, except where noted

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Gorog & Sinaga - A Tarsier Capture in Upper Montane Forest on Borneo

Implications Bornean mammals can be grouped into those that vary regionally (e.g., the subspecies of the treeshrews Tupaia minor, T. picta, and T. glis and of the tri-colored squirrel Callosciurus prevostii and white-fronted langur Presytis frontata) or altitudinally (e.g., Maxomys spp. and Sundamys spp.), and those that show little variation across the island (e.g., the macaques Macaca fascicularis and M. nemestrina, the rusa Cervus unicolor, and the sunbear Helarctos malayanus) (Medway 1977). Current taxonomy and distributional data suggest that Bornean T. bancanus falls into this latter category; as of yet, only one morphological subspecies of the Western tarsier (T. bancanus borneanus) is recognized on Borneo (Groves 2001). In their 1987 paper on the identity of T. pumilus, Musser & Dagosto examined distinguishing characteristics of the tarsier species and provided the last comprehensive review of tarsier morphology. Despite their broad sampling of Bornean specimens, which included specimens from Sabah, Sarawak, and West Kalimantan, the authors’ goal was not to evaluate variation in Bornean T. bancanus, and their study did not address the possibility of multiple differentiated forms on this island. This new record at Bukit Baka suggests a greater morphological diversity in tarsiers on Borneo than is currently recognized. Sharp differences in tail morphology of the Eastern, Western, and Philippine tarsier species provide useful diagnostic characters for identifying species (summarized in Musser & Dagosto 1987; Shekelle 2003). The tail of the Philippine species is covered by relatively sparse, short hairs. The tails of the Sulawesian species are the most heavily haired, with the terminal tuft covering one third to almost one half of the tail. The Western tarsier possesses a more distinct tuft of long hairs confined to the distal third of the tail. The tail of the tarsier we captured at Bukit Baka was scruffier and more hirsute than that of a typical Western tarsier, but less hirsute than the tails of Eastern, or Sulawesian, tarsiers. In combination with its brownish coloration, which is generally greyer in the Bornean T. bancanus, the Bukit Baka individual does not look like a typical Western tarsier (C. Groves & M. Shekelle, pers com).

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The high elevation tarsier we captured may represent a differentiated morph of T. bancanus and an altitudinal extension of the habitats thought to be occupied by this species. Alternatively, the individual captured at Bukit Baka may represent a new tarsier form. This is an interesting possibility given the existence of a distinct montane species, T. pumilus, on Sulawesi, but remains to be tested with specimens or genetic materials, neither of which could be collected from this animal. High elevation regions of Kalimantan represent an increasing proportion of remaining natural habitat on Borneo, as lowland forest is rapidly reduced by large-scale logging operations (Curran et al. 1999). Many mammal species endemic to montane habitat have been recorded in northern (Malaysian) Borneo (Medway 1977), and new species have been described recently (e.g., Emmons 1993) from the relatively well-studied north. In contrast, few high elevation surveys have been conducted in Kalimantan, and the fauna of Indonesian Borneo is almost certainly richer than is currently thought. We hope with this report to inspire additional survey work and research in montane areas of Kalimantan. ACKNOWLEDGEMENTS We thank LIPI (the Indonesian Institute of Sciences), the Museum Zoologicum Bogoriense, and PHKA (the Indonesian Department of Forest Protection and Nature Conservation) for supporting our field work in West Kalimantan. Special thanks to Gary Paoli, Agustinus Suyanto, Maharadatunkamsi, Rahmadi, and Medang. REFERENCES Curran, LM, I. Caniago, GD. Paoli, D. Astiani, D. Kusneti, M, Leighton, CE. Nirarita & H. Hacruman. 1999. Impact of El Niño and logging on canopy tree recruitment in Borneo. Science 286: 2184-2188. Dagosto M. & D. Gebo. 1997. A preliminary study of the Philippine tarsier in Leyte. Asian Primates 6:4-8.


Emmons, LH. 1993. A new genus and species of rat from Borneo (Rodentia: Muridae). Proc. Biol. Soc. Wash 106: 752-761. Gorog, AJ. 2003. Historical Biogeography of Small Mammals in the Sunda Region of Southeast Asia. Dissertation, University of Michigan, Ann Arbor, Michigan. Groves, C. 1998. Systematics of tarsiers and lorises. Primates 39: 13-27. Groves, C. 2001. Tarsiiformes. In: Primate Taxonomy. Eileen D’Araujo (ed.). Smithsonian Institution Press, Washington, D.C., pp. 121-125. Groves, C. This volume. Getting to Know the Tarsiers: Yesterday, Today and Tomorrow. Gursky, S. 1998. Conservation status of the spectral tarsier Tarsium spectrum: population density and home range size. Fol. Prim. Supplement 1: 191-203. Jarvie, JK., Ermayanti, U. Mahyar, U. Church & Ismail. 1998. The habitats and flora of Bukit BakaBukit Raya National Park. Tropical Biodiversity 5: 11-56. Kool, KM, & Y. Nawi. 1995. Catalogue of Mammal Skins in the Sarawak Museum. Universiti Malaysia Sarawak, Kuching, Sarawak, Malaysia. Le Gros Clark, WE. 1924. Notes on the living tarsier (Tarsius spectrum). Proceedings of the Zoological Society of London 1924: 216-217. MacKinnon, J, & K. MacKinnon. 1980. The Behavior of wild spectral tarsiers. International Journal of Primatology 1: 361-379. Maryanto, I & M. Yani. 2004. The third record of pygmy tarsier (Tarsius pumilus) from Lore

Lindu National Park, Central Sulawesi, Indonesia. Tropical Biodiversity 8(2): 79-85. Medway, G.H. 1977. Mammals of Borneo.: Printed for MBRAS by Perchetakan Mas Sdn. Bhd., Kuala Lumpur, Malaysia. Musser, G. & M. Dagosto. 1987. The identity of Tarsius pumilus, a pygmy species endemic to the montane mossy forests of central Sulawesi. Amer. Mus. Novit. 2867: 1-53. Neri-Arbodela, I., P. Stott, & NP. Arbodela. 2002. Home ranges, spatial movements and habitat association of the Philippine tarsier (Tarsius syrichta). J. Zool, London 257: 387-402. Niemitz, C. 1979. Results of a field study on the western tarsier (T. bancanus bancanus Horsfield 1821) in Sarawak. Sarawak Mus. J. 27: 171-228. Payne J. & CM. Francis. 1998. A Field Guide to the Mammals of Borneo. The Sabah Society, Kota Kinabalu, Malaysia. Rickart, EA, LR. Heaney,PD. Heideman & RCB. Utzurrum. 1993. The distriubtion and ecology of mammals on Leyte, Biliran and Maripipi Islands, Philippines. Field. Zool. 72: 1-62. Shekelle, M. 2003. Taxonomy and Biogeography of Eastern Tarsiers. Ph.D. thesis. Washington University in Saint Louis Shekelle, M., Leksono, SM, LLS. Ichwan & Y. Masala. 1997. The natural history of tarsiers of North and Central Sulawesi. Sulawesi Primate Newsletter 4: 4-11. Sussman, R. 1999. Tarsiiformes. In: Primate Ecology and Social Structure. Pearson Custom Publishers, Needham Heights, MA.

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DISTRIBUTION OF TARSIER ACOUSTIC FORMS, NORTH AND CENTRAL SULAWESI: WITH NOTES ON THE PRIMARY TAXONOMY OF SULAWESI’S TARSIERS Myron Shekelle Center for Biodiversity and Conservation Studies (CBCS-UI), Faculty of Mathematics and Science (F-MIPA), University of Indonesia, Depok 16424, Republic of Indonesia, Email: [email protected] ABSTRACT This study uses field surveys of wild tarsier populations to assess the relationship between described tarsier taxa and acoustic forms. Surveyed regions of North and Central Sulawesi contain eight acoustic forms and five described taxa. There is synonymy between acoustic form and taxonomic form in two instances, minimally, and two of the taxonomic forms appear to be synonymous with each other. Thus, if tarsier acoustic forms are distinct taxa, as has been hypothesized (MacKinnon and MacKinnon 1980, Niemitz et al. 1991, Nietsch and Kopp 1998), then as many as ten tarsier taxa may be present in the region that has been surveyed thus far. Acoustic forms were identified with playback tests using populations of wild tarsiers and corroborated with heuristic spectrographic analyses. Spectrograms of three previously undescribed acoustic forms of tarsiers are presented, along with spectrograms from four acoustic forms that were already known. The distributions of tarsier taxa and acoustic forms are presented. Comments are made regarding the nature and validity of each taxon. Tarsius sangirensis is recognized as a distinct species. Tarsius dianae is likely a junior synonym of T. dentatus. The whereabouts and location of the type locality of T. pumilus are discussed. Keywords: Distribution, Tarsius spp, vocalization

INTRODUCTION The primary taxonomy of Sulawesi’s tarsier has been in question for the past twenty years. Results of collecting expeditions from the eighteenth century up to 1949 led to the description of five distinct tarsier taxa from Sulawesi and its surrounding islands. By 1984, however, Niemitz had simplified the taxonomy, classifying Sulawesi’s tarsiers into a single species, Tarsius spectrum, with two subspecies, T. spectrum, and T. pumilus (Table 1). Tarsius spectrum is now accepted as a junior synonym of T. tarsier (see Groves et al. this volume). Just prior to this, MacKinnon and MacKinnon (1980) reported the first observations of wild Tarsius tarsier, wherein they commented that there were clearly several distinct taxa of tarsiers on Sulawesi. At the same time, the classification and taxonomy of nocturnal primates was undergoing substantial revision. Prompted in part by the Recognition Concept of Species (Paterson, 1985), numerous cryptic sibling species were ultimately identified where once taxonomists had recognized only a single species. This led to the argument that the

number of species in nocturnal taxa, in particular, had been underestimated (e.g. Bearder et al, 1995; Masters, 1998). In addition to this taxonomic revision of Sulawesi’s other primate, the macaque, showed as many as seven species where once there was thought to be just two (e.g. Fooden, 1980; Groves, 1980). This created awareness of Sulawesi’s interesting biogeographic phenomenon of colonization and radiation (Whitten et al. 1987), thereby lending further credence to the hypothesis that several cryptic sibling species exist among Sulawesi’s tarsiers. Prior to 1984, five distinct tarsier taxa had been described from the region of Sulawesi and its surrounding islands (Figure 1). These are: Tarsius tarsier Erxleben, 1777, type locality Makasar (see discussion); T. sangirensis Meyer, 1897, from Greater Sangihe Island, North Sulawesi; T. pumilus Miller and Hollister, 1921, from Rano Rano, Central Sulawesi; T. dentatus Miller and Hollister, 1921, from Labuan Sore, Central Sulawesi; and, T. pelengensis Sody, 1949, from Peleng Island. The taxonomic history of tarsiers, and specifically Sulawesian tarsiers, is confusing and riddled with nomenclatural arguments and instability.

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Shekelle- Distribution of Tarsier Acoustic Forms

Table 1. Taxonomic Revisions of Sulawesi’s Tarsiers 1949-1984

Taxon T. tarsier (=spectrum) T. sangirensis T. pumilus T. dentatus T. pelengensis

Sody 1949 species subspecies (not mentioned) subspecies subspecies

Hill 1955 species subspecies subspecies subspecies subspecies

Eastern Tarsier Taxa (prior to this study)

Niemitz et al. 1991

Niemitz 1984a species jr. synonym subspecies jr. synonym jr. synonym MacKinnon & MacKinnon 1980

Sampling Localities

Figure 1: Location of taxa, acoustic forms, and sampling localities. MacKinnon and MacKinnon (upper right) recognized three acoustic forms. Niemitz et al. (lower left) named T. dianae based upon comparisons with tarsiers from the northern tip of Sulawesi. Neither of these works addressed in detail the other described taxa of Eastern tarsiers (upper right). This study sampled a transect at approximately 100 km intervals.

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spots= sampling localities x= capture sites of T. pumillus

Figure 2. Distributions of Eastern tarsier taxa and acoustic forms.

functions, and which co-inhabit biogeographic faunal zones with Sulawesi’s macaques. Included with this hypothesis was the possibility of an altitudinal variant, the small-bodied montane tarsier of central Sulawesi, T. pumilus. They concluded by stating “there is clearly much more taxonomic work to be done to sort out the Sulawesi tarsiers, but we would predict that there are more forms to be found in southern Sulawesi, and on the offshore island groups of Selayar, Peleng, and Sangihe-Talaud.” Following the suggestion of MacKinnon and MacKinnon, several research teams began investigations into the primary taxonomy of

Sulawesian tarsiers. On one front, field primatologists began to collect data from wild Sulawesian tarsiers. Niemitz (1984b) surveyed tarsiers in Central Sulawesi and published preliminary spectrograms of tarsiers from Marena. Niemitz et al. (1991) conducted more surveys in North and Central Sulawesi that led to the description of a new species from the highlands of Central Sulawesi, Tarsius dianae (Niemitz et al. 1991). They made similar observations to those of MacKinnon and MacKinnon, stating “there may be a constellation of nocturnal tarsier species paralleling the set of closely related diurnal macaque species in Sulawesi” (Figure 1).

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Nietsch (1993, 1994) and Nietsch and Kopp (1998) continued investigations into the primary taxonomy of Sulawesian tarsiers, concentrating on the role of tarsier vocalizations. Nietsch documented the T. dianae acoustic form at Kebun Kopi (north of Palu along the Tawaeli-Toboli Road) and at Lake Poso, in addition to the type locality at Kamarora. She also reported hearing duets that sounded like the T. dianae acoustic form at Ampana and Morowali, but these were unconfirmed by playback or spectral analysis (Nietsch, 1994). Nietsch and Kopp (1998) also provided experimental evidence that “differences in duet structure are reliable indicators of taxonomic differentiation”, in that duets of heterospecifics were less effective in prompting responses from caged animals than were the calls of conspecifics. Based on analogies with song function in gibbons, she concluded that tarsiers from Tangkoko, Kamarora, and the Togian Islands were each likely to be a separate species. While fieldwork in Sulawesi was progressing, analyses of museum specimens were also being undertaken. Musser and Dagosto (1987) recommended the re-elevation of T. pumilus to full specific status as a small-bodied tarsier endemic to the montane forests of the central highlands. Feiler (1990) argued for the re-elevation of tarsiers from the Sangihe Islands to full specific status, T. sangirensis, based on cranial measurements. Groves (1998) concluded that the distinctive characters of Feiler were insignificant when compared with a larger sample, but he also argued for reviving T. sangirensis based upon morphometric variation in dental and cranial characteristics. Groves further mentioned the possible justification for separating the Sulawesian tarsiers from T. syrichta and T. bancanus at the generic level. In spite of the advances made by field surveys and analyses of museum specimens, some nagging issues remained, and new ones had been created. First, populations of, T. pumilus and T. pelengensis were not included in the recent field surveys. Second, the surveys of MacKinnon and MacKinnon (1980) and Niemitz et al. (1991) did not make thorough comparisons between acoustic forms and pre-existing taxa, nor did either study employ

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systematic surveys. While it is understandable that preliminary work be ad hoc, two issues of confusion were generated by the advances that these two studies made: (1) what were the relationships between acoustic forms and the five described taxa from Sulawesi? and, (2) what variation existed between the widely separated sample points of the field surveys? This project began with reconnaissance surveys in 1994, and collecting expeditions followed in 1995 and 1996. The goal was to use a transect to “connect-the-dots”, as it were. A transect that encircles Tomini Bay, with a few minor auxiliary transects, would pass through all of the type localities of all described tarsier taxa from Sulawesi, with the notable exception of T. tarsier, as well as all of the previously identified acoustic forms (Figure 2). Based on evidence available at the time, 200 km sampling intervals were initially indicated. The results of initial surveys, however, indicated greater diversity than predicted by the previous studies, and sampling intervals were reduced to 100 km. Even this proved insufficient in the region from Gorontalo to Palu. Preliminary findings included: (1) identification of seven acoustic forms in the areas of North and Central Sulawesi that were partially surveyed by MacKinnon and MacKinnon (1980) and by Niemitz et al. (1991); (2) additional evidence for the re-elevation T. sangirensis to full-specific status; and, (3) the possibility of a nomenclatural conflict between T. dianae and T. s. dentatus (Shekelle et al. 1997). METHODS Data were collected on wild tarsiers from 12 localities in North and Central Sulawesi (Figure 1). Nine of the localities lie at approximately 100 km intervals along a transect that connects Tangkoko (the reference population for T. tarsier), and Kamarora, the type locality of T. dianae. The other three localities lie along two auxiliary transects that connect island populations with the main transect: (1) Great Sangihe Island, about 200 km north of Sulawesi; and (2) two locations in the Togian Islands of Tomini Bay, Batudaka Island and Malenge Island.


Recordings of wild tarsier vocalizations were made using either a Sony WMD 6C with a Sennheiser MKE 300 microphone, or a Sony TR-600 Hi8 camcorder with either the internal microphone or with a Sennheiser MKE 300. Many recordings were made of naturally occurring vocal duets at dusk or dawn. Other recordings were made of tarsiers that were baited to sing by playing the recording of a conspecific. The current study does not discriminate natural from baited vocalizations, although this difference may be important for understanding variation within an acoustic form. For spectral analysis, recordings were replayed on the same machine that made the original field recording, and these were converted to digital “*.wav” files using an analog to digital converter. This was facilitated by the computer program “Cool 96” (copyright 1992-1996, Syntrillium Software). The following options were employed: sample rate (44100 Hz); resolution (1024 bands); windowing function option (Blackmann); spectral plot style (logarithmic energy plot with 120 dB range); dither transform results (on). Spectrogram files were pasted into Photoshop 5.0 (copyright 1989-1998 Adobe Systems Inc.) and were transformed to standardize the x- and y-axes, as well as to improve legibility. For playback experiments, a test tape was made in the field of unaltered wild tarsier recordings, one call per locality, each call being separated by a gap of silence. The duration of each duet call and the duration of each period of silence were standardized. Positioning of the speakers (Sony SRS 77G) and volume were standardized as well as could be done (speakers were positioned at a distance of 10-20 meters from the sleeping site, volume was set to full). An unhabituated group of tarsiers was exposed to the tape between 8 a.m. and 3 p.m. A positive response was recorded if the tarsiers in question began vocalizations that led to a duet call while a recorded duet was being played, or during the period of silence that followed. The time of day (8 a.m. to 3 p.m.) was chosen because tarsiers are normally sleeping and are not normally vocalizing. Thus any positive response should be the result of the experiment, not some other

factor. Also, a recording of the local duet call was played approximately one hour before and after the playback test. The playback test is, therefore, bracketed by positive responses, and this helps to ensure that any negative responses were not caused by other factors (e.g. the tarsiers did not hear the recording, the tarsiers had moved off to another site, the tarsiers were frightened into silence by the presence of researchers, etc.). If, during the course of the playback test, a positive result was recorded (i.e. the tarsiers began to sing), the test was paused for a minimum of 1/2 hour in order to let the tarsiers settle down. Thus, subsequent positive responses are likely to be the result of subsequent recordings, not because of continued excitability as a result of the previous positive response. Playback tests are time consuming. Typically, only one formal test was performed per locality. Results of the formal tests were often corroborated, however, through numerous informal tests. Informal tests occurred during survey and trapping, when trial-and-error of playback was used to locate tarsier nests and to bait the tarsiers into the nets. Since the playback tape was made in the field from recordings collected during survey, not all reciprocal tests could be conducted. Tarsiers from localities that were visited early in the study, such as Molibagu, were not exposed to recordings of tarsiers from localities that were visited subsequent to fieldwork at Molibagu. In other words, if tarsier recordings from locality x were played for tarsiers at locality y, it is not necessarily true that recordings from locality y were played for tarsiers at locality x. When conducted, however, the results of reciprocal tests were typically equal, i.e., the graph is symmetrical along the axis x = y. RESULTS Playback experiments reveal the presence of seven acoustic forms in the study area with geographically-structured variation (Figure 3). From north to south along the transect, the first acoustic form (site 1), the Sangihe form, is unique

39

Spectrograms


40


Figure 3. Results of Playback Tests Spectrograms for Seven Acoustic Forms of Sulawesian Tarsiers

and found only on Greater Sangihe Island. The second acoustic form (sites 2-5), the Manado form, is found at Tangkoko, Ratatotok/Basaan, Molibagu, and Suwawa. The third acoustic form (site 6), the Libuo form, is unique to Libuo. The fourth acoustic form (site 7), the Sejoli form, is unique. The fifth acoustic group (site 8), the Tinombo form, is unique. The sixth acoustic form (sites 9-10), the T. dianae form, is found at Marantale and Kamarora. The seventh acoustic group (sites 11-12), the Togian form, is found at

Malenge Island and Batudaka Island, in the Togian Islands. The seventh acoustic group is interesting. Results of reciprocal tests were unequal. Recordings of the duet call from all sites successfully baited these tarsiers to respond, i.e. a positive response. When recordings of the Togian Island form were played at other sites, however, the recordings did not bait the tarsiers to sing, i.e. a negative response. These results were tested and re-tested, always to the same effect.

41


Togian Island tarsiers seem not to discriminate among acoustic forms as do other tarsiers in the study group. The playback test from site 5, Suwawa, had an anomaly. During the course of the formal playback test, the target group responded to all calls. During informal tests, prior to the formal test, however, tarsiers from this locality did not respond to the duet calls of other acoustic forms. The formal test was conducted on the last day of fieldwork under sub-optimal conditions. Various conditions of the test were not met (e.g. the minimum pause of ½ hour between positive results was not observed). Time constraints did not allow for the formal test to be repeated. This study tentatively rejects the results of the formal test for those of the informal tests. Further testing is warranted. Recordings of wild tarsiers in this study were made under field conditions and are generally of poor quality. They are not well suited for spectral analysis. The following are very general descriptions of the vocal duets. These descriptions are presented with the principal goal of facilitating fuller understanding of what is illustrated in the spectrograms. They are not meant to be definitive statements of the characteristics of the given acoustic forms. The descriptions use the following terms: unit = one part of a multi-part call; call = one coordinated, repeated vocalization. The difference between a unit and a call is somewhat arbitrary, but it is nevertheless a useful distinction for describing tarsier vocal duets. The Sangihe form is a previously undescribed acoustic form. It is characterized by a two-unit female call and a rapid series of male calls (spectrogram 1a). The female contributions include the standard call, and at least one variant that occurred at the end of a duet (spectrogram 1b), both of which have two units. The first unit of the standard female call is a long whistle, over one second long with energy concentrated around 8 kHz (spectrogram 1b, far left). The second unit rapidly descends from over 14 kHz to below 6 kHz. The variant is shorter, and does not ascend above 10 kHz (spectrogram 1b, far right). Spacing between the female calls varies, but is typically 8-10 seconds from the start of one call to the start of the next (not pictured). The male calls are

42

wide-band chirps that rapidly rise and descend (7 kHz, to over 10 kHz, to less than 7 kHz) in a span of only 0.15 seconds. The male produces these calls at the rate of about 4-6 calls per second. The Manado form was originally described by MacKinnon and MacKinnon (1980), and was further examined by Niemitz et al. (1991), each of whom used recordings made at Tangkoko (spectrograms 2a and 2b) (Table 2). The duet is a series of synchronized male and female calls that precede a crescendo of ascending whistles by the female. Initially, the female call is a descending whistle that drops from around 10 kHz to below 6 kHz over the span of approximately 0.3 seconds. The female makes these calls about once per second. The female calls decrease the degree to which they descend in pitch, gradually flattening out, and finally, they begin to ascend. During this portion, the call can become highly synchronized (e.g., spectrogram 2d, seconds 6-8). In between, and on top of the female calls, are male calls. These are wideband chirps that rise and descend rapidly (6 kHz, to 13 kHz, to less than 6 kHz), all in a span of only 0.2 seconds. The male produces these at a rate of about 2 per second. The overall length of one such vocal phrase varies greatly but they do not usually repeat any faster than about once per 10 seconds. MacKinnon and MacKinnon (1980) originally described the Libuo form as the Gorontalo form (spectrogram 3a). This acoustic form is characterized by a two- or three-unit female call accompanied by male calls (spectrogram 3). The female call has a standard form (spectrogram 3b) and at least one variant (spectrogram 3c). The standard female call is a long whistle that descends from around 13 kHz to about 7 kHz in two or three units. A variant, in spectrogram 3c is similar to the standard call, but with 5-8 units that may take up to 7 seconds total, each unit being about 0.6-1.0 seconds and separated by a momentary pause. The female calls repeat with a minimum periodicity of around 6 seconds from the start of one call to the start of the next. The male calls, wide-band chirps that rise and descend (6 kHz, to 1012 kHz, and back to 6 kHz) in about 0.15 seconds, punctuate the spaces in the female call (e.g.

T. sangirensis Meyer 1897 T. dentatus Miller and Hollister 1921

T. pumilus Miller and Hollister, 1921 T. pelengensis Sody, 1949

T. lariang Merker & Groves 2006

T. tarsier population T. tarsier population

T. tarsier population



2.

4.

6.

7.

9.

10.

11.

8.

5.

3.

T. tarsier Erxleben 1777

1.

Taxon name

Togian form

Tinombo form

Sejoli form

Gorontalo form = Libuo form

Manado form

Palu form

Peleng form

?

T. dianae form

Sangihe form

Bantimurung form

Acoustic form

this paper; Nietsch, 1994; 1998; Shekelle et al, 1997

this paper; Shekelle et al, 1997

this paper; MacKinnon and MacKinnon, 1980 this paper; MacKinnon and MacKinnon, 1980; Shekelle et al 1997 this paper; Shekelle et al, 1997

MacKinnon and MacKinnon, 1980; Niemitz, 1984; Merker and Groves, 2006

Niemitz, 1985; Musser and Dagosto, 1987

Feiler, 1990; Shekelle et al, 1997; Groves, 1998 Niemitz et al, 1991; Shekelle et al, 1997

Unpublished data

Reference

Table 2: Provisional Assessment of Primary Taxonomy of Sulawesian Tarsiers

Malenge Is., Batudaka Is.

Tinombo

Sejoli

Tangkoko, Ratatotok, Molibagu, Suwawa Libuo

Gimpu, Palu Valley, including Marena

Labuan Sore, Kamarora, Marantale, Kebun Kopi, Lake Poso, Ampana(?), Morowali(?) Rano Rano, Latimojong Mts., Mt. Rorekatimbu Peleng Is.

Gr. Sangihe Is.

Makassar

Distribution (type locality = bold face)

Living specimens remain unobserved to science. Notable similarities between the duet form of this species and that of T. dentatus may indicate a close relationship, possibly at the subspecific level. Niemitz's (1984) T. pumilus from Marena is not T. pumilus, but more likely, the Palu form of MacKinnon and MacKinnon (1980) Most field studies of T. spectrum refer to this population Distribution reported here much smaller than that reported by MacKinnon and MacKinnon (1980) replaces MacKinnon and MacKinnon's (1980) Gorontalo form in the area of Sejoli replaces MacKinnon and MacKinnon's (1980) Gorontalo form in the area of Tinombo has been argued to be a distinct taxon based on experimental playback evidence (Nietsch, 1998), strongly supported by genetic data (Shekelle et al, this volume)

Ongoing investigations of the recently rediscovered type specimen may allow for a more accurate localization of the type locality The insular population will likely be shown to be taxonomically distinct. apparent nomenclatural conflict with T. dianae

Issue

Primates of The Oriental Night

43


spectrogram 3b, seconds 0-2), and then continue at the rate of about one per second between female calls. The Sejoli form is a previously undescribed acoustic form. The recordings from this locality are of particularly low quality, but even so, some resemblances to the Libuo form are apparent. This acoustic form has a four-unit female call accompanied by male calls (spectrogram 4a). The female call begins at about 12 kHz and descends in a series of four whistles to about 5 kHz. The first two units are rather smooth in their descent, but the final two have fine oscillations in pitch (spectrogram 4b, seconds 1.5-2.5). The entire call lasts about 2.5 seconds. The male calls, very faint in this spectrogram, are wide-band chirps that rise and fall from about 7 kHz to 11-12 kHz in about 0.15 seconds. The male repeats his calls with a periodicity of about 0.6 to 1.1 seconds. The period seems to gradually increase when the female is not calling. Relative to other tarsier duets, the duet in this spectrogram does not seem to be particularly well synchronized between the male and female calls. Few recordings were made from this locality, and it cannot be concluded whether this is characteristic of the Sejoli form. The Tinombo form is a previously undescribed acoustic form. It is remarkable for the vocal diversity of the female. In its simplest form, it bears similarities to the Togian form (see below), but the female repertoire is far greater than in Togian Island tarsier. Structurally, it is a simple duet with one female call followed by two to four male calls (spectrogram 5a). The female call is typically in two units, but is sometimes a single unit (not figured here), particularly in the early part of a duet. The basic female unit is a hook-shaped whistle that descends from around 12 kHz to about 5 kHz in about 0.4 seconds. Two of these units are sometimes given in rapid succession, the intervening gap being only 0.1 seconds (spectrogram 5b, far left). More often, the hookshaped unit is preceded by a peculiarly modulated whistle that begins at around 13 kHz, descends to below 10 kHz, rises again to a point higher than the initial frequency, and finally, descends to nearly 5 kHz, all in the span of only 0.3-0.4 seconds (spectrogram 5b, middle). Another female variant, much rarer than

44

the first two described forms, is a series of five hookshaped units that occur in rapid succession (spectrogram 5b, far right). Each of the units has a terminal frequency of about 5 kHz, but the maximum frequency of each unit gradually descends, the first having a maximum frequency of about 14 kHz and the last having a maximum frequency of just 10 kHz. The male calls are also quite interesting. They are wideband chirps, like other male tarsier calls, but they modulate from 5 kHz to over 13 kHz, and back again to 5 kHz, in about 0.10 seconds. The male produces these calls at a rate that varies from about 0.5-1.0 seconds, the interval lengthening when the female is not calling. The T. dianae form was originally described by Niemitz et al. (1991) based on recordings made from Kamarora. They published renderings of a spectrogram that has been re-scaled here for comparative purposes (spectrogram 6a). This acoustic form features a longer duet that is characterized by many repeated calls. It is a challenge to make accurate, legible spectrograms of these duets due to their length. The re-scaled version of the figure from Niemitz et al (1991) offers a glimpse at the overall character of the duet. In the early portion of the duet, the female gives fast, repetitive wide-band chirps that descend from around 15 kHz to around 5 kHz in only 0.3 seconds or less, at the rate of 2-3 calls per second. The rate of repetition gradually increases to about 7 calls per second, as the range of frequency modulation gradually narrows to a band centered at about 10-11 kHz (spectrograms 6b, seconds 6-12; 6c, seconds 49). The female gives about 7 relatively narrow-band calls that are between 10-11 kHz, and last about 0.7 seconds each. Following this, she begins again to give rapid chirps, first in a narrow band centered around 10 kHz, then gradually increasing the frequency range of the calls until they descend from about 12 kHz to 8 kHz. The male call is also a wideband chirp that descends from around 8 kHz to around 5 kHz. These are repeated at the rate of about two per second. The frequency range of these calls widens slightly as the female’s calls flatten out. It is during this portion (spectrograms 6b, seconds 6-12; 6c, seconds 4-9) that the duet becomes more highly


synchronized, with the male and female calls beginning in almost perfect unison (spectrograms 6d, seconds 4.0-6.5; 6e, seconds 4-7). Following this, synchronization of male and female calls remains tight with the female giving either two or three calls per male call (spectrograms 6d, seconds7-10; 6e, seconds 7-10). Spectrograms of the Togian form were originally published by Nietsch and Kopp (1998) (spectrogram 7a). Structurally, this is a simple duet with one female call being followed by two or three male calls. Like the Tinombo form, the female call is a hook-shaped whistle, although the top of the hook is less smooth in the Togian tarsier. The maximum pitch is about 12-13 kHz (although the figure by Nietsch shows this to be only about 10 kHz), and there is a sharp descent to around 6 kHz. The call lasts about 0.5 seconds and is repeated at the rate of about 1 call per 1.5 seconds. The male call is shaped like a temporally compressed version of the female call. Maximum pitch is around 10-11 kHz, and the call descends precipitously to 5 kHz or lower. The male call lasts only about 0.15 seconds. Male calls are performed as a series of 2 or 3 calls that gradually ascend in maximum pitch. DISCUSSION Acoustic Data: Results from this study reveal seven acoustic forms of tarsiers in the study area. Within a form, there are self-evident similarities in duet structure. There is also excellent interobserver reliability between MacKinnon and MacKinnon (1980), Niemitz et al. (1991), Nietsch and Kopp (1998), and myself, evidenced in the spectrograms. Spectrograms recorded from tarsiers at Tangkoko in the late 1970’s, late 1980’s, and late 1990’s show stability of form that is reassuring that form of tarsier call persists over time. Mate Recognition theory predicts that tarsier vocalizations are a species-specific system that evolves in such a way as to advertise the fitness of mating partners. It follows, then, that so too must the tarsier auditory system evolve in such a way as to receive and process those vocalizations, filtering

signal from noise. Thus, for the purposes of this study, an acoustic form of tarsiers is the most inclusive group of animals that have a similar and appropriate behavioral response to a given vocalization (e.g. groups of tarsiers that respond to a recorded vocal duet with the performance of a vocal duet). Hypothetically, each acoustic form is a distinct taxon, but this remains to be verified. It is easy to see from the spectrograms, that there is quantitative variation in the vocal duets within an acoustic form, and qualitative variation among acoustic forms. Some of the most obvious quantitative variation is the frequency (in kHz) of the female calls seen in spectrogram 2. For example, the final note of the female’s crescendo varies from around 9 kHz in spectrograms 2b and 2c, to 11 kHz in spectrogram 2a and 2e, to fully 15 kHz in spectrogram 2c. Since 2a, 2b, and 2c are all from one locality, Tangkoko, it is probable that this is variation that normally occurs within an acoustic form. In contrast, however, it is more difficult to make meaningful quantitative comparisons among the acoustic forms. What are the homologies, for example, between the crescendos of the Manado form and the hook-shaped female calls from the Togian Islands? The nature of quantitative comparisons of differences is that they are, in fact, comparisons of similarities. Things that are different are, simply, different. Thus it is with tarsier acoustic forms that some characters suitable for quantitative comparisons within a form are unsuitable for comparisons among forms. Homologies for quantitative comparison likely do exist among acoustic forms, but finding them will require further study. Notes on Tarsier Taxonomy: Several issues trouble the taxonomy and classification of Sulawesian tarsiers. Primary among these was, until recently, the lack of a type specimens for Tarsius tarsier (see Groves et al. this volume). Second to this is the likelihood of unrecognized cryptic taxa. Investigations into acoustic variation have uncovered eight distinct acoustic forms: the seven described in this study plus MacKinnon and MacKinnon’s (1980) Palu form. Third, there is a large

45


problem between two independent lines of investigation: surveys of museum specimens are based primarily on analyses of skeletons and pelts, while field surveys rely heavily on acoustic data and data from wild tarsiers that are trapped and released. While complementary studies often lead to dynamic advances in understanding, the unfortunate situation at hand is that many diagnostic characters used in the museum studies are impractical to score on a living tarsier (e.g. relative inflation of the auditory bulla anterior to the carotid foramen), and museum specimens cannot be scored for acoustic forms. Thus, the kernel of the problem is complementary taxonomic investigations have produced data sets that cannot be compared with each other. A clear taxonomic statement that identifies T. tarsier, clarifies the relationship between known acoustic forms and described taxa, and which states the distribution of these forms, where known, is needed. Tarsius tarsier: This taxon is based on Buffon’s tarsier and is believed to come from Makassar (Groves et al. this volume). Makassar was not sampled in this study, but subsequent surveys show a highly distinctive duet from near to Makassar (unpublished data). Thus, each of the acoustic forms discussed here are likely to be distinct taxa. Tarsius sangirensis: Although this taxon was treated as a subspecies by both Sody (1949) and Hill (1955) and synonymized with T. spectrum by Niemitz (1984a), there is general agreement between Feiler (1990), Shekelle et al. (1997), and Groves (1998) that this is a valid species. The type locality is Greater Sangihe Island and the type specimen, according to Hill (1955) is in the Dresden Museum. This taxon is distributed sparsely throughout Greater Sangihe Island. There are reports that tarsiers exist on other islands in the Sangihe Island group (e.g. Siau Island). Subsequent surveys indicate tarsiers are still present on Siau, although they are quite rare, and the acoustic form is distinct from that of T. sangirensis. The local name is sengkasi (bahasa Sangihe). One family referred to tarsiers as higo. Sangihe Island tarsiers can be easily and confidently diagnosed from T. tarsier by the tail and

46

the tarsi, both of which are more sparsely haired with hairs that are shorter than in T. tarsier—the characters on which this taxon was based (Meyer, 1897). These distinctive characteristics of T. sangirensis are intermediate between T. tarsier and T. syrichta, which is curious because Greater Sangihe Island is about midway between Sulawesi and the Philippine island of Mindanao. Tarsius sangirensis, nevertheless, is clearl related to the T. tarsier-complex. Regarding Sangihe Island tarsiers, Musser and Dagosto (1987) state that “the tail, although less densely haired than in typical T. spectrum, is not at all similar to the sparsely haired tail of T. syrichta.” While this is true, it does not argue against the uniqueness of T. sangirensis. They also state that, “the tarsus is sparsely haired, but some individuals of T. spectrum do resemble T. syrichta in this regard”. I disagree. None of the mainland Sulawesian tarsiers in this study approximated the condition in T. syrichta, nor did they resemble T. sangirensis. Furriness of the tarsus changes with age: infants have densely haired tarsi with hair that extends onto the hands and feet. Adults gradually lose some of that hair, particularly on the hands, feet and ventral/superior aspect of the tarsi, which may appear nearly nude in adults (unpublished data). The dorsal/inferior aspect of the tarsi of T. tarsier are always haired. The same is true of T. sangirensis, but the hair is shorter and less dense. Groves (1998) found that T. sangirensis is distinctive from all other Sulawesian tarsiers in having large and broad skulls, long toothrows, and short lateral incisors. Shekelle et al. (1997) found them to be distinguished from other Sulawesian taxa in having a higher average body weight, a unique acoustic form, and several unusual behavioral characteristics including a tendency toward less sociality while sleeping, and a preference for more exposed sleeping sites—which may be due, in part, to habitat degradation. Some authors including Groves (1998) have indicated that T. sangirensis may have a less distinctive postauricular white spot (a synapomorphy that links all Sulawesian taxa), and finer, less wooly fur. To the former, I disagree. The fur of T. sangirensis is perhaps finer and less wooly than that of T. tarsier,


but it is also most certainly lighter. The dorsal aspect of the body and limbs is a light, milk chocolate-like brown. It has less of the distinctive brown and black mottled appearance of T. spectrum. The underside is almost pure white as is the postauricular white spot (see photo of T. sangirensis in Rowe, 1996, p.55—the postauricular white spot is visible at the base of the ear, and, faintly, at the top of the ear). It may be that the museum specimens bear some artifacts of preservation or aging that have turned the pelts dark. Tarsius dentatus: This taxon was treated as a questionably valid subspecies by both Sody (1949) and Hill (1955), and was synonymized with T. spectrum by Niemitz (1984). The infant tarsier in Rowe (1996) that is labeled as T. dentatus is misidentified. It is a tarsier from Libuo. The type locality of T. dentatus is Labua Sore. Dr. Lenora Bynum studied macaques in that region for several years in the early 1990’s and her surveys indicate that the site, which is also important for macaque taxonomy, goes by the name Labuan Sore (pers. comm.). When I visited there in April and May of 1996 local people agreed that there is a coastal site called Labuan Sore. [This is, perhaps, a corruption of labuhan sore, or, “evening anchorage”]. It is coastal and treeless, so I surveyed the nearby agricultural lands around the village of Marantale and used these as my reference sample for T. dentatus. Tarsiers at Marantale exhibited the vocal duets of T. dianae. Thus, it raises the strong possibility of nomenclatural conflict. Tarsius pumilus: There is agreement that T. pumilus is a valid taxon (Niemitz 1985, Musser and Dagosto 1987, Groves 1998, and Maryanto and Yani 2004). It is known from only three localities: the type locality, Rano Rano, at 1800 m in Central Sulawesi, the Latimojong Mountains at 2200 m in South Sulawesi, and from 2200 m on Mt. Rorekatimbu, but it is thought to be distributed throughout the mossy montane forests of the central region of Sulawesi at elevations over 1800 m. It is distinctive in its very small body size, head and body length being about 75% that of T. tarsier (Musser and Dagosto, 1987). The controversy with this taxon is not its validity, but its whereabouts. Tremble et al. (1993)

surveyed the locality listed in Musser and Dagosto (1987) as being the type locality for over one month without finding any sign of tarsiers (Yakob Muskita, pers. comm.). An experienced six-member team spent a chilly night at 1800 m on the flank of Mt. Nokilalaki for this study without finding evidence of tarsiers. Musser spent considerable time in the montane forests of Central Sulawesi in the 1970s without encountering tarsiers (Musser and Dagosto, 1987). The question remains where is T. pumilus? Tarsius pelengensis: This taxon was described by Sody (1949) but considered weak by Hill (1955) and synonymized with T. spectrum by Niemitz (1984a). Musser and Dagosto (1987) noted that museum samples from Peleng were distinctively large, but they refrained from confirming its status as a valid subspecies, conclusions that were also reached by Groves (1998). Acoustic surveys were conducted by James Burton (Nietsch and Burton 2002), and the resulting spectromgrams show clear similarities with those of T. dentatus. Tarsius dianae: Described as a distinct species by Niemitz et al (1991) based upon a unique vocal duet, several minor characters of appearance, some behavioral differences, and possibly a unique karyotype. As mentioned previously, there is a likely nomenclatural conflict between this taxon and T. dentatus. Manado form: This form exists as an acoustic variant and not yet a recognized taxon. It is synonymous with the Manado form of MacKinnon and MacKinnon (1980) and Shekelle et al (1997). Based on acoustic data, the distribution is from the northeastern tip of Sulawesi to the faunal break at Gorontalo. It includes Tangkoko Nature Reserve, from where most research on wild Tarsius spectrum originates. The most common local names are tangkasi (Bahasa Minahasa) in the northern part of the range, and mimito (Bahasa Gorontalo) in the southern part. Libuo form: This form exists as an acoustic variant and not yet a recognized taxon. It is synonymous with the Gorontalo form of MacKinnon and MacKinnon (1980) and the Libuo form of Shekelle et al (1997). Acoustic surveys presented here suggest

47


that it has a much more restricted range than that presented by MacKinnon and MacKinnon, who report the range as being the same as that of M. hecki, i.e. the entire northern peninsula from Gorontalo to just north of Palu. My acoustic surveys indicate that the distribution of this acoustic form is limited to an area no greater than that bounded by Gorontalo in the east, and Moutong/Molosipat in the west. The local name of tarsiers in this region is mimito (Bahasa Gorontalo). Sejoli form: This form is an acoustic variant and not yet a recognized taxon. It is synonymous with the Sejoli form of Shekelle et al. (1997), and replaces the Gorontalo form of MacKinnon and MacKinnon (1980) in the area around the North Sulawesi-Central Sulawesi provincial boundary. Sejoli is a small village in the vicinity of Moutong and Molosipat. Acoustic surveys indicate that the distribution of this acoustic form is limited to an area no greater than that bounded by Tanjung Panjang in the east, and Tinombo in the west. Tinombo form: This form is an acoustic variant and not yet a recognized taxon. It is synonymous with the Tinombo form of Shekelle et al. (1997), and replaces the Gorontalo form of MacKinnon and MacKinnon (1980) in the vicinity of Tinombo. Acoustic surveys indicate that the distribution of this acoustic form is limited to an area no greater than that bounded by Sejoli in the east, and Marantale in the south. Togian form: This form is an acoustic variant and not a recognized taxon. It is synonymous with the Togian form of Shekelle et al. (1997), and the Togian tarsiers of Nietsch and Kopp (1998). The confirmed distribution of this acoustic form is limited to the islands of Malenge and Batudaka, but it is reasonable to assume that its distribution extends to all of the Togian Islands (except perhaps Una Una), as the Togian Islands were a single land mass and were possibly connected to Sulawesi as recently as the last Ice Age (Whitten et al. 1987). Nietsch and Kopp (1998) has argued for the taxonomic separation of this acoustic form on the strength of experimental evidence from playback tests where captive T. tarsier were exposed to recordings of the vocalizations of the

48

Togian tarsiers, as well as those of T. dentatus, and conspecific T. tarsier. Several language groups exist in the Togian Islands and there are likely to be many local names. I recorded a few including: bunsing, tangkasi, and podi. Palu form: MacKinnon and MacKinnon (1980) originally described this acoustic form. They list the distribution as being the valley of the Palu River. This form has recently been described as T. lariang by Merker and Groves (2006). Other acoustic forms: MacKinnon and MacKinnon (1980) reported that a colleague, Dr. Dick Watling, recorded three additional tarsier acoustic forms, all from Central Sulawesi, but they did not state where in Central Sulawesi he made these recordings. It is not necessary to assume that Watling’s forms are all new and unpublished. For example, it could be that his forms are, say, T. dianae, the Tinombo form, and the Togian form, all of which come from Central Sulawesi. Nevertheless, additional acoustic forms almost certainly exist, undiscovered, on Sulawesi. ACKNOWLEDGEMENTS I thank Dr. Jatna Supriatna, Dr. Noviar Andayani, Suroso Mukti Leksono, Luluk Lely Soraya Ichwan, and Yunus Masala. Permits and logistical support were arranged for by LIPI; Department of Forestry; KSDA in Manado, Bitung, Gorontalo, and Palu; Lore Lindu National Park; and Dumoga-Bone National Park. Special thanks are due to Ibu Wati (LIPI), Pak Endang (SBKSDA Manado), Pak Rolex Lameande (KSDA Palu). Also notable is the assistance and advice provided by Dr. Joe Erwin, Dr. Ed Mulligan, and Dr. Mitchell Sommers. Terry Gleason read drafts of this paper and made important contributions to the section on biogeography. Jacinta Beehner and Kellie Glasscock also read drafts and made useful comments. Financial support was provided by the following organizations: National Science Foundation, Primate Conservation, Inc., Washington University Department of Anthropology, L.S.B. Leakey Foundation, Explorer ’s Club, Wenner Gren Foundation, Garuda Indonesia Airlines.


REFERENCENS Banks, E. 1949 Bornean Mammals. Kuching, Malaysia: The Kuching Press. Bearder, SK, PE. Honess & L. Ambrose. Species diversity among galagos with special reference to mate recognition. In: Alterman L et al., editors. Creatures of the Dark: The Nocturnal Prosimians. New York, Plenum press. p 331-352. Feiler, A. 1990. Ueber die Saugetiere der Sangiheund talaud-Inslen- der Beitrag AB Meyers Fur ihre Erforschung (Mammalia). Zoologische Abhandlungen Staatliche Museum fur Tierkunde in Dresden 46:75-94. Fooden, J. 1980. Classification and distribution of living macaques (Macaca Lacepede, 1799). In Lindburg DG, editor. The Macaques: Studies in Ecology, Behavior, and Evolution. New York: Van Nostrand Reinhold Company. p1-9. Groves, CP. 1980. Speciation in Macaca: The view from Sulawesi. In Lindburg DG, editor. The Macaques: Studies in Ecology, Behavior, and Evolution. New York: Van Nostrand Reinhold Company. Groves, C. 1998. Systematics of tarsiers and lorises. Primates 39(1):13-27. Gursky, S. 1994. Infant care in the spectral tarsier. International Journal of Primatology 15(6):843-855. Gursky, S. 1995. Group size and composition in the spectral tarsier, Tarsius spectrum: implications for social organization. Tropical Biodiversity 3(1):57-62. Gursky, S. 1997. Modeling maternal time budgets: the impact of lactation and infant transport on the time budget of the spectral tarsier, Tarsius spectrum. Dissertation Thesis. SUNY Stony Brook. Gursky, S. 1998. Conservation status of the spectral tarsier Tarsius spectrum: population density and home range size. Folia Primatoligica 1998:69(suppl 1):191-203.

Hill, WCO. 1953. Notes on the taxonomy of the genus Tarsius. Proceedings of the Zoological Society of London 123:13-16. Hill, WCO. 1955. Primates: Comparative Anatomy and Taxonomy. II. Haplorhini: Tarsioidea. Edinburgh: Edinburgh University Press. Horsfield, T. 1821. Zoological Researches in Java. London: Black, Kingsbury, Parbury, Allen. Clark, WEL. 1924. Notes on the living tarsier (Tarsius spectrum). Proceedings of the Zoological Society of London p217-223. MacKinnon, J & K. MacKinnon. 1980. The behavior of wild spectral tarsiers. International Journal of Primatology 1(4):361-379. Maryanto, I & M. Yani. 2004. The third record of pygmy tarsier (Tarsius pumilus) from Lore Lindu National Park, Central Sulawesi, Indonesia. Tropical Biodiversity 8(2): 79-85. Masters JC. 1998. Speciation in the lesser galagos. Folia Primatologica 69(suppl 1):357-370 Miller Jr., GS, & Hollister N. 1921. Twenty new mammals collected by H. C. Raven in Celebes. Proceedings of the Biological Society of Washington 34:93-104. Musser, GG, & M. Dagosto. 1987 The identity of Tarsius pumilus, a pygmy species endemic to the montane mossy forests of Central Sulawesi. American Museum Novitates (2867):1-53. Niemitz, C. 1984a. Taxonomy and distribution of the genus Tarsius Storr, 1780. In Niemitz C, editor. The Biology of Tarsiers. New York: Gustav Fischer Verlag. p1-16. Niemitz , C. 1984b. Vocal communication of two tarsier species (Tarsius bancanus and Tarsius spectrum). In Niemitz C, editor. The Biology of Tarsiers. New York: Gustav Fischer Verlag. p129-142. Niemitz, C. 1985 Der Koboldmaki-Evolutionsforschung an einem Primaten. Naturwiss Runsch 38:43-49. Niemitz, C, A. Nietsch, S. Warter, & Y. Rumpler. 1991. Tarsius dianae: A new primate species from Central Sulawesi(Indonesia).” Fol ia Primatologica 56:105-116.

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Nietsch A. 1993. Vocal acoustics and social behavior in tarsiers. In Creatures of the Dark: The Nocturnal Prosimians Conference in Durham, North Carolina. Nietsch A. 1994. A comparative study of vocal communication in Sulawesi tarsiers. ICongress of the International Primatological Society in Denpasar, Bali, Indonesia. p310 1994. Nietsch, A & C. Niemitz. 1993. Diversity of Sulawesi tarsiers. Deutsche Gesellschaft fur Saugetierkunde 67:45-46. Nietsch, A & M. Kopp. 1998. Role of vocalizations in species differentiation of Sulawesi tarsiers. Folia Primatologica 69(suppl 1)371-378. Nietsch, A & J. Burton. 2002. Tarsier Species in Southwest and Southeast Sulawesi. Abstracts, The XIXth Congress of the International Primatological Society (IPS), 49 Aug. 2002, Beijing, China: 20-21. Pallas, PS. 1778. Novae species quad e glirium ordine cum illustrationibus variis complurium ex hoc ordine animalium. Erlangen: W. Walther. Paterson, HEH. 1985. The recognition concept of species. In Vrba ES. editor. Species and Speciation. Pretoria: Transvaal Museum. p2129 Patton JL, MNF. da Silva, & JR. Malcolm. 1994. Gene genealogy and differentiation among arboreal

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spiny rats (rodentia: echimydae) of the Amazon basin: a test of the riverine barrier hypothesis. Peres, CA, JL. Patton, & MNF. da Silva. 1996. Riverine boundaries and gene flow in Amazonian saddle-back tamarins. Folia Primatologica 67:113-124. Rowe, N. 1996. Pictorial Guide to the Primates. New York: Pogonia Press. Shekelle, M, S. Mukti, LLS. Ichwan & Y. Masala Y. 1997. The natural history of the tarsiers of North and Central Sulawesi. Sulawesi Primate Project Newsletter. Sody, HJV. 1949. Notes on some Primates, Carnivora, and the babirusa from the Indo-Malayan and indo-Australian regions. Treubia 20:121-185. Tremble, M, Y. Muskita & J. Supriatna. 1993. Field observations of Tarsius dianae at Lore Lindu Nation Park, Central Sulawesi, Indonesia. Tropical Biodiversity I(2):67-76. Wallace, AR. 1876. The Geographical Distribution of Animals, Vol. 1. London: MacMillan. Whitten, A, M. Mustafa & G. Henderson. 1987. The Ecology of Sulawesi. Yogyakarta, Indonesia: University of Gajah Mada Press. Woollard, HH. 1925. The anatomy of Tarsius spectrum. Proceedings of the Zoological Society of London 70:1071-1184.


DISTRIBUTION OF TARSIER HAPLOTYPES FOR SOME PARTS OF NORTHERN AND CENTRAL SULAWESI Myron Shekelle1, Juan Carlos Morales2, Carsten Niemitz3, Luluk Lely Soraya Ichwan1, Don Melnick2 1

Center for Biodiversity and Conservation Studies, Faculty of Mathematics and Natural Sciences University of Indonesia, Depok 16421, Indonesia, Email: [email protected] 2 Center for Environmental Research and Conservation, Columbia University, New York, NY 10027, USA Email: [email protected]; [email protected] 3 Institute of Human Biology, Free University Berlin 14195 Berlin, Germany ABSTRACT DNA sequence data was taken from hair samples of wild Eastern tarsiers that were trapped-and-released. Twelve tarsier populations were sampled at approximately 100 km intervals along a transect that encircles Tomini Bay, running from Sangihe Island in the north, to the Togian Islands in the southeast. This study reports mtDNA haplotype data for 43 Eastern Tarsiers, and compares those with published sequences from Philippine and Western Tarsiers, as well as non-tarsier outgroups. A broad scale analysis, which included 21 unique tarsier haplotypes from 28 individuals, non-tarsier primates, and other mammals, found tarsiers to be a robustly supported monophyletic clade. The Eastern-Western-Philippine tarsier trichotomy was not resolved. Tarsier populations from Sangihe Island (T. sangirensis), which lies between Sulawesi and the Philippine island of Mindanao, and from the Togian Islands in Tomini Bay, were robustly supported monophyletic clades. Robust support was also provided for the basal position of T. sangirensis with respect to other Eastern tarsiers in this data set. A fine scale analysis, using only tarsiers and which included 26 unique haplotypes from 27 Eastern tarsiers samples (but used only the 3’ end of the 12s gene), also found the Sangihe and Togian populations to be robustly supported monophyletic clades. The basal position of T. sangirensis had only weak support in the fine scale analysis, however. In both analyses, broad scale and fine scale, other populations of Eastern tarsiers in this data set were generally paraphyletic or polyphyletic. Hypothesis testing found the most-parsimonious tree to be significantly shorter than trees constrained by by the assumption of monophyletic clades in by the assumption of monophyletic clades in regions of macaque endemism, geological microplates that compose Sulawesi, but could not refute the null hypothesis of no difference in overall tree length when constrained by the assumption of monophyletic clades within tarsier acoustic groups. Keywords: Tarsius tarsier, T. spectrum, T. bancanus, T. syrichta, T. dianae, T. sangirensis, T. dentatus molecular phylogeny, 12s, mtDNA

INTRODUCTION While tarsiers are commonly represented in molecular phylogenetic studies of primates, rarely has more than a single taxon been represented. Dijan and Green (1991) sequenced the involucrin gene for both T. bancanus and T. syrichta, and Adkins and Honeycutt (1994) sequenced the cytochrome oxidase c subunit II mtDNA gene for the same two taxa. Meireles et al. (2003) analyzed nuclear DNA sequence for those same two taxa at the globin locus. Never before has DNA sequence data been published for any Eastern Tarsier. The lack of knowledge about DNA sequence variation among tarsiers raises questions about the appropriate analysis of Eastern tarsiers. What is the relationship among Eastern, Western, and Philippine tarsiers? are each of the three species groups monophyletic? What is the most appropriate outgroup for an analysis of Eastern tarsiers?

In order to analyze patterns of haplotype variation among Eastern tarsiers (= Hill’s, 1955, Tarsius spectrum), it was necessary to conduct a broad scale analysis to address the larger questions about tarsier phylogenetics mentioned above. Since tarsiers are such a deep branch in the primate evolutionary tree, and since the outgroup to tarsiers has not been definitively determined despite the widespread acceptance of a monophyletic Haplorhini (see Morales et al. 1999, Yoder 2003), a fairly slowly evolving section of DNA was required. The 12s ribosomal RNA gene of the mtDNA genome has been used for addressing phylogenetic questions regarding Primates and superordinal relationships of mammals, and there is a substantial amount of comparative sequence data available (e.g. Springer and Douzery 1996, McNiff and Allard 1998). The 12s gene also has some hypervariable regions in the stem-and-loop structure,

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Shekelle, Morales, Niem itz, Ichwan & Melnick - Distribution of Tarsier Haplotypes

notably a long loop near the 3’ end of the gene, that are valuable for population level analyses. Secondary structure of the gene product facilitates alignment of this variable-length gene (Springer and Douzery 1996). The 12s gene, therefore, is a practical compromise for this study, because it contains conservative regions with which to address issues of broad scale tarsier phylogeny as well as hyper-variable regions for a population level analysis of Eastern tarsiers. Shekelle et al. (2001) reported results of a preliminary analysis of this data set. Eastern, Western, and Philippine tarsiers were found to be an unresolved trichotomy. Genetic distances among the three tarsier species were comparable to genetic distances among Hylobates and two other hominoid genera, Pan and Homo, measured at the same locus, indicating a relatively old split, conceivably dating to the middle Miocene. Tarsius sangirensis was found to be the outgroup of other Eastern tarsiers in the data set reported here: large areas of Sulawesi remain unsurveyed for tarsier genetic diversity, so it has not been verified that T. sangirensis is the outgroup of all Eastern tarsiers, nor even that Eastern Tarsiers, as a whole, are monophyletic. Togian tarsiers were an autapomorphic subset with a diagnostic 2 base pair deletion in the hyper-variable loop near the 3’ end of the 12s gene. The taxonomy of Eastern Tarsiers bears on the question of Sulawesi biogeography. There are two broad categories of hypotheses regarding this topic. One such category derives from empirical biological data, notably the Sulawesi macaques. MacKinnon and Mackinnon (1980) offered an implicit hypothesis that a unique taxon of tarsier would coinhabit the distribution of each of seven macaque taxa, thus creating zones of primate endemism. They further observed that regions that are biogeographically linked to Sulawesi, which possess native tarsier populations, but which lack native macaque populations, represent distinct biogeographic regions where one could expect to find endemic tarsier taxa, e.g. the offshore island groups of Selayar, Banggai, and Sangihe, A similar hypothesis was implied by Niemitz et al. (1991). A second category of biogeographic hypotheses for Sulawesi derives from empirical

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geological data. Prior to its current form, Sulawesi was an archipelago formed of numerous microplates of Asian, Australian, and oceanic origin. Hall (1996, 2001) reconstructed the geological evolution of Sulawesi by identifying these microplates and charting their movement over the past 50 million years. Evans et al. (2003) used genetic surveys of two distantly related taxa, primates of the genus Macaca and toads of the genus Bufo, to address hypotheses of Sulawesi biogeography. They found concordant distributions of macaques and toads, which they interpreted to indicate a shared history of range fragmentation. The faunal boundaries in their study showed little correspondence with the microplates identified by Hall (1996). Shekelle and Leksono (2004) used the distributions of tarsier acoustic forms to address the same topic. Using classic tools of biogeography, they layered the map of Evans et al. onto the map of Hall. Then they plotted the distributions of tarsier acoustic forms on the composite map. They found a nearly one-to-one correspondence between the distributions of tarsier acoustic forms and the composite map that combined the biological data and geological data. They reasoned that macaques were relatively recent immigrants to Sulawesi with much of their evolution occurring during the Pleistocene, after tectonic activity had already formed Sulawesi in its modern state. Macaque biogeography was, therefore, likely to have been shaped by Pleistocene range fragmentation/vicariance events. Indeed, many of the faunal boundaries in Evans et al.’s study appear to be consistent with geographic boundaries that are influenced by ocean level (e.g. the isthmus of Gorontalo, the Tempe depression). Tarsiers, on the other hand, were an older radiation that probably immigrated to Sulawesi in the Miocene. Tarsier biogeography would, therefore, be influenced by the geologic history of the microplates to a much greater extent than would that of the macaques, which may have colonized Sulawesi after the microplates had already coalesced. The tips of the tarsier branches would, nonetheless, be reshaped by the Pleistocene events that shaped the biogeography of macaques, and thus, tarsier biogeography also has elements of


macaque biogeography. Shekelle and Leksono called this the “hybrid biogeographic hypothesis” for Sulawesi, because it combined empirical data from biology and geology and made explicit the observation that the time of dispersal to Sulawesi was one critical component that would affect biogeography. METHODS DNA sequence data were collected from hair samples from 101 wild-caught Eastern tarsiers (Figure 1). Geographic representation included: Sangihe (n = 5), Tangkoko (n = 21), Basaan (=Ratatotok) (n = 5), Molibagu (n = 14), Suwawa (n = 7), Libuo (n = 15), Sejoli (n = 6), Tinombo (n = 8), Marantale (n = 6), Kamarora (n = 7), Malenge (n = 5), Batudaka (=Wakai) (n = 2). This was supplemented by published sequence for T. bancanus borneanus, T. syrichta syrichta, and other mammals (from gen bank). Incomplete sequence data required many specimens to be excluded from the analysis presented here. Extraction of total genomic DNA (tDNA) from samples was accomplished using Qiagen extraction kits (#29304 and #29306). Tissue samples from wildcaught tarsiers were from plucked hair. DNA

concentration varied, and was adjusted accordingly using an estimate of the gel visualization to produce template DNA of nearly the same concentration. The target DNA was amplified with the polymerase chain reaction (PCR). A 50 microliter (μL) PCR reaction consisted of the following volumes: 30 μL deionized water (dH20), 10 μL 5X buffer solution 8.5 pH, 5 μL dNTP, 1 μL primer one (20 pM/μL), 1 μL primer two (20 pM/μL), 1 μL Taq polymerase, 3.5 mM Mg++ (1 heat-released bead), 1 μL template DNA. The 12s gene is about 950 base pairs (bp) in length. The following primers were used in various combinations to amplify the 12s gene in 1, 2, or 3 segments: 651f, 891f, 1247f, 933r, 1259r, and 1559r (Table 1). The primer names correspond roughly to the nucleotide number of the human sequence of the primer’s 5’ end. The reaction was placed in a thermal cycle machine set to the following cycle parameters: “hot start” = 94° (15 sec.) (first cycle only); 35 cycles of denaturation = 94° (30 sec.), annealing = 58° (30 sec.), and extension = 72° (60 sec.); final extension = 72° (7 min.) (last cycle only); and hold = 4° (infinity). The annealing temperature was sometimes varied to improve amplification with various primer pair combinations. Numerous other permutations of

Figure 1: Sampling localities for this study.

53


Table 1a. PCR and sequencing primers

1 2

Primer Name

Length

Sequence

651f (= 378)

18-mer

AGG TTT GGT CCT AGC CTT

891f (tarsier)

21-mer

A GG GTT GGT CAA TTT CGT GCC

925r-T.spec

17-mer

GCT TTA CGC CGT GCT TT

930r-T.ban

18-mer

CGC TTT ACG CCG GAT ATT

933r

20-mer

ATC TAA AAC ACT CTT TAC GC

1169r (tarsier)

23-mer

GGG A TG TGA AGC ACC GCC AAG TC

1247f (tarsier)

24-mer

CCC GAT A AA CCT TAC CAC CCC TTG

1259r

21-mer

GGT TTG CTG AA G ATG GCG GTA

1559r (=550r)

24-mer

CCA GTA CAC TTA CCA TGT TAC GAC

CA in T. syrichta G in T. syrichta

3 4

1

2

3

4

T,C also present GG in DUPC 6343

Table 1b. Some primer products and annealing temperatures (from Shekelle 2003)

Primer 1

Primer 2

Length

Optimal Annealing Temperature

651f

925r-T.spec

294 bp

53.5º

“

930r-T.ban

299 bp

53.7º

“

933r

302 bp

51.6º

891f

1259r

409 bp

56.3º

1247f

1559r

359 bp

54.4º

1247f

1169r

16,538 bp

58.3º

thermal cycle parameters were experimented with, but the above setting was deemed to be the best. Purification of the PCR product was achieved with the Qiagen PCR purification kit (#28106). Products were gel visualized with “DNA quant ladder” to estimate DNA concentration, evaporated on a speed vac, and then resuspended in a quantity of dH20 sufficient to make the concentration of all of the purified samples approximately equal. Sequencing of the purified PCR product used the Big Dye kit. A 10 mL sequencing reaction used the following volumes: 4 mL dH20, 4 mL “Big Dye” mix, 1 mL primer (20 pM/mL concentration), 1 mL purified PCR product. The same primers that were used for PCR were also used for sequencing. The reaction was placed in a thermal cycle machine set to the following cycle parameters: 35 cycles of

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denaturation = 96° (05 sec.), annealing = 55° (10 sec.), extension = 60° (4 min.). Sequencing reactions were cleaned of impurities using sephadex. Five grams of sephadex and 80 mL of dH20 were combined and stirred until thoroughly mixed. An amount equal to 750-800 mL of mixture was aliquoted into spin columns. The columns were spun for 1 min. at 3000 rpm to remove excess moisture. The reactions were added to the top of the spin columns and were spun for 2 min. at 3500 RPM. The purified reactions were captured in 1.5 mL Eppendorf tubes, dried in a speed vac, and resuspended in 3 mL of loading dye (formamide dye mixed with 70 mL of loading solution). The samples were electrophoresed on a polyacrylamide gel (29:1) and were scored by an ABI 377 PRISM automated DNA sequencer. Both


complementary strands were sequenced in order to double-check the reliability of the sequence data. Raw data were processed and pieced together usi ng Autoassembl er (ABI, Perkin El mer). Alignment was made by eye using comparative data from GENBANK and assumptions about the secondary structure of the 12s ribosomal RNA (Springer and Douzery 1996). A) Broad Scale Analysis of Tarsier Phylogenetics A broad scale analysis of tarsier phylogenetics was performed using DNA sequence data from the 12s ribosomal RNA region of the mitochondrial DNA genome. A data matrix was constructed of 900+ b.p. for 36 haplotypes. The matrix included unique haplotypes of 21 tarsiers, 1 strepsirhine, 10 anthropoids, 1 tree shrew, 1 flying lemur, 1 megabat, and 1 microbat. Eastern tarsiers were represented by 28 individuals. Individuals with identical haplotypes were grouped. Geographic representation was as follows: Sangihe (three haplotypes: ET048, ET049, ET050), Tangkoko (two haplotypes: ET001-002-005014-082, ET083); Basaan(=Ratatotok) (two haplotypes: ET084, ET085), Molibagu (three haplotypes: ET018020-023-024-027-029, ET019, ET026), Suwawa (not represented in the broad scale analysis), Libuo (two haplotypes: ET038, ET041), Sejoli (two haplotypes: ET096, ET100), Tinombo (one haplotype: ET074), Marantale (not represented in the broad scale analysis), Kamarora (one haplotype: ET062), Togian (three haplotypes: ET052, ET056, ET057). Also represented in the data matrix were other sequences taken from the literature: 1 Philippine tarsier (T. syrichta syrichta), 1 Western tarsier (T. bancanus borneanus), 1 strepsirhine (Lemur catta), 10 anthropoids (Homo sapiens, Pan troglodytes— two individuals, Pan paniscus, Gorilla gorilla, Pongo pymaeus—two individuals, Hylobates lar— two individuals, Papio hamadryas, and primate outgroups, the flying lemur (Cynocephalus variegatus), a tree shrew (Tupaia glis), a megabat (Donsonia mollucensis)), and a microbat (Eptesicus fuscus).

Forty-five base pairs were trimmed from the 5’ end of the gene, and 43 b.p. were trimmed from the 3’ end of the gene to accommodate for the PCR primers and areas where missing data predominated. This left a data matrix with 935 characters including gaps. The data set was rooted with the four non-primate taxa (the tree shrew, flying lemur and the two bats) using the “assume outgroup to be paraphyletic” option in PAUP. A parsimony analysis using PAUP [version 4.0b10 for Macintosh (PPC)] was used to produce strict consensus and bootstrap trees using two separate sequential approximation analyses. A sequential approximation analysis uses successive heuristic analyses, with characters being reweighted based upon the rescaled consistency index after each heuristic search. Heuristic searches, followed by character reweightings, are performed until successive analyses produce identical results. The rationale for this method is to allow the data themselves to adjust the weighting of relatively consistent characters versus relatively inconsistent ones. This method is particularly applicable for the 12s gene, since it includes both highly conserved and highly variable sites and saturation of some sites reduces their utility for older phylogenetic questions (Springer and Douzery 1996). The first heuristic search used equal weights for each character. Of the 935 total characters, 477 characters were constant and 118 characters were parsimony uninformative. This left 340 parsimony informative characters. The stepwise addition option was used, with 10 random replicates. Other options employed included: gaps are treated as “missing”, multistate taxa interpreted as uncertainty, branchswapping algorithm = tree-bisection-reconnection (TBR), steepest descent option not in effect, initial ‘MaxTrees’ setting = 100 (will be auto-increased by 100), branches collapsed (creating polytomies) if maximum branch length is zero, ‘MulTrees’ option in effect, topological constraints not enforced, trees are unrooted. A total of 108 most-parsimonious trees were found, each with a tree length of 1337. Following the first heuristic search, characters were reweighted based upon the rescaled consistency index using a base score of 100.

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Characters were thus assigned a weight between 0 and 100, the latter number indicating a character that was completely consistent across the tree. A second heuristic search was performed using the same settings as the first, the only change being the reweighted characters. Four most parsimonious trees were found, each with a tree length of 50438 (because the reweighted characters use a base score of 100, the second heuristic search had a tree length that was 1 to 2 orders of magnitude greater than the first search). Following the second heuristic search, characters were again reweighted based upon the rescaled consistency index, and a third heuristic search was performed. Results of the third heuristic search were identical to the results of the second heuristic search and the sequential approximation analysis was deemed to be complete. B) Fine Scale Analysis of Eastern Tarsier Phylogenetics A second sequential approximation analysis was performed on a data set that used only the 3’ half of the 12s gene (~500 b.p.). Twenty-six unique haplotypes from 27 individuals were included in the analysis. Although the data matrix was comprised of only about half as many characters as in the broad scale analysis, it include the complete hyper-variable loop near the 3’ end of the 12s gene, which is more applicable to fine scale analyses. The geographic representation of Eastern tarsiers was as follows: Sangihe (two haplotypes: ET048, ET049), Tangkoko (three haplotypes: ET001, ET003, ET010); Basaan (=Ratatotok) (two haplotypes: ET 084, ET085), Molibagu (three haplotypes: ET018, ET019, ET025), Suwawa (two haplotypes: ET089, ET090), Libuo (two haplotypes: ET 032, ET034), Sejoli (three haplotypes: ET096, ET097, ET100), Tinombo (two haplotypes: ET072, ET077), Marantale (two haplotypes: ET066, ET068), Kamarora (two haplotypes: ET062, ET063), Togian (three haplotypes: ET052, ET054, ET056-058). The Philippine and Western tarsiers were used to root the analysis. The “root as basal polytomy” option in PAUP was employed.

56

The same PAUP settings were used, as were used in the broad scale analysis. The fine scale analysis had 518 characters, of which, 413 were constant. Fifty-eight characters were parsimony uninformative, leaving 47 informative characters. A total of 131,967 most-parsimonious trees were found, each with a tree length of 150. After reweighting of characters based upon the rescaled consistency index, 222 most-parsimonious trees, each with a tree length of 10931 were found. In the third and fourth heuristic searches, following reweighting of the characters after each search, 221 most-parsimonious trees were found, each with a tree length of 10931. RESULTS A) Broad Scale Analysis of Tarsier Phylogenetics Major elements of the strict consensus tree (Figure 2) included the erroneous placement of the flying lemur within Primates, a monophyletic Prosimii, and a monophyletic Philippine-Western tarsier clade. Within Eastern tarsiers, T. sangirensis was a basal outgroup, and Togian tarsiers and Tangkoko tarsiers were autapomorphic subsets. Tinombo and Kamarora tarsiers were represented by a single specimen and necessarily monophyletic. Sejoli, Libuo, and Molibagu tarsiers were each paraphyletic assemblages. Basaan (=Ratatotok) tarsiers were polyphyletic, one haplotype being basal to the Tangkoko clade and the other haplotype nested within the Molibagu clade. A bootstrap analysis using 1000 replicates was performed using the character weights that resulted from the sequential approximation analysis (Figure 3). All other options were the same as in the heuristic parsimony analyses. Highly supported elements of the bootstrap tree included 100% bootstrap value support for the monophyly of the following clades: Tarsius, Eastern tarsiers, T. sangirensis, and Togian tarsiers. Other phylogenetic structure that appeared in the strict consensus tree either collapsed or was supported by lower bootstrap values, in the range of 50-83%.


B) Fine Scale Analysis of Eastern Tarsier Phylogenetics Major elements of the strict consensus tree (Figure 4) included a monophyletic clade of Sangihe tarsiers (T. sangirensis) being basal to other Eastern tarsiers in the data set. The Togian tarsier formed a monophyletic clade that was basal to the remaining tarsiers (i.e. non-Sangihe Eastern tarsiers). The remaining tarsiers clustered in a series of clades where, generally, primitive-to-derived haplotypes followed a south-to-north pattern (i.e. the most derived haplotypes are on the extreme northern end of Sulawesi), but where haplotypes from a given locality were not monophyletic. Haplotypes from three localities, Marantale, Sejoli, and Ratatotok were polyphyletic. Haplotypes from Kamarora, Tinombo, Libuo, Suwawa, and Molibagu, and Tangkoko were paraphyletic. The data set for the fine scale analysis was computationally intensive, probably because there were too few characters relative to taxa, and the bootstrap analysis was stopped after 230 replicates (Figure 5). The bootstrap analysis of the fine scale data set provided robust support for the monophyly of Eastern tarsiers, T. sangirensis, the Togian Island tarsier population, and T. dentatus, represented by a clade that consisted of two haplotypes found at Kamarora and one haplotype found at Marantale. Each of these clades was supported by bootstrap values between 91-100%. There was one major change in topology, with the bootstrap analysis finding the Togian Island tarsier population to be basal to other Eastern tarsiers in the data set, but this result was supported by a very low bootstrap value of only 54%. Other phylogenetic structure that appeared in the strict consensus tree either collapsed or was supported by lower bootstrap values, in the range of 66-81%. C) Other Analyses A final sequential approximation analysis was attempted using T. sangirensis to root the remaining Eastern tarsiers in the data set (not figured). This analysis was abandoned when it was found that there were only 31 parsimony informative characters for 26 taxa, many of those characters preferentially located on the branch that defines T. sangirensis.

D) Hypothesis Testing The mtDNA phylogeny produced in the finescale analysis was used to directly address questions about tarsier biogeography. 1. Do tarsiers co-inhabit regions of primate endemism with Sulawesi macaques, such as was hypothesized by MacKinnon and MacKinnon (1980) and Niemitz et al. (1991), and which would be consistent with the biogeography of macaques and toads found by Evans et al. (2003)? 2. Do tarsiers inhabit regions of endemism identified by the microplates of Sulawesi, such as might be predicted by Sulawesi’s geologic history as an archipelago? (Hall 2001) 3. Are tarsier acoustic and genetic groups statistically congruent and do tarsier acoustic groups diagnose discrete taxa, such as might be predicted by the mate recognition species concept of Paterson (1985), and MacKinnon and MacKinnon (1980), Niemitz et al. (1991), several papers by Nietsch (e.g. Nietsch and Niemitz 1993, Nietsch and Kopp 1998, Nietsch 1999), and therefore consistent with the hybrid biogeographic hypothesis for Sulawesi by Shekelle and Leksono (2004)? These three hypotheses, abbreviated as (1) “macaque”, (2) “microplates”, and (3) “acoustic form”, were tested by constructing constraint trees in MacClade and loading them into PAUP. In each case the constraint tree assumed a trichotomy among tarsiers, and monophyletic tarsier clades that were arranged in a star phylogeny (Figures 6, 7, 8). Thus, the acoustic form hypothesis test enforced a constraint tree in which each acoustic form had a monophyletic clade of haplotypes, but no other constraints on the topology were enforced, either within or among acoustic forms. A parsimony analysis to produce the most-parsimonious constrained tree was conducted for each hypothesis using the same PAUP settings that were used in the fine scale analysis, the only difference being the topological constraints. The macaque test found 48 mostparsimonious trees each with a tree length of 11,516. The acoustic form test found 34 most-parsimonious trees each with a tree length of 11,330. The microplate

57


Figure 2. Broad scale phylogenetic analysis—strict consensus tree.

58


Figure 3. Broad scale analysis—bootstrap tree.

59


Figure 4. Fine scale analysis—strict consensus tree.

60


Figure 5. Fine scale analysis—bootstrap tree.

61

62

monophyletic tarsier clades from those localities that share an acoustic form.

Figure 6. Acoustic constraint tree. This tree enforces

Figure 7. Macaque constraint tree. This tree enforces monophyletic tarsier clades from those localities that lie within each region of endemism identified by macaque distributions on Sulawesi.

Figure 8. Microplate constraint tree. This tree enforces monophyletic tarsier clades from those localities that lie within each region of endemism identified by the microplates that form Sulawesi.

Shekelle, Morales, Niemitz, Ichwan & Melnick - Distribution of Tarsier Haplotypes


test found 235 most-parsimonious trees each with a tree length of 11,411. Most-parsimonious constrained trees generated by each hypothesis were tested against the most-parsimonious unconstrained tree with the non-parametric test (=Templeton test) in PAUP, assuming a one-tailed test. In the macaque and microplate analyses, the null hypothesis of no significant difference in tree length between constrained tree and unconstrained tree was very confidently rejected (P0.01

macaque

11,516

12

2.7477

4

10

3.84, partial F to remove

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