Scandentia

Tree Shrews

(Tupaiidae)

Class Mammalia

Order Scandentia

Family Tupaiidae

Number of families 1

Thumbnail description
Small, squirrel-like mammals with relatively dense fur and a prominent tail (bushy in Tupaiinae; naked and scaly with a terminal tuft of hairs in Ptilocercinae); ears large and membranous; colors range from gray to dark brown dorsally and white to yellowish brown ventrally; species in the subfamily Tupaiinae are diurnal, whereas the pen-tailed tree shrew (Ptilocercinae) is nocturnal

Size
Relatively small body size, ranging from the pentailed tree shrew (head/body length 5 in [13 cm]; tail length 4.5 in [11 cm]; body mass 1.5 oz [43 g]) to the Philippine tree shrew (head/body length 9.5 in [24 cm]; tail length 7 in [18 cm]; body mass 12 oz [340 g])

Number of genera, species
5 genera; 19 species

Habitat
Primarily inhabitants of evergreen tropical rainforests

Conservation status
Endangered: 2 species; Vulnerable: 4 species; Lower Risk/Near Threatened: 1 species

Distribution
Southern and Southeast Asia

Evolution and systematics

Tree shrews have attracted considerable interest because of the possibility that they might be related to primates. The family Tupaiidae was originally included within the order Insectivora. Then, in Simpson's seminal classification of 1945, tree shrews were formally transferred to the order Primates. This was particularly because of Le Gros Clark's reports of a series of morphological similarities in the skull and brain and because of Carlsson's account of similarities in the musculature. However, the postulated link between tree shrews and primates was increasingly questioned from 1965 onwards and, following Butler (1972), it is now customary to allocate tree shrews to their own order Scandentia. This change in interpretation was partly due to recognition of the fundamental principle that reliable reconstruction of phylogenetic relationships depends on identification of novel, derived characters to the exclusion of retained primitive features. In fact, the undoubted morphological similarities between tree shrews and primates are arguably attributable to retention of many primitive features augmented by a number of convergent adaptations for arboreal life. For

instance, tree shrews resemble primates in possessing a cecum in the digestive tract, whereas this feature is lacking from typical insectivores. However, it is highly likely that ancestral placental mammals already possessed a cecum, so retention of this feature does not indicate a specific link between tree shrews and primates. For certain other features, independent development of similar characters may have occurred. For example, both tree shrews and primates have a bony strut (postorbital bar) along the outer margin of the eye socket. This is not a primitive feature, as it was undoubtedly lacking from ancestral placental mammals, but it has been developed independently in several mammalian groups, including many hoofed mammals (ungulates), some carnivores, and hyraxes. The likelihood of convergent similarity between tree shrews and primates is increased by the observation that arboreal tree shrew species show closer similarity to primates than do terrestrial tree shrew species. All tree shrews lack all of the clearly defining features of primates that are identifiable in the skull, brain, and reproductive system. Moreover, given the general reliance on dental similarities in reconstructing mammalian evolution, it is surprising that any resemblance between the molar teeth of tree shrews and those of primates has never been proposed. Superficially, tree shrews do resemble strepsirrhine primates (lemurs and lorises) in possessing a tooth comb in the lower jaw. However, in tree shrews the comb is formed by six incisors, whereas in strepsirrhine primates it is formed by two canines and four incisors, so convergent evolution is again the most likely explanation. Analyses of sequences for both nuclear and mitochondrial DNA have consistently failed to indicate any link

between tree shrews and primates. Instead, there have been several indications that tree shrews may be related to Lagomorpha (rabbits, hares, and pikas).

When tree shrews were still included in the order Insectivora, they were united with the elephant shrews (Macroscelidea) in the suborder Menotyphla, partially because of shared possession of a caecum, while all other insectivores lacking a cecum were placed in the suborder Lipotyphla. Subsequently, it was suggested that the super-order Archonta should be established for Menotyphla, Chiroptera (bats), Dermoptera (colugos), and Primates together. Now that the tree shrews have generally been excluded from the order Primates, there have been several attempts to resurrect the superorder Archonta (while discarding the elephant shrews from this assemblage). However, this alternative attempt to link tree shrews to primates along with certain other mammals is subject to the same problems as inclusion of tree shrews in the order Primates. The characters supposedly linking primates, tree shrews, colugos, and bats can be attributed to a combination of retained primitive features and convergent arboreal adaptations. DNA sequences provide no convincing evidence for any link between bats, primates, or tree

shrews, although there is some indication that colugos may be related to primates (but not tree shrews or bats).

The fossil record for tree shrews is very sparse, and many proposed fossil relatives have now been excluded from the group. It was originally believed that the Oligocene Anagale from North America was directly allied to tree shrews, but detailed examination instead suggested a link to lagomorphs (rabbits and their allies). However, some fragmentary material (partial skulls, isolated teeth, and possibly a ribcage) from Miocene deposits of India (Palaeotupaia), Pakistan (unnamed genus), and China (Prodendrogale) has been convincingly attributed to tree shrews. Furthermore, a possible early fossil relative of tree shrews (Eodendrogale) has also been reported from Eocene deposits of China.

Physical characteristics

Tree shrews are relatively small mammals that generally resemble squirrels in appearance, habitat, and behavior. All except the pen-tailed tree shrew have a squirrel-like bushy tail. Indeed, the Malay word tupai is used indiscriminately to refer to tree shrews and squirrels. As in squirrels, the eyes are moderate in size and oriented mainly laterally (except in the pen-tailed tree shrew, where they are rotated forward to some extent). In the skull, there is a bony strut (postorbital bar) on the outer margin of the eye socket. The dentition contains a total of 38 teeth with a dental formula of I2/3 C1/1 P3/3 M3/3. In the lower jaw, the crowns of the six incisors (three on each side) are angled forward to form a dental comb that is used in feeding and in grooming the fur. All digits of the hand and foot bear sharp claws. Tree shrews are quadrupedal, scansorial mammals that range from essentially arboreal to essentially terrestrial in habits. Arboreal species are small with short snouts and relatively long tails while terrestrial species are large with long snouts and relatively short tails. Semi-terrestrial species (the majority) are intermediate in these features. Sexual dimorphism in body size is virtually absent in all tree shrew species.

Distribution

Range extends from northwestern India eastwards to Mindanao in the Philippines and from southern China southwards to Java, including most of the islands in the Malayan Archipelago.

Habitat

Generally inhabitants of evergreen tropical rainforests.

Behavior

Tree shrews of the subfamily Tupaiinae are diurnal, whereas the pen-tailed tree shrew is nocturnal. All tree shrews use nests of some kind. As far as is known, tree shrews live in monogamous pairs that occupy a common territory and show aggression towards unfamiliar conspecifics. Scent marking is carried out both with droplets of urine and with secretions of specialized skin glands located on the chest and belly. Like squirrels, tree shrews commonly squat on their hind quarters and hold food items in their hands while eating.

Feeding ecology and diet

The basic diet of all tree shrew species includes a mixture of fruit and arthropods, and in most species, a large proportion of the activity period is spent in fruiting trees or searching for fallen fruit on the ground. Processing of fruit is unusual because tree shrews often spit out fibers rather than swallowing them. Transit times through the digestive tract are also remarkably short (just a few hours), resembling the extreme condition found in fruit-eating bats. All tree shrews consume a variety of arthropod species, but there are marked interspecific differences in prey selection and other kinds of prey may be taken.

Reproductive biology

Tree shrews live in monogamous pairs. The reproduction of tree shrews is highly unusual because, at least in members of the Tupaiinae studied to date, the offspring are born in a separate nest and suckled only once every 48 hours. This "absentee" system of maternal care was first discovered with Tupaia belangeri in captivity and subsequently reported for Tupaia minor and Tupaia tana as well. Field observations have confirmed the separate nest and 48-hour suckling rhythm for Tupaia tana. It is not yet known whether the same pattern of maternal behavior occurs in Anathana, Dendrogale, Urogale, and/or Ptilocercus. Tree shrews give birth to small litters of poorly developed (altricial) offspring that are naked at birth, with their eyes and ears sealed with membranes. The only other mammals known to give birth to altricial offspring in a separate nest and suckle them at long intervals are rabbits, which have 24-hour suckling intervals. According to species, the typical litter size of tree shrews is one to three offspring and females correspondingly have one to three pairs of teats (mammae). Gestation lasts between 43 and 56 days, with the average value differing by a few days between species. Tree shrews also have an unusual form of moderately invasive (endotheliochorial) placentation with twin placental discs attaching to special pads in the uterine wall. Development during the one-month nest phase and thereafter is rapid. In captivity, tree shrews reach sexual maturity at the age of four months, although under natural conditions breeding my be delayed until they are one year old.

Conservation status

Most species are relatively common, but some are subject to varying degrees of threat. Two species are Endangered (Tupaia longipes and Tupaia nicobarica), four are Vulnerable (Dendrogale melanura, Tupaia chrysogaster, Tupaia palawanensis and Urogale everetti) and one is Lower Risk/Near Threatened (Anathana ellioti).

Significance to humans

Tree shrews seem to be of no real significance to local human populations and it has in fact been reported that they are unpalatable.

Species accounts

List of Species

Indian tree shrew

Anathana ellioti

subfamily

Tupaiinae

taxonomy

Anathana ellioti (Waterhouse, 1850), Andhra Pradesh, India. Three subspecies recognized.

other common names

French: Toupaie d'Elliot; German: Indisches Spithzhörnchen.

physical characteristics

Head and body length 7.5 in (19 cm); tail length 7.5 in (19 cm); body mass 5.5 oz (160 g). Fur reddish brown to gray-brown dorsally and buff or white ventrally; oblique pale buff or white shoulder stripe present. Eyes surrounded by pale markings. Ears noticeably large and hairy. Tail equal in length to head and body combined. Relatively short snout. Canine teeth weakly developed.

distribution

Three main areas in peninsular India south of the Ganges River.

habitat

Evergreen tropical rainforests and thorny jungles.

behavior

Diurnal and semiterrestrial. Use nests, sometimes in holes among rocks.

feeding ecology and diet

Forage mainly on the ground, eating a basic diet of fruit and insects and also digging for worms.

reproductive biology

Females have three pairs of teats. No other specific information on reproduction is available, as this species has rarely been kept in captivity. Probably monogamous.

conservation status

Lower Risk/Near Threatened.

significance to humans

None known.

Bornean smooth-tailed tree shrew

Dendrogale melanura

subfamily

Tupaiinae

taxonomy

Dendrogale melanura (Thomas, 1892), Sarawak, Malaysia.

other common names

German: Bergspitzhörnchen; Spanish: Tupaya de Borneo.

physical characteristics

Head and body length 5 in (13 cm); tail length 4.5 in (11 cm); body mass 1.5 oz (43 g). Small-bodied. Dark brown fur dor-sally and pale buff ventrally. Short snout; ear flaps large. Prominent orange-brown rings around eyes. Weakly marked facial streaks present on either side of the face, extending from the snout to the ear. No shoulder stripes present. Claws notably sharp. Tail covered with fine smooth hair and darkening towards the tip.

distribution

Northern Borneo.

habitat

Evergreen tropical rainforests.

behavior

Diurnal and predominantly arboreal.

feeding ecology and diet

Little studied in the wild. Seems to feed predominantly on insects.

reproductive biology

Monogamous. Females have one pair of teats. No other specific information on reproduction available.

conservation status

Listed as Vulnerable.

significance to humans

None known.

Common tree shrew

Tupaia glis

subfamily

Tupaiinae

taxonomy

Tupaia glis (Diard, 1820), Penang Island, Malaysia. Several sub-species recognized.

other common names

French: Toupaie; German: Spitzhörnchen.

physical characteristics

Head and body length 7.5 in (19.5 cm); tail length 6.5 in (16.5 cm). Body mass 5 oz (142 g). Fur dark brown and sometimes almost black dorsally and orange-rufous ventrally. No conspicuous markings on head, but an oblique pale shoulder stripe is usually recognizable. Ears relatively small. Tail very dark and somewhat shorter than the combined length of the head and body.

distribution

Range extends south of the Isthmus of Kra in Thailand, down the Malayan Peninsula and into Sumatra, Java, and surrounding islands.

habitat

Evergreen tropical rainforests.

behavior

Diurnal and semi-terrestrial. Uses nests that are typically in tree hollows. Monogamous pairs live in defended territories.

feeding ecology and diet

Feeds primarily on the ground. Diet consists mainly of fruit and arthropods (including ants), but leaves have also been found in stomach contents.

reproductive biology

Monogamous. Females have two pairs of teats. Gestation period approximately 46 days.

conservation status

Relatively common and not immediately threatened.

significance to humans

None known.

Terrestrial tree shrew

Tupaia tana

subfamily

Tupaiinae

taxonomy

Tupaia tana Raffles, 1821, Sumatra, Indonesia.

other common names

French: Toupaie terrestre.

physical characteristics

Head and body length 8.5 in (22 cm); tail length 7 in (18 cm). Body mass 7 oz (198 g). Large-bodied. Fur dark rufous brown dorsally and orange-red or rusty red ventrally. Well-marked, pale yellowish stripe present on each shoulder and a conspicuous dark brown to black midline streak along the back. Anteriorly, this dorsal stripe is fainter and highlighted by pale areas on either side. Tail bushy and distinctly shorter than the combined length of head and body. Snout markedly elongated; canine teeth well developed. Claws robust and elongated.

distribution

Borneo, Sumatra, and several nearby islands.

habitat

Evergreen tropical rainforests.

behavior

Diurnal and essentially terrestrial.

feeding ecology and diet

Foraging typically takes place on the ground, including nosing through leaf litter and digging beneath it. The diet primarily includes fallen fruit and a large proportion of arthropods from a wide range of groups, including beetles, ants, spiders, orthopterans (cockroaches and crickets), centipedes, and millipedes. Also feeds regularly on earthworms.

reproductive biology

Presumably monogamous. Females have two pairs of teats.

conservation status

Relatively common and not immediately threatened.

significance to humans

None known.

Philippine tree shrew

Urogale everetti

subfamily

Tupaiinae

taxonomy

Urogale everetti (Thomas, 1892), Mindanao, Philippines.

other common names

French: Toupaie des Philippines; German: Philippinenspitzhörnchen.

physical characteristics

Head and body length 9.5 in (24 cm); tail length 7 in (18 cm). Body mass 9 oz (255 g). Largest-bodied, stocky tree shrew species. Fur dark brown dorsally and yellowish or rufous ventrally; pale shoulder stripe present. Tail markedly shorter than length of head and body combined and covered in dense rufous fur. Snout conspicuously elongated. Dentition distinctive in that the second pair of upper incisors is markedly enlarged to produce functional canines, while the third pair of lower incisors is reduced. Forelimb unique among tree shrews in showing adaptations for scratch-digging.

distribution

Mindanao Island and nearby islands (Dinigat and Siargao).

habitat

Predominantly found in the brush zone and the thick vegetation along river beds.

behavior

Diurnal and fully terrestrial.

feeding ecology and diet

Little is known about the natural diet, which is said to be omnivorous. Probably feeds predominantly on insects and fruits, like other tree shrew species, but the canine-like incisors suggest a greater emphasis on predation, perhaps including vertebrates.

reproductive biology

Probably forms monogamous pairs. Females have two pairs of teats. Gestation period reportedly about 55 days.

conservation status

Listed as Vulnerable because of progressive population decline.

significance to humans

None known.

Pen-tailed tree shrew

Ptilocercus lowii

subfamily

Ptilocercinae

taxonomy

Ptilocercus lowii Gray, 1848, Sarawak, Malaysia.

other common names

French: Ptilocerque; German: Federschwanzspitzhörnchen.

physical characteristics

Head and body length 5 in (13 cm); tail length 4.5 in (11 cm). Body mass 1.5 oz (43 g). Small-bodied. Fur dark gray dorsally and pale gray or buff ventrally. Dark facial stripe extends from the snout to behind the eye on each side. No shoulder stripe present. Short snout; upper incisors enlarged. Eyes more forward-facing than in other tree shrews but not enlarged. In association with their nocturnal habits, pen-tailed tree shrews have a reflecting layer (tapetum) behind the retina, producing a silvery eyeshine that is unique among mammals. Ear flaps large, membranous and mobile. Tail approximately equal in length to combined head and body length and covered with scales, except for the tip, which bears two rows of long, stiff white hairs on either side. In the foot, the first toe (hallux) is divergent but not opposable.

distribution

Disjunct distribution on the southern end of the Malayan peninsula, northwestern Borneo, northeastern Sumatra, and a few neighboring islands.

habitat

Evergreen tropical rainforests.

behavior

Nocturnal and essentially arboreal. Reportedly rest in tree holes lines with dried leaves during daytime.

feeding ecology and diet

Food is sought exclusively in trees. Typically forage on the surfaces of tree trunks, branches, and lianas rather than in foliage. At least some fruits are included in the diet, but there may be a heavy concentration on arthropods.

reproductive biology

Pen-tailed tree shrews have rarely been maintained in captivity and little is known about their reproduction. Females have two pairs of teats, indicating that the typical litter size is two offspring. Usually forms monogamous pairs.

conservation status

Rarely encountered and little studied in the wild, but not currently recognized as endangered. Because of the disjunct distribution, the overall geographical range is quite large, but this species may be locally quite rare.

significance to humans

None known.

Resources

Books

Butler, Percy M. "The Problem of Insectivore Classification." In Studies in Vertebrate Evolution, edited by Kenneth A. Joysey and Timothy S. Kemp, 253–265. Edinburgh: Oliver and Boyd, 1972.

Emmons, Louise H. Tupai: A Field Study of Bornean Treeshrews. Berkeley: University of California Press, 2000.

Le Gros Clark, Wilfred E. The Antecedents of Man. Edinburgh: Edinburgh University Press, 1971.

Luckett, W. Patrick. Comparative Biology and Evolutionary Relationships of Tree Shrews. New York: Plenum Press, 1980.

Martin, Robert D. Primate Origins and Evolution: A Phylogenetic Reconstruction. Princeton: Princeton University Press, 1990.

Wilson, Don E. "Order Scandentia." In Mammal Species of the World: A Taxonomic and Geographic Reference, edited by Don E. Wilson and DeeAnn M. Reeder. Washington, DC: Smithsonian Institution Press, 1993, 131–133.

Periodicals

Campbell, C., and G. Boyd. "On the Phyletic Relationships of the Tree Shrews." Mammal Review 4 (1974): 125–143.

D'Souza, Frances, and Robert D. Martin. "Maternal Behaviour and the Effects of Stress in Tree Shrews." Nature (London) 251 (1974): 309–311.

Emmons, Louise H. "Frugivory in Tree Shrews (Tupaia)." American Naturalist 138 (1991): 642–649.

Emmons, Louise H., and Alim Biun. "Malaysian Treeshrews: Maternal Behavior of a Wild Tree Shrew, Tupaia tana, in Sabah." National Geographic Research 7 (1991): 70–81.

Hill, John P. "On the Placentation of Tupaia." Journal of Zoology (London) 146 (1965): 278–304.

Kawamichi, Takeo, and Mieko Kawamichi. "Social System and Independence of Offspring of Tree Shrews." Primates 23 (1982): 189–205.

Lim, Boo L. "Note on the Food Habits of Ptilocercus lowii Gray (Pentail Tree-shrew) and Echinosorex gymnurus Raffles (Moonrat) in Malaya with Remarks on "Ecological Labelling" by Parasite Patterns." Journal of Zoology (London) 152 (1967): 375–379.

Martin, Robert D. "Reproduction and Ontogeny in Tree-shrews (Tupaia belangeri) with Reference to Their General Behaviour and Taxonomic Relationships." Zeitschrift fur Tierzuchtung und Zuchtungsbiologie 25 (1968): 409–532.

——. "Treeshrews: Unique Reproductive Mechanism of Systematic Importance." Science 152 (1966): 1402–1404.

Sargis, Eric J. "Functional Morphology of the Forelimb of Tupaiids (Mammalia, Scandentia) and Its Phylogenetic Implications." Journal of Morphology 253 (2002): 10–42.

——. "Functional Morphology of the Hindlimb of Tupaiids (Mammalia, Scandentia) and Its Phylogenetic Implications." Journal of Morphology 254 (2002): 149–185.

——. "The Postcranial Morphology of Ptilocercus lowii (Scandentia, Tupaiidae): An Analysis of Primatomorphan and Volitantian Characters." Journal of Mammalian Evolution 9 (2002): 137–160.

Schmitz, Jürgen, Martina Ohme, and Hans Zischler. "The Complete Mitochondrial Genome of Tupaia belangeri and the Phylogenetic affiliation of Scandentia to Other Eutherian Orders." Molecular Biology and Evolution 17 (2000): 1334–1343.

Simpson, George G. "The Principles of Classification and a Classification of Mammals." Bulletin of the American Museum of Natural History 85 (1945): 1–350.

Robert D. Martin, PhD