Dermoptera

Colugos

(Cynocephalidae)

Class Mammalia

Order Dermoptera

Family Cynocephalidae

Number of families 1

Thumbnail description
Specialized herbivorous gliding mammals with a furred membrane extending around almost the entire margin of the body

Size
Cat-sized mammals with an overall length of approximately 30 in (75 cm) and a body weight of about 3 lb (1.35 kg)

Number of genera, species
1 genus; 2 species

Habitat
Evergreen tropical rainforest

Conservation status
Vulnerable: 1 species

Distribution
Southeast Asia

Evolution and systematics

Colugos (also misleadingly labeled flying lemurs, although they are not lemurs and do not fly) exhibit a mosaic of features, some of which show individual similarities to bats, insectivores, or prosimian primates, while others are unique. Their most striking characteristics are adaptations for gliding. Because of their many unique features, the two colugo species have long been classified in an independent order of placental mammals (Dermoptera, literally meaning "skin-wings").

Although colugos are now generally regarded as an unusual and isolated mammalian lineage, they have been variously linked to insectivores (Insectivora), bats (Chiroptera), and/or primates (Primates). Some affinity to bats has often been suspected because of the potential link between gliding and actual flight. Perhaps the most influential suggestion has been that colugos, bats, tree shrews, and primates (with or without elephant shrews) should be allocated to a superorder labeled Archonta. However, the apparent morphological affinities between mammals allocated to the Archonta may be largely or exclusively attributable to retention of primitive adaptations for arboreal life that were present in ancestral

placental mammals. The unusual molar morphology of colugos, their small, very primitive brains, and their highly unusual ear region all indicate that there is no real link to primates. Molecular evidence concerning the affinities of colugos has been equivocal, reflecting the fact that it is difficult to resolve the position of an isolated, species-poor lineage that diverged at a very early stage. Indeed, evidence from complete mitochondrial DNA sequences seems to indicate that colugos are actually closer to higher primates than the latter are to prosimians. However, other molecular evidence clearly conflicts with this highly unlikely interpretation. While an early link between colugos and primates in the mammalian tree cannot be ruled out, there is still no strong evidence to support it.

As might be expected from the existence of only two modern species, the fossil record of colugos is very poorly documented. It was long accepted that the Plagiomenidae, a

poorly documented group of North American fossil mammals from mid-Paleocene to early Eocene deposits (approximately 50–60 million years old), are related to the colugos. However recent re-examinations of the Plagiomenidae indicate that supposed dental similarities to colugos are superficial and that there is no real affinity. A more recent alternative suggestion is that North American Paleocene forms in the family Mixodectidae are related to colugos, but this possibility requires further examination. In fact, a more likely prospect is provided by dental fossils discovered in Eocene deposits of Thailand, attributed to the genus Dermotherium major and identified more convincingly as related to colugos. There have been suggestions that some members of the Plesiadapiformes (a largely Paleocene group of mammals from Europe and North America usually allocated to the order Primates) show affinities to colugos. Indirect evidence was cited to support the interpretation that some plesiadapiforms (notably members of the family Paromomyidae) were adapted for gliding. This led to a variety of suggested relationships between colugos, Plesidapiformes, and primates of modern aspect. However, the supposed evidence for gliding adaptations in plesiadapiforms has now been largely discredited and there is little else to suggest a link to colugos.

Physical characteristics

Colugos are medium-sized arboreal mammals with very soft, dense fur. The pelage shows considerable variation in color, although the dorsal fur is typically brown in males and grayish brown in females. The color of the ventral fur varies

from yellow through bright orange to brownish red. The eyes are relatively large, reflecting adaptation for active movement at night, while the ears are small and almost naked. The snout is relatively long, giving the head a doglike appearance and accounting for the genus name Cynocephalus (literally "dog's head"). The skull is broad and relatively flat. The auditory bullae, which are also quite flat, are highly unusual among mammals both because of their bony composition and because the eardrum (tympanic membrane) is almost horizontal, a very primitive condition. The brain is also unusually small relative to body size and morphologically very primitive.

The most obvious gliding adaptation is a special membrane (patagium) extending around almost the entire margin of the body. All four limbs are relatively long and slender and the neck is long and mobile. During gliding, three dorsally furred membranes become stretched out on either side of the body: an anterior membrane (propatagium) between the side of the neck and the forelimb, an extensive lateral membrane (plagiopatagium) between the forelimb and hindlimb, and a large posterior membrane (uropatagium) between the hindlimb and the tail. Other gliding mammals (certain rodents and marsupials) lack a uropatagium and have a long tail, whereas the tail is quite short in colugos. Furthermore, the patagium in colugos extends between the fingers and toes, such that the term "mitten-gliders" has been used. In contrast to bats, the colugo's membranes are not used for actual flight but merely for gliding, so there is always some loss of height during aerial movement between trees. Some degree of steering is achieved by altering the positions of the limbs and tail. The fingers and toes bear prominent, strongly curving claws that are used to cling to trees.

The gastrointestinal tract is very specialized as a reflection of the strictly herbivorous diet. Surprisingly, the stomach is relatively small and narrow, and there is an abbreviated small intestine, which is shorter than the colon. However, the caecum is greatly enlarged, providing a chamber for symbiotic bacteria that assist in digesting plant material. The dental formula is 2.1.2.3/3.1.3.3, giving a total of 34 teeth, and there are a number of dental peculiarities. All canine teeth and the posterior incisors in the upper jaw are double-rooted, an unusual feature otherwise found only in a few insectivores. In mammals generally, these teeth usually have only a single root. The first two incisors on either side of the lower jaw, which are tilted forwards (procumbent), are unique among mammals in that in each one the crown is notched and comblike, with up to 20 tines on each tooth. (There is a superficial resemblance here to the toothcomb found in lemurs and lorises among primates and in tree shrews, but in those mammals individual teeth form single tines of the "comb.") The function of the comblike lower incisors of colugos is unknown, although it has been suggested that they may be used in grooming the fur. It is highly likely that these special teeth are also used during feeding in some way. The molar teeth are relatively primitive, showing a simple three-cusped pattern in the upper jaw.

Distribution

Colugos are found throughout much of Southeast Asia, including southern Myanmar, Thailand, Laos, Cambodia, Vietnam, Malay Peninsula, Sumatra, Java, Borneo, and parts of the Philippines (southern Mindanao, Basilan, Samar, Leyte, Bohol).

Habitat

Primary evergreen rainforest.

Behavior

Colugos are nocturnal and apparently solitary in habits when active, although sometimes small nesting groups are found. During the day, they sleep in tree hollows or clinging to tree trunks or the undersides of large branches, using their well-developed claws. At night, they can move along the undersides of branches quite rapidly and scramble up tree trunks with a series of leaps, thus reaching the necessary height to glide to another tree. Single glides of up to 230 ft (70 m) are quite common, and a maxiumum of 450 ft (135 m) has been reported.

Feeding ecology and diet

Colugos are strictly herbivorous, eating leaves, buds, flowers, some fruit, and pods.

Reproductive biology

Colugos have rarely been kept in captivity, so few details of their reproduction are known. Birth of a single infant is typical, although twins can occur, and there is a single pair of teats (mammae) located near the armpits. In contrast to other medium-sized mammals with single births, the gestation period is short (about 60 days) and the newborn infant (neonate) is small (1.2 oz or 35 g) and very poorly developed, almost like a marsupial offspring. Up until weaning (at about six months of age), the infant is carried on the mother's belly, enclosed within her patagium. The mother may carry her infant with her even when gliding, although some reports indicate that the infant may also be "parked." The offspring grows slowly and does not reach maturity until about two to three years of age.

Conservation status

The Philippine colugo (Cynocephalus volans) is listed as Vulnerable by the IUCN. Although colugos are sometimes hunted for their meat and soft fur, they are not severely threatened by humans and are, in fact, protected in certain areas by local taboos. The greatest threat to these unusual animals comes from rampant deforestation in the areas they inhabit.

Significance to humans

Apart from occasional hunting, colugos seem to be of little significance to humans.

Species accounts

List of Species

Malayan colugo

Cynocephalus variegatus

taxonomy

Galeopithecus variegatus (Audebert, 1799), Java, Indonesia. The Malayan colugo has sometimes been placed in the separate genus Galeopterus, but the degree of difference from the Philippine colugo is not really sufficient to justify separation at this level.

other common names

English: Malayan flying lemur.

physical characteristics

Head and body length 15 in (38 cm); tail length 10 in (25 cm); body weight 3.3 lb (1.5 kg). Width of spread patagium 28 in (70 cm). Dorsal fur typically brown/reddish brown in males and grayish brown in females, with conspicuous white spots, particularly on the patagium, in both sexes. Ventral fur orange-yellow to orange.

distribution

Thailand, Indochina, peninsular Malaya, Sumatra, Java, Borneo, and some adjacent islands.

habitat

Primary evergreen rainforest.

behavior

Nocturnal and apparently solitary when active.

feeding ecology and diet

Strictly herbivorous, eating leaves, buds, flowers, some fruit, and pods.

reproductive biology

Mating system is unknown. Single births and a single pair of teats typical. Gestation period is approximately 60 days. Infant small and poorly developed at birth. Weaning at about 6 months.

conservation status

Not threatened.

significance to humans

Apart from occasional hunting, colugos seem to be of little significance to humans.

Philippine colugo

Cynocephalus volans

taxonomy

Lemur volans (Linnaeus, 1758), Luzon, Philippines. There has been little discussion surrounding this species.

other common names

English: Philippine flying lemur.

physical characteristics

Head and body length 14 in (35 cm); tail length 10 in (25 cm); body weight 2.8 lb (1.25 kg). The Philippine colugo is somewhat smaller and darker than the Malayan species and lacks conspicuous white spots. Dorsal fur typically brown in males and grayish in females. Ventral fur orange to brownish red.

distribution

Philippine Islands (Mindanao, Basilan, Samar, Leyte, Bohol).

habitat

Primary evergreen rainforest.

behavior

Nocturnal and apparently solitary when active.

feeding ecology and diet

Strictly herbivorous, eating leaves, buds, flowers, some fruit, and pods.

reproductive biology

Mating system is unknown. Single births and a single pair of teats typical. Gestation period is approximately 60 days. Infant small and poorly developed at birth. Weaning at about 6 months.

conservation status

Listed as Vulnerable by the IUCN, primarily because of deforestation.

significance to humans

Apart from occasional hunting, colugos seem to be of little significance to humans.

Resources

Books

Beard, K. Christopher. "Phylogenetic Systematics of the Primatomorpha, with Special Reference to Dermoptera." In Mammal Phylogeny. Vol. 2, Placentals, edited by Frederick S. Szalay, Michael J. Novacek, and Malcolm C. McKenna. New York: Springer-Verlag, 1993.

Hayssen, Virginia D., Ari Van Tienhoven, and Ans Van Tienhoven. Asdell's Patterns of Mammalian Reproduction: A Compendium of Species-Specific Data. Ithaca, NY: Comstock Publishing Associates, Cornell University Press, 1993.

Lekagul, Boonsong, and Jeffrey A. McNeely. Mammals of Thailand. Bangkok: Sahakarnbhat Co., 1977.

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

Medway, Lord. The Wild Mammals of Malaya and Singapore. 2nd ed. London: Oxford University Press, 1978.

Nowak, Ronald M., and John L. Paradiso. Walker's Mammals of the World. 4th ed. Baltimore: Johns Hopkins University Press, 1983

Stucky, R. K., and Malcolm C. McKenna. "Mammalia." In The Fossil Record II, edited by Michael J. Benton, 739–771. London: Chapman & Hall, 1993.

Periodicals

Aimi, M., and H. Inagaki. "Grooved Lower Incisors in Flying Lemurs." Journal of Mammalogy 69 (1988): 138–140.

Arnason, Ulfur, et al. "Mammalian Mitogenomic Relationships and the Root of the Eutherian Tree." Proceedings of the National Academy of Sciences U.S.A. 99 (2002): 8151–8156.

Beard, K. "Gliding Behaviour and Palaeoecology of the Alleged Primate Family Paromomyidae (Mammalia, Dermoptera)." Nature, London 345 (1990): 340–341.

Ducrocq, Stéphane, et al. "First Fossil Flying Lemur: A Dermopteran from the Late Eocene of Thailand." Palaeontology 35 (1992): 373–380.

Hamrick, Mark W., Burt A. Rosenman, and Jason A. Brush. "Phalangeal Morphology of the Paromomyidae (Primates, Plesiadapiformes): The Evidence for Gliding Behavior Reconsidered." American Journal of Physical Anthropology 109 (1999): 397–413.

Hunt, Robert M., and William W. Korth. "The Auditory Region of Dermoptera: Morphology and Function Relative to Other Living Mammals." Journal of Morphology 164 (1980): 167–211.

Kay, Richard F., Richard W. Thorington, and Peter Houde. "Eocene Plesiadapiform shows Affinities with Flying Lemurs, not Primates." Nature, London 345 (1990): 342–344.

Krause, David W. "Were Paromomyids Gliders? Maybe, Maybe Not." Journal of Human Evolution 21 (1991): 177–188.

Lim, Boo Liat "Observations on the Food Habits and Ecological Habitat of the Malaysian Flying Lemur." International Zoo Yearbook 7 (1967): 196–197.

MacPhee, Russell D. E., Matt Cartmill, and Kenneth D. Rose. "Craniodental Morphology and Relationships of the supposed Eocene Dermopteran Plagiomene (Mammalia)." Journal of Vertebrate Paleontology 9 (1989): 329–349.

Martin, Robert D. "Some Relatives take a Dive." Nature, London 345 (1990): 291–292.

——. "Primate Origins: Plugging the Gaps." Nature, London 363 (1993): 223–234.

Murphy, William J., et al. "Resolution of the Early Placental Mammal Radiation using Bayesian Phylogenetics." Science 294 (December 14, 2001): 2348–2351.

Pirlot, P., and T. Kamiya. "Relative Size of Brain and Brain Components in Three Gliding Placentals (Dermoptera; Rodentia)." Canadian Journal of Zoology 60 (1982): 565–572.

Rose, Kenneth D., and Elwyn L. Simons. "Dental Function in the Plagiomenidae: Origin and Relationships of the Mammalian order Dermoptera." Contributions of the Museum of Palentology of the University of Michigan 24 (1977): 221–236.

Runestad, Jacqueline A., and Christopher B. Ruff. "Structural Adaptations for Gliding in Mammals with Implications for Locomotor Behavior in Paromomyids." American Journal of Physical Anthropology 98 (1995): 101–119.

Schmitz, Jürgen, Martina Ohme, Bambang Suryobroto, and Hans Zischler. "The Colugo (Cynocephalus variegatus, Dermoptera): The Primates' Gliding Sister?" Molecular Biology and Evolution 19 (2002): 2308–2312.

Stafford, B. J., and Frederick S. Szalay. "Craniodental Functional Morphology and Taxonomy of Dermopterans." Journal of Mammalogy 81 (2000): 360–385.

Szalay, Frederick S., and S. G. Lucas. "The postcranial Morphology of Paleocene Chriacus and Mixodectes and the Phylogenetic Relationships of Archontan Mammals." Bulletin of the New Mexico Museum of Natural History and Science 7 (1996): 1–47.

Wharton, Charles H. "Notes on the Life History of the Flying Lemur." Journal of Mammalogy 31 (1950): 269–273.

Wible, John R. "Cranial Circulation and Relationships of the Colugo Cynocephalus (Dermoptera, Mammalia)." American Museum Novitates 3072 (1993): 1–27.

Robert D. Martin, PhD